Expression of thermal tolerance genes in two Drosophila species with different acclimation capacities

Jesper Givskov Sørensen; Marta Puig Giribets; Rosa Tarrío; Francisco Rodríguez-Trelles; Mads Fristrup Schou; Volker Loeschcke

doi:10.1016/j.jtherbio.2019.07.005

Expression of thermal tolerance genes in two Drosophila species with different acclimation capacities

Jesper Givskov Sørensen^*, Marta Puig Giribets, Rosa Tarrío, Francisco Rodríguez-Trelles, Mads Fristrup Schou, Volker Loeschcke

^*Corresponding author af dette arbejde

Institut for Biologi - Genetik, økologi og evolution

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

19 Citationer (Scopus)

Abstract

Heat tolerance increases at higher acclimation temperatures in D. melanogaster, but not in D. subobscura. The two species represent separate lineages of the subgenus Sophophora of Drosophila with contrasting tropical African and temperate Palearctic evolutionary histories. D. melanogaster has five copies of the inducible hsp70 gene distributed in two clusters, named A (with two copies) and B (three copies), while D. subobscura has only two copies arranged similarly to cluster A of D. melanogaster. The hsp70s of the two species also differ in their cis-regulatory regions, with D. melanogaster exhibiting features of a faster and more productive promoter. We predicted that the interspecific variation in acclimation capacity of heat tolerance is explained by evolved variation in expression of the major group of heat shock proteins. To test this prediction, we compared basal levels of gene expression at different developmental temperatures within each of the two species. Furthermore, we explored the heat hardening dynamics by measuring the induction of gene expression during a ramping assay. The prediction of a stronger heat shock protein response in D. melanogaster as compared to D. subobscura was confirmed for both long-term acclimation and short-term hardening. For D. melanogaster the upregulation with temperature ramping ranged from less than two fold (hsp26) to 2500 fold (hsp70A) increase. In all cases induction in D. melanogaster exceeded that of D. subobscura homologs. These differences correlate with structural differences in the regulatory regions of hsp70, and might explain differences in acclimation capacity among species. Finally, in D. melanogaster we found an indication of an inverse relationship between basal and induced levels of hsp70A and hsp83 expression, suggesting a divergent role for thermal adaptation of these genes at benign and stressful temperatures, respectively. Summary statement. Drosophila melanogaster and D. subobscura differ in heat shock protein expression levels, likely mediated by evolved differences in promoter regions. This corroborates differences in acclimation capacities between the two species.

Originalsprog	Engelsk
Tidsskrift	Journal of Thermal Biology
Vol/bind	84
Sider (fra-til)	200-207
Antal sider	8
ISSN	0306-4565
DOI	https://doi.org/10.1016/j.jtherbio.2019.07.005
Status	Udgivet - 2019

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Citationsformater

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title = "Expression of thermal tolerance genes in two Drosophila species with different acclimation capacities",

abstract = "Heat tolerance increases at higher acclimation temperatures in D. melanogaster, but not in D. subobscura. The two species represent separate lineages of the subgenus Sophophora of Drosophila with contrasting tropical African and temperate Palearctic evolutionary histories. D. melanogaster has five copies of the inducible hsp70 gene distributed in two clusters, named A (with two copies) and B (three copies), while D. subobscura has only two copies arranged similarly to cluster A of D. melanogaster. The hsp70s of the two species also differ in their cis-regulatory regions, with D. melanogaster exhibiting features of a faster and more productive promoter. We predicted that the interspecific variation in acclimation capacity of heat tolerance is explained by evolved variation in expression of the major group of heat shock proteins. To test this prediction, we compared basal levels of gene expression at different developmental temperatures within each of the two species. Furthermore, we explored the heat hardening dynamics by measuring the induction of gene expression during a ramping assay. The prediction of a stronger heat shock protein response in D. melanogaster as compared to D. subobscura was confirmed for both long-term acclimation and short-term hardening. For D. melanogaster the upregulation with temperature ramping ranged from less than two fold (hsp26) to 2500 fold (hsp70A) increase. In all cases induction in D. melanogaster exceeded that of D. subobscura homologs. These differences correlate with structural differences in the regulatory regions of hsp70, and might explain differences in acclimation capacity among species. Finally, in D. melanogaster we found an indication of an inverse relationship between basal and induced levels of hsp70A and hsp83 expression, suggesting a divergent role for thermal adaptation of these genes at benign and stressful temperatures, respectively. Summary statement. Drosophila melanogaster and D. subobscura differ in heat shock protein expression levels, likely mediated by evolved differences in promoter regions. This corroborates differences in acclimation capacities between the two species.",

keywords = "Drosophila melanogaster, Drosophila subobscura, Gene expression, Heat tolerance, Hsp, Plasticity",

author = "S{\o}rensen, {Jesper Givskov} and Giribets, {Marta Puig} and Rosa Tarr{\'i}o and Francisco Rodr{\'i}guez-Trelles and Schou, {Mads Fristrup} and Volker Loeschcke",

year = "2019",

doi = "10.1016/j.jtherbio.2019.07.005",

language = "English",

volume = "84",

pages = "200--207",

journal = "Journal of Thermal Biology",

issn = "0306-4565",

publisher = "Elsevier Ltd",

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TY - JOUR

T1 - Expression of thermal tolerance genes in two Drosophila species with different acclimation capacities

AU - Sørensen, Jesper Givskov

AU - Giribets, Marta Puig

AU - Tarrío, Rosa

AU - Rodríguez-Trelles, Francisco

AU - Schou, Mads Fristrup

AU - Loeschcke, Volker

PY - 2019

Y1 - 2019

N2 - Heat tolerance increases at higher acclimation temperatures in D. melanogaster, but not in D. subobscura. The two species represent separate lineages of the subgenus Sophophora of Drosophila with contrasting tropical African and temperate Palearctic evolutionary histories. D. melanogaster has five copies of the inducible hsp70 gene distributed in two clusters, named A (with two copies) and B (three copies), while D. subobscura has only two copies arranged similarly to cluster A of D. melanogaster. The hsp70s of the two species also differ in their cis-regulatory regions, with D. melanogaster exhibiting features of a faster and more productive promoter. We predicted that the interspecific variation in acclimation capacity of heat tolerance is explained by evolved variation in expression of the major group of heat shock proteins. To test this prediction, we compared basal levels of gene expression at different developmental temperatures within each of the two species. Furthermore, we explored the heat hardening dynamics by measuring the induction of gene expression during a ramping assay. The prediction of a stronger heat shock protein response in D. melanogaster as compared to D. subobscura was confirmed for both long-term acclimation and short-term hardening. For D. melanogaster the upregulation with temperature ramping ranged from less than two fold (hsp26) to 2500 fold (hsp70A) increase. In all cases induction in D. melanogaster exceeded that of D. subobscura homologs. These differences correlate with structural differences in the regulatory regions of hsp70, and might explain differences in acclimation capacity among species. Finally, in D. melanogaster we found an indication of an inverse relationship between basal and induced levels of hsp70A and hsp83 expression, suggesting a divergent role for thermal adaptation of these genes at benign and stressful temperatures, respectively. Summary statement. Drosophila melanogaster and D. subobscura differ in heat shock protein expression levels, likely mediated by evolved differences in promoter regions. This corroborates differences in acclimation capacities between the two species.

AB - Heat tolerance increases at higher acclimation temperatures in D. melanogaster, but not in D. subobscura. The two species represent separate lineages of the subgenus Sophophora of Drosophila with contrasting tropical African and temperate Palearctic evolutionary histories. D. melanogaster has five copies of the inducible hsp70 gene distributed in two clusters, named A (with two copies) and B (three copies), while D. subobscura has only two copies arranged similarly to cluster A of D. melanogaster. The hsp70s of the two species also differ in their cis-regulatory regions, with D. melanogaster exhibiting features of a faster and more productive promoter. We predicted that the interspecific variation in acclimation capacity of heat tolerance is explained by evolved variation in expression of the major group of heat shock proteins. To test this prediction, we compared basal levels of gene expression at different developmental temperatures within each of the two species. Furthermore, we explored the heat hardening dynamics by measuring the induction of gene expression during a ramping assay. The prediction of a stronger heat shock protein response in D. melanogaster as compared to D. subobscura was confirmed for both long-term acclimation and short-term hardening. For D. melanogaster the upregulation with temperature ramping ranged from less than two fold (hsp26) to 2500 fold (hsp70A) increase. In all cases induction in D. melanogaster exceeded that of D. subobscura homologs. These differences correlate with structural differences in the regulatory regions of hsp70, and might explain differences in acclimation capacity among species. Finally, in D. melanogaster we found an indication of an inverse relationship between basal and induced levels of hsp70A and hsp83 expression, suggesting a divergent role for thermal adaptation of these genes at benign and stressful temperatures, respectively. Summary statement. Drosophila melanogaster and D. subobscura differ in heat shock protein expression levels, likely mediated by evolved differences in promoter regions. This corroborates differences in acclimation capacities between the two species.

KW - Drosophila melanogaster

KW - Drosophila subobscura

KW - Gene expression

KW - Heat tolerance

KW - Hsp

KW - Plasticity

UR - http://www.scopus.com/inward/record.url?scp=85068447358&partnerID=8YFLogxK

U2 - 10.1016/j.jtherbio.2019.07.005

DO - 10.1016/j.jtherbio.2019.07.005

M3 - Journal article

C2 - 31466754

AN - SCOPUS:85068447358

SN - 0306-4565

VL - 84

SP - 200

EP - 207

JO - Journal of Thermal Biology

JF - Journal of Thermal Biology

ER -

Expression of thermal tolerance genes in two Drosophila species with different acclimation capacities

Abstract

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