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Yuan W, Huang YC, LeBlanc C, Poulet A, De Luna Vitorino FN, Valsakumar D, Dean R, Garcia BA, van Wolfswinkel JC, Voigt P, Jacob Y. H3.1K27M-induced misregulation of the TONSOKU-H3.1 pathway causes genomic instability. Nat Commun 2025; 16:3547. [PMID: 40229276 PMCID: PMC11997104 DOI: 10.1038/s41467-025-58892-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/26/2024] [Accepted: 04/03/2025] [Indexed: 04/16/2025] Open
Abstract
The oncomutation lysine 27-to-methionine in histone H3 (H3K27M) is frequently identified in tumors of patients with diffuse midline glioma-H3K27 altered (DMG-H3K27a). H3K27M inhibits the deposition of the histone mark H3K27me3, which affects the maintenance of transcriptional programs and cell identity. Cells expressing H3K27M are also characterized by defects in genome integrity, but the mechanisms linking expression of the oncohistone to DNA damage remain mostly unknown. In this study, we demonstrate that expression of H3.1K27M in the model plant Arabidopsis thaliana interferes with post-replicative chromatin maturation mediated by the H3.1K27 methyltransferases ATXR5 and ATXR6. As a result, H3.1 variants on nascent chromatin remain unmethylated at K27 (H3.1K27me0), leading to ectopic activity of TONSOKU (TSK/TONSL), which induces DNA damage and genomic alterations. Elimination of TSK activity suppresses the genome stability defects associated with H3.1K27M expression, while inactivation of specific DNA repair pathways prevents survival of H3.1K27M-expressing plants. Overall, our results suggest that H3.1K27M disrupts the chromatin-based mechanisms regulating TSK activity, which causes genomic instability and may contribute to the etiology of DMG-H3K27a.
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Affiliation(s)
- Wenxin Yuan
- Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences, Yale University, New Haven, CT, USA
| | - Yi-Chun Huang
- Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences, Yale University, New Haven, CT, USA
| | - Chantal LeBlanc
- Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences, Yale University, New Haven, CT, USA
| | - Axel Poulet
- Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences, Yale University, New Haven, CT, USA
- Yale Stem Cell Center, Yale School of Medicine, New Haven, CT, USA
- Center for RNA Science and Medicine, Yale School of Medicine, New Haven, CT, USA
| | - Francisca N De Luna Vitorino
- Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St Louis, MO, USA
| | - Devisree Valsakumar
- Wellcome Centre for Cell Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, UK
- Epigenetics Programme, Babraham Institute, Cambridge, UK
| | - Renee Dean
- Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St Louis, MO, USA
| | - Benjamin A Garcia
- Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St Louis, MO, USA
| | - Josien C van Wolfswinkel
- Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences, Yale University, New Haven, CT, USA
- Yale Stem Cell Center, Yale School of Medicine, New Haven, CT, USA
- Center for RNA Science and Medicine, Yale School of Medicine, New Haven, CT, USA
| | - Philipp Voigt
- Epigenetics Programme, Babraham Institute, Cambridge, UK
| | - Yannick Jacob
- Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences, Yale University, New Haven, CT, USA.
- Yale Cancer Center, Yale School of Medicine, New Haven, CT, USA.
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Li J, Liang W, He XQ, Qian W. DNA damage triggers heritable alterations in DNA methylation patterns in Arabidopsis. MOLECULAR PLANT 2025; 18:501-512. [PMID: 39863921 DOI: 10.1016/j.molp.2025.01.019] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/25/2024] [Revised: 01/02/2025] [Accepted: 01/23/2025] [Indexed: 01/27/2025]
Abstract
It has been hypothesized that DNA damage has the potential to induce DNA hypermethylation, contributing to carcinogenesis in mammals. However, there is no sufficient evidence to support that DNA damage can cause genome-wide DNA hypermethylation. In this study, we demonstrated that DNA single-strand breaks with 3' blocked ends (DNA 3' blocks) not only can reinforce DNA methylation at normally methylated loci but also can induce DNA methylation at normally nonmethylated loci in plants. The CG and CHG hypermethylation tend to localize within gene bodies, with a significant proportion being de novo generated. In contrast, the CHH hypermethylation is concentrated in centromeric and pericentromeric regions, primarily being reinforced methylation. Mechanistically, DNA 3' blocks regulate the DREAM complex to induce CG and CHG methylation. Moreover, they utilize the RdDM pathway to induce CHH hypermethylation. Intriguingly, repair of DNA damage or blocking the DNA damage response can fully abolish CHH hypermethylation and partially rescue CHG hypermethylation but rarely alter CG hypermethylation, indicating that DNA damage-induced symmetric DNA methylation can serve as a form of genetic imprinting. Collectively, these results suggest that DNA damage is an important force driving the emergence and evolution of genomic DNA methylation levels and patterns in plants.
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Affiliation(s)
- Jinchao Li
- State Key Laboratory of Wheat Improvement, School of Advanced Agricultural Sciences, Peking University, Beijing 100871, China; School of Life Sciences, Fudan University, Shanghai 200438, China.
| | - Wenjie Liang
- School of Life Sciences, Fudan University, Shanghai 200438, China
| | - Xin-Qiang He
- School of Life Sciences, Peking University, Beijing 100871, China
| | - Weiqiang Qian
- State Key Laboratory of Wheat Improvement, School of Advanced Agricultural Sciences, Peking University, Beijing 100871, China; Beijing Life Science Academy, Beijing 102299, China.
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Cawood GL, Ton J. Decoding resilience: ecology, regulation, and evolution of biosynthetic gene clusters. TRENDS IN PLANT SCIENCE 2025; 30:185-198. [PMID: 39393973 DOI: 10.1016/j.tplants.2024.09.008] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/13/2024] [Revised: 08/28/2024] [Accepted: 09/13/2024] [Indexed: 10/13/2024]
Abstract
Secondary metabolism is crucial for plant survival and can generate chemistry with nutritional, therapeutic, and industrial value. Biosynthetic genes of selected secondary metabolites cluster within localised chromosomal regions. The arrangement of these biosynthetic gene clusters (BGCs) challenges the long-held model of random gene order in eukaryotes, raising questions about their regulation, ecological significance, and evolution. In this review, we address these questions by exploring the contribution of BGCs to ecologically relevant plant-biotic interactions, while also evaluating the molecular-(epi)genetic mechanisms controlling their coordinated stress- and tissue-specific expression. Based on evidence that BGCs have distinct chromatin signatures and are enriched with transposable elements (TEs), we integrate emerging hypotheses into an updated evolutionary model emphasising how stress-induced epigenetic processes have shaped BGC formation.
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Affiliation(s)
- George Lister Cawood
- Plants, Photosynthesis and Soil, School of Biosciences, The University of Sheffield, Western Bank, Sheffield, S10 2TN, UK.
| | - Jurriaan Ton
- Plants, Photosynthesis and Soil, School of Biosciences, The University of Sheffield, Western Bank, Sheffield, S10 2TN, UK.
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Sall SO, Alioua A, Staerck S, Graindorge S, Pellicioli M, Schuler J, Galindo C, Raffy Q, Rousseau M, Molinier J. Characterization of radiations-induced genomic structural variations in Arabidopsis thaliana. THE PLANT JOURNAL : FOR CELL AND MOLECULAR BIOLOGY 2025; 121:e17180. [PMID: 39616610 PMCID: PMC11712536 DOI: 10.1111/tpj.17180] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/04/2024] [Revised: 11/05/2024] [Accepted: 11/18/2024] [Indexed: 01/11/2025]
Abstract
DNA, is assaulted by endogenous and exogenous agents that lead to the formation of damage. In order to maintain genome integrity DNA repair pathways must be efficiently activated to prevent mutations and deleterious chromosomal rearrangements. Conversely, genome rearrangement is also necessary to allow genetic diversity and evolution. The antagonist interaction between maintenance of genome integrity and rearrangements determines genome shape and organization. Therefore, it is of great interest to understand how the whole linear genome structure behaves upon formation and repair of DNA damage. For this, we used long reads sequencing technology to identify and to characterize genomic structural variations (SV) of wild-type Arabidopsis thaliana somatic cells exposed either to UV-B, to UV-C or to protons irradiations. We found that genomic regions located in heterochromatin are more prone to form SVs than those located in euchromatin, highlighting that genome stability differs along the chromosome. This holds true in Arabidopsis plants deficient for the expression of master regulators of the DNA damage response (DDR), ATM (Ataxia-telangiectasia-mutated) and ATR (Ataxia-telangiectasia-mutated and Rad3-related), suggesting that independent and alternative surveillance processes exist to maintain integrity in genic regions. Finally, the analysis of the radiations-induced deleted regions allowed determining that exposure to UV-B, UV-C and protons induced the microhomology-mediated end joining mechanism (MMEJ) and that both ATM and ATR repress this repair pathway.
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Affiliation(s)
- Salimata Ousmane Sall
- Institut de biologie moléculaire des plantes du CNRS12 rue du Général Zimmer67000StrasbourgFrance
| | - Abdelmalek Alioua
- Institut de biologie moléculaire des plantes du CNRS12 rue du Général Zimmer67000StrasbourgFrance
| | - Sébastien Staerck
- Institut de biologie moléculaire des plantes du CNRS12 rue du Général Zimmer67000StrasbourgFrance
| | - Stéfanie Graindorge
- Institut de biologie moléculaire des plantes du CNRS12 rue du Général Zimmer67000StrasbourgFrance
| | - Michel Pellicioli
- Institut pluridisciplinaire Hubert CurienCampus de Cronenbourg23 rue LoessBP 28 67037Strasbourg CedexFrance
| | - Jacky Schuler
- Institut pluridisciplinaire Hubert CurienCampus de Cronenbourg23 rue LoessBP 28 67037Strasbourg CedexFrance
| | - Catherine Galindo
- Institut pluridisciplinaire Hubert CurienCampus de Cronenbourg23 rue LoessBP 28 67037Strasbourg CedexFrance
| | - Quentin Raffy
- Institut pluridisciplinaire Hubert CurienCampus de Cronenbourg23 rue LoessBP 28 67037Strasbourg CedexFrance
| | - Marc Rousseau
- Institut pluridisciplinaire Hubert CurienCampus de Cronenbourg23 rue LoessBP 28 67037Strasbourg CedexFrance
- Present address:
Ecole Nationale Supérieure d'Ingénieurs de CaenLaboratoire de physique corpusculaire6 Boulevard du maréchal Juin14050Caen Cedex 4France
| | - Jean Molinier
- Institut de biologie moléculaire des plantes du CNRS12 rue du Général Zimmer67000StrasbourgFrance
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Farkas D, Dobránszki J. Vegetal memory through the lens of transcriptomic changes - recent progress and future practical prospects for exploiting plant transcriptional memory. PLANT SIGNALING & BEHAVIOR 2024; 19:2383515. [PMID: 39077764 PMCID: PMC11290777 DOI: 10.1080/15592324.2024.2383515] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/11/2024] [Revised: 07/12/2024] [Accepted: 07/15/2024] [Indexed: 07/31/2024]
Abstract
Plant memory plays an important role in the efficient and rapid acclimation to a swiftly changing environment. In addition, since plant memory can be inherited, it is also of adaptive and evolutionary importance. The ability of a plant to store, retain, retrieve and delete information on acquired experience is based on cellular, biochemical and molecular networks in the plants. This review offers an up-to-date overview on the formation, types, checkpoints of plant memory based on our current knowledge and focusing on its transcriptional aspects, the transcriptional memory. Roles of long and small non-coding RNAs are summarized in the regulation, formation and the cooperation between the different layers of the plant memory, i.e. in the establishment of epigenetic changes associated with memory formation in plants. The RNA interference mechanisms at the RNA and DNA level and the interplays between them are also presented. Furthermore, this review gives an insight of how exploitation of plant transcriptional memory may provide new opportunities for elaborating promising cost-efficient, and effective strategies to cope with the ever-changing environmental perturbations, caused by climate change. The potentials of plant memory-based methods, such as crop priming, cross acclimatization, memory modification by miRNAs and associative use of plant memory, in the future's agriculture are also discussed.
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Affiliation(s)
- Dóra Farkas
- Centre for Agricultural Genomics and Biotechnology, Faculty of the Agricultural and Food Science and Environmental Management, University of Debrecen, Nyíregyháza, Hungary
| | - Judit Dobránszki
- Centre for Agricultural Genomics and Biotechnology, Faculty of the Agricultural and Food Science and Environmental Management, University of Debrecen, Nyíregyháza, Hungary
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Yuan W, Huang YC, LeBlanc C, Poulet A, Valsakumar D, van Wolfswinkel JC, Voigt P, Jacob Y. H3.1K27M-induced misregulation of the TSK/TONSL-H3.1 pathway causes genomic instability. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2024:2024.12.09.627617. [PMID: 39713323 PMCID: PMC11661185 DOI: 10.1101/2024.12.09.627617] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Indexed: 12/24/2024]
Abstract
The oncomutation lysine 27-to-methionine in histone H3 (H3K27M) is frequently identified in tumors of patients with diffuse midline glioma-H3K27 altered (DMG-H3K27a). H3K27M inhibits the deposition of the histone mark H3K27me3, which affects the maintenance of transcriptional programs and cell identity. Cells expressing H3K27M are also characterized by defects in genome integrity, but the mechanisms linking expression of the oncohistone to DNA damage remain mostly unknown. In this study, we demonstrate that expression of H3.1K27M in the model plant Arabidopsis thaliana interferes with post-replicative chromatin maturation mediated by the H3.1K27 methyltransferases ATXR5 and ATXR6. As a result, H3.1 variants on nascent chromatin remain unmethylated at K27 (H3.1K27me0), leading to ectopic activity of TONSOKU (TSK), which induces DNA damage and genomic alterations. Elimination of TSK activity suppresses the genome stability defects associated with H3.1K27M expression, while inactivation of specific DNA repair pathways prevents survival of H3.1K27M-expressing plants. Overall, our results suggest that H3.1K27M disrupts the chromatin-based mechanisms regulating TSK/TONSL activity, which causes genomic instability and may contribute to the etiology of DMG-H3K27a.
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Affiliation(s)
- Wenxin Yuan
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
| | - Yi-Chun Huang
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
| | - Chantal LeBlanc
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
| | - Axel Poulet
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
- Yale Stem Cell Center, Yale School of Medicine, New Haven, CT 06511, USA
- Center for RNA science and medicine, Yale School of Medicine, New Haven. CT 06511, USA
| | - Devisree Valsakumar
- Wellcome Centre for Cell Biology, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3BF, United Kingdom
- Epigenetics Programme, Babraham Institute, Cambridge CB22 3AT, United Kingdom
| | - Josien C. van Wolfswinkel
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
- Yale Stem Cell Center, Yale School of Medicine, New Haven, CT 06511, USA
- Center for RNA science and medicine, Yale School of Medicine, New Haven. CT 06511, USA
| | - Philipp Voigt
- Epigenetics Programme, Babraham Institute, Cambridge CB22 3AT, United Kingdom
| | - Yannick Jacob
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
- Yale Cancer Center, Yale School of Medicine; New Haven, Connecticut 06511, USA
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7
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Wu W, Guo L, Yin L, Cai B, Li J, Li X, Yang J, Zhou H, Tao Z, Li Y. Genomic convergence in terrestrial root plants through tandem duplication in response to soil microbial pressures. Cell Rep 2024; 43:114786. [PMID: 39331502 DOI: 10.1016/j.celrep.2024.114786] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/25/2024] [Revised: 08/04/2024] [Accepted: 09/06/2024] [Indexed: 09/29/2024] Open
Abstract
Despite increasing reports of convergent adaptation, evidence for genomic convergence across diverse species worldwide is lacking. Here, our study of 205 Archaeplastida genomes reveals evidence of genomic convergence through tandem duplication (TD) across different lineages of root plants despite their genomic diversity. TD-derived genes, notably prevalent in trees with developed root systems embedded in soil, are enriched in enzymatic catalysis and biotic stress responses, suggesting adaptations to environmental pressures. Correlation analyses suggest that many factors, particularly those related to soil microbial pressures, are significantly associated with TD dynamics. Conversely, flora transitioned to aquatic, parasitic, halophytic, or carnivorous lifestyles-reducing their interaction with soil microbes-exhibit a consistent decline in TD frequency. This trend is further corroborated in mangroves that independently adapted to hypersaline intertidal soils, characterized by diminished microbial activity. Our findings propose TD-driven genomic convergence as a widespread adaptation to soil microbial pressures among terrestrial root plants.
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Affiliation(s)
- Wenwu Wu
- State Key Laboratory of Subtropical Silviculture, School of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, China; Zhejiang Key Laboratory of Forest Genetics and Breeding, Hangzhou 311400, China.
| | - Liangyu Guo
- State Key Laboratory of Subtropical Silviculture, School of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, China
| | - Liufan Yin
- State Key Laboratory of Subtropical Silviculture, School of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, China
| | - Bijun Cai
- State Key Laboratory of Subtropical Silviculture, School of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, China
| | - Jing Li
- State Key Laboratory of Subtropical Silviculture, School of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, China
| | - Xiaoxiao Li
- Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang University, Hangzhou 310058, China
| | - Jian Yang
- State Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China
| | - Haichao Zhou
- MNR Key Laboratory for Geo-Environmental Monitoring of Great Bay Area, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518071, China
| | - Zeng Tao
- Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang University, Hangzhou 310058, China.
| | - Yan Li
- State Key Laboratory of Subtropical Silviculture, School of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, China.
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8
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Caporale LH. Evolutionary feedback from the environment shapes mechanisms that generate genome variation. J Physiol 2024; 602:2601-2614. [PMID: 38194279 DOI: 10.1113/jp284411] [Citation(s) in RCA: 1] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/17/2023] [Accepted: 12/14/2023] [Indexed: 01/10/2024] Open
Abstract
Darwin recognized that 'a grand and almost untrodden field of inquiry will be opened, on the causes and laws of variation.' However, because the Modern Synthesis assumes that the intrinsic probability of any individual mutation is unrelated to that mutation's potential adaptive value, attention has been focused on selection rather than on the intrinsic generation of variation. Yet many examples illustrate that the term 'random' mutation, as widely understood, is inaccurate. The probabilities of distinct classes of variation are neither evenly distributed across a genome nor invariant over time, nor unrelated to their potential adaptive value. Because selection acts upon variation, multiple biochemical mechanisms can and have evolved that increase the relative probability of adaptive mutations. In effect, the generation of heritable variation is in a feedback loop with selection, such that those mechanisms that tend to generate variants that survive recurring challenges in the environment would be captured by this survival and thus inherited and accumulated within lineages of genomes. Moreover, because genome variation is affected by a wide range of biochemical processes, genome variation can be regulated. Biochemical mechanisms that sense stress, from lack of nutrients to DNA damage, can increase the probability of specific classes of variation. A deeper understanding of evolution involves attention to the evolution of, and environmental influences upon, the intrinsic variation generated in gametes, in other words upon the biochemical mechanisms that generate variation across generations. These concepts have profound implications for the types of questions that can and should be asked, as omics databases become more comprehensive, detection methods more sensitive, and computation and experimental analyses even more high throughput and thus capable of revealing the intrinsic generation of variation in individual gametes. These concepts also have profound implications for evolutionary theory, which, upon reflection it will be argued, predicts that selection would increase the probability of generating adaptive mutations, in other words, predicts that the ability to evolve itself evolves.
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Zou M, Shabala S, Zhao C, Zhou M. Molecular mechanisms and regulation of recombination frequency and distribution in plants. TAG. THEORETICAL AND APPLIED GENETICS. THEORETISCHE UND ANGEWANDTE GENETIK 2024; 137:86. [PMID: 38512498 PMCID: PMC10957645 DOI: 10.1007/s00122-024-04590-4] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/11/2023] [Accepted: 02/28/2024] [Indexed: 03/23/2024]
Abstract
KEY MESSAGE Recent developments in understanding the distribution and distinctive features of recombination hotspots are reviewed and approaches are proposed to increase recombination frequency in coldspot regions. Recombination events during meiosis provide the foundation and premise for creating new varieties of crops. The frequency of recombination in different genomic regions differs across eukaryote species, with recombination generally occurring more frequently at the ends of chromosomes. In most crop species, recombination is rare in centromeric regions. If a desired gene variant is linked in repulsion with an undesired variant of a second gene in a region with a low recombination rate, obtaining a recombinant plant combining two favorable alleles will be challenging. Traditional crop breeding involves combining desirable genes from parental plants into offspring. Therefore, understanding the mechanisms of recombination and factors affecting the occurrence of meiotic recombination is important for crop breeding. Here, we review chromosome recombination types, recombination mechanisms, genes and proteins involved in the meiotic recombination process, recombination hotspots and their regulation systems and discuss how to increase recombination frequency in recombination coldspot regions.
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Affiliation(s)
- Meilin Zou
- Tasmanian Institute of Agriculture, University of Tasmania, Private Bag 1375, Prospect, TAS, 7250, Australia
| | - Sergey Shabala
- Tasmanian Institute of Agriculture, University of Tasmania, Private Bag 1375, Prospect, TAS, 7250, Australia
- School of Biological Sciences, University of Western Australia, 35 Stirling Highway, Perth, 6009, Australia
| | - Chenchen Zhao
- Tasmanian Institute of Agriculture, University of Tasmania, Private Bag 1375, Prospect, TAS, 7250, Australia
| | - Meixue Zhou
- Tasmanian Institute of Agriculture, University of Tasmania, Private Bag 1375, Prospect, TAS, 7250, Australia.
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Thulasi Devendrakumar K, Goldstein M, Kronstad J, Li X. Deletions within intronic T-DNA lead to reversion of T-DNA mutant phenotypes. THE PLANT JOURNAL : FOR CELL AND MOLECULAR BIOLOGY 2024; 117:161-176. [PMID: 37773774 DOI: 10.1111/tpj.16482] [Citation(s) in RCA: 2] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 01/24/2023] [Accepted: 09/15/2023] [Indexed: 10/01/2023]
Abstract
Agrobacterium-mediated transformation enables random transfer-DNA (T-DNA) insertion into plant genomes. T-DNA insertion into a gene's exons, introns or untranscribed regions close to the start or stop codon can disrupt gene function. Such T-DNA mutants have been useful for reverse genetics analysis, especially in Arabidopsis thaliana. As T-DNAs are inserted into genomic DNA, they are generally believed to be stably inherited. Here, we report a phenomenon of reversion of intronic T-DNA mutant phenotypes. From a suppressor screen using intronic T-DNA pi4kβ1,2 double mutant, we recovered intragenic mutants of pi4kβ1, which suppressed the autoimmunity of the double mutant. These mutants carried deletions in the intronic T-DNAs, resulting in elevated transcription of normal PI4Kβ1. Such reversion of T-DNA insertional mutant phenotype stresses the need for caution when using intronic T-DNA mutants and reiterates the importance of using irreversible null mutant alleles in genetic analyses.
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Affiliation(s)
- Karen Thulasi Devendrakumar
- Michael Smith Laboratories, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada
- Department of Botany, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada
| | - Madeleine Goldstein
- Michael Smith Laboratories, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada
| | - James Kronstad
- Michael Smith Laboratories, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada
| | - Xin Li
- Michael Smith Laboratories, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada
- Department of Botany, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada
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Jeong HW, Ryu TH, Lee HJ, Kim KH, Jeong RD. DNA Damage Triggers the Activation of Immune Response to Viral Pathogens via Salicylic Acid in Plants. THE PLANT PATHOLOGY JOURNAL 2023; 39:449-465. [PMID: 37817492 PMCID: PMC10580055 DOI: 10.5423/ppj.oa.08.2023.0112] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 08/15/2023] [Revised: 09/04/2023] [Accepted: 09/06/2023] [Indexed: 10/12/2023]
Abstract
Plants are challenged by various pathogens throughout their lives, such as bacteria, viruses, fungi, and insects; consequently, they have evolved several defense mechanisms. In addition, plants have developed localized and systematic immune responses due to biotic and abiotic stress exposure. Animals are known to activate DNA damage responses (DDRs) and DNA damage sensor immune signals in response to stress, and the process is well studied in animal systems. However, the links between stress perception and immune response through DDRs remain largely unknown in plants. To determine whether DDRs induce plant resistance to pathogens, Arabidopsis plants were treated with bleomycin, a DNA damage-inducing agent, and the replication levels of viral pathogens and growth of bacterial pathogens were determined. We observed that DDR-mediated resistance was specifically activated against viral pathogens, including turnip crinkle virus (TCV). DDR increased the expression level of pathogenesis-related (PR) genes and the total salicylic acid (SA) content and promoted mitogen-activated protein kinase signaling cascades, including the WRKY signaling pathway in Arabidopsis. Transcriptome analysis further revealed that defense- and SA-related genes were upregulated by DDR. The atm-2atr-2 double mutants were susceptible to TCV, indicating that the main DDR signaling pathway sensors play an important role in plant immune responses. In conclusion, DDRs activated basal immune responses to viral pathogens.
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Affiliation(s)
- Hwi-Won Jeong
- Department of Applied Biology, Chonnam National University, Gwangju 61185, Korea
| | - Tae Ho Ryu
- Department of Applied Biology, Chonnam National University, Gwangju 61185, Korea
| | - Hyo-Jeong Lee
- Department of Applied Biology, Chonnam National University, Gwangju 61185, Korea
| | - Kook-Hyung Kim
- Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea
| | - Rae-Dong Jeong
- Department of Applied Biology, Chonnam National University, Gwangju 61185, Korea
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Zhang X, Li J, Cao Y, Huang J, Duan Q. Genome-Wide Identification and Expression Analysis under Abiotic Stress of BrAHL Genes in Brassica rapa. Int J Mol Sci 2023; 24:12447. [PMID: 37569822 PMCID: PMC10420281 DOI: 10.3390/ijms241512447] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/12/2023] [Revised: 07/31/2023] [Accepted: 08/01/2023] [Indexed: 08/13/2023] Open
Abstract
The AT-hook motif nuclear localized (AHL) gene family is a highly conserved transcription factor critical for the growth, development, and stress tolerance of plants. However, the function of the AHL gene family in Brassica rapa (B. rapa) remains unclear. In this study, 42 AHL family members were identified from the B. rapa genome and mapped to nine B. rapa chromosomes. Two clades have formed in the evolution of the AHL gene family. The results showed that most products encoded by AHL family genes are located in the nucleus. Gene duplication was common and expanded the BrAHL gene family. According to the analysis of cis-regulatory elements, the genes interact with stress responses (osmotic, cold, and heavy metal stress), major hormones (abscisic acid), and light responses. In addition, the expression profiles revealed that BrAHL genes are widely expressed in different tissues. BrAHL16 was upregulated at 4 h under drought stress, highly expressed under cadmium conditions, and downregulated in response to cold conditions. BrAHL02 and BrAHL24 were upregulated at the initial time point and peaked at 12 h under cold and cadmium stress, respectively. Notably, the interactions between AHL genes and proteins under drought, cold, and heavy metal stresses were observed when predicting the protein-protein interaction network.
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Affiliation(s)
| | | | | | - Jiabao Huang
- College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an 271018, China; (X.Z.); (J.L.); (Y.C.)
| | - Qiaohong Duan
- College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an 271018, China; (X.Z.); (J.L.); (Y.C.)
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13
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Ramos RS, Spampinato CP. Deficiency of the Arabidopsis mismatch repair MSH6 attenuates Pseudomonas syringae invasion. PLANT SCIENCE : AN INTERNATIONAL JOURNAL OF EXPERIMENTAL PLANT BIOLOGY 2023; 332:111713. [PMID: 37068662 DOI: 10.1016/j.plantsci.2023.111713] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 03/24/2023] [Revised: 04/12/2023] [Accepted: 04/14/2023] [Indexed: 05/27/2023]
Abstract
The MutS homolog 6 (MSH6) is a nuclear DNA mismatch repair (MMR) gene that encodes the MSH6 protein. MSH6 interacts with MSH2 to form the MutSα heterodimer. MutSα corrects DNA mismatches and unpaired nucleotides arising during DNA replication, deamination of 5-methylcytosine, and recombination between non-identical DNA sequences. In addition to correcting DNA biosynthetic errors, MutSα also recognizes chemically damaged DNA bases. Here, we show that inactivation of MSH6 affects the basal susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv tomato DC3000. The msh6 T-DNA insertional mutant exhibited a reduced susceptibility to the bacterial invasion. This heightened basal resistance of msh6 mutants appears to be dependent on an increased stomatal closure, an accumulation of H2O2 and double-strand breaks (DSBs) and a constitutive expression of pathogenesis-related (NPR1 and PR1) and DNA damage response (RAD51D and SOG1) genes. Complementation of this mutant with the MSH6 wild type allele under the control of its own promoter resulted in reversal of the basal bacterial resistance phenotype and the stomatal closure back to wild type levels. Taken together, these results demonstrate that inactivation of MSH6 increases Arabidopsis basal susceptibility to the bacterial pathogen and suggests a link between DNA repair and stress signaling in plants.
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Affiliation(s)
- Rocío S Ramos
- Centro de Estudios Fotosintéticos y Bioquímicos (CEFOBI), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Suipacha 531, 2000 Rosario, Argentina
| | - Claudia P Spampinato
- Centro de Estudios Fotosintéticos y Bioquímicos (CEFOBI), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Suipacha 531, 2000 Rosario, Argentina.
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14
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Vega-Muñoz I, Herrera-Estrella A, Martínez-de la Vega O, Heil M. ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response. Front Immunol 2023; 14:1175786. [PMID: 37256140 PMCID: PMC10225592 DOI: 10.3389/fimmu.2023.1175786] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/28/2023] [Accepted: 04/27/2023] [Indexed: 06/01/2023] Open
Abstract
Background The plant immune response to DNA is highly self/nonself-specific. Self-DNA triggered stronger responses by early immune signals such as H2O2 formation than nonself-DNA from closely related plant species. Plants lack known DNA receptors. Therefore, we aimed to investigate whether a differential sensing of self-versus nonself DNA fragments as damage- versus pathogen-associated molecular patterns (DAMPs/PAMPs) or an activation of the DNA-damage response (DDR) represents the more promising framework to understand this phenomenon. Results We treated Arabidopsis thaliana Col-0 plants with sonicated self-DNA from other individuals of the same ecotype, nonself-DNA from another A. thaliana ecotype, or nonself-DNA from broccoli. We observed a highly self/nonself-DNA-specific induction of H2O2 formation and of jasmonic acid (JA, the hormone controlling the wound response to chewing herbivores) and salicylic acid (SA, the hormone controlling systemic acquired resistance, SAR, to biotrophic pathogens). Mutant lines lacking Ataxia Telangiectasia Mutated (ATM) or ATM AND RAD3-RELATED (ATR) - the two DDR master kinases - retained the differential induction of JA in response to DNA treatments but completely failed to induce H2O2 or SA. Moreover, we observed H2O2 formation in response to in situ-damaged self-DNA from plants that had been treated with bleomycin or SA or infected with virulent bacteria Pseudomonas syringae pv. tomato DC3000 or pv. glycinea carrying effector avrRpt2, but not to DNA from H2O2-treated plants or challenged with non-virulent P. syringae pv. glycinea lacking avrRpt2. Conclusion We conclude that both ATM and ATR are required for the complete activation of the plant immune response to extracellular DNA whereas an as-yet unknown mechanism allows for the self/nonself-differential activation of the JA-dependent wound response.
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Affiliation(s)
- Isaac Vega-Muñoz
- Laboratorio de Ecología de Plantas, Departamento de Ingeniería Genética, Centro de Investigación y de Estudios Avanzados (CINVESTAV)—Unidad Irapuato, Irapuato, GTO, Mexico
| | - Alfredo Herrera-Estrella
- Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados (CINVESTAV)—Unidad de Genómica Avanzada, Irapuato, GTO, Mexico
| | - Octavio Martínez-de la Vega
- Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados (CINVESTAV)—Unidad de Genómica Avanzada, Irapuato, GTO, Mexico
| | - Martin Heil
- Laboratorio de Ecología de Plantas, Departamento de Ingeniería Genética, Centro de Investigación y de Estudios Avanzados (CINVESTAV)—Unidad Irapuato, Irapuato, GTO, Mexico
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15
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Chen H, Neubauer M, Wang JP. Enhancing HR Frequency for Precise Genome Editing in Plants. FRONTIERS IN PLANT SCIENCE 2022; 13:883421. [PMID: 35592579 PMCID: PMC9113527 DOI: 10.3389/fpls.2022.883421] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 02/25/2022] [Accepted: 03/29/2022] [Indexed: 06/15/2023]
Abstract
Gene-editing tools, such as Zinc-fingers, TALENs, and CRISPR-Cas, have fostered a new frontier in the genetic improvement of plants across the tree of life. In eukaryotes, genome editing occurs primarily through two DNA repair pathways: non-homologous end joining (NHEJ) and homologous recombination (HR). NHEJ is the primary mechanism in higher plants, but it is unpredictable and often results in undesired mutations, frameshift insertions, and deletions. Homology-directed repair (HDR), which proceeds through HR, is typically the preferred editing method by genetic engineers. HR-mediated gene editing can enable error-free editing by incorporating a sequence provided by a donor template. However, the low frequency of native HR in plants is a barrier to attaining efficient plant genome engineering. This review summarizes various strategies implemented to increase the frequency of HDR in plant cells. Such strategies include methods for targeting double-strand DNA breaks, optimizing donor sequences, altering plant DNA repair machinery, and environmental factors shown to influence HR frequency in plants. Through the use and further refinement of these methods, HR-based gene editing may one day be commonplace in plants, as it is in other systems.
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Affiliation(s)
- Hao Chen
- Department of Plant and Microbial Biology, Program in Genetics, North Carolina State University, Raleigh, NC, United States
- College of Forestry, Shandong Agricultural University, Tai’an, China
| | - Matthew Neubauer
- Department of Plant and Microbial Biology, Program in Genetics, North Carolina State University, Raleigh, NC, United States
| | - Jack P. Wang
- Department of Forestry and Environmental Resources, Forest Biotechnology Group, North Carolina State University, Raleigh, NC, United States
- State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, China
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16
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Davarinejad H, Huang YC, Mermaz B, LeBlanc C, Poulet A, Thomson G, Joly V, Muñoz M, Arvanitis-Vigneault A, Valsakumar D, Villarino G, Ross A, Rotstein BH, Alarcon EI, Brunzelle JS, Voigt P, Dong J, Couture JF, Jacob Y. The histone H3.1 variant regulates TONSOKU-mediated DNA repair during replication. Science 2022; 375:1281-1286. [PMID: 35298257 PMCID: PMC9153895 DOI: 10.1126/science.abm5320] [Citation(s) in RCA: 33] [Impact Index Per Article: 11.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/24/2022]
Abstract
The tail of replication-dependent histone H3.1 varies from that of replication-independent H3.3 at the amino acid located at position 31 in plants and animals, but no function has been assigned to this residue to demonstrate a unique and conserved role for H3.1 during replication. We found that TONSOKU (TSK/TONSL), which rescues broken replication forks, specifically interacts with H3.1 via recognition of alanine 31 by its tetratricopeptide repeat domain. Our results indicate that genomic instability in the absence of ATXR5/ATXR6-catalyzed histone H3 lysine 27 monomethylation in plants depends on H3.1, TSK, and DNA polymerase theta (Pol θ). This work reveals an H3.1-specific function during replication and a common strategy used in multicellular eukaryotes for regulating post-replicative chromatin maturation and TSK, which relies on histone monomethyltransferases and reading of the H3.1 variant.
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Affiliation(s)
- Hossein Davarinejad
- Ottawa Institute of Systems Biology; Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa; Ottawa, Ontario K1H 8M5, Canada
| | - Yi-Chun Huang
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
| | - Benoit Mermaz
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
| | - Chantal LeBlanc
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
| | - Axel Poulet
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
| | - Geoffrey Thomson
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
| | - Valentin Joly
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
| | - Marcelo Muñoz
- Ottawa Institute of Systems Biology; Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa; Ottawa, Ontario K1H 8M5, Canada
| | - Alexis Arvanitis-Vigneault
- Ottawa Institute of Systems Biology; Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa; Ottawa, Ontario K1H 8M5, Canada
| | - Devisree Valsakumar
- Wellcome Centre for Cell Biology, School of Biological Sciences, University of Edinburgh; Edinburgh, EH9 3BF, United Kingdom
- Epigenetics Programme, Babraham Institute; Cambridge, CB22 3AT, United Kingdom
| | - Gonzalo Villarino
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
| | - Alex Ross
- BEaTS Research Laboratory, Division of Cardiac Surgery, University of Ottawa Heart Institute; Ottawa, ON K1Y4W7, Canada
- Department of Biochemistry, Microbiology, and Immunology, Faculty of Medicine, University of Ottawa; Ottawa, ON K1H 8M5, Canada
| | - Benjamin H. Rotstein
- Department of Biochemistry, Microbiology, and Immunology, Faculty of Medicine, University of Ottawa; Ottawa, ON K1H 8M5, Canada
- University of Ottawa Heart Institute; Ottawa, ON K1Y4W7, Canada
| | - Emilio I. Alarcon
- BEaTS Research Laboratory, Division of Cardiac Surgery, University of Ottawa Heart Institute; Ottawa, ON K1Y4W7, Canada
- Department of Biochemistry, Microbiology, and Immunology, Faculty of Medicine, University of Ottawa; Ottawa, ON K1H 8M5, Canada
| | - Joseph S. Brunzelle
- Feinberg School of Medicine, Department of Molecular Pharmacology and Biological Chemistry, Northwestern University; Chicago, Illinois 60611, USA
| | - Philipp Voigt
- Wellcome Centre for Cell Biology, School of Biological Sciences, University of Edinburgh; Edinburgh, EH9 3BF, United Kingdom
- Epigenetics Programme, Babraham Institute; Cambridge, CB22 3AT, United Kingdom
| | - Jie Dong
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
- Institute of Crop Science, Zhejiang University; Hangzhou 310058, China
| | - Jean-François Couture
- Ottawa Institute of Systems Biology; Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa; Ottawa, Ontario K1H 8M5, Canada
| | - Yannick Jacob
- Yale University, Department of Molecular, Cellular and Developmental Biology, Faculty of Arts and Sciences; 260 Whitney Avenue, New Haven, Connecticut 06511, USA
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17
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Milsted C, Dai B, Garcia N, Yin L, He Y, Kianian S, Pawlowski W, Chen C. Genome-wide investigation of maize RAD51 binding affinity through phage display. BMC Genomics 2022; 23:199. [PMID: 35279087 PMCID: PMC8917730 DOI: 10.1186/s12864-022-08419-6] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/24/2021] [Accepted: 02/18/2022] [Indexed: 11/10/2022] Open
Abstract
BACKGROUND RAD51 proteins, which are conserved in all eukaryotes, repair DNA double-strand breaks. This is critical to homologous chromosome pairing and recombination enabling successful reproduction. Work in Arabidopsis suggests that RAD51 also plays a role in plant defense; the Arabidopsis rad51 mutant is more susceptible to Pseudomonas syringae. However, the defense functions of RAD51 and the proteins interacting with RAD51 have not been thoroughly investigated in maize. Uncovering ligands of RAD51 would help to understand meiotic recombination and possibly the role of RAD51 in defense. This study used phage display, a tool for discovery of protein-protein interactions, to search for proteins interacting with maize RAD51A1. RESULTS Maize RAD51A1 was screened against a random phage library. Eleven short peptide sequences were recovered from 15 phages which bound ZmRAD51A1 in vitro; three sequences were found in multiple successfully binding phages. Nine of these phage interactions were verified in vitro through ELISA and/or dot blotting. BLAST searches did not reveal any maize proteins which contained the exact sequence of any of the selected phage peptides, although one of the selected phages had a strong alignment (E-value = 0.079) to a binding domain of maize BRCA2. Therefore, we designed 32 additional short peptides using amino acid sequences found in the predicted maize proteome. These peptides were not contained within phages. Of these synthesized peptides, 14 bound to ZmRAD51A1 in a dot blot experiment. These 14 sequences are found in known maize proteins including transcription factors putatively involved in defense. CONCLUSIONS These results reveal several peptides which bind ZmRAD51A1 and support a potential role for ZmRAD51A1 in transcriptional regulation and plant defense. This study also demonstrates the applicability of phage display to basic science questions, such as the search for binding partners of a known protein, and raises the possibility of an iterated approach to test peptide sequences that closely but imperfectly align with the selected phages.
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Affiliation(s)
- Claire Milsted
- School of Life Sciences, Arizona State University, 427 E Tyler Mall, Tempe, AZ, 85287, USA
- Department of Horticultural Science, University of Minnesota, 1970 Folwell Avenue, St. Paul, MN, 55108, USA
| | - Bo Dai
- Department of Horticultural Science, University of Minnesota, 1970 Folwell Avenue, St. Paul, MN, 55108, USA
| | - Nelson Garcia
- Department of Horticultural Science, University of Minnesota, 1970 Folwell Avenue, St. Paul, MN, 55108, USA
- Calyxt Inc, 2800 Mount Ridge Rd, Roseville, MN, 55113, USA
| | - Lu Yin
- School of Life Sciences, Arizona State University, 427 E Tyler Mall, Tempe, AZ, 85287, USA
- Department of Horticultural Science, University of Minnesota, 1970 Folwell Avenue, St. Paul, MN, 55108, USA
| | - Yan He
- School of Integrative Plant Science, Cornell University, 401 Bradfield Hall, Ithaca, NY, 14853, USA
- National Maize Improvement Center of China, College of Agronomy and Biotechnology, China Agricultural University, Beijing, 100094, China
| | - Shahryar Kianian
- Department of Horticultural Science, University of Minnesota, 1970 Folwell Avenue, St. Paul, MN, 55108, USA
- Cereal Disease Lab, USDA-ARS, St. Paul, MN, 55108, USA
| | - Wojciech Pawlowski
- School of Integrative Plant Science, Cornell University, 401 Bradfield Hall, Ithaca, NY, 14853, USA
| | - Changbin Chen
- School of Life Sciences, Arizona State University, 427 E Tyler Mall, Tempe, AZ, 85287, USA.
- Department of Horticultural Science, University of Minnesota, 1970 Folwell Avenue, St. Paul, MN, 55108, USA.
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18
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Hannan Parker A, Wilkinson SW, Ton J. Epigenetics: a catalyst of plant immunity against pathogens. THE NEW PHYTOLOGIST 2022; 233:66-83. [PMID: 34455592 DOI: 10.1111/nph.17699] [Citation(s) in RCA: 48] [Impact Index Per Article: 16.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 03/12/2021] [Accepted: 07/20/2021] [Indexed: 05/11/2023]
Abstract
The plant immune system protects against pests and diseases. The recognition of stress-related molecular patterns triggers localised immune responses, which are often followed by longer-lasting systemic priming and/or up-regulation of defences. In some cases, this induced resistance (IR) can be transmitted to following generations. Such transgenerational IR is gradually reversed in the absence of stress at a rate that is proportional to the severity of disease experienced in previous generations. This review outlines the mechanisms by which epigenetic responses to pathogen infection shape the plant immune system across expanding time scales. We review the cis- and trans-acting mechanisms by which stress-inducible epigenetic changes at transposable elements (TEs) regulate genome-wide defence gene expression and draw particular attention to one regulatory model that is supported by recent evidence about the function of AGO1 and H2A.Z in transcriptional control of defence genes. Additionally, we explore how stress-induced mobilisation of epigenetically controlled TEs acts as a catalyst of Darwinian evolution by generating (epi)genetic diversity at environmentally responsive genes. This raises questions about the long-term evolutionary consequences of stress-induced diversification of the plant immune system in relation to the long-held dichotomy between Darwinian and Lamarckian evolution.
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Affiliation(s)
- Adam Hannan Parker
- Department of Animal and Plant Sciences, Institute for Sustainable Food, Western Bank, University of Sheffield, Sheffield, S10 2TN, UK
| | - Samuel W Wilkinson
- Department of Animal and Plant Sciences, Institute for Sustainable Food, Western Bank, University of Sheffield, Sheffield, S10 2TN, UK
| | - Jurriaan Ton
- Department of Animal and Plant Sciences, Institute for Sustainable Food, Western Bank, University of Sheffield, Sheffield, S10 2TN, UK
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19
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Bulankova P, Sekulić M, Jallet D, Nef C, van Oosterhout C, Delmont TO, Vercauteren I, Osuna-Cruz CM, Vancaester E, Mock T, Sabbe K, Daboussi F, Bowler C, Vyverman W, Vandepoele K, De Veylder L. Mitotic recombination between homologous chromosomes drives genomic diversity in diatoms. Curr Biol 2021; 31:3221-3232.e9. [PMID: 34102110 DOI: 10.1016/j.cub.2021.05.013] [Citation(s) in RCA: 19] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/08/2020] [Revised: 03/17/2021] [Accepted: 05/06/2021] [Indexed: 01/31/2023]
Abstract
Diatoms, an evolutionarily successful group of microalgae, display high levels of intraspecific genetic variability in natural populations. However, the contribution of various mechanisms generating such diversity is unknown. Here we estimated the genetic micro-diversity within a natural diatom population and mapped the genomic changes arising within clonally propagated diatom cell cultures. Through quantification of haplotype diversity by next-generation sequencing and amplicon re-sequencing of selected loci, we documented a rapid accumulation of multiple haplotypes accompanied by the appearance of novel protein variants in cell cultures initiated from a single founder cell. Comparison of the genomic changes between mother and daughter cells revealed copy number variation and copy-neutral loss of heterozygosity leading to the fixation of alleles within individual daughter cells. The loss of heterozygosity can be accomplished by recombination between homologous chromosomes. To test this hypothesis, we established an endogenous readout system and estimated that the frequency of interhomolog mitotic recombination was under standard growth conditions 4.2 events per 100 cell divisions. This frequency is increased under environmental stress conditions, including treatment with hydrogen peroxide and cadmium. These data demonstrate that copy number variation and mitotic recombination between homologous chromosomes underlie clonal variability in diatom populations. We discuss the potential adaptive evolutionary benefits of the plastic response in the interhomolog mitotic recombination rate, and we propose that this may have contributed to the ecological success of diatoms.
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Affiliation(s)
- Petra Bulankova
- VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium.
| | - Mirna Sekulić
- VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium; Protistology and Aquatic Ecology, Department of Biology, Ghent University, 9000 Ghent, Belgium
| | - Denis Jallet
- TBI, Université de Toulouse, CNRS, INRAE, INSA, 135 Avenue de Rangueil, 31077 Toulouse, France
| | - Charlotte Nef
- Institut de Biologie de l'École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, PSL Université Paris, 75005 Paris, France
| | - Cock van Oosterhout
- School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK
| | - Tom O Delmont
- Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91000 Evry, France
| | - Ilse Vercauteren
- VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium
| | - Cristina Maria Osuna-Cruz
- VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium; Bioinformatics Institute Ghent, Ghent University, Technologiepark 71, 9052 Ghent, Belgium
| | - Emmelien Vancaester
- VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium; Bioinformatics Institute Ghent, Ghent University, Technologiepark 71, 9052 Ghent, Belgium
| | - Thomas Mock
- School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK
| | - Koen Sabbe
- Protistology and Aquatic Ecology, Department of Biology, Ghent University, 9000 Ghent, Belgium
| | - Fayza Daboussi
- TBI, Université de Toulouse, CNRS, INRAE, INSA, 135 Avenue de Rangueil, 31077 Toulouse, France
| | - Chris Bowler
- Institut de Biologie de l'École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, PSL Université Paris, 75005 Paris, France
| | - Wim Vyverman
- Protistology and Aquatic Ecology, Department of Biology, Ghent University, 9000 Ghent, Belgium
| | - Klaas Vandepoele
- VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium; Bioinformatics Institute Ghent, Ghent University, Technologiepark 71, 9052 Ghent, Belgium
| | - Lieven De Veylder
- VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium.
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20
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Rajewski A, Carter-House D, Stajich J, Litt A. Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture. BMC Genomics 2021; 22:201. [PMID: 33752605 PMCID: PMC7986286 DOI: 10.1186/s12864-021-07489-2] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/30/2020] [Accepted: 02/26/2021] [Indexed: 11/29/2022] Open
Abstract
BACKGROUND Datura stramonium (Jimsonweed) is a medicinally and pharmaceutically important plant in the nightshade family (Solanaceae) known for its production of various toxic, hallucinogenic, and therapeutic tropane alkaloids. Recently, we published a tissue-culture based transformation protocol for D. stramonium that enables more thorough functional genomics studies of this plant. However, the tissue culture process can lead to undesirable phenotypic and genomic consequences independent of the transgene used. Here, we have assembled and annotated a draft genome of D. stramonium with a focus on tropane alkaloid biosynthetic genes. We then use mRNA sequencing and genome resequencing of transformants to characterize changes following tissue culture. RESULTS Our draft assembly conforms to the expected 2 gigabasepair haploid genome size of this plant and achieved a BUSCO score of 94.7% complete, single-copy genes. The repetitive content of the genome is 61%, with Gypsy-type retrotransposons accounting for half of this. Our gene annotation estimates the number of protein-coding genes at 52,149 and shows evidence of duplications in two key alkaloid biosynthetic genes, tropinone reductase I and hyoscyamine 6 β-hydroxylase. Following tissue culture, we detected only 186 differentially expressed genes, but were unable to correlate these changes in expression with either polymorphisms from resequencing or positional effects of transposons. CONCLUSIONS We have assembled, annotated, and characterized the first draft genome for this important model plant species. Using this resource, we show duplications of genes leading to the synthesis of the medicinally important alkaloid, scopolamine. Our results also demonstrate that following tissue culture, mutation rates of transformed plants are quite high (1.16 × 10- 3 mutations per site), but do not have a drastic impact on gene expression.
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Affiliation(s)
- Alex Rajewski
- Department of Botany and Plant Science, University of California, Riverside, California 92521 USA
| | - Derreck Carter-House
- Department of Microbiology and Plant Pathology, University of California, Riverside, California 92521 USA
| | - Jason Stajich
- Department of Microbiology and Plant Pathology, University of California, Riverside, California 92521 USA
| | - Amy Litt
- Department of Botany and Plant Science, University of California, Riverside, California 92521 USA
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Harvey EF, Cristescu ME, Dale J, Hunter H, Randall C, Crease TJ. Metal exposure causes rDNA copy number to fluctuate in mutation accumulation lines of Daphnia pulex. AQUATIC TOXICOLOGY (AMSTERDAM, NETHERLANDS) 2020; 226:105556. [PMID: 32652413 DOI: 10.1016/j.aquatox.2020.105556] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/12/2019] [Revised: 05/29/2020] [Accepted: 06/26/2020] [Indexed: 06/11/2023]
Abstract
Ribosomal (r)DNA is a highly dynamic, conserved, multigene family whose sequence homogeneity is thought to be maintained by intra- and interchromosomal recombination, which are capable of changing rDNA copy number. It is generally not known how environmental stress such as sublethal exposure to environmentally relevant concentrations of metals impacts rDNA copy number. To determine how chronic metal exposure affects rDNA, we measured copy number of the 18S rRNA gene in 355 copper and nickel-exposed samples and 132 metal-free samples derived from 325 mutation accumulation (MA) lines of two genetically distinct Daphnia pulex lineages. The MA lines were sampled at four time points over 100+ generations of clonal propagation. The copy number of rDNA was also measured in 15 individuals sampled from a metal-free non-MA control population established from the same progenitor as one of the MA lineages. We found that mean rDNA copy number fluctuated across lines exposed to metals with a tendency to decrease over time. In contrast, mean rDNA copy number in the metal-free control lines and the non-MA population remained stable over time. It is generally accepted that extreme rDNA loss results in the loss of organism fitness. Thus, fluctuations in rDNA copy number, including losses, could affect the long-term viability of natural populations of Daphnia in metal-contaminated habitats.
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Affiliation(s)
- Eleanor F Harvey
- Department of Integrative Biology, University of Guelph, 50 Stone Road West, Guelph, ON, N1G 2W1, Canada
| | - Melania E Cristescu
- Biology Department, McGill University, Stewart Biology Building, 1205 Dr Penfield Ave, Montreal, QC, H3A 1B1, Canada
| | - Jenna Dale
- Department of Integrative Biology, University of Guelph, 50 Stone Road West, Guelph, ON, N1G 2W1, Canada
| | - Hailey Hunter
- Department of Integrative Biology, University of Guelph, 50 Stone Road West, Guelph, ON, N1G 2W1, Canada
| | - Connor Randall
- Department of Integrative Biology, University of Guelph, 50 Stone Road West, Guelph, ON, N1G 2W1, Canada
| | - Teresa J Crease
- Department of Integrative Biology, University of Guelph, 50 Stone Road West, Guelph, ON, N1G 2W1, Canada.
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22
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Gratias A, Geffroy V. Deciphering the Impact of a Bacterial Infection on Meiotic Recombination in Arabidopsis with Fluorescence Tagged Lines. Genes (Basel) 2020; 11:genes11070832. [PMID: 32708324 PMCID: PMC7397157 DOI: 10.3390/genes11070832] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/14/2020] [Revised: 06/25/2020] [Accepted: 07/10/2020] [Indexed: 12/12/2022] Open
Abstract
Plants are under strong evolutionary pressure to maintain surveillance against pathogens. One major disease resistance mechanism is based on NB-LRR (NLR) proteins that specifically recognize pathogen effectors. The cluster organization of the NLR gene family could favor sequence exchange between NLR genes via recombination, favoring their evolutionary dynamics. Increasing data, based on progeny analysis, suggest the existence of a link between the perception of biotic stress and the production of genetic diversity in the offspring. This could be driven by an increased rate of meiotic recombination in infected plants, but this has never been strictly demonstrated. In order to test if pathogen infection can increase DNA recombination in pollen meiotic cells, we infected Arabidopsis Fluorescent Tagged Lines (FTL) with the virulent bacteria Pseudomonas syringae. We measured the meiotic recombination rate in two regions of chromosome 5, containing or not an NLR gene cluster. In all tested intervals, no significant difference in genetic recombination frequency between infected and control plants was observed. Although it has been reported that pathogen exposure can sometimes increase the frequency of recombinant progeny in plants, our findings suggest that meiotic recombination rate in Arabidopsis may be resilient to at least some pathogen attack. Alternative mechanisms are discussed.
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Affiliation(s)
- Ariane Gratias
- Institute of Plant Sciences Paris-Saclay (IPS2), Université Paris-Saclay, CNRS, INRAE, Univ Evry, 91405 Orsay, France;
- Institute of Plant Sciences Paris-Saclay (IPS2), Université de Paris, CNRS, INRAE, 91405 Orsay, France
| | - Valérie Geffroy
- Institute of Plant Sciences Paris-Saclay (IPS2), Université Paris-Saclay, CNRS, INRAE, Univ Evry, 91405 Orsay, France;
- Institute of Plant Sciences Paris-Saclay (IPS2), Université de Paris, CNRS, INRAE, 91405 Orsay, France
- Correspondence: ; Tel.: +33-1-69-15-33-65
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23
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Camborde L, Raynaud C, Dumas B, Gaulin E. DNA-Damaging Effectors: New Players in the Effector Arena. TRENDS IN PLANT SCIENCE 2019; 24:1094-1101. [PMID: 31699522 DOI: 10.1016/j.tplants.2019.09.012] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 03/26/2019] [Revised: 06/24/2019] [Accepted: 09/17/2019] [Indexed: 06/10/2023]
Abstract
In animal cells, nuclear DNA is the target of genotoxins produced by bacterial pathogens that cause genomic mutations eventually leading to apoptosis, senescence, and carcinogenic development. In response to the insult, the DNA damage response (DDR) is activated to ensure lesion repair. Accumulation of DNA breaks is also detected in plants during microbial infection. In this opinion article we propose that phytopathogens can produce DNA-damaging effectors. The recent identification of a functional genotoxin in devastating eukaryotic plant pathogens, such as oomycetes, supports the concept that DNA-damaging effectors may contribute to pathogenicity. Additionally, this raises the question of how plants can perceive these damages and whether this perception can be connected to the plant immune system.
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Affiliation(s)
- Laurent Camborde
- Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, France
| | - Cécile Raynaud
- Institute of Plant Sciences Paris-Saclay (IPS2), CNRS, INRA, Université Paris-Sud, Université Évry, Université Paris-Saclay, 91405, Orsay, Paris, France
| | - Bernard Dumas
- Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, France
| | - Elodie Gaulin
- Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, France.
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24
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Tirnaz S, Batley J. DNA Methylation: Toward Crop Disease Resistance Improvement. TRENDS IN PLANT SCIENCE 2019; 24:1137-1150. [PMID: 31604599 DOI: 10.1016/j.tplants.2019.08.007] [Citation(s) in RCA: 47] [Impact Index Per Article: 7.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 04/18/2019] [Revised: 08/13/2019] [Accepted: 08/22/2019] [Indexed: 05/23/2023]
Abstract
Crop diseases, in conjunction with climate change, are a major threat to global crop production. DNA methylation is an epigenetic mark and is involved in plants' biological processes, including development, stress adaptation, and genome evolution. By providing a new source of variation, DNA methylation introduces novel direction to both scientists and breeders with its potential in disease resistance enhancement. Here, we discuss the impact of pathogen-induced DNA methylation modifications on a host's transcriptome reprogramming and genome stability, as part of the plant's defense mechanisms. We also highlight the knowledge gaps that need to be investigated for understanding the entire role of DNA methylation in plant pathogen interactions. This will ultimately assist breeders toward improving resistance and decreasing yield losses.
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Affiliation(s)
- Soodeh Tirnaz
- School of Biological Sciences, University of Western Australia, Perth, WA, 6009, Australia
| | - Jacqueline Batley
- School of Biological Sciences, University of Western Australia, Perth, WA, 6009, Australia.
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25
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Wilkinson SW, Magerøy MH, López Sánchez A, Smith LM, Furci L, Cotton TEA, Krokene P, Ton J. Surviving in a Hostile World: Plant Strategies to Resist Pests and Diseases. ANNUAL REVIEW OF PHYTOPATHOLOGY 2019; 57:505-529. [PMID: 31470772 DOI: 10.1146/annurev-phyto-082718-095959] [Citation(s) in RCA: 84] [Impact Index Per Article: 14.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/09/2023]
Abstract
As primary producers, plants are under constant pressure to defend themselves against potentially deadly pathogens and herbivores. In this review, we describe short- and long-term strategies that enable plants to cope with these stresses. Apart from internal immunological strategies that involve physiological and (epi)genetic modifications at the cellular level, plants also employ external strategies that rely on recruitment of beneficial organisms. We discuss these strategies along a gradient of increasing timescales, ranging from rapid immune responses that are initiated within seconds to (epi)genetic adaptations that occur over multiple plant generations. We cover the latest insights into the mechanistic and evolutionary underpinnings of these strategies and present explanatory models. Finally, we discuss how knowledge from short-lived model species can be translated to economically and ecologically important perennials to exploit adaptive plant strategies and mitigate future impacts of pests and diseases in an increasingly interconnected and changing world.
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Affiliation(s)
- Samuel W Wilkinson
- Plant Production and Protection Institute and Department of Animal and Plant Sciences, The University of Sheffield, Western Bank, Sheffield S10 2TN, United Kingdom;
- Department of Molecular Plant Biology, Division for Biotechnology and Plant Health, Norwegian Institute for Bioeconomy Research, 1431 Ås, Norway
| | - Melissa H Magerøy
- Department of Molecular Plant Biology, Division for Biotechnology and Plant Health, Norwegian Institute for Bioeconomy Research, 1431 Ås, Norway
| | - Ana López Sánchez
- Plant Production and Protection Institute and Department of Animal and Plant Sciences, The University of Sheffield, Western Bank, Sheffield S10 2TN, United Kingdom;
- Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología, Campus de Cantoblanco, Universidad Autónoma de Madrid, 28049 Madrid, Spain
| | - Lisa M Smith
- Plant Production and Protection Institute and Department of Animal and Plant Sciences, The University of Sheffield, Western Bank, Sheffield S10 2TN, United Kingdom;
| | - Leonardo Furci
- Plant Production and Protection Institute and Department of Animal and Plant Sciences, The University of Sheffield, Western Bank, Sheffield S10 2TN, United Kingdom;
| | - T E Anne Cotton
- Plant Production and Protection Institute and Department of Animal and Plant Sciences, The University of Sheffield, Western Bank, Sheffield S10 2TN, United Kingdom;
| | - Paal Krokene
- Department of Molecular Plant Biology, Division for Biotechnology and Plant Health, Norwegian Institute for Bioeconomy Research, 1431 Ås, Norway
| | - Jurriaan Ton
- Plant Production and Protection Institute and Department of Animal and Plant Sciences, The University of Sheffield, Western Bank, Sheffield S10 2TN, United Kingdom;
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26
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Abstract
When first asked to write a review of my life as a scientist, I doubted anyone would be interested in reading it. In addition, I did not really want to compose my own memorial. However, after discussing the idea with other scientists who have written autobiographies, I realized that it might be fun to dig into my past and to reflect on what has been important for me, my life, my family, my friends and colleagues, and my career. My life and research has taken me from bacteriophage to Agrobacterium tumefaciens-mediated DNA transfer to plants to the plant genome and its environmentally induced changes. I went from being a naïve, young student to a postdoc and married mother of two to the leader of an ever-changing group of fantastic coworkers-a journey made rich by many interesting scientific milestones, fascinating exploration of all corners of the world, and marvelous friendships.
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Affiliation(s)
- Barbara Hohn
- Friedrich Miescher Institute for Biomedical Research, CH-4058 Basel, Switzerland;
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27
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Nisa MU, Huang Y, Benhamed M, Raynaud C. The Plant DNA Damage Response: Signaling Pathways Leading to Growth Inhibition and Putative Role in Response to Stress Conditions. FRONTIERS IN PLANT SCIENCE 2019; 10:653. [PMID: 31164899 PMCID: PMC6534066 DOI: 10.3389/fpls.2019.00653] [Citation(s) in RCA: 137] [Impact Index Per Article: 22.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 04/01/2019] [Accepted: 04/30/2019] [Indexed: 05/02/2023]
Abstract
Maintenance of genome integrity is a key issue for all living organisms. Cells are constantly exposed to DNA damage due to replication or transcription, cellular metabolic activities leading to the production of Reactive Oxygen Species (ROS) or even exposure to DNA damaging agents such as UV light. However, genomes remain extremely stable, thanks to the permanent repair of DNA lesions. One key mechanism contributing to genome stability is the DNA Damage Response (DDR) that activates DNA repair pathways, and in the case of proliferating cells, stops cell division until DNA repair is complete. The signaling mechanisms of the DDR are quite well conserved between organisms including in plants where they have been investigated into detail over the past 20 years. In this review we summarize the acquired knowledge and recent advances regarding the DDR control of cell cycle progression. Studying the plant DDR is particularly interesting because of their mode of development and lifestyle. Indeed, plants develop largely post-embryonically, and form new organs through the activity of meristems in which cells retain the ability to proliferate. In addition, they are sessile organisms that are permanently exposed to adverse conditions that could potentially induce DNA damage in all cell types including meristems. In the second part of the review we discuss the recent findings connecting the plant DDR to responses to biotic and abiotic stresses.
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28
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Zilio G, Moesch L, Bovet N, Sarr A, Koella JC. The effect of parasite infection on the recombination rate of the mosquito Aedes aegypti. PLoS One 2018; 13:e0203481. [PMID: 30300349 PMCID: PMC6177114 DOI: 10.1371/journal.pone.0203481] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/24/2018] [Accepted: 08/21/2018] [Indexed: 12/29/2022] Open
Abstract
Sexual reproduction and meiotic recombination generate new genetic combinations and may thereby help an individual infected by a parasite to protect its offspring from being infected. While this idea is often used to understand the evolutionary forces underlying the maintenance of sex and recombination, it also suggests that infected individuals should increase plastically their rate of recombination. We tested the latter idea with the mosquito Aedes aegypti and asked whether females infected by the microsporidian Vavraia culicis were more likely to have recombinant offspring than uninfected females. To measure the rate of recombination over a chromosome we analysed combinations of microsatellites on chromosome 3 in infected and uninfected females, in the (uninfected) males they copulated with and in their offspring. As predicted, the infected females were more likely to have recombinant offspring than the uninfected ones. These results show the ability of a female to diversify her offspring in response to parasitic infection by plastically increasing her recombination rate.
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Affiliation(s)
- Giacomo Zilio
- Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
| | - Lea Moesch
- Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
- Department of Environmental Systems Science, ETHZ, Zurich, Switzerland
| | - Nathalie Bovet
- Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
| | - Anouk Sarr
- Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
| | - Jacob C. Koella
- Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
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29
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Fuchs LK, Jenkins G, Phillips DW. Anthropogenic Impacts on Meiosis in Plants. FRONTIERS IN PLANT SCIENCE 2018; 9:1429. [PMID: 30323826 PMCID: PMC6172301 DOI: 10.3389/fpls.2018.01429] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/29/2018] [Accepted: 09/07/2018] [Indexed: 05/18/2023]
Abstract
As the human population grows and continues to encroach on the natural environment, organisms that form part of such ecosystems are becoming increasingly exposed to exogenous anthropogenic factors capable of changing their meiotic landscape. Meiotic recombination generates much of the genetic variation in sexually reproducing species and is known to be a highly conserved pathway. Environmental stresses, such as variations in temperature, have long been known to change the pattern of recombination in both model and crop plants, but there are other factors capable of causing genome damage, infertility and meiotic abnormalities. Our agrarian expansion and our increasing usage of agrochemicals unintentionally affect plants via groundwater contamination or spray drift; our industrial developments release heavy metals into the environment; pathogens are spread by climate change and a globally mobile population; imperfect waste treatment plants are unable to remove chemical and pharmaceutical residues from sewage leading to the release of xenobiotics, all with potentially deleterious meiotic effects. In this review, we discuss the major classes of exogenous anthropogenic factors known to affect meiosis in plants, namely environmental stresses, agricultural inputs, heavy metals, pharmaceuticals and pathogens. The possible evolutionary fate of plants thrust into their new anthropogenically imposed environments are also considered.
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Affiliation(s)
| | | | - Dylan W. Phillips
- Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, United Kingdom
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30
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Abstract
Meiosis halves diploid chromosome numbers to haploid levels that are essential for sexual reproduction in most eukaryotes. Meiotic recombination ensures the formation of bivalents between homologous chromosomes (homologs) and their subsequent proper segregation. It also results in genetic diversity among progeny that influences evolutionary responses to selection. Moreover, crop breeding depends upon the action of meiotic recombination to rearrange elite traits between parental chromosomes. An understanding of the molecular mechanisms that drive meiotic recombination is important for both fundamental research and practical applications. This review emphasizes advances made during the past 5 years, primarily in Arabidopsis and rice, by summarizing newly characterized genes and proteins and examining the regulatory mechanisms that modulate their action.
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Affiliation(s)
- Yingxiang Wang
- State Key Laboratory of Genetic Engineering and Collaborative Innovation Center of Genetics and Development, Ministry of Education Key Laboratory of Biodiversity Sciences and Ecological Engineering, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai 200438, China;
| | - Gregory P Copenhaver
- Department of Biology and the Integrative Program for Biological and Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-3280, USA;
- Lineberger Comprehensive Cancer Center, University of North Carolina School of Medicine, Chapel Hill, North Carolina 27599-3280, USA
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31
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Keppler BD, Song J, Nyman J, Voigt CA, Bent AF. 3-Aminobenzamide Blocks MAMP-Induced Callose Deposition Independently of Its Poly(ADPribosyl)ation Inhibiting Activity. FRONTIERS IN PLANT SCIENCE 2018; 9:1907. [PMID: 30619442 PMCID: PMC6305757 DOI: 10.3389/fpls.2018.01907] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 05/17/2018] [Accepted: 12/07/2018] [Indexed: 05/15/2023]
Abstract
Cell wall reinforcement with callose is a frequent plant response to infection. Poly(ADP-ribosyl)ation is a protein post-translational modification mediated by poly(ADP-ribose) polymerases (PARPs). Poly(ADP-ribosyl)ation has well-known roles in DNA damage repair and has more recently been shown to contribute to plant immune responses. 3-aminobenzamide (3AB) is an established PARP inhibitor and it blocks the callose deposition elicited by flg22 or elf18, two microbe-associated molecular patterns (MAMPs). However, we report that an Arabidopsis parp1parp2parp3 triple mutant does not exhibit loss of flg22-induced callose deposition. Additionally, the more specific PARP inhibitors PJ-34 and INH2BP inhibit PARP activity in Arabidopsis but do not block MAMP-induced callose deposition. These data demonstrate off-target activity of 3AB and indicate that 3AB inhibits callose deposition through a mechanism other than poly(ADP-ribosyl)ation. POWDERY MILDEW RESISTANT 4 (PMR4) is the callose synthase responsible for the majority of MAMP- and wound-induced callose deposition in Arabidopsis. 3AB does not block wound-induced callose deposition, and 3AB does not reduce the PMR4 mRNA abundance increase in response to flg22. Levels of PMR4-HA protein increase in response to flg22, and increase even more in flg22 + 3AB despite no callose being produced. The callose synthase inhibitor 2-deoxy-D-glucose does not cause similar impacts on PMR4-HA protein levels. Beyond MAMPs, we find that 3AB also reduces callose deposition induced by powdery mildew (Golovinomyces cichoracearum) and impairs the penetration resistance of a PMR4 overexpression line. 3AB thus reveals pathogenesis-associated pathways that activate callose synthase enzymatic activity distinct from those that elevate PMR4 mRNA and protein abundance.
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Affiliation(s)
- Brian D. Keppler
- Department of Plant Pathology, University of Wisconsin–Madison, Madison, WI, United States
| | - Junqi Song
- Department of Plant Pathology, University of Wisconsin–Madison, Madison, WI, United States
| | - Jackson Nyman
- Department of Plant Pathology, University of Wisconsin–Madison, Madison, WI, United States
| | - Christian A. Voigt
- Phytopathology and Biochemistry, Biocenter Klein Flottbek, University of Hamburg, Hamburg, Germany
| | - Andrew F. Bent
- Department of Plant Pathology, University of Wisconsin–Madison, Madison, WI, United States
- *Correspondence: Andrew F. Bent,
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32
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Stevison LS, Sefick S, Rushton C, Graze RM. Recombination rate plasticity: revealing mechanisms by design. Philos Trans R Soc Lond B Biol Sci 2017; 372:20160459. [PMID: 29109222 PMCID: PMC5698621 DOI: 10.1098/rstb.2016.0459] [Citation(s) in RCA: 20] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 08/01/2017] [Indexed: 12/13/2022] Open
Abstract
For over a century, scientists have known that meiotic recombination rates can vary considerably among individuals, and that environmental conditions can modify recombination rates relative to the background. A variety of external and intrinsic factors such as temperature, age, sex and starvation can elicit 'plastic' responses in recombination rate. The influence of recombination rate plasticity on genetic diversity of the next generation has interesting and important implications for how populations evolve. Further, many questions remain regarding the mechanisms and molecular processes that contribute to recombination rate plasticity. Here, we review 100 years of experimental work on recombination rate plasticity conducted in Drosophila melanogaster We categorize this work into four major classes of experimental designs, which we describe via classic studies in D. melanogaster Based on these studies, we highlight molecular mechanisms that are supported by experimental results and relate these findings to studies in other systems. We synthesize lessons learned from this model system into experimental guidelines for using recent advances in genotyping technologies, to study recombination rate plasticity in non-model organisms. Specifically, we recommend (1) using fine-scale genome-wide markers, (2) collecting time-course data, (3) including crossover distribution measurements, and (4) using mixed effects models to analyse results. To illustrate this approach, we present an application adhering to these guidelines from empirical work we conducted in Drosophila pseudoobscuraThis article is part of the themed issue 'Evolutionary causes and consequences of recombination rate variation in sexual organisms'.
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Affiliation(s)
- Laurie S Stevison
- Department of Biological Sciences, Auburn University, Auburn, AL 36849, USA
| | - Stephen Sefick
- Department of Biological Sciences, Auburn University, Auburn, AL 36849, USA
| | - Chase Rushton
- Department of Biological Sciences, Auburn University, Auburn, AL 36849, USA
| | - Rita M Graze
- Department of Biological Sciences, Auburn University, Auburn, AL 36849, USA
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33
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Hite JL, Penczykowski RM, Shocket MS, Griebel KA, Strauss AT, Duffy MA, Cáceres CE, Hall SR. Allocation, not male resistance, increases male frequency during epidemics: a case study in facultatively sexual hosts. Ecology 2017; 98:2773-2783. [PMID: 28766698 DOI: 10.1002/ecy.1976] [Citation(s) in RCA: 15] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/18/2017] [Revised: 06/23/2017] [Accepted: 07/18/2017] [Indexed: 12/19/2022]
Abstract
Why do natural populations vary in the frequency of sexual reproduction? Virulent parasites may help explain why sex is favored during disease epidemics. To illustrate, we show a higher frequency of males and sexually produced offspring in natural populations of a facultative parthenogenetic host during fungal epidemics. In a multi-year survey of 32 lakes, the frequency of males (an index of sex) was higher in populations of zooplankton hosts with larger epidemics. A lake mesocosm experiment established causality: experimental epidemics produced a higher frequency of males relative to disease-free controls. One common explanation for such a pattern involves Red Queen (RQ) dynamics. However, this particular system lacks key genetic specificity mechanisms required for the RQ, so we evaluated two other hypotheses. First, individual females, when stressed by infection, could increase production of male offspring vs. female offspring (a tenant of the "Abandon Ship" theory). Data from a life table experiment supports this mechanism. Second, higher male frequency during epidemics could reflect a purely demographic process (illustrated with a demographic model): males could resist infection more than females (via size-based differences in resistance and mortality). However, we found no support for this resistance mechanism. A size-based model of resistance, parameterized with data, revealed why: higher male susceptibility negated the lower exposure (a size-based advantage) of males. These results suggest that parasite-mediated increases in allocation to sex by individual females, rather than male resistance, increased the frequency of sex during larger disease epidemics.
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Affiliation(s)
- Jessica L Hite
- Department of Biology, Indiana University, Bloomington, Indiana, 47405, USA
| | | | - Marta S Shocket
- Department of Biology, Indiana University, Bloomington, Indiana, 47405, USA
| | | | | | - Meghan A Duffy
- Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, 48109, USA
| | - Carla E Cáceres
- School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois, 61801, USA
| | - Spencer R Hall
- Department of Biology, Indiana University, Bloomington, Indiana, 47405, USA
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34
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Müller V, de Boer RJ, Bonhoeffer S, Szathmáry E. An evolutionary perspective on the systems of adaptive immunity. Biol Rev Camb Philos Soc 2017; 93:505-528. [PMID: 28745003 DOI: 10.1111/brv.12355] [Citation(s) in RCA: 61] [Impact Index Per Article: 7.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/21/2016] [Revised: 06/28/2017] [Accepted: 06/30/2017] [Indexed: 12/22/2022]
Abstract
We propose an evolutionary perspective to classify and characterize the diverse systems of adaptive immunity that have been discovered across all major domains of life. We put forward a new function-based classification according to the way information is acquired by the immune systems: Darwinian immunity (currently known from, but not necessarily limited to, vertebrates) relies on the Darwinian process of clonal selection to 'learn' by cumulative trial-and-error feedback; Lamarckian immunity uses templated targeting (guided adaptation) to internalize heritable information on potential threats; finally, shotgun immunity operates through somatic mechanisms of variable targeting without feedback. We argue that the origin of Darwinian (but not Lamarckian or shotgun) immunity represents a radical innovation in the evolution of individuality and complexity, and propose to add it to the list of major evolutionary transitions. While transitions to higher-level units entail the suppression of selection at lower levels, Darwinian immunity re-opens cell-level selection within the multicellular organism, under the control of mechanisms that direct, rather than suppress, cell-level evolution for the benefit of the individual. From a conceptual point of view, the origin of Darwinian immunity can be regarded as the most radical transition in the history of life, in which evolution by natural selection has literally re-invented itself. Furthermore, the combination of clonal selection and somatic receptor diversity enabled a transition from limited to practically unlimited capacity to store information about the antigenic environment. The origin of Darwinian immunity therefore comprises both a transition in individuality and the emergence of a new information system - the two hallmarks of major evolutionary transitions. Finally, we present an evolutionary scenario for the origin of Darwinian immunity in vertebrates. We propose a revival of the concept of the 'Big Bang' of vertebrate immunity, arguing that its origin involved a 'difficult' (i.e. low-probability) evolutionary transition that might have occurred only once, in a common ancestor of all vertebrates. In contrast to the original concept, we argue that the limiting innovation was not the generation of somatic diversity, but the regulatory circuitry needed for the safe operation of amplifiable immune responses with somatically acquired targeting. Regulatory complexity increased abruptly by genomic duplications at the root of the vertebrate lineage, creating a rare opportunity to establish such circuitry. We discuss the selection forces that might have acted at the origin of the transition, and in the subsequent stepwise evolution leading to the modern immune systems of extant vertebrates.
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Affiliation(s)
- Viktor Müller
- Parmenides Center for the Conceptual Foundations of Science, 82049 Pullach/Munich, Germany.,Department of Plant Systematics, Ecology and Theoretical Biology, Institute of Biology, Eötvös Loránd University, 1117 Budapest, Hungary.,Evolutionary Systems Research Group, MTA Centre for Ecological Research, 8237 Tihany, Hungary
| | - Rob J de Boer
- Theoretical Biology, Department of Biology, Utrecht University, 3584 CH Utrecht, The Netherlands
| | - Sebastian Bonhoeffer
- Institute of Integrative Biology, Department of Environmental Systems Science, ETH Zurich, 8092 Zurich, Switzerland
| | - Eörs Szathmáry
- Parmenides Center for the Conceptual Foundations of Science, 82049 Pullach/Munich, Germany.,Department of Plant Systematics, Ecology and Theoretical Biology, Institute of Biology, Eötvös Loránd University, 1117 Budapest, Hungary.,Evolutionary Systems Research Group, MTA Centre for Ecological Research, 8237 Tihany, Hungary
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Saini R, Singh AK, Dhanapal S, Saeed TH, Hyde GJ, Baskar R. Brief temperature stress during reproductive stages alters meiotic recombination and somatic mutation rates in the progeny of Arabidopsis. BMC PLANT BIOLOGY 2017; 17:103. [PMID: 28615006 PMCID: PMC5471674 DOI: 10.1186/s12870-017-1051-1] [Citation(s) in RCA: 15] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/23/2016] [Accepted: 06/01/2017] [Indexed: 05/02/2023]
Abstract
BACKGROUND Plants exposed to environmental stresses draw upon many genetic and epigenetic strategies, with the former sometimes modulated by the latter. This can help the plant, and its immediate progeny, at least, to better endure the stress. Some evidence has led to proposals that (epi) genetic changes can be both selective and sustainably heritable, while other evidence suggests that changes are effectively stochastic, and important only because they induce genetic variation. One type of stress with an arguably high level of stochasticity in its effects is temperature stress. Studies of how heat and cold affect the rates of meiotic recombination (MR) and somatic mutations (SMs, which are potentially heritable in plants) report increases, decreases, or no effect. Collectively, they do not point to any consistent patterns. Some of this variability, however, might arise from the stress being applied for such an extended time, typically days or weeks. Here, we adopted a targeted approach by (1) limiting exposure to one hour; and (2) timing it to coincide with (a) gamete, and early gametophyte, development, a period of high stress sensitivity; and (b) a late stage of vegetative development. RESULTS For plants (Arabidopsis thaliana) otherwise grown at 22 °C, we measured the effects of a 1 h exposure to cold (12 °C) or heat (32 °C) on the rates of MR, and four types of SMs (frameshift mutations; intrachromosomal recombination; base substitutions; transpositions) in the F1 progeny. One parent (wild type) was stressed, the other (unstressed) carried a genetic event detector. When rates were compared to those in progeny of control (both parents unstressed) two patterns emerged. In the progeny of younger plants (stressed at 36 days; pollinated at 40 days) heat and cold either had no effect (on MR) or (for SMs) had effects that were rare and stochastic. In the progeny of older plants (stressed at 41 days; pollinated at 45 days), while effects were also infrequent, those that were seen followed a consistent pattern: rates of all five genetic events were lowest at 12 °C and highest at 32 °C, i.e. they varied in a "dose-response" manner. This pattern was strongest (or, in the case of MR, only apparent) in progeny whose stressed parent was female. CONCLUSION While the infrequency of effects suggests the need for cautious inference, the consistency of responses in the progeny of older plants, indicate that in some circumstances the level of stochasticity in inherited genetic responses to heat or cold stress can be context-dependent, possibly reflecting life-cycle stages in the parental generation that are variably stress sensitive.
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Affiliation(s)
- Ramswaroop Saini
- Department of Biotechnology, Indian Institute of Technology–Madras, Bhupat and Jyoti Mehta School of Biosciences, Chennai, 600 036 India
| | - Amit Kumar Singh
- Department of Biotechnology, Indian Institute of Technology–Madras, Bhupat and Jyoti Mehta School of Biosciences, Chennai, 600 036 India
| | - Shanmuhapreya Dhanapal
- Department of Biotechnology, Indian Institute of Technology–Madras, Bhupat and Jyoti Mehta School of Biosciences, Chennai, 600 036 India
| | - Thoufeequl Hakeem Saeed
- Department of Biotechnology, Indian Institute of Technology–Madras, Bhupat and Jyoti Mehta School of Biosciences, Chennai, 600 036 India
| | - Geoffrey J. Hyde
- Write about Research, 14 Randwick Street, Randwick, Sydney, 2031 Australia
| | - Ramamurthy Baskar
- Department of Biotechnology, Indian Institute of Technology–Madras, Bhupat and Jyoti Mehta School of Biosciences, Chennai, 600 036 India
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Danchenko M, Klubicova K, Krivohizha MV, Berezhna VV, Sakada VI, Hajduch M, Rashydov NM. Systems biology is an efficient tool for investigation of low-dose chronic irradiation influence on plants in the Chernobyl zone. CYTOL GENET+ 2016. [DOI: 10.3103/s0095452716060050] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/08/2023]
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Ram Y, Hadany L. Condition-dependent sex: who does it, when and why? Philos Trans R Soc Lond B Biol Sci 2016; 371:20150539. [PMID: 27619702 PMCID: PMC5031623 DOI: 10.1098/rstb.2015.0539] [Citation(s) in RCA: 55] [Impact Index Per Article: 6.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 07/28/2016] [Indexed: 01/09/2023] Open
Abstract
We review the phenomenon of condition-dependent sex-where individuals' condition affects the likelihood that they will reproduce sexually rather than asexually. In recent years, condition-dependent sex has been studied both theoretically and empirically. Empirical results in microbes, fungi and plants support the theoretical prediction that negative condition-dependent sex, in which individuals in poor condition are more likely to reproduce sexually, can be evolutionarily advantageous under a wide range of settings. Here, we review the evidence for condition-dependent sex and its potential implications for the long-term survival and adaptability of populations. We conclude by asking why condition-dependent sex is not more commonly observed, and by considering generalizations of condition-dependent sex that might apply even for obligate sexuals.This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'.
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Affiliation(s)
- Yoav Ram
- Department of Molecular Biology and Ecology of Plants, Tel Aviv University, Tel Aviv 6997801, Israel
| | - Lilach Hadany
- Department of Molecular Biology and Ecology of Plants, Tel Aviv University, Tel Aviv 6997801, Israel
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38
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Chen W, Zhu Q, Liu Y, Zhang Q. Chromatin Remodeling and Plant Immunity. ADVANCES IN PROTEIN CHEMISTRY AND STRUCTURAL BIOLOGY 2016; 106:243-260. [PMID: 28057214 DOI: 10.1016/bs.apcsb.2016.08.006] [Citation(s) in RCA: 12] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/23/2022]
Abstract
Chromatin remodeling, an important facet of the regulation of gene expression in eukaryotes, is performed by two major types of multisubunit complexes, covalent histone- or DNA-modifying complexes, and ATP-dependent chromosome remodeling complexes. Snf2 family DNA-dependent ATPases constitute the catalytic subunits of ATP-dependent chromosome remodeling complexes, which accounts for energy supply during chromatin remodeling. Increasing evidence indicates a critical role of chromatin remodeling in the establishment of long-lasting, even transgenerational immune memory in plants, which is supported by the findings that DNA methylation, histone deacetylation, and histone methylation can prime the promoters of immune-related genes required for disease defense. So what are the links between Snf2-mediated ATP-dependent chromosome remodeling and plant immunity, and what mechanisms might support its involvement in disease resistance?
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Affiliation(s)
- W Chen
- State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Life Sciences, South China Agricultural University, Guangzhou, China
| | - Q Zhu
- State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Life Sciences, South China Agricultural University, Guangzhou, China
| | - Y Liu
- State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Life Sciences, South China Agricultural University, Guangzhou, China
| | - Q Zhang
- State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Life Sciences, South China Agricultural University, Guangzhou, China; Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, College of Life Sciences, South China Agricultural University, Guangzhou, China.
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Ma H, Song T, Wang T, Wang S. Influence of Human p53 on Plant Development. PLoS One 2016; 11:e0162840. [PMID: 27648563 PMCID: PMC5029891 DOI: 10.1371/journal.pone.0162840] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/29/2016] [Accepted: 08/29/2016] [Indexed: 11/19/2022] Open
Abstract
Mammalian p53 is a super tumor suppressor and plays a key role in guarding genome from DNA damage. However, p53 has not been found in plants which do not bear cancer although they constantly expose to ionizing radiation of ultraviolet light. Here we introduced p53 into the model plant Arabidopsis and examined p53-conferred phenotype in plant. Most strikingly, p53 caused early senescence and fasciation. In plants, fasciation has been shown as a result of the elevated homologous DNA recombination. Consistently, a reporter with overlapping segments of the GUS gene (1445) showed that the frequency of homologous recombination was highly induced in p53-transgenic plants. In contrast to p53, SUPPRESSOR OF NPR1-1 INDUCIBLE 1 (SNI1), as a negative regulator of homologous recombination in plants, is not present in mammals. Comet assay and clonogenic survival assay demonstrated that SNI1 inhibited DNA damage repair caused by either ionizing radiation or hydroxyurea in human osteosarcoma U2OS cancer cells. RAD51D is a recombinase in homologous recombination and functions downstream of SNI1 in plants. Interestingly, p53 rendered the sni1 mutants madly branching of inflorescence, a phenotype of fasciation, whereas rad51d mutant fully suppressed the p53-induced phenotype, indicating that human p53 action in plant is mediated by the SNI1-RAD51D signaling pathway. The reciprocal species-swap tests of p53 and SNI1 in human and Arabidopsis manifest that these species-specific proteins play a common role in homologous recombination across kingdoms of animals and plants.
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Affiliation(s)
- Huimin Ma
- Development Center of Plant Germplasm Resources, College of Life and Environmental Sciences, Shanghai Normal University, Shanghai 200234, China
| | - Teng Song
- Development Center of Plant Germplasm Resources, College of Life and Environmental Sciences, Shanghai Normal University, Shanghai 200234, China
| | - Tianhua Wang
- Development Center of Plant Germplasm Resources, College of Life and Environmental Sciences, Shanghai Normal University, Shanghai 200234, China
| | - Shui Wang
- Development Center of Plant Germplasm Resources, College of Life and Environmental Sciences, Shanghai Normal University, Shanghai 200234, China
- * E-mail:
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40
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41
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Jia N, Liu X, Gao H. A DNA2 Homolog Is Required for DNA Damage Repair, Cell Cycle Regulation, and Meristem Maintenance in Plants. PLANT PHYSIOLOGY 2016; 171:318-33. [PMID: 26951435 PMCID: PMC4854720 DOI: 10.1104/pp.16.00312] [Citation(s) in RCA: 22] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 02/28/2016] [Accepted: 03/04/2016] [Indexed: 05/18/2023]
Abstract
Plant meristem cells divide and differentiate in a spatially and temporally regulated manner, ultimately giving rise to organs. In this study, we isolated the Arabidopsis jing he sheng 1 (jhs1) mutant, which exhibited retarded growth, an abnormal pattern of meristem cell division and differentiation, and morphological defects such as fasciation, an irregular arrangement of siliques, and short roots. We identified JHS1 as a homolog of human and yeast DNA Replication Helicase/Nuclease2, which is known to be involved in DNA replication and damage repair. JHS1 is strongly expressed in the meristem of Arabidopsis. The jhs1 mutant was sensitive to DNA damage stress and had an increased DNA damage response, including increased expression of genes involved in DNA damage repair and cell cycle regulation, and a higher frequency of homologous recombination. In the meristem of the mutant plants, cell cycle progression was delayed at the G2 or late S phase and genes essential for meristem maintenance were misregulated. These results suggest that JHS1 plays an important role in DNA replication and damage repair, meristem maintenance, and development in plants.
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Affiliation(s)
- Ning Jia
- College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, China (N.J., X.L., H.G.)
| | - Xiaomin Liu
- College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, China (N.J., X.L., H.G.)
| | - Hongbo Gao
- College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, China (N.J., X.L., H.G.)
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42
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Stuttmann J, Peine N, Garcia AV, Wagner C, Choudhury SR, Wang Y, James GV, Griebel T, Alcázar R, Tsuda K, Schneeberger K, Parker JE. Arabidopsis thaliana DM2h (R8) within the Landsberg RPP1-like Resistance Locus Underlies Three Different Cases of EDS1-Conditioned Autoimmunity. PLoS Genet 2016; 12:e1005990. [PMID: 27082651 PMCID: PMC4833295 DOI: 10.1371/journal.pgen.1005990] [Citation(s) in RCA: 34] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/29/2015] [Accepted: 03/24/2016] [Indexed: 11/18/2022] Open
Abstract
Plants have a large panel of nucleotide-binding/leucine rich repeat (NLR) immune receptors which monitor host interference by diverse pathogen molecules (effectors) and trigger disease resistance pathways. NLR receptor systems are necessarily under tight control to mitigate the trade-off between induced defenses and growth. Hence, mis-regulated NLRs often cause autoimmunity associated with stunting and, in severe cases, necrosis. Nucleocytoplasmic ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1) is indispensable for effector-triggered and autoimmune responses governed by a family of Toll-Interleukin1-Receptor-related NLR receptors (TNLs). EDS1 operates coincidently or immediately downstream of TNL activation to transcriptionally reprogram cells for defense. We show here that low levels of nuclear-enforced EDS1 are sufficient for pathogen resistance in Arabidopsis thaliana, without causing negative effects. Plants expressing higher nuclear EDS1 amounts have the genetic, phenotypic and transcriptional hallmarks of TNL autoimmunity. In a screen for genetic suppressors of nuclear EDS1 autoimmunity, we map multiple, independent mutations to one gene, DM2h, lying within the polymorphic DANGEROUS MIX2 cluster of TNL RPP1-like genes from A. thaliana accession Landsberg erecta (Ler). The DM2 locus is a known hotspot for deleterious epistatic interactions leading to immune-related incompatibilities between A. thaliana natural accessions. We find that DM2hLer underlies two further genetic incompatibilities involving the RPP1-likeLer locus and EDS1. We conclude that the DM2hLer TNL protein and nuclear EDS1 cooperate, directly or indirectly, to drive cells into an immune response at the expense of growth. A further conclusion is that regulating the available EDS1 nuclear pool is fundamental for maintaining homeostatic control of TNL immune pathways. Plants tune their cellular and developmental programs to different environmental stimuli. Central players in the plant biotic stress response network are intracellular NLR receptors which intercept specific disease-inducing molecules (effectors) produced by pathogenic microbes. Variation in NLR gene repertoires between plant genetic lines is driven by pathogen selection pressure. One evolutionary question is how new, functional NLRs are assembled within a plant genome without mis-activating defense pathways, which can have strong negative effects on growth and fitness. This study focuses on a large, polymorphic sub-class of NLR receptors called TNLs present in dicotyledenous plant lineages. TNL receptors confer immunity to a broad range of pathogens. They also frequently underlie autoimmunity caused by their mis-regulation or deleterious allelic interactions with other genes in crosses between different genetic lines (hybrid incompatibility, HI). TNL pathogen-triggered and autoimmune responses require the conserved nucleocytoplasmic protein EDS1 to transcriptionally reprogram cells for defense. We discover in Arabidopsis thaliana that high levels of nuclear-enriched EDS1 induce transcriptional activation of defenses and growth inhibition without a pathogen effector stimulus. In a mutational screen, we identify one rapidly evolving TNL gene, DM2hLer, as a driver of nuclear EDS1 autoimmunity. DM2hLer also contributes to two separate cases of EDS1-dependent autoimmunity. Genetic cooperation between DM2hLer and EDS1 suggests a functional relationship in the transcriptional feed-forward regulation of defense pathways.
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Affiliation(s)
- Johannes Stuttmann
- Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, Cologne, Germany
- Department of Genetics, Martin Luther University Halle (Saale), Halle, Germany
- * E-mail: (JS); (JEP)
| | - Nora Peine
- Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, Cologne, Germany
| | - Ana V. Garcia
- Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, Cologne, Germany
| | - Christine Wagner
- Department of Genetics, Martin Luther University Halle (Saale), Halle, Germany
| | - Sayan R. Choudhury
- Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, Cologne, Germany
| | - Yiming Wang
- Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, Cologne, Germany
| | - Geo Velikkakam James
- Department of Plant Developmental Biology, Max-Planck Institute for Plant Breeding Research, Cologne, Germany
| | - Thomas Griebel
- Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, Cologne, Germany
| | - Ruben Alcázar
- Department of Natural Products, Plant Biology and Soil Science, Faculty of Pharmacy, University of Barcelona, Barcelona, Spain
| | - Kenichi Tsuda
- Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, Cologne, Germany
| | - Korbinian Schneeberger
- Department of Plant Developmental Biology, Max-Planck Institute for Plant Breeding Research, Cologne, Germany
| | - Jane E. Parker
- Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, Cologne, Germany
- * E-mail: (JS); (JEP)
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Dubrovina AS, Kiselev KV. Age-associated alterations in the somatic mutation and DNA methylation levels in plants. PLANT BIOLOGY (STUTTGART, GERMANY) 2016; 18:185-196. [PMID: 26211365 DOI: 10.1111/plb.12375] [Citation(s) in RCA: 39] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 04/06/2015] [Accepted: 07/21/2015] [Indexed: 05/18/2023]
Abstract
Somatic mutations of the nuclear and mitochondrial DNA and alterations in DNA methylation levels in mammals are well known to play important roles in ageing and various diseases, yet their specific contributions await further investigation. For plants, it has also been proposed that unrepaired DNA damage and DNA polymerase errors accumulate in plant cells and lead to increased somatic mutation rate and alterations in transcription, which eventually contribute to plant ageing. A number of studies also show that DNA methylation levels vary depending on the age of plant tissue and chronological age of a whole plant. Recent studies reveal that prolonged cultivation of plant cells in vitro induces single nucleotide substitutions and increases global DNA methylation level in a time-dependent fashion. Changes in DNA methylation are known to influence DNA repair and can lead to altered mutation rates, and, therefore, it is interesting to investigate both the genetic and epigenetic integrity in relationship to ageing in plants. This review will summarise and discuss the current studies investigating somatic DNA mutation and DNA methylation levels in relation to plant ageing and senescence. The analysis has shown that there still remains a lack of clarity concerning plant biological ageing and the role of the genetic and epigenetic instabilities in this process.
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Affiliation(s)
- A S Dubrovina
- Laboratory of Biotechnology, Institute of Biology and Soil Science, Far East Branch of Russian Academy of Sciences, Vladivostok, Russia
| | - K V Kiselev
- Laboratory of Biotechnology, Institute of Biology and Soil Science, Far East Branch of Russian Academy of Sciences, Vladivostok, Russia
- Department of Biochemistry, Microbiology and Biotechnology, The School of Natural Sciences, Far Eastern Federal University, Vladivostok, Russia
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Gu Y, Xing S, He C. Genome-Wide Analysis Indicates Lineage-Specific Gene Loss during Papilionoideae Evolution. Genome Biol Evol 2016; 8:635-48. [PMID: 26868598 PMCID: PMC4824202 DOI: 10.1093/gbe/evw021] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 02/01/2016] [Indexed: 02/07/2023] Open
Abstract
Gene loss is the driving force for changes in genome and morphology; however, this particular evolutionary event has been poorly investigated in leguminous plants. Legumes (Fabaceae) have some lineage-specific and diagnostic characteristics that are distinct from other angiosperms. To understand the potential role of gene loss in the evolution of legumes, we compared six genome-sequenced legume species of Papilionoideae, the largest representative clade of Fabaceae, such as Glycine max, with 34 nonlegume plant species, such as Arabidopsis thaliana. The results showed that the putative orthologs of the 34 Arabidopsis genes belonging to 29 gene families were absent in these legume species but these were conserved in the sequenced nonlegume angiosperm lineages. Further evolutionary analyses indicated that the orthologs of these genes were almost completely lost in the Papillionoideae ancestors, thus designated as the legume lost genes (LLGs), and these underwent purifying selection in nonlegume plants. Most LLGs were functionally unknown. In Arabidopsis, two LLGs were well-known genes that played a role in plant immunity such as HARMLESS TO OZONE LAYER 1 and HOPZ-ACTIVATED RESISTANCE 1, and 16 additional LLGs were predicted to participate in plant-pathogen interactions in in silico expression and protein-protein interaction network analyses. Most of these LLGs' orthologs in various plants were also found to be associated with biotic stress response, indicating the conserved role of these genes in plant defense. The evolutionary implication of LLGs during the development of the ability of symbiotic nitrogen fixation involving plant and bacterial interactions, which is a well-known characteristic of most legumes, is also discussed. Our work sheds light on the evolutionary implication of gene loss events in Papilionoideae evolution, as well as provides new insights into crop design to improve nitrogen fixation capacity.
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Affiliation(s)
- Yongzhe Gu
- State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, Beijing 100093, China Graduate University, Chinese Academy of Sciences, Yuquan Road 19, Beijing 100049, China
| | - Shilai Xing
- State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, Beijing 100093, China Graduate University, Chinese Academy of Sciences, Yuquan Road 19, Beijing 100049, China
| | - Chaoying He
- State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, Beijing 100093, China
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Dumont BL, Devlin AA, Truempy DM, Miller JC, Singh ND. No Evidence that Infection Alters Global Recombination Rate in House Mice. PLoS One 2015; 10:e0142266. [PMID: 26550833 PMCID: PMC4638334 DOI: 10.1371/journal.pone.0142266] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/09/2015] [Accepted: 10/20/2015] [Indexed: 12/13/2022] Open
Abstract
Recombination rate is a complex trait, with genetic and environmental factors shaping observed patterns of variation. Although recent studies have begun to unravel the genetic basis of recombination rate differences between organisms, less attention has focused on the environmental determinants of crossover rates. Here, we test the effect of one ubiquitous environmental pressure-bacterial infection-on global recombination frequency in mammals. We applied MLH1 mapping to assay global crossover rates in male mice infected with the pathogenic bacterium Borrelia burgdorferi, the causative agent of Lyme Disease, and uninfected control animals. Despite ample statistical power to identify biologically relevant differences between infected and uninfected animals, we find no evidence for a global recombination rate response to bacterial infection. Moreover, broad-scale patterns of crossover distribution, including the number of achiasmate bivalents, are not affected by infection status. Although pathogen exposure can plastically increase recombination in some species, our findings suggest that recombination rates in house mice may be resilient to at least some forms of infection stress. This negative result motivates future experiments with alternative house mouse pathogens to evaluate the generality of this conclusion.
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Affiliation(s)
- Beth L. Dumont
- Initiative in Biological Complexity, North Carolina State University, Raleigh, North Carolina, United States of America
- Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, United States of America
| | - Amy A. Devlin
- Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, United States of America
| | - Dana M. Truempy
- Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, United States of America
| | - Jennifer C. Miller
- Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, United States of America
| | - Nadia D. Singh
- Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, United States of America
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Shah JM, Ramakrishnan AM, Singh AK, Ramachandran S, Unniyampurath U, Jayshankar A, Balasundaram N, Dhanapal S, Hyde G, Baskar R. Suppression of different classes of somatic mutations in Arabidopsis by vir gene-expressing Agrobacterium strains. BMC PLANT BIOLOGY 2015; 15:210. [PMID: 26307100 PMCID: PMC4549908 DOI: 10.1186/s12870-015-0595-1] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 02/28/2015] [Accepted: 08/14/2015] [Indexed: 06/04/2023]
Abstract
BACKGROUND Agrobacterium infection, which is widely used to generate transgenic plants, is often accompanied by T-DNA-linked mutations and transpositions in flowering plants. It is not known if Agrobacterium infection also affects the rates of point mutations, somatic homologous recombinations (SHR) and frame-shift mutations (FSM). We examined the effects of Agrobacterium infection on five types of somatic mutations using a set of mutation detector lines of Arabidopsis thaliana. To verify the effect of secreted factors, we exposed the plants to different Agrobacterium strains, including wild type (Ach5), its derivatives lacking vir genes, oncogenes or T-DNA, and the heat-killed form for 48 h post-infection; also, for a smaller set of strains, we examined the rates of three types of mutations at multiple time-points. The mutation detector lines carried a non-functional β-glucuronidase gene (GUS) and a reversion of mutated GUS to its functional form resulted in blue spots. Based on the number of blue spots visible in plants grown for a further two weeks, we estimated the mutation frequencies. RESULTS For plants co-cultivated for 48 h with Agrobacterium, if the strain contained vir genes, then the rates of transversions, SHRs and FSMs (measured 2 weeks later) were lower than those of uninfected controls. In contrast, co-cultivation for 48 h with any of the Agrobacterium strains raised the transposition rates above control levels. The multiple time-point study showed that in seedlings co-cultivated with wild type Ach5, the reduced rates of transversions and SHRs after 48 h co-cultivation represent an apparent suppression of an earlier short-lived increase in mutation rates (peaking for plants co-cultivated for 3 h). An increase after 3 h co-cultivation was also seen for rates of transversions (but not SHR) in seedlings exposed to the strain lacking vir genes, oncogenes and T-DNA. However, the mutation rates in plants co-cultivated for longer times with this strain subsequently dropped below levels seen in uninfected controls, consistent with the results of the single time-point study. CONCLUSIONS The rates of various classes of mutations that result from Agrobacterium infection depend upon the duration of infection and the type of pathogen derived factors (such as Vir proteins, oncoproteins or T-DNA) possessed by the strain. Strains with vir genes, including the type used for plant transformation, suppressed selected classes of somatic mutations. Our study also provides evidence of a pathogen that can at least partly counter the induction of mutations in an infected plant.
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Affiliation(s)
- Jasmine M Shah
- Department of Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology-Madras, Chennai, 600036, India.
- Department of Plant Science, Central University of Kerala, Kasaragod, 671328, India.
| | - Anantha Maharasi Ramakrishnan
- Department of Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology-Madras, Chennai, 600036, India.
| | - Amit Kumar Singh
- Department of Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology-Madras, Chennai, 600036, India.
| | - Subalakshmi Ramachandran
- Department of Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology-Madras, Chennai, 600036, India.
| | | | - Ajitha Jayshankar
- Department of Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology-Madras, Chennai, 600036, India.
| | - Nithya Balasundaram
- Department of Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology-Madras, Chennai, 600036, India.
| | - Shanmuhapreya Dhanapal
- Department of Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology-Madras, Chennai, 600036, India.
| | - Geoff Hyde
- , 14 Randwick St, Sydney, 2031, Australia.
| | - Ramamurthy Baskar
- Department of Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology-Madras, Chennai, 600036, India.
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47
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Chen P, Umeda M. DNA double-strand breaks induce the expression of flavin-containing monooxygenase and reduce root meristem size in Arabidopsis thaliana. Genes Cells 2015; 20:636-46. [PMID: 26033196 DOI: 10.1111/gtc.12255] [Citation(s) in RCA: 20] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/21/2015] [Accepted: 05/06/2015] [Indexed: 01/06/2023]
Abstract
Plants use various mechanisms to cope with environmental stresses, which often threaten genome integrity. In Arabidopsis, DNA double-strand breaks (DSBs) reduce root meristem size in a SOG1-dependent manner. SOG1 is a key transcription factor controlling the response to DNA damage. However, the underlying mechanism remains largely unknown. In this study, we found that treatment with the DSB inducer zeocin increased the accumulation of H2O2 in root tips. Chromatin immunoprecipitation analysis showed that SOG1 directly binds to the promoter of FMO1, which encodes a flavin-containing monooxygenase and is associated with the production of reactive oxygen species (ROS), H2O2 in particular. Indeed, zeocin induced the expression of FMO1 in a SOG1-dependent manner, and neither the sog1 nor the fmo1 knockout mutant exhibited higher H2O2 accumulation in root tips. Consequently, both sog1 and fmo1 could tolerate exposure to zeocin, in terms of root growth and the maintenance of the meristem size. However, transgenic plants over-expressing FMO1 also accumulated H2O2 in response to zeocin exposure, suggesting that other ROS-synthesis genes are also involved in the regulation of ROS production. We conclude that SOG1-mediated regulation of ROS homeostasis plays a key role in the reduction of root meristem size under DNA stress conditions.
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Affiliation(s)
- Poyu Chen
- Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara, 630-0192, Japan
| | - Masaaki Umeda
- Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara, 630-0192, Japan
- JST, CREST, 8916-5 Takayama, Ikoma, Nara, 630-0192, Japan
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48
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The DNA damage response and immune signaling alliance: Is it good or bad? Nature decides when and where. Pharmacol Ther 2015; 154:36-56. [PMID: 26145166 DOI: 10.1016/j.pharmthera.2015.06.011] [Citation(s) in RCA: 120] [Impact Index Per Article: 12.0] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/10/2015] [Accepted: 06/10/2015] [Indexed: 12/15/2022]
Abstract
The characteristic feature of healthy living organisms is the preservation of homeostasis. Compelling evidence highlight that the DNA damage response and repair (DDR/R) and immune response (ImmR) signaling networks work together favoring the harmonized function of (multi)cellular organisms. DNA and RNA viruses activate the DDR/R machinery in the host cells both directly and indirectly. Activation of DDR/R in turn favors the immunogenicity of the incipient cell. Hence, stimulation of DDR/R by exogenous or endogenous insults triggers innate and adaptive ImmR. The immunogenic properties of ionizing radiation, a prototypic DDR/R inducer, serve as suitable examples of how DDR/R stimulation alerts host immunity. Thus, critical cellular danger signals stimulate defense at the systemic level and vice versa. Disruption of DDR/R-ImmR cross talk compromises (multi)cellular integrity, leading to cell-cycle-related and immune defects. The emerging DDR/R-ImmR concept opens up a new avenue of therapeutic options, recalling the Hippocrates quote "everything in excess is opposed by nature."
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Si W, Yuan Y, Huang J, Zhang X, Zhang Y, Zhang Y, Tian D, Wang C, Yang Y, Yang S. Widely distributed hot and cold spots in meiotic recombination as shown by the sequencing of rice F2 plants. THE NEW PHYTOLOGIST 2015; 206:1491-502. [PMID: 25664766 DOI: 10.1111/nph.13319] [Citation(s) in RCA: 69] [Impact Index Per Article: 6.9] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/02/2014] [Accepted: 12/29/2014] [Indexed: 05/02/2023]
Abstract
Numerous studies have argued that environmental variations may contribute to evolution through the generation of novel heritable variations via meiotic recombination, which plays a crucial role in crop domestication and improvement. Rice is one of the most important staple crops, but no direct estimate of recombination events has yet been made at a fine scale. Here, we address this limitation by sequencing 41 rice individuals with high sequencing coverage and c. 900 000 accurate markers. An average of 33.9 crossover (c. 4.53 cM Mb(-1) ) and 2.47 non-crossover events were detected per F2 plant, which is similar to the values in Arabidopsis. Although not all samples in the stress treatment group showed an increased number of crossover events, environmental stress increased the recombination rate in c. 28.5% of samples. Interestingly, the crossovers showed a highly uneven distribution among and along chromosomes, with c. 13.9% of the entire genome devoid of crossovers, including 11 of the 12 centromere regions, and c. 0.72% of the genome containing large numbers of crossovers (> 50 cM Mb(-1) ). The gene ontology (GO) categories showed that genes clustered within the recombination hot spot regions primarily tended to be involved in responses to environmental stimuli, suggesting that recombination plays an important role for adaptive evolution in rapidly changing environments.
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Affiliation(s)
- Weina Si
- State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210093, China
| | - Yang Yuan
- State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210093, China
| | - Ju Huang
- State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210093, China
| | - Xiaohui Zhang
- State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210093, China
| | - Yanchun Zhang
- State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210093, China
| | - Yadong Zhang
- Institute of Food Crops, Jiangsu Academy of Agricultural Science, Nanjing, 210014, China
| | - Dacheng Tian
- State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210093, China
| | - Cailin Wang
- Institute of Food Crops, Jiangsu Academy of Agricultural Science, Nanjing, 210014, China
| | - Yonghua Yang
- State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210093, China
| | - Sihai Yang
- State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210093, China
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50
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Ranade SS, Ganea LS, Razzak AM, García Gil MR. Fungal Infection Increases the Rate of Somatic Mutation in Scots Pine (Pinus sylvestris L.). J Hered 2015; 106:386-94. [PMID: 25890976 DOI: 10.1093/jhered/esv017] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/25/2014] [Accepted: 03/16/2015] [Indexed: 11/13/2022] Open
Abstract
Somatic mutations are transmitted during mitosis in developing somatic tissue. Somatic cells bearing the mutations can develop into reproductive (germ) cells and the somatic mutations are then passed on to the next generation of plants. Somatic mutations are a source of variation essential to evolve new defense strategies and adapt to the environment. Stem rust disease in Scots pine has a negative effect on wood quality, and thus adversely affects the economy. It is caused by the 2 most destructive fungal species in Scandinavia: Peridermium pini and Cronartium flaccidum. We studied nuclear genome stability in Scots pine under biotic stress (fungus-infected, 22 trees) compared to a control population (plantation, 20 trees). Stability was assessed as accumulation of new somatic mutations in 10 microsatellite loci selected for genotyping. Microsatellites are widely used as molecular markers in population genetics studies of plants, and are particularly used for detection of somatic mutations as their rate of mutation is of a much higher magnitude when compared with other DNA markers. We report double the rate of somatic mutation per locus in the fungus-infected trees (4.8×10(-3) mutations per locus), as compared to the controls (2.0×10(-3) mutations per locus) when individual samples were analyzed at 10 different microsatellite markers. Pearson's chi-squared test indicated a significant effect of the fungal infection which increased the number of mutations in the fungus-infected trees (χ(2) = 12.9883, df = 1, P = 0.0003134).
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Affiliation(s)
- Sonali Sachin Ranade
- From the Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre (UPSC), Swedish University of Agricultural Sciences, SE 901-83 Umeå, Sweden (Ranade, Ganea, Razzak, and García Gil)
| | - Laura-Stefana Ganea
- From the Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre (UPSC), Swedish University of Agricultural Sciences, SE 901-83 Umeå, Sweden (Ranade, Ganea, Razzak, and García Gil)
| | - Abdur M Razzak
- From the Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre (UPSC), Swedish University of Agricultural Sciences, SE 901-83 Umeå, Sweden (Ranade, Ganea, Razzak, and García Gil)
| | - M R García Gil
- From the Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre (UPSC), Swedish University of Agricultural Sciences, SE 901-83 Umeå, Sweden (Ranade, Ganea, Razzak, and García Gil).
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