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1
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Podlesnik J. Pupal Development and Adult Acclimation Temperatures Influence the Cold and Heat Tolerance in Tenebrio molitor (Coleoptera: Tenebrionidae). INSECTS 2025; 16:402. [PMID: 40332878 PMCID: PMC12028052 DOI: 10.3390/insects16040402] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 03/12/2025] [Revised: 04/07/2025] [Accepted: 04/09/2025] [Indexed: 05/08/2025]
Abstract
Temperature plays a crucial role in shaping the biology of insects. Developmental temperature and acclimation temperatures influence their ability to cope with extreme thermal conditions. This study investigates the effects of developmental temperatures during the pupal stage and adult acclimation temperatures on the thermal tolerance of Tenebrio molitor Linnaeus, 1758. We investigated cold tolerance based on chill-coma recovery time and heat tolerance based on heat knockdown time. Beetles were reared at five developmental temperatures (16, 21, 25, 30 and 35 °C) and later exposed to corresponding adult acclimation temperatures. From developmental temperatures of 21 and 30 °C, the group of beetles was subjected to different temperatures to induce adult acclimation at a different temperature than the developmental temperature. In cold-tolerance tests, beetles reared at lower temperatures showed better recovery from chill coma, while beetles reared at higher temperatures showed greater resistance to heat shock. Adult beetles acclimated to lower temperatures showed better cold tolerance, while those acclimated to higher temperatures performed better in the heat tolerance test. Interestingly, the developmental temperatures during the pupal stage also contributed to resistance, particularly in the heat-tolerance test. However, pupal stage temperatures had no effect on cold-shock resistance, as indicated by chill-coma recovery time. The results could provide insights into the rearing of T. molitor.
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Affiliation(s)
- Jan Podlesnik
- Faculty of Natural Sciences and Mathematics, University of Maribor, 2000 Maribor, Slovenia
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2
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Lenhart A, Ahsan A, McHaty M, Bergland AO. Improvement of starvation resistance via periodic fasting is genetically variable in Drosophila melanogaster. PHYSIOLOGICAL ENTOMOLOGY 2024; 49:270-278. [PMID: 39130127 PMCID: PMC11315414 DOI: 10.1111/phen.12443] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 02/07/2024] [Accepted: 04/23/2024] [Indexed: 08/13/2024]
Abstract
Organisms subjected to periodic nutrient limitation early in life exhibit improvements in aspects of survival, including resistance to some environmental stressors. Recent findings indicate that forms of periodic fasting such as intermittent fasting and time restricted feeding can improve starvation resistance. However, it remains unclear to what extent this survival improvement persists across different genetic backgrounds. In this study, we examine fasting-induced starvation resistance across a broad survey of wild-derived lineages and document genetic variation within this trait. We adopt a standard dietary intervention and show improvement to starvation resistance within a common laboratory lineage, replicating previous results. Next, we examine fasting-induced starvation resistance across isofemale lines collected across latitudes and in different seasons, and among inbred lines derived from flies collected on different continents. We discover genetic variation of fasting-induced starvation resistance, and show that fasting improved starvation resistance as often as it worsened starvation resistance. Fasted flies generally showed reduced fat concentration, and their starvation survival varied with sex, season of collection, and geographic origin. While specific lineages common to the laboratory can show a specific fasting-induced phenotype, we show that this result is not consistent across genetic backgrounds, reinforcing the idea that phenotypes observed in historic laboratory strains may not be conserved across a species.
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Affiliation(s)
- Adam Lenhart
- Department of Biology, University of Virginia, Charlottesville, Virginia, 22554
| | - Ayesha Ahsan
- Department of Biology, University of Virginia, Charlottesville, Virginia, 22554
| | - Margaret McHaty
- Department of Biology, University of Virginia, Charlottesville, Virginia, 22554
| | - Alan O. Bergland
- Department of Biology, University of Virginia, Charlottesville, Virginia, 22554
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3
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Juul-Kristensen T, Keller JG, Borg KN, Hansen NY, Foldager A, Ladegaard R, Ho YP, Loeschcke V, Knudsen BR. Topoisomerase 1 Activity Is Reduced in Response to Thermal Stress in Fruit Flies and in Human HeLa Cells. BIOSENSORS 2023; 13:950. [PMID: 37998125 PMCID: PMC10669382 DOI: 10.3390/bios13110950] [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: 09/22/2023] [Revised: 10/17/2023] [Accepted: 10/18/2023] [Indexed: 11/25/2023]
Abstract
In the modern world with climate changes and increasing pollution, different types of stress are becoming an increasing challenge. Hence, the identification of reliable biomarkers of stress and accessible sensors to measure such biomarkers are attracting increasing attention. In the current study, we demonstrate that the activity, but not the expression, of the ubiquitous enzyme topoisomerase 1 (TOP1), as measured in crude cell extracts by the REEAD sensor system, is markedly reduced in response to thermal stress in both fruit flies (Drosophila melanogaster) and cultivated human cells. This effect was observed in response to both mild-to-moderate long-term heat stress and more severe short-term heat stress in D. melanogaster. In cultivated HeLa cells a reduced TOP1 activity was observed in response to both cold and heat stress. The reduced TOP1 activity appeared dependent on one or more cellular pathways since the activity of purified TOP1 was unaffected by the utilized stress temperatures. We demonstrate successful quantitative measurement of TOP1 activity using an easily accessible chemiluminescence readout for REEAD pointing towards a sensor system suitable for point-of-care assessment of stress responses based on TOP1 as a biomarker.
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Affiliation(s)
- Trine Juul-Kristensen
- Department of Molecular Biology and Genetics, Aarhus University, 8000 Aarhus, Denmark; (T.J.-K.); (J.G.K.); (K.N.B.); (N.Y.H.); (A.F.); (R.L.)
| | - Josephine Geertsen Keller
- Department of Molecular Biology and Genetics, Aarhus University, 8000 Aarhus, Denmark; (T.J.-K.); (J.G.K.); (K.N.B.); (N.Y.H.); (A.F.); (R.L.)
| | - Kathrine Nygaard Borg
- Department of Molecular Biology and Genetics, Aarhus University, 8000 Aarhus, Denmark; (T.J.-K.); (J.G.K.); (K.N.B.); (N.Y.H.); (A.F.); (R.L.)
- Department of Biomedical Engineering, The Chinese University of Hong Kong, Hong Kong SAR, China;
| | - Noriko Y. Hansen
- Department of Molecular Biology and Genetics, Aarhus University, 8000 Aarhus, Denmark; (T.J.-K.); (J.G.K.); (K.N.B.); (N.Y.H.); (A.F.); (R.L.)
| | - Amalie Foldager
- Department of Molecular Biology and Genetics, Aarhus University, 8000 Aarhus, Denmark; (T.J.-K.); (J.G.K.); (K.N.B.); (N.Y.H.); (A.F.); (R.L.)
| | - Rasmus Ladegaard
- Department of Molecular Biology and Genetics, Aarhus University, 8000 Aarhus, Denmark; (T.J.-K.); (J.G.K.); (K.N.B.); (N.Y.H.); (A.F.); (R.L.)
| | - Yi-Ping Ho
- Department of Biomedical Engineering, The Chinese University of Hong Kong, Hong Kong SAR, China;
- Centre for Biomaterials, The Chinese University of Hong Kong, Hong Kong SAR, China
- Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics, Hong Kong SAR, China
- State Key Laboratory of Marine Pollution, City University of Hong Kong, Hong Kong SAR, China
| | | | - Birgitta R. Knudsen
- Department of Molecular Biology and Genetics, Aarhus University, 8000 Aarhus, Denmark; (T.J.-K.); (J.G.K.); (K.N.B.); (N.Y.H.); (A.F.); (R.L.)
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4
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Gleason GS, Starr K, Sanger TJ, Gunderson AR. Rapid heat hardening in embryos of the lizard Anolis sagrei. Biol Lett 2023; 19:20230174. [PMID: 37433329 PMCID: PMC10335855 DOI: 10.1098/rsbl.2023.0174] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/18/2023] [Accepted: 06/20/2023] [Indexed: 07/13/2023] Open
Abstract
Adaptive thermal tolerance plasticity can dampen the negative effects of warming. However, our knowledge of tolerance plasticity is lacking for embryonic stages that are relatively immobile and may benefit the most from an adaptive plastic response. We tested for heat hardening capacity (a rapid increase in thermal tolerance that manifests in minutes to hours) in embryos of the lizard Anolis sagrei. We compared the survival of a lethal temperature exposure between embryos that either did (hardened) or did not (not hardened) receive a high but non-lethal temperature pre-treatment. We also measured heart rates (HRs) at common garden temperatures before and after heat exposures to assess metabolic consequences. 'Hardened' embryos had significantly greater survival after lethal heat exposure relative to 'not hardened' embryos. That said, heat pre-treatment led to a subsequent increase in embryo HR that did not occur in embryos that did not receive pre-treatment, indicative of an energetic cost of mounting the heat hardening response. Our results are not only consistent with adaptive thermal tolerance plasticity in these embryos (greater heat survival after heat exposure), but also highlight associated costs. Thermal tolerance plasticity may be an important mechanism by which embryos respond to warming that warrants greater consideration.
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Affiliation(s)
- Grace S. Gleason
- Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118-5665, USA
| | - Katherine Starr
- Department of Biology, Loyola University Chicago, Chicago, IL 60611-2001, USA
| | - Thomas J. Sanger
- Department of Biology, Loyola University Chicago, Chicago, IL 60611-2001, USA
| | - Alex R. Gunderson
- Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118-5665, USA
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5
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Gonzalez VH, Oyen K, Aguilar ML, Herrera A, Martin RD, Ospina R. High thermal tolerance in high-elevation species and laboratory-reared colonies of tropical bumble bees. Ecol Evol 2022; 12:e9560. [PMID: 36479027 PMCID: PMC9720000 DOI: 10.1002/ece3.9560] [Citation(s) in RCA: 12] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/11/2022] [Revised: 11/07/2022] [Accepted: 11/10/2022] [Indexed: 12/12/2022] Open
Abstract
Bumble bees are key pollinators with some species reared in captivity at a commercial scale, but with significant evidence of population declines and with alarming predictions of substantial impacts under climate change scenarios. While studies on the thermal biology of temperate bumble bees are still limited, they are entirely absent from the tropics where the effects of climate change are expected to be greater. Herein, we test whether bees' thermal tolerance decreases with elevation and whether the stable optimal conditions used in laboratory-reared colonies reduces their thermal tolerance. We assessed changes in the lower (CTMin) and upper (CTMax) critical thermal limits of four species at two elevations (2600 and 3600 m) in the Colombian Andes, examined the effect of body size, and evaluated the thermal tolerance of wild-caught and laboratory-reared individuals of Bombus pauloensis. We also compiled information on bumble bees' thermal limits and assessed potential predictors for broadscale patterns of variation. We found that CTMin decreased with increasing elevation, while CTMax was similar between elevations. CTMax was slightly higher (0.84°C) in laboratory-reared than in wild-caught bees while CTMin was similar, and CTMin decreased with increasing body size while CTMax did not. Latitude is a good predictor for CTMin while annual mean temperature, maximum and minimum temperatures of the warmest and coldest months are good predictors for both CTMin and CTMax. The stronger response in CTMin with increasing elevation, and similar CTMax, supports Brett's heat-invariant hypothesis, which has been documented in other taxa. Andean bumble bees appear to be about as heat tolerant as those from temperate areas, suggesting that other aspects besides temperature (e.g., water balance) might be more determinant environmental factors for these species. Laboratory-reared colonies are adequate surrogates for addressing questions on thermal tolerance and global warming impacts.
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Affiliation(s)
- Victor H. Gonzalez
- Undergraduate Biology Program and Department of Ecology and Evolutionary BiologyUniversity of KansasLawrenceKansasUSA
| | - Kennan Oyen
- Department of Biological Sciences, McMicken College of Arts and SciencesUniversity of CincinnatiCincinnatiOhioUSA
| | | | - Andres Herrera
- Undergraduate Biology Program and Department of Ecology and Evolutionary BiologyUniversity of KansasLawrenceKansasUSA
| | | | - Rodulfo Ospina
- Laboratorio de Investigaciones en AbejasUniversidad Nacional de ColombiaSanta Fé de BogotáColombia
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6
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Singh K, Arun Samant M, Prasad NG. Evolution of cross-tolerance in Drosophila melanogaster as a result of increased resistance to cold stress. Sci Rep 2022; 12:19536. [PMID: 36376445 PMCID: PMC9663562 DOI: 10.1038/s41598-022-23674-z] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/09/2022] [Accepted: 11/03/2022] [Indexed: 11/16/2022] Open
Abstract
Cold stress is a critical environmental challenge that affects an organism's fitness-related traits. In Drosophila, increased resistance to specific environmental stress may lead to increased resistance to other kinds of stress. In the present study, we aimed to understand whether increased cold stress resistance in Drosophila melanogaster can facilitate their ability to tolerate other environmental stresses. For the current study, we used successfully selected replicate populations of D. melanogaster against cold shock and their control population. These selected populations have evolved several reproductive traits, including increased egg viability, mating frequency, male mating ability, ability to sire progenies, and faster recovery for mating latency under cold shock conditions. In the present work, we investigated egg viability and mating frequency with and without heat and cold shock conditions in the selected and their control populations. We also examined resistance to cold shock, heat shock, desiccation, starvation, and survival post-challenge with Staphylococcus succinus subsp. succinus PK-1 in the selected and their control populations. After cold-shock treatment, we found a 1.25 times increase in egg viability and a 1.57 times increase in mating frequency in the selected populations compared to control populations. Moreover, more males (0.87 times) and females (1.66 times) of the selected populations survived under cold shock conditions relative to their controls. After being subjected to heat shock, the selected population's egg viability and mating frequency increased by 0.30 times and 0.57 times, respectively, compared to control populations. Additionally, more selected males (0.31 times) and females (0.98 times) survived under heat shock conditions compared to the control populations. Desiccation resistance slightly increased in the females of the selected populations relative to their control, but we observed no change in the case of males. Starvation resistance decreased in males and females of the selected populations compared to their controls. Our findings suggest that the increased resistance to cold shock correlates with increased tolerance to heat stress, but this evolved resistance comes at a cost, with decreased tolerance to starvation.
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Affiliation(s)
- Karan Singh
- grid.458435.b0000 0004 0406 1521Department of Biological Sciences, Indian Institute of Science Education and Research Mohali, Knowledge City, Sector 81, SAS Nagar, PO Manauli, Ajitgarh, Punjab 140306 India ,grid.137628.90000 0004 1936 8753Present Address: Department of Cell Biology, NYU Grossman School of Medicine, 595 Medical Science Building, 550 First Ave, New York, NY 10016 USA
| | - Manas Arun Samant
- grid.458435.b0000 0004 0406 1521Department of Biological Sciences, Indian Institute of Science Education and Research Mohali, Knowledge City, Sector 81, SAS Nagar, PO Manauli, Ajitgarh, Punjab 140306 India
| | - Nagaraj Guru Prasad
- grid.458435.b0000 0004 0406 1521Department of Biological Sciences, Indian Institute of Science Education and Research Mohali, Knowledge City, Sector 81, SAS Nagar, PO Manauli, Ajitgarh, Punjab 140306 India
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7
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Guillén L, Pascacio-Villafán C, Osorio-Paz I, Ortega-Casas R, Enciso-Ortíz E, Altúzar-Molina A, Velázquez O, Aluja M. Coping with global warming: Adult thermal thresholds in four pestiferous Anastrepha species determined under experimental laboratory conditions and development/survival times of immatures and adults under natural field conditions. Front Physiol 2022; 13:991923. [PMID: 36304579 PMCID: PMC9593313 DOI: 10.3389/fphys.2022.991923] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/12/2022] [Accepted: 09/20/2022] [Indexed: 12/02/2022] Open
Abstract
Climate change, particularly global warming, is disturbing biological processes in unexpected ways and forcing us to re-study/reanalyze the effects of varying temperatures, among them extreme ones, on insect functional traits such as lifespan and fecundity/fertility. Here we experimentally tested, under both laboratory and field conditions, the effects of an extreme range of temperatures (5, 10, 15, 20, 30, 40, and 45 °C, and the naturally varying conditions experienced in the field), on survivorship/lifespan, fecundity, and fertility of four pestiferous fruit fly species exhibiting contrasting life histories and belonging to two phylogenetic groups within the genus Anastrepha: A. ludens, A. obliqua, A. striata, and A. serpentina. In the field, we also measured the length of the entire life cycle (egg to adult), and in one species (A. ludens), the effect on the latter of the host plant (mango and grapefruit). Under laboratory conditions, none of the adults, independent of species, could survive a single day when exposed to a constant temperature of 45 °C, but A. striata and A. serpentina females/males survived at the highly contrasting temperatures of 5 and 40 °C at least 7 days. Maximum longevity was achieved in all species at 15 °C (375, 225, 175 and 160 days in A. ludens, A. serpentina, A. striata and A. obliqua females, respectively). Anastrepha ludens layed many eggs until late in life (368 days) at 15 °C, but none eclosed. Eclosion was only observed in all species at 20 and 30 °C. Under natural conditions, flies lived ca. 100 days less than in the laboratory at 15 °C, likely due to the physiological cost of dealing with the highly varying environmental patterns over 24 h (minimum and maximum temperatures and relative humidity of ca. 10–40 °C, and 22–100%, respectively). In the case of A. ludens, the immature’s developmental time was shorter in mango, but adult survival was longer than in grapefruit. We discuss our results considering the physiological processes regulating the traits measured and tie them to the increasing problem of global warming and its hidden effects on the physiology of insects, as well as the ecological and pest management implications.
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Affiliation(s)
| | | | | | | | | | | | | | - Martín Aluja
- *Correspondence: Larissa Guillén, ; Martín Aluja,
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8
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Sandfeld T, Malmos KG, Nielsen CB, Lund MB, Aagaard A, Bechsgaard J, Wurster M, Lalk M, Johannsen M, Vosegaard T, Bilde T, Schramm A. Metabolite Profiling of the Social Spider Stegodyphus dumicola Along a Climate Gradient. Front Ecol Evol 2022. [DOI: 10.3389/fevo.2022.841490] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/13/2022] Open
Abstract
Animals experience climatic variation in their natural habitats, which may lead to variation in phenotypic responses among populations through local adaptation or phenotypic plasticity. In ectotherm arthropods, the expression of thermoprotective metabolites such as free amino acids, sugars, and polyols, in response to temperature stress, may facilitate temperature tolerance by regulating cellular homeostasis. If populations experience differences in temperatures, individuals may exhibit population-specific metabolite profiles through differential accumulation of metabolites that facilitate thermal tolerance. Such thermoprotective metabolites may originate from the animals themselves or from their associated microbiome, and hence microbial symbionts may contribute to shape the thermal niche of their host. The social spider Stegodyphus dumicola has extremely low genetic diversity, yet it occupies a relatively broad temperature range occurring across multiple climate zones in Southern Africa. We investigated whether the metabolome, including thermoprotective metabolites, differs between populations, and whether population genetic structure or the spider microbiome may explain potential differences. To address these questions, we assessed metabolite profiles, phylogenetic relationships, and microbiomes in three natural populations along a temperature gradient. The spider microbiomes in three genetically distinct populations of S. dumicola showed no significant population-specific pattern, and none of its dominating genera (Borrelia, Diplorickettsia, and Mycoplasma) are known to facilitate thermal tolerance in hosts. These results do not support a role of the microbiome in shaping the thermal niche of S. dumicola. Metabolite profiles of the three spider populations were significantly different. The variation was driven by multiple metabolites that can be linked to temperature stress (e.g., lactate, succinate, or xanthine) and thermal tolerance (e.g., polyols, trehalose, or glycerol): these metabolites had higher relative abundance in spiders from the hottest geographic region. These distinct metabolite profiles are consistent with a potential role of the metabolome in temperature response.
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9
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Gu X, Chen W, Perry T, Batterham P, Hoffmann AA. Genomic knockout of hsp23 both decreases and increases fitness under opposing thermal extremes in Drosophila melanogaster. INSECT BIOCHEMISTRY AND MOLECULAR BIOLOGY 2021; 139:103652. [PMID: 34562590 DOI: 10.1016/j.ibmb.2021.103652] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 08/10/2021] [Revised: 09/10/2021] [Accepted: 09/19/2021] [Indexed: 06/13/2023]
Abstract
Under exposure to harmful environmental stresses, organisms exhibit a general stress response involving upregulation of the expression of heat shock proteins (HSPs) which is thought to be adaptive. Small heat shock proteins (sHSPs) are key components of this response, although shsp genes may have other essential roles in development. However, the upregulation of expression of a suite of genes under stress may not necessarily be evidence of an adaptive response to stress that involves those genes. To explore this issue, we used the CRISPR/Cas9 system to investigate pleiotropic effects of the hsp23 gene in Drosophila melanogaster. Transgenic flies carrying a pCFD5 plasmid containing sgRNAs were created to generate a complete knockout of the hsp23 gene. The transgenic line lacking hsp23 showed an increased hatch rate and no major fitness costs under an intermediate temperature used for culturing the flies. In addition, hsp23 knockout affected tolerance to hot and cold temperature extremes but in opposing directions; knockout flies had reduced tolerance to cold, but increased tolerance to heat. Despite this, hsp23 expression (in wild type flies) was increased under both hot and cold conditions. The hsp23 gene was required for heat hardening at the pupal stage, but not at the 1st-instar larval stage, even though the gene was upregulated in wild type controls at that life stage. The phenotypic effects of hsp23 were not compensated for by expression changes in other shsps. Our study shows that the fitness consequences of an hsp gene knockout depends on environmental conditions, with potential fitness benefits of gene loss even under conditions when the gene is normally upregulated.
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Affiliation(s)
- Xinyue Gu
- School of BioSciences, Bio21 Institute, University of Melbourne, Parkville, Victoria, Australia.
| | - Wei Chen
- School of BioSciences, Bio21 Institute, University of Melbourne, Parkville, Victoria, Australia
| | - Trent Perry
- School of BioSciences, Bio21 Institute, University of Melbourne, Parkville, Victoria, Australia
| | - Philip Batterham
- School of BioSciences, Bio21 Institute, University of Melbourne, Parkville, Victoria, Australia
| | - Ary A Hoffmann
- School of BioSciences, Bio21 Institute, University of Melbourne, Parkville, Victoria, Australia
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10
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Hime GR, Stonehouse SLA, Pang TY. Alternative models for transgenerational epigenetic inheritance: Molecular psychiatry beyond mice and man. World J Psychiatry 2021; 11:711-735. [PMID: 34733638 PMCID: PMC8546770 DOI: 10.5498/wjp.v11.i10.711] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/24/2021] [Revised: 07/19/2021] [Accepted: 08/25/2021] [Indexed: 02/06/2023] Open
Abstract
Mental illness remains the greatest chronic health burden globally with few in-roads having been made despite significant advances in genomic knowledge in recent decades. The field of psychiatry is constantly challenged to bring new approaches and tools to address and treat the needs of vulnerable individuals and subpopulations, and that has to be supported by a continuous growth in knowledge. The majority of neuropsychiatric symptoms reflect complex gene-environment interactions, with epigenetics bridging the gap between genetic susceptibility and environmental stressors that trigger disease onset and drive the advancement of symptoms. It has more recently been demonstrated in preclinical models that epigenetics underpins the transgenerational inheritance of stress-related behavioural phenotypes in both paternal and maternal lineages, providing further supporting evidence for heritability in humans. However, unbiased prospective studies of this nature are practically impossible to conduct in humans so preclinical models remain our best option for researching the molecular pathophysiologies underlying many neuropsychiatric conditions. While rodents will remain the dominant model system for preclinical studies (especially for addressing complex behavioural phenotypes), there is scope to expand current research of the molecular and epigenetic pathologies by using invertebrate models. Here, we will discuss the utility and advantages of two alternative model organisms-Caenorhabditis elegans and Drosophila melanogaster-and summarise the compelling insights of the epigenetic regulation of transgenerational inheritance that are potentially relevant to human psychiatry.
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Affiliation(s)
- Gary R Hime
- Department of Anatomy and Physiology, The University of Melbourne, Parkville 3010, VIC, Australia
| | - Sophie LA Stonehouse
- Mental Health Theme, The Florey Institute of Neuroscience and Mental Health, Parkville 3052, VIC, Australia
| | - Terence Y Pang
- Department of Anatomy and Physiology, The University of Melbourne, Parkville 3010, VIC, Australia
- Mental Health Theme, The Florey Institute of Neuroscience and Mental Health, Parkville 3052, VIC, Australia
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11
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Willot Q, Loos B, Terblanche JS. Interactions between developmental and adult acclimation have distinct consequences for heat tolerance and heat stress recovery. J Exp Biol 2021; 224:271049. [PMID: 34308995 DOI: 10.1242/jeb.242479] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/22/2021] [Accepted: 07/21/2021] [Indexed: 11/20/2022]
Abstract
Developmental and adult thermal acclimation can have distinct, even opposite, effects on adult heat resistance in ectotherms. Yet, their relative contribution to heat-hardiness of ectotherms remains unclear despite the broad ecological implications thereof. Furthermore, the deterministic relationship between heat knockdown and recovery from heat stress is poorly understood but significant for establishing causal links between climate variability and population dynamics. Here, using Drosophila melanogaster in a full-factorial experimental design, we assessed the heat tolerance of flies in static stress assays, and document how developmental and adult acclimation interact with a distinct pattern to promote survival to heat stress in adults. We show that warmer adult acclimation is the initial factor enhancing survival to constant stressful high temperatures in flies, but also that the interaction between adult and developmental acclimation becomes gradually more important to ensure survival as the stress persists. This provides an important framework revealing the dynamic interplay between these two forms of acclimation that ultimately enhance thermal tolerance as a function of stress duration. Furthermore, by investigating recovery rates post-stress, we also show that the process of heat-hardening and recovery post-heat knockdown are likely to be based on set of (at least partially) divergent mechanisms. This could bear ecological significance as a trade-off may exist between increasing thermal tolerance and maximizing recovery rates post-stress, constraining population responses when exposed to variable and stressful climatic conditions.
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Affiliation(s)
- Quentin Willot
- Center for Invasion Biology, Department of Conservation Ecology & Entomology, Stellenbosch University, Stellenbosch 7602, South Africa
| | - Ben Loos
- Department of Physiological Sciences, Stellenbosch University, Stellenbosch 7602, South Africa
| | - John S Terblanche
- Center for Invasion Biology, Department of Conservation Ecology & Entomology, Stellenbosch University, Stellenbosch 7602, South Africa
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12
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Tian M, Xia Y, Cai D, Mao J, Luo S. Proteomic investigation of Peristenus spretus ovary and characterization of an ovary-enriched heat shock protein. BULLETIN OF ENTOMOLOGICAL RESEARCH 2021; 111:270-281. [PMID: 32993843 DOI: 10.1017/s0007485320000607] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/11/2023]
Abstract
Peristenus spretus (Hymenoptera: Braconidae) is one of the most important endoparasitoids used for biological control of the green mirid bug, Apolygus lucorum Meyer-Dür (Heteroptera: Miridae). However, what we know about its reproductive genetics is very limited. Here, the composition of ovarian proteins in P. spretus was analyzed. Mass spectrum data searched against the non-redundant NCBI protein and UniProt protein database identified 1382 proteins and revealed an enrichment of the heat shock protein 83 (HSP83) in P. spretus ovary. The Pshsp83 complete cDNA is 2175 bp in length and encodes a protein of 724 amino acids with a calculated molecular mass of 83.4 kDa and a theoretical isoelectric point of 4.87. Transcription of Pshsp83 appeared from days 1 to 13 post-emergence and peaked at 13th day. Immuno-localization showed that the HSP83 protein was present in cytoplasm of germarium and in egg chambers of the whole ovariole. The transcript abundance of Pshsp83 fluctuated drastically after heat shocks at different temperatures and the maximum emerged at 35°C. The exposure to 35°C caused no dramatic effects on reproductive parameters of adult females such as pupation rate, cocoon weight, emergence rate, sex ratio and developmental duration, but did on longevity. These results suggested that the HSP83 protein is involved in life-span regulation in the P. spretus.
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Affiliation(s)
- Miaomiao Tian
- IPPCAAS - State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection (IPP), Chinese Academy of Agricultural Sciences (CAAS), Beijing, China
- College of Plant Protection, Hainan University, Hainan Haikou, China
| | - Yayun Xia
- IPPCAAS - State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection (IPP), Chinese Academy of Agricultural Sciences (CAAS), Beijing, China
- College of Plant Protection, Hainan University, Hainan Haikou, China
| | - Ducheng Cai
- College of Plant Protection, Hainan University, Hainan Haikou, China
| | - Jianjun Mao
- IPPCAAS - State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection (IPP), Chinese Academy of Agricultural Sciences (CAAS), Beijing, China
| | - Shuping Luo
- IPPCAAS - State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection (IPP), Chinese Academy of Agricultural Sciences (CAAS), Beijing, China
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13
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Lapwong Y, Dejtaradol A, Webb JK. Plasticity in thermal hardening of the invasive Asian house gecko. Evol Ecol 2021. [DOI: 10.1007/s10682-021-10116-x] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/19/2022]
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14
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Yi J, Liu J, Li D, Sun D, Li J, An Y, Wu H. Transcriptome responses to heat and cold stress in prepupae of Trichogramma chilonis. Ecol Evol 2021; 11:4816-4825. [PMID: 33976850 PMCID: PMC8093697 DOI: 10.1002/ece3.7383] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/09/2020] [Revised: 02/02/2021] [Accepted: 02/05/2021] [Indexed: 11/13/2022] Open
Abstract
Trichogramma is a useful species that is widely applied in biocontrol. Temperature profoundly affects the commercial application of T. chilonis. Different developmental transcriptomes of prepupae and pupae of T. chilonis under 10, 25, and 40°C were obtained from our previous study. In this study, transcriptomic analysis was further conducted to gain a clear understanding of the molecular changes in the prepupae of T. chilonis under different thermal conditions. A total of 37,295 unigenes were identified from 3 libraries of prepupae of T. chilonis, 17,293 of which were annotated. Differential expression analysis showed that 408 and 108 differentially expressed genes (DEGs) were identified after heat and cold treatment, respectively. Under heat stress, the pathway of protein processing in endoplasmic reticulum was found to be active. Most of the genes involved in this pathway were annotated as lethal (2) essential for life [l(2)efl] and heat shock protein genes (hsps), which were both highly upregulated. Nevertheless, most of the genes involved in another significantly enriched pathway of starch and sucrose metabolism were downregulated, including 1 alpha-glucosidase gene and 2 beta-glucuronidase genes. Under cold stress, no significantly enriched pathway was found, and the significantly enriched GO terms were related to the interaction with host and immune defenses. Together, these results provide us with a comprehensive view of the molecular mechanisms of T. chilonis in response to temperature stresses and will provide new insight into the mass rearing and utilization of T. chilonis.
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Affiliation(s)
- Jiequn Yi
- Guangdong Engineering Research Center for Pesticide and FertilizerInstitute of BioengineeringGuangdong Academy of SciencesGuangzhouChina
| | - Jianbai Liu
- Guangdong Engineering Research Center for Pesticide and FertilizerInstitute of BioengineeringGuangdong Academy of SciencesGuangzhouChina
| | - Dunsong Li
- Guangdong Provincial Key Laboratory of High Technology for Plant Protection/Plant Protection Research InstituteGuangdong Academy of Agricultural SciencesGuangzhouChina
| | - Donglei Sun
- Guangdong Engineering Research Center for Pesticide and FertilizerInstitute of BioengineeringGuangdong Academy of SciencesGuangzhouChina
| | - Jihu Li
- Guangdong Engineering Research Center for Pesticide and FertilizerInstitute of BioengineeringGuangdong Academy of SciencesGuangzhouChina
| | - Yuxing An
- Guangdong Engineering Research Center for Pesticide and FertilizerInstitute of BioengineeringGuangdong Academy of SciencesGuangzhouChina
| | - Han Wu
- Guangdong Engineering Research Center for Pesticide and FertilizerInstitute of BioengineeringGuangdong Academy of SciencesGuangzhouChina
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15
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Shifts in thermal tolerance of the invasive Asian house gecko (Hemidactylus frenatus) across native and introduced ranges. Biol Invasions 2021. [DOI: 10.1007/s10530-020-02441-z] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/13/2023]
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16
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Deery SW, Rej JE, Haro D, Gunderson AR. Heat hardening in a pair of Anolis lizards: constraints, dynamics and ecological consequences. J Exp Biol 2021; 224:238102. [PMID: 34424976 DOI: 10.1242/jeb.240994] [Citation(s) in RCA: 13] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/19/2020] [Accepted: 02/17/2021] [Indexed: 01/19/2023]
Abstract
Heat tolerance plasticity is predicted to be an important buffer against global warming. Nonetheless, basal heat tolerance often correlates negatively with tolerance plasticity ('trade-off hypothesis'), a constraint that could limit plasticity benefits. We tested the trade-off hypothesis at the individual level with respect to heat hardening in two lizard species, Anolis carolinensis and Anolis sagrei. Heat hardening is a rapid increase in heat tolerance after heat shock that is rarely measured in reptiles but is generally considered to be a first line of physiological defense against heat. We also employed a biophysical model of operative habitat temperatures to estimate the performance consequences of hardening under ecologically relevant conditions. Anolis carolinensis hardened by 2 h post-heat shock and maintained hardening for several hours. However, A. sagrei did not harden. Biophysical models showed that hardening in A. carolinensis reduces their overheating risk in the field. Therefore, while not all lizards heat harden, hardening has benefits for species that can. We initially found a negative relationship between basal tolerance and hardening within both species, consistent with the trade-off hypothesis. However, permutation analyses showed that the apparent trade-offs could not be differentiated from statistical artifact. We found the same result when we re-analyzed published data supporting the trade-off hypothesis in another lizard species. Our results show that false positives may be common when testing the trade-off hypothesis. Statistical approaches that account for this are critical to ensure that the hypothesis, which has broad implications for thermal adaptation and responses to warming, is assessed appropriately.
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Affiliation(s)
- Sean W Deery
- Department of Ecology & Evolutionary Biology, Tulane University, 6823 St Charles Avenue, Lindy Boggs Building Room 400, New Orleans, LA 70118-5698, USA
| | - Julie E Rej
- Department of Ecology & Evolutionary Biology, Tulane University, 6823 St Charles Avenue, Lindy Boggs Building Room 400, New Orleans, LA 70118-5698, USA
| | - Daniel Haro
- Department of Ecology & Evolutionary Biology, Tulane University, 6823 St Charles Avenue, Lindy Boggs Building Room 400, New Orleans, LA 70118-5698, USA
| | - Alex R Gunderson
- Department of Ecology & Evolutionary Biology, Tulane University, 6823 St Charles Avenue, Lindy Boggs Building Room 400, New Orleans, LA 70118-5698, USA
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17
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Rivera HE, Aichelman HE, Fifer JE, Kriefall NG, Wuitchik DM, Wuitchik SJS, Davies SW. A framework for understanding gene expression plasticity and its influence on stress tolerance. Mol Ecol 2021; 30:1381-1397. [PMID: 33503298 DOI: 10.1111/mec.15820] [Citation(s) in RCA: 66] [Impact Index Per Article: 16.5] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/03/2020] [Revised: 12/10/2020] [Accepted: 01/20/2021] [Indexed: 12/18/2022]
Abstract
Phenotypic plasticity can serve as a stepping stone towards adaptation. Recently, studies have shown that gene expression contributes to emergent stress responses such as thermal tolerance, with tolerant and susceptible populations showing distinct transcriptional profiles. However, given the dynamic nature of gene expression, interpreting transcriptomic results in a way that elucidates the functional connection between gene expression and the observed stress response is challenging. Here, we present a conceptual framework to guide interpretation of gene expression reaction norms in the context of stress tolerance. We consider the evolutionary and adaptive potential of gene expression reaction norms and discuss the influence of sampling timing, transcriptomic resilience, as well as complexities related to life history when interpreting gene expression dynamics and how these patterns relate to host tolerance. We highlight corals as a case study to demonstrate the value of this framework for non-model systems. As species face rapidly changing environmental conditions, modulating gene expression can serve as a mechanistic link from genetic and cellular processes to the physiological responses that allow organisms to thrive under novel conditions. Interpreting how or whether a species can employ gene expression plasticity to ensure short-term survival will be critical for understanding the global impacts of climate change across diverse taxa.
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Affiliation(s)
- Hanny E Rivera
- Department of Biology, Boston University, Boston, MA, USA
| | | | - James E Fifer
- Department of Biology, Boston University, Boston, MA, USA
| | | | | | - Sara J S Wuitchik
- Department of Biology, Boston University, Boston, MA, USA.,FAS Informatics, Harvard University, Cambridge, MA, USA
| | - Sarah W Davies
- Department of Biology, Boston University, Boston, MA, USA
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18
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Zhang W, Storey KB, Dong Y. Synchronization of seasonal acclimatization and short‐term heat hardening improves physiological resilience in a changing climate. Funct Ecol 2021. [DOI: 10.1111/1365-2435.13768] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/27/2023]
Affiliation(s)
- Wen‐yi Zhang
- State Key Laboratory of Marine Environmental Science College of Ocean and Earth Sciences Xiamen University Xiamen China
- Institute of Animal Genetic Resource Nanjing Normal University Nanjing China
| | - Kenneth B. Storey
- Institute of Biochemistry and Department of Biology Carleton University Ottawa ON Canada
| | - Yun‐wei Dong
- Key Laboratory of Mariculture Ministry of Education Fisheries College Ocean University of China Qingdao China
- Function Laboratory for Marine Fisheries Science and Food Production Processes Qingdao National Laboratory for Marine Science and Technology Qingdao China
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19
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Verspagen N, Leiva FP, Janssen IM, Verberk WCEP. Effects of developmental plasticity on heat tolerance may be mediated by changes in cell size in Drosophila melanogaster. INSECT SCIENCE 2020; 27:1244-1256. [PMID: 31829515 PMCID: PMC7687148 DOI: 10.1111/1744-7917.12742] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/21/2019] [Revised: 11/07/2019] [Accepted: 11/27/2019] [Indexed: 05/25/2023]
Abstract
There is a growing interest in the physiology underpinning heat tolerance of ectotherms and their responses to the ongoing rise in temperature. However, there is no consensus about the underlying physiological mechanisms. According to "the maintain aerobic scope and regulate oxygen supply" hypothesis, responses to warming at different organizational levels contribute to the ability to safeguard energy metabolism via aerobic pathways. At the cellular level, a decrease in cell size increases the capacity for the uptake of resources (e.g., food and oxygen), but the maintenance of electrochemical gradients across cellular membranes implies greater energetic costs in small cells. In this study, we investigated how different rearing temperatures affected cell size and heat tolerance in the fruit fly Drosophila melanogaster. We tested the hypothesis that smaller-celled flies are more tolerant to acute, intense heat stress whereas larger-celled flies are more tolerant to chronic, mild heat stress. We used the thermal tolerance landscape framework, which incorporates the intensity and duration of thermal challenge. Rearing temperatures strongly affected both cell size and survival times. We found different effects of developmental plasticity on tolerance to either chronic or acute heat stress. Warm-reared flies had both smaller cells and exhibited higher survival times under acute, intense heat stress when compared to cold-reared flies. However, under chronic, mild heat stress, the situation was reversed and cold-reared flies, consisting of larger cells, showed better survival. These differences in heat tolerance could have resulted from direct effects of rearing temperature or they may be mediated by the correlated changes in cell size. Notably, our results are consistent with the idea that a smaller cell size may confer tolerance to acute temperatures via enhanced oxygen supply, while a larger cell may confer greater tolerance to chronic and less intense heat stress via more efficient use of resources.
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Affiliation(s)
- Nadja Verspagen
- Department of Animal Ecology and Physiology, Institute for Water and Wetland ResearchRadboud UniversityNijmegenThe Netherlands
| | - Félix P. Leiva
- Department of Animal Ecology and Physiology, Institute for Water and Wetland ResearchRadboud UniversityNijmegenThe Netherlands
| | - Irene M. Janssen
- Department of Human Genetics, Radboud University Medical CenterRadboud Institute for Molecular Life SciencesNijmegenThe Netherlands
| | - Wilco C. E. P. Verberk
- Department of Animal Ecology and Physiology, Institute for Water and Wetland ResearchRadboud UniversityNijmegenThe Netherlands
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20
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Jin J, Li Y, Zhou Z, Zhang H, Guo J, Wan F. Heat Shock Factor Is Involved in Regulating the Transcriptional Expression of Two Potential Hsps ( AhHsp70 and AhsHsp21) and Its Role in Heat Shock Response of Agasicles hygrophila. Front Physiol 2020; 11:562204. [PMID: 33041860 PMCID: PMC7522579 DOI: 10.3389/fphys.2020.562204] [Citation(s) in RCA: 11] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/14/2020] [Accepted: 08/25/2020] [Indexed: 01/14/2023] Open
Abstract
Heat shock proteins are molecular chaperones that are involved in numerous normal cellular processes and stress responses, and heat shock factors are transcriptional activators of heat shock proteins. Heat shock factors and heat shock proteins are coordinated in various biological processes. The regulatory function of heat shock factors in the expression of genes encoding heat shock proteins (Hsps) has been documented in some model insects, however, the role of transcription factors in modulating Hsps in other insects is still limited. In this study, one heat shock factor gene (AhHsf) was isolated and its two potential target genes (AhHsp70 and AhsHsp21) were confirmed from Agasicles hygrophila. AhHsf sequence analysis indicated that it belongs to the Hsfs gene family. RT-qPCR showed that expression levels of heat shock factors and of two heat shock proteins significantly increased under heat stress. Injection with double-stranded Hsf RNA in freshly emerged adult beetles significantly inhibited expression of AhHsp70 and AhsHsp21, shortened the adult survival, drastically reduced egg production, and ultimately led to a decrease in fecundity. RNA interference (RNAi)-mediated suppression of AhHsp70 or AhsHsp21 expression also significantly affected expression of AhHsf. Our findings revealed a potential transcriptional function of AhHsf to regulate expression of AhHsp70 and AhsHsp21, which may play a key role in A. hygrophila thermotolerance. Our results improve our understanding of the molecular mechanisms of the AhHsf - AhHsps signaling pathway in A. hygrophila.
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Affiliation(s)
- Jisu Jin
- College of Plant Protection, Hunan Agricultural University, Changsha, China.,State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
| | - Youzhi Li
- College of Plant Protection, Hunan Agricultural University, Changsha, China
| | - Zhongshi Zhou
- State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
| | - Hong Zhang
- State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
| | - Jianying Guo
- State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
| | - Fanghao Wan
- College of Plant Protection, Hunan Agricultural University, Changsha, China.,State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
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21
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Sørensen JG, Winther ML, Salachan PV, MacLean HJ. Drawing the line: Linear or non-linear reaction norms in response to adult acclimation on lower thermal limits. JOURNAL OF INSECT PHYSIOLOGY 2020; 124:104075. [PMID: 32540466 DOI: 10.1016/j.jinsphys.2020.104075] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 02/13/2020] [Revised: 06/09/2020] [Accepted: 06/09/2020] [Indexed: 06/11/2023]
Abstract
Estimates of lower thermal limits are widely used to infer sensitivity to climate variability, local adaptation and adaptive acclimation responses in ectotherms. These inferences build on the ecological relevance of the tolerance estimates and assume that estimates can be extrapolated to relevant conditions. Methodological effects for upper thermal limits have been extensively investigated, with different ramping rates and acclimation regimes giving rise to varying, and even disparate, conclusions. However, methodological effects have received much less attention for lower thermal limits. In this study, we explicitly test whether methodology could affect estimates of lower thermal limits in interaction with acclimation temperature and thermal variability, by acclimating adult Drosophila melanogaster to different constant and fluctuating temperature regimes and generating reaction norms at different ramping rates. We find that ramping rates have no significant effect on the lower thermal limits. Constant temperature acclimation resulted in non-linear reaction norms, while the introduction of thermal variability during adult life result in linear reaction norms. Thus, applying ecologically relevant conditions (here thermal variability) potentially impacts the results and conclusions of insect low temperature tolerance and acclimation capacity.
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Affiliation(s)
- Jesper Givskov Sørensen
- Department of Biology, Aarhus University, Ny Munkegade 114, Bldg. 1540, 8000 Aarhus C, Denmark.
| | - Marius Løssl Winther
- Department of Biology, Aarhus University, Ny Munkegade 114, Bldg. 1540, 8000 Aarhus C, Denmark
| | - Paul Vinu Salachan
- Department of Biology, Aarhus University, Ny Munkegade 114, Bldg. 1540, 8000 Aarhus C, Denmark
| | - Heidi Joan MacLean
- Department of Biology, Aarhus University, Ny Munkegade 114, Bldg. 1540, 8000 Aarhus C, Denmark
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22
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Javal M, Thomas S, Lehmann P, Barton MG, Conlong DE, Du Plessis A, Terblanche JS. The Effect of Oxygen Limitation on a Xylophagous Insect's Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy. Front Physiol 2019; 10:1426. [PMID: 31824337 PMCID: PMC6879455 DOI: 10.3389/fphys.2019.01426] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/01/2019] [Accepted: 11/04/2019] [Indexed: 12/21/2022] Open
Abstract
Temperature has a profound impact on insect fitness and performance via metabolic, enzymatic or chemical reaction rate effects. However, oxygen availability can interact with these thermal responses in complex and often poorly understood ways, especially in hypoxia-adapted species. Here we test the hypothesis that thermal limits are reduced under low oxygen availability - such as might happen when key life-stages reside within plants - but also extend this test to attempt to explain that the magnitude of the effect of hypoxia depends on variation in key respiration-related parameters such as aerobic scope and respiratory morphology. Using two life-stages of a xylophagous cerambycid beetle, Cacosceles (Zelogenes) newmannii we assessed oxygen-limitation effects on metabolic performance and thermal limits. We complement these physiological assessments with high-resolution 3D (micro-computed tomography scan) morphometry in both life-stages. Results showed that although larvae and adults have similar critical thermal maxima (CTmax) under normoxia, hypoxia reduces metabolic rate in adults to a greater extent than it does in larvae, thus reducing aerobic scope in the former far more markedly. In separate experiments, we also show that adults defend a tracheal oxygen (critical) setpoint more consistently than do larvae, indicated by switching between discontinuous gas exchange cycles (DGC) and continuous respiratory patterns under experimentally manipulated oxygen levels. These effects can be explained by the fact that the volume of respiratory anatomy is positively correlated with body mass in adults but is apparently size-invariant in larvae. Thus, the two life-stages of C. newmannii display key differences in respiratory structure and function that can explain the magnitude of the effect of hypoxia on upper thermal limits.
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Affiliation(s)
- Marion Javal
- Department of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South Africa
| | - Saskia Thomas
- Department of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South Africa
| | - Philipp Lehmann
- Department of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South Africa
- Department of Zoology, Stockholm University, Stockholm, Sweden
| | - Madeleine G. Barton
- Department of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South Africa
| | - Desmond E. Conlong
- Department of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South Africa
- South African Sugarcane Research Institute, Mount Edgecombe, South Africa
| | - Anton Du Plessis
- CT Scanner Facility, Central Analytical Facilities, Stellenbosch University, Stellenbosch, South Africa
- Physics Department, Stellenbosch University, Stellenbosch, South Africa
| | - John S. Terblanche
- Department of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South Africa
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23
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Salachan PV, Burgaud H, Sørensen JG. Testing the thermal limits: Non-linear reaction norms drive disparate thermal acclimation responses in Drosophila melanogaster. JOURNAL OF INSECT PHYSIOLOGY 2019; 118:103946. [PMID: 31525352 DOI: 10.1016/j.jinsphys.2019.103946] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/02/2019] [Revised: 09/12/2019] [Accepted: 09/13/2019] [Indexed: 06/10/2023]
Abstract
Critical thermal limits are important ecological parameters for studying thermal biology and for modelling species' distributions under current and changing climatic conditions (including predicting the risk of extinction for species from future warming). However, estimates of the critical thermal limits are biased by the choice of assay and assay conditions, which differ among studies. Furthermore, estimates of the potential for phenotypic plasticity (thermal acclimation) to buffer against thermal variability are usually based on single assay conditions and (usually linear) extrapolation from a few acclimation temperatures. We produced high resolution estimates of adult acclimation capacity for upper tolerance limits at different assay conditions (ramping rates and knock-down temperatures) using CTmax (dynamic) and knock-down (static) thermal assays in the model species Drosophila melanogaster. We found the reaction norms to be highly dependent on assay conditions. We confirmed that progressively lower ramping rates or higher knock-down temperatures led to overall lower tolerance estimates. More surprisingly, extended assays (lower ramping rates or lower knock-down temperatures) also led to increasingly non-linear reaction norms for upper thermal tolerance across adult acclimation temperatures. Our results suggest that the magnitude (capacity) and direction (beneficial or detrimental) of acclimation responses are highly sensitive to assay conditions. The results offer a framework for comparison of acclimation responses between different assay conditions and a potential for explaining disparate acclimation capacity theories. We advocate cautious interpretation of acclimation capacities and careful consideration of assay conditions, which should represent realistic environmental conditions based on species' ecological niches.
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Affiliation(s)
- Paul Vinu Salachan
- Department of Bioscience, Aarhus University, Ny Munkegade 116, 8000 Aarhus C, Denmark.
| | - Hélène Burgaud
- Department of Bioscience, Aarhus University, Ny Munkegade 116, 8000 Aarhus C, Denmark
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24
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Chen H, Solangi GS, Zhao C, Yang L, Guo J, Wan F, Zhou Z. Physiological Metabolic Responses of Ophraella communa to High Temperature Stress. Front Physiol 2019; 10:1053. [PMID: 31507435 PMCID: PMC6718515 DOI: 10.3389/fphys.2019.01053] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/31/2019] [Accepted: 08/02/2019] [Indexed: 11/13/2022] Open
Abstract
Considering the predicted rising temperatures under current climate change and heat wave scenarios, organisms are expected to suffer more intense and frequent thermal stress. Induced heat is accumulated by organisms and can cause a variety of physiological stress responses. Ophraella communa is an effective biological control agent of common ragweed, Ambrosia artemisiifolia, but the responses of this biocontrol agent to heat stress have not been fully elucidated and, therefore, its potential responses to climate change are uncertain. We investigated the physiological metabolism of subsequent O. communa adults after: (1) different developmental stages (egg, larval, pupal, and adult) were exposed to thermal stress for 3 h each day for 3, 5, 5, and 5 days, respectively (by stage); and (2) individuals were exposed to thermal stress throughout the egg-to-adult period for 3 h each day. The high temperatures of 40, 42, and 44°C were used to induce thermal stress. A control group was reared at 28 ± 2°C. The results showed that short- or long-term exposure to daily phasic high temperatures significantly decreased water and lipid contents and significantly increased glycogen and glycerol contents in all adults (i.e., after exposure of different stages or throughout the egg-to-adult period). However, the total sugar content significantly increased in adults after the eggs and larvae were exposed to brief short-term thermal stress. Compared to the control, the total sugar content was also significantly higher in the adults and pupae exposed to 44°C. Total sugar content in females increased significantly in response to long-term phasic thermal stress at 40°C. However, sugar content of males exposed to 44°C decreased significantly. After long-term phasic thermal stress, water and glycogen contents in males were significantly higher than in females; however, females had higher total sugar and lipid contents. Therefore, our study provides a basic understanding of the metabolic responses of O. communa to thermal stress and offers insights into its potential as a natural biocontrol agent against A. artemisiifolia during the summer season and under predicted climate change scenarios.
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Affiliation(s)
- Hongsong Chen
- State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.,Guangxi Key Laboratory for Biology of Crop Diseases and Insect Pests, Institute of Plant Protection, Guangxi Academy of Agricultural Sciences, Nanning, China
| | - Ghulam Sarwar Solangi
- Department of Entomology, Sindh Agriculture University Sub Campus, Umerkot, Pakistan
| | - Chenchen Zhao
- State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.,State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Henan, China
| | - Lang Yang
- Guangxi Key Laboratory for Biology of Crop Diseases and Insect Pests, Institute of Plant Protection, Guangxi Academy of Agricultural Sciences, Nanning, China
| | - Jianying Guo
- State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
| | - Fanghao Wan
- State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
| | - Zhongshi Zhou
- State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
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Kühnhold H, Steinmann N, Huang YH, Indriana L, Meyer A, Kunzmann A. Temperature-induced aerobic scope and Hsp70 expression in the sea cucumber Holothuria scabra. PLoS One 2019; 14:e0214373. [PMID: 30901348 PMCID: PMC6430385 DOI: 10.1371/journal.pone.0214373] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/23/2018] [Accepted: 03/12/2019] [Indexed: 11/29/2022] Open
Abstract
The Aerobic Scope (AS), which reflects the functional capacity for biological fitness, is a highly relevant proxy to determine thermal tolerance in various taxa. Despite the importance of this method, its implementation is often hindered, due to lacking techniques to accurately measure standard- (SMR) and maximal- (MMR) metabolic rates, especially in sluggish marine invertebrates with low oxygen consumption rates, such as sea cucumbers. In this study the AS concept was modified to define a Temperature-induced Aerobic Scope (TAS), based on metabolic rate changes due to temperature adjustments rather than traditionally used physical activity patterns. Consequentially, temperature dependent peak and bottom O2 consumption rates, defined as Temperature-induced Maximal- (TMMR) and Standard Metabolic Rates (TSMR), respectively, served as MMR and SMR alternatives for the sea cucumber Holothuria scabra. TMMR and TSMR were induced through acute temperature change (2°C per hour; 17–41°C) until critical warm (WTcrit) and cold (CTcrit) temperatures were reached, respectively. In addition, Hsp70 gene expression linked to respiration rates served as synergistic markers to confirm critical threshold temperatures. O2 consumption of H. scabra peaked distinctly at WTcrit of 38°C (TMMR = 33.2 ± 4.7 μgO2 g-1 h-1). A clear metabolic bottom line was reached at CTcrit of 22°C (TSMR = 2.2 ± 1.4 μgO2 g-1 h-1). Within the thermal window of 22–38°C H. scabra sustained positive aerobic capacity, with assumed optimal performance range between 29–31.5°C (13.85–18.7 μgO2 g-1 h-1). Between 39–41°C H. scabra decreased respiration progressively, while gene expression levels of Hsp70 increased significantly at 41°C, indicating prioritization of heat shock response (HSR) and homeostatic disruption. At the cold end (17–22°C) homeostatic disruption was visible through incrementally increasing energetic expenses to fuel basal maintenance costs, but no Hsp70 overexpression occurred. TMMR, TSMR and TAS proved to be reliable metrics, similar to the traditional energetic key parameters MMR, SMR and AS, to determine a specific aerobic performance window for the sluggish bottom dwelling species H. scabra. In addition, the linkage between respiration physiology and molecular defense mechanisms showed valuable analytical synergies in terms of mechanistic prioritization as response to thermal stress. Overall, this study will help to define lethal temperatures for aquaculture and to predict the effects of environmental stress, such as ocean warming, in H. scabra.
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Affiliation(s)
- Holger Kühnhold
- Department of Ecology, Leibniz Centre for Tropical Marine Research (ZMT), Bremen, Germany
- * E-mail:
| | - Nuri Steinmann
- Department of Ecology, Leibniz Centre for Tropical Marine Research (ZMT), Bremen, Germany
| | - Yi-Hsuan Huang
- Department of Ecology, Leibniz Centre for Tropical Marine Research (ZMT), Bremen, Germany
| | - Lisa Indriana
- Research Centre for Oceanography, Indonesian Institute of Science (LIPI), Lombok, Indonesia
| | - Achim Meyer
- Department of Ecology, Leibniz Centre for Tropical Marine Research (ZMT), Bremen, Germany
| | - Andreas Kunzmann
- Department of Ecology, Leibniz Centre for Tropical Marine Research (ZMT), Bremen, Germany
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Königer A, Grath S. Transcriptome Analysis Reveals Candidate Genes for Cold Tolerance in Drosophila ananassae. Genes (Basel) 2018; 9:genes9120624. [PMID: 30545157 PMCID: PMC6315829 DOI: 10.3390/genes9120624] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/27/2018] [Revised: 11/19/2018] [Accepted: 12/03/2018] [Indexed: 12/25/2022] Open
Abstract
Coping with daily and seasonal temperature fluctuations is a key adaptive process for species to colonize temperate regions all over the globe. Over the past 18,000 years, the tropical species Drosophila ananassae expanded its home range from tropical regions in Southeast Asia to more temperate regions. Phenotypic assays of chill coma recovery time (CCRT) together with previously published population genetic data suggest that only a small number of genes underlie improved cold hardiness in the cold-adapted populations. We used high-throughput RNA sequencing to analyze differential gene expression before and after exposure to a cold shock in cold-tolerant lines (those with fast chill coma recovery, CCR) and cold-sensitive lines (slow CCR) from a population originating from Bangkok, Thailand (the ancestral species range). We identified two candidate genes with a significant interaction between cold tolerance and cold shock treatment: GF14647 and GF15058. Further, our data suggest that selection for increased cold tolerance did not operate through the increased activity of heat shock proteins, but more likely through the stabilization of the actin cytoskeleton and a delayed onset of apoptosis.
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Affiliation(s)
- Annabella Königer
- Division of Evolutionary Biology, Faculty of Biology, LMU Munich, Grosshaderner Str. 2, 82152 Planegg-Martinsried, Germany.
| | - Sonja Grath
- Division of Evolutionary Biology, Faculty of Biology, LMU Munich, Grosshaderner Str. 2, 82152 Planegg-Martinsried, Germany.
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Mir AH, Qamar A. Effects of Starvation and Thermal Stress on the Thermal Tolerance of Silkworm, Bombyx mori: Existence of Trade-offs and Cross-Tolerances. NEOTROPICAL ENTOMOLOGY 2018; 47:610-618. [PMID: 28956278 DOI: 10.1007/s13744-017-0559-2] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 01/23/2017] [Accepted: 08/30/2017] [Indexed: 06/07/2023]
Abstract
Organisms, in nature, are often subjected to multiple stressors, both biotic and abiotic. Temperature and starvation are among the main stressors experienced by organisms in their developmental cycle and the responses to these stressors may share signaling pathways, which affects the way these responses are manifested. Temperature is a major factor governing the performance of ectothermic organisms in ecosystems worldwide and, therefore, the thermal tolerance is a central issue in the thermobiology of these organisms. Here, we investigated the effects of starvation as well as mild heat and cold shocks on the thermal tolerance of the larvae of silkworm, Bombyx mori (Linnaeus). Starvation acted as a meaningful or positive stressor as it improved cold tolerance, measured as chill coma recovery time (CCRT), but, at the same time, it acted as a negative stressor and impaired the heat tolerance, measured as heat knockdown time (HKT). In the case of heat tolerance, starvation negated the positive effects of both mild cold as well as mild heat shocks and thus indicated the existence of trade-off between these stressors. Both mild heat and cold shocks improved the thermal tolerance, but the effects were more prominent when the indices were measured in response to a stressor of same type, i.e., a mild cold shock improved the cold tolerance more than the heat tolerance and vice versa. This improvement in thermal tolerance by both mild heat as well as cold shocks indicated the possibility of cross-tolerance between these stressors.
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Affiliation(s)
- A H Mir
- Section of Entomology, Dept of Zoology, Aligarh Muslim Univ, Aligarh, 202002, India.
| | - A Qamar
- Section of Entomology, Dept of Zoology, Aligarh Muslim Univ, Aligarh, 202002, India
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Brankatschk M, Gutmann T, Knittelfelder O, Palladini A, Prince E, Grzybek M, Brankatschk B, Shevchenko A, Coskun Ü, Eaton S. A Temperature-Dependent Switch in Feeding Preference Improves Drosophila Development and Survival in the Cold. Dev Cell 2018; 46:781-793.e4. [DOI: 10.1016/j.devcel.2018.05.028] [Citation(s) in RCA: 55] [Impact Index Per Article: 7.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/28/2017] [Revised: 03/17/2018] [Accepted: 08/27/2018] [Indexed: 01/01/2023]
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Nyamukondiwa C, Chidawanyika F, Machekano H, Mutamiswa R, Sands B, Mgidiswa N, Wall R. Climate variability differentially impacts thermal fitness traits in three coprophagic beetle species. PLoS One 2018; 13:e0198610. [PMID: 29874290 PMCID: PMC5991409 DOI: 10.1371/journal.pone.0198610] [Citation(s) in RCA: 25] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/09/2017] [Accepted: 05/22/2018] [Indexed: 01/10/2023] Open
Abstract
While the impacts of extreme and rising mean temperatures are well documented, increased thermal variability associated with climate change may also threaten ectotherm fitness and survival, but remains poorly explored. Using three wild collected coprophagic species Copris elphenor, Metacatharsius opacus and Scarabaeus zambezianus, we explored the effects of thermal amplitude around the mean on thermal tolerance. Using standardized protocols, we measured traits of high- (critical thermal maxima [CTmax] and heat knockdown time [HKDT]) and -low temperature tolerance (critical thermal minima [CTmin], chill coma recovery time [CCRT] and supercooling points [SCPs]) following variable temperature pulses (δ0, δ3, δ6 and δ9°C) around the mean (27°C). Our results show that increased temperature variability may offset basal and plastic responses to temperature and differs across species and metrics tested. Furthermore, we also show differential effects of body mass, body water content (BWC) and body lipid content (BLC) on traits of thermal tolerance. For example, body mass significantly influenced C. elphenor and S. zambezianus CTmax and S. zambezianus HKDT but not CTmin and CCRT. BWC significantly affected M. opacus and C. elphenor CTmax and in only M. opacus HKDT, CTmin and CCRT. Similarly, BLC only had a significant effect for M opacus CTmin. These results suggest differential and species dependent effects of climate variability of thermal fitness traits. It is therefore likely that the ecological services provided by these species may be constrained in the face of climate change. This implies that, to develop more realistic predictions for the effects of climate change on insect biodiversity and ecosystem function, thermal variability is a significant determinant.
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Affiliation(s)
- Casper Nyamukondiwa
- Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology (BIUST), Palapye, Botswana
- * E-mail:
| | - Frank Chidawanyika
- Agricultural Research Council, Plant Protection Research Institute, Weeds Division, Hilton, South Africa
- School of Lifesciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa
| | - Honest Machekano
- Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology (BIUST), Palapye, Botswana
| | - Reyard Mutamiswa
- Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology (BIUST), Palapye, Botswana
| | - Bryony Sands
- School of Biological Sciences, University of Bristol, United Kingdom
| | - Neludo Mgidiswa
- Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology (BIUST), Palapye, Botswana
| | - Richard Wall
- School of Biological Sciences, University of Bristol, United Kingdom
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Bar-Ziv MA, Scharf I. Thermal acclimation is not induced by habitat-of-origin, maintenance temperature, or acute exposure to low or high temperatures in a pit-building wormlion (Vermileo sp.). J Therm Biol 2018; 74:181-186. [PMID: 29801625 DOI: 10.1016/j.jtherbio.2018.03.024] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/14/2018] [Revised: 03/20/2018] [Accepted: 03/23/2018] [Indexed: 11/18/2022]
Abstract
Wormlions are sit-and-wait insect predators that construct pit-traps to capture arthropod prey. They require loose soil and shelter from direct sun, both common in Mediterranean cities, and explaining their high abundance in urban habitats. We studied different aspects of thermal acclimation in wormlions. We compared chill-coma recovery time (CCRT) and heat-shock recovery time (HSRT) of wormlions from urban, semi-urban and natural habitats, expecting those originating from the urban habitat to be more heat tolerant and less cold tolerant. However, no differences were detected among the three habitats. We then examined whether maintenance temperature affects CCRT and HSRT, and expected beneficial acclimation. However, CCRT was unaffected by maintenance temperature, while temperature affected HSRT in an opposite direction to our prediction: wormlions maintained under the higher temperatures took longer to recover. When testing with two successive thermal shocks, wormlions took longer to recover from both cold and heat shock after applying an initial cold shock. We therefore conclude that cold shock inflicts some damage rather than induces acclimation. Finally, both cold- and heat-shocked wormlions constructed smaller pits than wormlions of a control group. Smaller pits probably translate to a lower likelihood of capturing prey and also limit the size of the prey, indicating a concrete cost of thermal shock. In summary, we found no evidence for thermal acclimation related either to the habitat-of-origin or to maintenance temperatures, but, rather, negative effects of unfavorable temperatures.
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Affiliation(s)
- Michael A Bar-Ziv
- School of Zoology, Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel
| | - Inon Scharf
- School of Zoology, Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel.
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31
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Gilad T, Koren R, Moalem Y, Subach A, Scharf I. Effect of continuous and alternating episodes of starvation on behavior and reproduction in the red flour beetle. J Zool (1987) 2018. [DOI: 10.1111/jzo.12556] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
Affiliation(s)
- T. Gilad
- School of Zoology; Faculty of Life Sciences; Tel Aviv University; Tel Aviv Israel
| | - R. Koren
- School of Zoology; Faculty of Life Sciences; Tel Aviv University; Tel Aviv Israel
| | - Y. Moalem
- School of Zoology; Faculty of Life Sciences; Tel Aviv University; Tel Aviv Israel
| | - A. Subach
- School of Zoology; Faculty of Life Sciences; Tel Aviv University; Tel Aviv Israel
| | - I. Scharf
- School of Zoology; Faculty of Life Sciences; Tel Aviv University; Tel Aviv Israel
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32
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Sun PY, Foley HB, Wu L, Nguyen C, Chaudhry S, Bao VWW, Leung KMY, Edmands S. Long-term laboratory culture causes contrasting shifts in tolerance to two marine pollutants in copepods of the genus Tigriopus. ENVIRONMENTAL SCIENCE AND POLLUTION RESEARCH INTERNATIONAL 2018; 25:3183-3192. [PMID: 29019110 DOI: 10.1007/s11356-017-0398-z] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 05/16/2017] [Accepted: 10/02/2017] [Indexed: 06/07/2023]
Abstract
Organismal chemical tolerance is often used to assess ecological risk and monitor water quality, yet tolerance can differ between field- and lab-raised organisms. In this study, we examined how tolerance to copper (Cu) and tributyltin oxide (TBTO) in two species of marine copepods, Tigriopus japonicus and T. californicus, changed across generations under benign laboratory culture (in the absence of pre-exposure to chemicals). Both copepod species exhibited similar chemical-specific changes in tolerance, with laboratory maintenance resulting in increased Cu tolerance and decreased TBTO tolerance. To assess potential factors underlying these patterns, chemical tolerance was measured in conjunction with candidate environmental variables (temperature, UV radiation, diet type, and starvation). The largest chemical-specific effect was found for starvation, which decreased TBTO tolerance but had no effect on Cu tolerance. Understanding how chemical-specific tolerance can change in the laboratory will be critical in strengthening bioassays and their applications for environmental protection and chemical management.
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Affiliation(s)
- Patrick Y Sun
- Department of Biological Science and Wrigley Institute for Environmental Studies, University of Southern California, 3616 Trousdale PKWY STE 107, Los Angeles, CA, 90089, USA.
| | - Helen B Foley
- Department of Biological Science and Wrigley Institute for Environmental Studies, University of Southern California, 3616 Trousdale PKWY STE 107, Los Angeles, CA, 90089, USA
| | - Leslie Wu
- Department of Biological Science and Wrigley Institute for Environmental Studies, University of Southern California, 3616 Trousdale PKWY STE 107, Los Angeles, CA, 90089, USA
| | - Charlene Nguyen
- Department of Biological Science and Wrigley Institute for Environmental Studies, University of Southern California, 3616 Trousdale PKWY STE 107, Los Angeles, CA, 90089, USA
| | - Shiven Chaudhry
- Department of Biological Science and Wrigley Institute for Environmental Studies, University of Southern California, 3616 Trousdale PKWY STE 107, Los Angeles, CA, 90089, USA
| | - Vivien W W Bao
- The Swire Institute of Marine Science and School of Biological Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China
| | - Kenneth M Y Leung
- The Swire Institute of Marine Science and School of Biological Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China
- State Key Laboratory in Marine Pollution, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China
| | - Suzanne Edmands
- Department of Biological Science and Wrigley Institute for Environmental Studies, University of Southern California, 3616 Trousdale PKWY STE 107, Los Angeles, CA, 90089, USA
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33
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Matsumura T, Matsumoto H, Hayakawa Y. Heat stress hardening of oriental armyworms is induced by a transient elevation of reactive oxygen species during sublethal stress. ARCHIVES OF INSECT BIOCHEMISTRY AND PHYSIOLOGY 2017; 96:e21421. [PMID: 28872705 DOI: 10.1002/arch.21421] [Citation(s) in RCA: 22] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/07/2023]
Abstract
Pre-exposure to mild heat stress enhances the thermotolerance of insects. Stress hardening is a beneficial physiological plasticity, but the mechanism underlying it remains elusive. Here we report that reactive oxygen species (ROS) concentrations were quickly and transiently elevated in the armyworms, Mythimna separata, by exposing them to 40°C, but not other tested temperatures. Larvae exposed to 40°C had subsequently elevated antioxidant activity and the highest survival of all tested heating conditions. The elevation of ROS after lethal heating at 44°C for 1 h was approximately twofold compared to heating at 40°C. Injection of an optimal amount of hydrogen peroxide (H2 O2 ) similarly caused sequential elevation of ROS and antioxidant activity in the test larval hemolymph, which led to significantly enhanced survival after lethal heat stress. The H2 O2 -induced thermotolerance was abolished by coinjection of potent antioxidants such as ascorbic acid or N-acetylcysteine. Both preheating at 40°C and H2 O2 injection enhanced expression of genes encoding superoxide dismutase 1, catalase, and heat shock protein 70 in the fat body of test larvae, indicating the adequate heat stress induced a transient elevation of ROS, followed by upregulation of antioxidant activity. We infer that thermal stress hardening is induced by a small timely ROS elevation that triggers a reduction-oxidation signaling mechanism.
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Affiliation(s)
- Takashi Matsumura
- Department of Applied Biological Sciences, Saga University, Saga, Japan
| | - Hitoshi Matsumoto
- Department of Applied Biological Sciences, Saga University, Saga, Japan
| | - Yoichi Hayakawa
- Department of Applied Biological Sciences, Saga University, Saga, Japan
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34
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Alemu T, Alemneh T, Pertoldi C, Ambelu A, Bahrndorff S. Costs and benefits of heat and cold hardening in a soil arthropod. Biol J Linn Soc Lond 2017. [DOI: 10.1093/biolinnean/blx092] [Citation(s) in RCA: 21] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/13/2022]
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Dou W, Tian Y, Liu H, Shi Y, Smagghe G, Wang JJ. Characteristics of six small heat shock protein genes from Bactrocera dorsalis: Diverse expression under conditions of thermal stress and normal growth. Comp Biochem Physiol B Biochem Mol Biol 2017; 213:8-16. [PMID: 28735974 DOI: 10.1016/j.cbpb.2017.07.005] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/28/2017] [Revised: 07/11/2017] [Accepted: 07/17/2017] [Indexed: 11/29/2022]
Abstract
To explore the functions of small heat shock proteins (sHsps) in relation to thermal stress and development in Bactrocera dorsalis (Hendel), one of the most economically important pest species attacking a wide range of fruits and vegetables, six full-length cDNAs of sHsp genes (BdHsp17.7, 18.4, 20.4, 20.6, 21.6 and 23.8) were cloned, and the expression patterns in different developmental stages and tissues, as well as in response to both thermal and 20-hydroxyecdysone (20E) exposures, were examined using real time quantitative PCR. The open reading frames (ORFs) of six sHsps are 453, 489, 537, 543, 567 and 630bp in length, encoding proteins with molecular weights of 17.7, 18.4, 20.4, 20.6, 21.6 and 23.8kDa, respectively. BdHsp18.4 and BdHsp20.4 maintained lower expression levels in both eggs and larvae, whereas remarkably up-regulated after the larval-pupal transformation, suggesting that these two sHsps may be involved in metamorphosis. Significant tissue specificity exists among sHsps: the highest expression of BdHsp20.6 and BdHsp23.8 in the Malpighian tubules and ovary, respectively, versus a peak in the fat body for others. BdHsp20.4 and BdHsp20.6 were significantly up-regulated by thermal stress. In contrast, BdHsp18.4 and BdHsp23.8 reacted only to heat stress. BdHsp17.7 and BdHsp21.6 were insensitive to both heat and cold stresses. The degree of sHsps response depends on intensity of 20E treatment, i.e., dose and time. These results strongly suggest functional differentiation within the sHsp subfamily in B. dorsalis. The physiological function of sHsp members under thermal stress and normal growth remains the subjects of further investigation.
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Affiliation(s)
- Wei Dou
- Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400715, China.
| | - Yi Tian
- Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400715, China.
| | - Hong Liu
- Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400715, China.
| | - Yan Shi
- Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400715, China.
| | - Guy Smagghe
- Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400715, China; Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, B-9000 Ghent, Belgium.
| | - Jin-Jun Wang
- Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400715, China.
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Xiao W, Chen P, Xiao J, Wang L, Liu T, Wu Y, Dong F, Jiang Y, Pan M, Zhang Y, Lu C. Comparative transcriptome profiling of a thermal resistant vs. sensitive silkworm strain in response to high temperature under stressful humidity condition. PLoS One 2017; 12:e0177641. [PMID: 28542312 PMCID: PMC5436693 DOI: 10.1371/journal.pone.0177641] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/15/2017] [Accepted: 05/01/2017] [Indexed: 11/25/2022] Open
Abstract
Thermotolerance is important particularly for poikilotherms such as insects. Understanding the mechanisms by which insects respond to high temperatures can provide insights into their adaptation to the environment. Therefore, in this study, we performed a transcriptome analysis of two silkworm strains with significantly different resistance to heat as well as humidity; the thermo-resistant strain 7532 and the thermos-sensitive strain Knobbed. We identified in total 4,944 differentially expressed genes (DEGs) using RNA-Seq. Among these, 4,390 were annotated and 554 were novel. Gene Ontology (GO) analysis of 747 DEGs identified between RT_48h (Resistant strain with high-temperature Treatment for 48 hours) and ST_48h (Sensitive strain with high-temperature Treatment for 48 hours) showed significant enrichment of 12 GO terms including metabolic process, extracellular region and serine-type peptidase activity. Moreover, we discovered 12 DEGs that may contribute to the heat-humidity stress response in the silkworm. Our data clearly showed that 48h post-exposure may be a critical time point for silkworm to respond to high temperature and humidity. These results provide insights into the genes and biological processes involved in high temperature and humidity tolerance in the silkworm, and advance our understanding of thermal tolerance in insects.
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Affiliation(s)
- Wenfu Xiao
- State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture, Southwest University, Chongqing, China
- Sericultural Research Institute Sichuan Academy of Agricultural Sciences, Sichuan Nanchong, China
| | - Peng Chen
- State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture, Southwest University, Chongqing, China
| | - Jinshu Xiao
- Sericultural Research Institute Sichuan Academy of Agricultural Sciences, Sichuan Nanchong, China
| | - La Wang
- State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture, Southwest University, Chongqing, China
| | - Taihang Liu
- State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture, Southwest University, Chongqing, China
| | - Yunfei Wu
- State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture, Southwest University, Chongqing, China
| | - Feifan Dong
- State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture, Southwest University, Chongqing, China
| | - Yaming Jiang
- State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture, Southwest University, Chongqing, China
| | - Minhui Pan
- State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture, Southwest University, Chongqing, China
| | - Youhong Zhang
- Sericultural Research Institute Sichuan Academy of Agricultural Sciences, Sichuan Nanchong, China
- * E-mail: (CL); (YZ)
| | - Cheng Lu
- State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture, Southwest University, Chongqing, China
- * E-mail: (CL); (YZ)
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Enriquez T, Colinet H. Basal tolerance to heat and cold exposure of the spotted wing drosophila, Drosophila suzukii. PeerJ 2017; 5:e3112. [PMID: 28348931 PMCID: PMC5366067 DOI: 10.7717/peerj.3112] [Citation(s) in RCA: 54] [Impact Index Per Article: 6.8] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/24/2016] [Accepted: 02/21/2017] [Indexed: 11/20/2022] Open
Abstract
The spotted wing Drosophila, Drosophila suzukii, is a new pest in Europe and America which causes severe damages, mostly to stone fruit crops. Temperature and humidity are among the most important abiotic factors governing insect development and fitness. In many situations, temperature can become stressful thus compromising survival. The ability to cope with thermal stress depends on basal level of thermal tolerance. Basic knowledge on temperature-dependent mortality of D. suzukii is essential to facilitate management of this pest. The objective of the present study was to investigate D. suzukii basal cold and heat tolerance. Adults and pupae were subjected to six low temperatures (-5-7.5 °C) and seven high temperatures (30-37 °C) for various durations, and survival-time-temperature relationships were investigated. Data showed that males were globally more cold tolerant than females. At temperature above 5 °C, adult cold mortality became minor even after prolonged exposures (e.g., only 20% mortality after one month at 7.5 °C). Heat tolerance of males was lower than that of females at the highest tested temperatures (34, 35 and 37 °C). Pupae appeared much less cold tolerant than adults at all temperatures (e.g., Lt50 at 5° C: 4-5 d for adults vs. 21 h for pupae). Pupae were more heat tolerant than adults at the most extreme high temperatures (e.g., Lt50 at 37 °C: 30 min for adults vs. 4 h for pupae). The pupal thermal tolerance was further investigated under low vs. high humidity. Low relative humidity did not affect pupal cold survival, but it reduced survival under heat stress. Overall, this study shows that survival of D. suzukii under heat and cold conditions can vary with stress intensity, duration, humidity, sex and stage, and the methodological approach used here, which was based on thermal tolerance landscapes, provides a comprehensive description of D. suzukiithermal tolerance and limits.
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Affiliation(s)
- Thomas Enriquez
- Université de Rennes I, UMR CNRS 6553 ECOBIO, Rennes, France
| | - Hervé Colinet
- Université de Rennes I, UMR CNRS 6553 ECOBIO, Rennes, France
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Manenti T, Sørensen JG, Moghadam NN, Loeschcke V. Few genetic and environmental correlations between life history and stress resistance traits affect adaptation to fluctuating thermal regimes. Heredity (Edinb) 2016; 117:149-54. [PMID: 27273321 DOI: 10.1038/hdy.2016.34] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/13/2015] [Revised: 03/14/2016] [Accepted: 03/30/2016] [Indexed: 11/09/2022] Open
Abstract
Laboratory selection in thermal regimes that differed in the amplitude and the predictability of daily fluctuations had a marked effect on stress resistance and life history traits in Drosophila simulans. The observed evolutionary changes are expected to be the result of both direct and correlated responses to selection. Thus, a given trait might not evolve independently from other traits because of genetic correlations among these traits. Moreover, different test environments can induce novel genetic correlations because of the activation of environmentally dependent genes. To test whether and how genetic correlations among stress resistance and life history traits constrain evolutionary adaptation, we used three populations of D. simulans selected for 20 generations in constant, predictable and unpredictable daily fluctuating thermal regimes and tested each of these selected populations in the same three thermal regimes. We explored the relationship between genetic correlations between traits and the evolutionary potential of D. simulans by comparing genetic correlation matrices in flies selected and tested in different thermal test regimes. We observed genetic correlations mainly between productivity, body size, starvation and desiccation tolerance, suggesting that adaptation to the three thermal regimes was affected by correlations between these traits. We also found that the correlations between some traits such as body size and productivity or starvation tolerance and productivity were determined by test regime rather than selection regime that is expected to limit genetic adaptation to thermal regimes in these traits. The results of this study suggest that several traits and several environments are needed to explore adaptive responses, as genetic and environmentally induced correlations between traits as results obtained in one environment cannot be used to predict the response of the same population in another environment.
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Affiliation(s)
- T Manenti
- Section for Genetics, Ecology and Evolution, Department of Bioscience, Aarhus University, Aarhus, Denmark
| | - J G Sørensen
- Section for Genetics, Ecology and Evolution, Department of Bioscience, Aarhus University, Aarhus, Denmark
| | - N N Moghadam
- Section for Genetics, Ecology and Evolution, Department of Bioscience, Aarhus University, Aarhus, Denmark
| | - V Loeschcke
- Section for Genetics, Ecology and Evolution, Department of Bioscience, Aarhus University, Aarhus, Denmark
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39
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The negative effect of starvation and the positive effect of mild thermal stress on thermal tolerance of the red flour beetle, Tribolium castaneum. Naturwissenschaften 2016; 103:20. [DOI: 10.1007/s00114-016-1344-5] [Citation(s) in RCA: 35] [Impact Index Per Article: 3.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/11/2015] [Revised: 02/02/2016] [Accepted: 02/04/2016] [Indexed: 11/26/2022]
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40
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Fisker KV, Holmstrup M, Sørensen JG. Freezing of body fluids induces metallothionein gene expression in earthworms (Dendrobaena octaedra). Comp Biochem Physiol C Toxicol Pharmacol 2016; 179:44-8. [PMID: 26325206 DOI: 10.1016/j.cbpc.2015.08.008] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/10/2015] [Revised: 08/14/2015] [Accepted: 08/23/2015] [Indexed: 12/22/2022]
Abstract
The molecular mechanisms activated by environmental contaminants and natural stressors such as freezing need to be investigated in order to better understand the mechanisms of interaction and potential effects that combined stressors may have on organisms. Using the freeze-tolerant earthworm Dendrobaena octaedra as model species, we exposed worms to freezing and exposure to sublethal copper in a factorial design and investigated the transcription of candidate genes for metal and cold stress. We hypothesised that both freezing and copper would induce transcription of genes coding for heat shock proteins (hsp10 and hsp70), metallothioneins (mt1 and mt2), and glutathione-S-transferase (gst), and that the combined effects of these two stressors would be additive. The gene transcripts hsp10, hsp70, and gst were significantly upregulated by freezing, but only hsp10 was upregulated by copper. We found that copper at the time of sampling had no effect on transcription of two metallothionein genes whereas transcription was strongly upregulated by freezing. Moreover, there was a significant interaction causing more than additive transcription rates of mt1 in the copper/freezing treatment suggesting that freeze-induced cellular dehydration increases the concentration of free copper ions in the cytosol. This metallothionein response to freezing is likely adaptive and possibly provides protection against freeze-induced elevated metal concentrations in the cytosol and excess ROS levels due to hypoxia during freezing.
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Affiliation(s)
- Karina Vincents Fisker
- Section of Soil Fauna Ecology and Ecotoxicology, Department of Bioscience, Aarhus University, Vejlsøvej 25, DK-8600 Silkeborg, Denmark
| | - Martin Holmstrup
- Section of Soil Fauna Ecology and Ecotoxicology, Department of Bioscience, Aarhus University, Vejlsøvej 25, DK-8600 Silkeborg, Denmark.
| | - Jesper Givskov Sørensen
- Section of Genetics, Ecology and Evolution, Department of Bioscience, Aarhus University, Ny Munkegade 116, DK-8000 Aarhus C, Denmark
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41
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Shang Q, Pan Y, Peng T, Yang S, Lu X, Wang Z, Xi J. PROTEOMICS ANALYSIS OF OVEREXPRESSED PLASMA PROTEINS IN RESPONSE TO COLD ACCLIMATION IN Ostrinia furnacalis. ARCHIVES OF INSECT BIOCHEMISTRY AND PHYSIOLOGY 2015; 90:195-208. [PMID: 26440752 DOI: 10.1002/arch.21302] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/05/2023]
Abstract
Many insects in temperate regions overwinter in diapause. In these insects, one of the metabolic adaptations to cold stress is the synthesis of responsive proteins. Using proteomic analysis, an investigation aimed to a better understanding of the molecular adaptation mechanisms to cold stress was carried out in Ostrinia furnacalis larva. Proteins were extracted from the larval hemolymph collected from both control and overwintering larva. By polyethylene glycol precipitation, approximately 560 protein spots were separated and visualized on two-dimensional (2D) gels after silver staining. Eighteen protein spots were found to be upregulated in overwinter larval plasma in different patterns. As an initial work, 13 of these proteins were identified using MALDI TOF/TOF MS. The differentially overexpressed proteins include heat shock 70 kDa cognate protein, small heat shock protein (sHSP), putative aliphatic nitrilase, arginine kinase, phosphoglyceromutase, triosephosphateisomerase, and glutathione transferase. Alterations in the levels of these proteins were further confirmed by qPCR. This study is the first analysis of differentially expressed plasma proteins in O. furnacalis diapause larvae under extremely low temperature conditions and gives new insights into the acclimation mechanisms responsive to cold stress. Our results also support the idea that energy metabolism, alanine and proline metabolism, and antioxidative reaction act in the cold acclimation of O. furnacalis diapause larvae.
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Affiliation(s)
- Qingli Shang
- College of Plant Science, Jilin University, Changchun, P.R. China
| | - Yiou Pan
- College of Plant Science, Jilin University, Changchun, P.R. China
| | - Tianfei Peng
- College of Plant Science, Jilin University, Changchun, P.R. China
| | - Shuang Yang
- College of Plant Science, Jilin University, Changchun, P.R. China
| | - Xin Lu
- Jilin Academy of Agricultural Sciences, Changchun, P.R. China
| | - Zhenying Wang
- The State Key Lab for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Science, Beijing, P.R. China
| | - Jinghui Xi
- College of Plant Science, Jilin University, Changchun, P.R. China
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42
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Boardman L, Sørensen JG, Terblanche JS. Physiological and molecular mechanisms associated with cross tolerance between hypoxia and low temperature in Thaumatotibia leucotreta. JOURNAL OF INSECT PHYSIOLOGY 2015; 82:75-84. [PMID: 26376454 DOI: 10.1016/j.jinsphys.2015.09.001] [Citation(s) in RCA: 12] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 05/20/2015] [Revised: 07/24/2015] [Accepted: 09/03/2015] [Indexed: 06/05/2023]
Abstract
Biochemical adaptations allow insects to withstand exposures to hypoxia and/or hypothermia. Exposure to hypoxia may interact either synergistically or antagonistically with standard low temperature stress responses yet this has not been systematically researched and no clear mechanism has been identified to date. Using larvae of false codling moth Thaumatotibia leucotreta, a pest of southern Africa, we investigated the physiological and molecular responses to hypoxia or temperature stress pre-treatments, followed by a standard low temperature exposure. Survival rates were significantly influenced by pre-treatment conditions, although T. leucotreta shows relatively high basal resistance to various stressors (4% variation in larval survival across all pre-treatments). Results showed that mild pre-treatments with chilling and hypoxia increased resistance to low temperatures and that these responses were correlated with increased membrane fluidity (increased UFA:SFA) and/or alterations in heat shock protein 70 (HSP70); while general mechanical stress (shaking) and heat (2h at 35°C) do not elicit cross tolerance (no change in survival or molecular responses). We therefore found support for some limited cold hardening and cross tolerance responses. Given that combined exposure to hypoxia and low temperature is used to sterilize commodities in post-harvest pest management programs, researchers can now exploit these mechanisms involved in cross tolerance to develop more targeted control methods.
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Affiliation(s)
- Leigh Boardman
- Department of Conservation Ecology and Entomology, Centre for Invasion Biology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa.
| | - Jesper G Sørensen
- Section for Genetics, Ecology & Evolution, Department of Bioscience, Aarhus University, Ny Munkegade 116, DK-8000 Aarhus C, Denmark
| | - John S Terblanche
- Department of Conservation Ecology and Entomology, Centre for Invasion Biology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
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43
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Hangartner S, Hoffmann AA. Evolutionary potential of multiple measures of upper thermal tolerance in
D
rosophila melanogaster. Funct Ecol 2015. [DOI: 10.1111/1365-2435.12499] [Citation(s) in RCA: 60] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
Affiliation(s)
- Sandra Hangartner
- School of BioSciences The University of Melbourne 30 Flemington Road Parkville Vic.3010 Australia
- School of Biological Sciences Monash University, Clayton Campus Building 18Vic.3800 Australia
| | - Ary A. Hoffmann
- School of BioSciences The University of Melbourne 30 Flemington Road Parkville Vic.3010 Australia
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44
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Tungjitwitayakul J, Tatun N, Vajarasathira B, Sakurai S. Expression of Heat Shock Protein Genes in Different Developmental Stages and After Temperature Stress in the Maize Weevil (Coleoptera: Curculionidae). JOURNAL OF ECONOMIC ENTOMOLOGY 2015; 108:1313-1323. [PMID: 26470260 DOI: 10.1093/jee/tov051] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/22/2014] [Accepted: 02/16/2015] [Indexed: 06/05/2023]
Abstract
The maize weevil, Sitophilus zeamais Motschulsky, is a major pest of rice and other postharvest grain stocks in tropical countries. Heating and cooling treatments have been adopted to control this pest. Because heat shock protein (hsp) genes respond to temperature stress, we examined the association of hsp genes with development and thermal stress in S. zeamais. The temperature response of the insect to heat and cold treatments was assessed at four developmental stages: egg, larva, pupa, and adult. LT50 values at high temperatures were similar among the four developmental stages, while adults were the most tolerant to low temperatures, and eggs, larvae, and pupae exhibited similar LT50 values. Expression levels of three hsps--Szhsp70, Szhsc70, and Szhsp90--fluctuated substantially throughout the four stages at a rearing temperature of 28°C. Heat shock and cold shock increased the expression of all three hsps, and the highest upregulation was observed at 40°C, although the intensity of upregulation varied among the three genes: strongly in Szhsp70, moderately in Szhsp90, and slightly in Szhsc70. Basal expression of the three hsps at 28°C and gene responses to heat and cold shock also varied significantly at the tissue level.
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Affiliation(s)
| | - Nujira Tatun
- School of Science, University of Phayao, Phayao 56000, Thailand
| | - Boongeua Vajarasathira
- Department of Zoology, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand
| | - Sho Sakurai
- Creative Science Museum, Komatsunomori, Komatsu 923-8610, Japan
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45
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Abstract
Insect heat shock proteins include ATP-independent small heat shock proteins and the larger ATP-dependent proteins, Hsp70, Hsp90, and Hsp60. In concert with cochaperones and accessory proteins, heat shock proteins mediate essential activities such as protein folding, localization, and degradation. Heat shock proteins are synthesized constitutively in insects and induced by stressors such as heat, cold, crowding, and anoxia. Synthesis depends on the physiological state of the insect, but the common function of heat shock proteins, often working in networks, is to maintain cell homeostasis through interaction with substrate proteins. Stress-induced expression of heat shock protein genes occurs in a background of protein synthesis inhibition, but in the course of diapause, a state of dormancy and increased stress tolerance, these genes undergo differential regulation without the general disruption of protein production. During diapause, when ATP concentrations are low, heat shock proteins may sequester rather than fold proteins.
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Affiliation(s)
- Allison M King
- Department of Biology, Dalhousie University, Halifax, NS, B3H 4R2, Canada; ,
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46
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Hariharan R, Hoffman JM, Thomas AS, Soltow QA, Jones DP, Promislow DEL. Invariance and plasticity in the Drosophila melanogaster metabolomic network in response to temperature. BMC SYSTEMS BIOLOGY 2014; 8:139. [PMID: 25540032 PMCID: PMC4302152 DOI: 10.1186/s12918-014-0139-6] [Citation(s) in RCA: 18] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 08/19/2014] [Accepted: 12/11/2014] [Indexed: 12/31/2022]
Abstract
Background Metabolomic responses to extreme thermal stress have recently been investigated in Drosophila melanogaster. However, a network level understanding of metabolomic responses to longer and less drastic temperature changes, which more closely reflect variation in natural ambient temperatures experienced during development and adulthood, is currently lacking. Here we use high-resolution, non-targeted metabolomics to dissect metabolomic changes in D. melanogaster elicited by moderately cool (18°C) or warm (27°C) developmental and adult temperature exposures. Results We find that temperature at which larvae are reared has a dramatic effect on metabolomic network structure measured in adults. Using network analysis, we are able to identify modules that are highly differentially expressed in response to changing developmental temperature, as well as modules whose correlation structure is strongly preserved across temperature. Conclusions Our results suggest that the effect of temperature on the metabolome provides an easily studied and powerful model for understanding the forces that influence invariance and plasticity in biological networks. Electronic supplementary material The online version of this article (doi:10.1186/s12918-014-0139-6) contains supplementary material, which is available to authorized users.
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Affiliation(s)
- Ramkumar Hariharan
- Department of Pathology, University of Washington, Box 357705, Seattle, WA, 98195, USA. .,Laboratory for Integrated Bioinformatics, RIKEN Center for Integrative Medical Sciences, Yokohama, Kanagawa, 230-0045, Japan.
| | - Jessica M Hoffman
- Department of Genetics, University of Georgia, Athens, GA, 30602, USA.
| | - Ariel S Thomas
- Department of Genetics, University of Georgia, Athens, GA, 30602, USA. .,Washington University School of Medicine, 660 S. Euclid Avenue, St. Louis, MO, 63108, USA.
| | - Quinlyn A Soltow
- Division of Pulmonary Allergy & Critical Care Medicine, Emory University, Atlanta, GA, 30322, USA. .,Department of Medicine, Clinical Biomarkers Laboratory, Emory University, Atlanta, GA, 30322, USA. .,ClinMet Inc, 3210 Merryfield Row, San Diego, CA, 92121, USA.
| | - Dean P Jones
- Division of Pulmonary Allergy & Critical Care Medicine, Emory University, Atlanta, GA, 30322, USA. .,Department of Medicine, Clinical Biomarkers Laboratory, Emory University, Atlanta, GA, 30322, USA.
| | - Daniel E L Promislow
- Department of Pathology, University of Washington, Box 357705, Seattle, WA, 98195, USA. .,Department of Biology, University of Washington, Seattle, WA, 98195, USA.
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47
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Scharf I, Galkin N, Halle S. Disentangling the Consequences of Growth Temperature and Adult Acclimation Temperature on Starvation and Thermal Tolerance in the Red Flour Beetle. Evol Biol 2014. [DOI: 10.1007/s11692-014-9298-z] [Citation(s) in RCA: 24] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/18/2023]
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48
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Parker CD, Prins C, Saliba C, Gutierrez G, Serrar M. Effect of TEX-OE®treatment on the development of heat shock proteins in commercial broiler chicks and the impact on performance indicators in the grow-out period. Br Poult Sci 2014; 55:592-7. [DOI: 10.1080/00071668.2014.956287] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/24/2022]
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49
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Manenti T, Sørensen JG, Moghadam NN, Loeschcke V. Predictability rather than amplitude of temperature fluctuations determines stress resistance in a natural population of Drosophila simulans. J Evol Biol 2014; 27:2113-22. [DOI: 10.1111/jeb.12463] [Citation(s) in RCA: 53] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/15/2014] [Revised: 07/12/2014] [Accepted: 07/15/2014] [Indexed: 11/30/2022]
Affiliation(s)
- T. Manenti
- Section for Genetics, Ecology and Evolution; Department of Bioscience; Aarhus University; Aarhus C Denmark
| | - J. G. Sørensen
- Section for Genetics, Ecology and Evolution; Department of Bioscience; Aarhus University; Aarhus C Denmark
| | - N. N. Moghadam
- Section for Genetics, Ecology and Evolution; Department of Bioscience; Aarhus University; Aarhus C Denmark
| | - V. Loeschcke
- Section for Genetics, Ecology and Evolution; Department of Bioscience; Aarhus University; Aarhus C Denmark
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50
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Song HM, Mu XD, Gu DE, Luo D, Yang YX, Xu M, Luo JR, Zhang JE, Hu YC. Molecular characteristics of the HSP70 gene and its differential expression in female and male golden apple snails (Pomacea canaliculata) under temperature stimulation. Cell Stress Chaperones 2014; 19:579-89. [PMID: 24368711 PMCID: PMC4041941 DOI: 10.1007/s12192-013-0485-0] [Citation(s) in RCA: 24] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/11/2013] [Revised: 12/05/2013] [Accepted: 12/06/2013] [Indexed: 01/09/2023] Open
Abstract
Heat-shock protein 70 (HSP70) is one of the most important heat-shock proteins that helps organisms to modulate stress response via over-expression. The HSP70 gene from Pomacea canaliculata was cloned using the RACE approach; the gene is 2,767 bp in length and contains an open reading frame of 1,932 bp, which is encoded by a polypeptide of 643 amino acids. BLAST analysis showed that the predicted amino acid sequence of the P. canaliculata HSP70 gene shared a relatively high similarity with that of other known eukaryotic species that display conserved HSP characteristics. The phylogeny demonstrated a separate clustering of the apple snail HSP70 with other constitutive members from other mollusk species. Quantitative real-time RT-PCR was used to detect the differential expression of HSP70 in both sexes of P. canaliculata at different temperature conditions. These results showed that HSP70 transcript levels decreased slightly under cold shock and increased significantly under heat-shock conditions in both sexes compared to normal temperatures (26 °C). Under cold-shock treatment, the sex effect was not significant. With heat treatment, HSP70 expression could be induced at 36 °C in both females and males, and it peaked at 42 and 39 °C in females and males, respectively. In addition, a clear time-dependent HSP70 expression pattern of the apple snail exposed to the same high temperature (36 °C) was observed at different time points. The maximal induction of HSP70 expression appeared at 12 and 48 h in males and females after heat shock, respectively. The maximal induction in females was significantly higher compared to males under heat stimulus. Taken together, these results strongly suggested that males were more susceptible to heat than females and provided useful molecular information for the ecological adaptability of P. canaliculata against extreme environmental stress.
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Affiliation(s)
- Hong-Mei Song
- />Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Guangzhou, Guangdong 510380 China
| | - Xi-Dong Mu
- />Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Guangzhou, Guangdong 510380 China
| | - Dang-En Gu
- />Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Guangzhou, Guangdong 510380 China
| | - Du Luo
- />Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Guangzhou, Guangdong 510380 China
| | - Ye-Xin Yang
- />Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Guangzhou, Guangdong 510380 China
| | - Meng Xu
- />Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Guangzhou, Guangdong 510380 China
| | - Jian-Ren Luo
- />Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Guangzhou, Guangdong 510380 China
| | - Jia-En Zhang
- />Department of Ecology, College of Agriculture, South China Agricultural University, Key Laboratory of Ecological Agriculture, Guangzhou, 510642 China
| | - Yin-Chang Hu
- />Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Guangzhou, Guangdong 510380 China
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