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

Sørensen, Jesper Givskov; Giribets, Marta Puig; Tarrío, Rosa; Rodríguez-Trelles, Francisco; Schou, Mads Fristrup LU and Loeschcke, Volker (2019) In Journal of Thermal Biology 84. p.200-207
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... (More)

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.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Drosophila melanogaster, Drosophila subobscura, Gene expression, Heat tolerance, Hsp, Plasticity
in
Journal of Thermal Biology
volume
84
pages
8 pages
publisher
Elsevier
external identifiers
  • scopus:85068447358
ISSN
0306-4565
DOI
10.1016/j.jtherbio.2019.07.005
language
English
LU publication?
yes
id
09ef97a1-55c0-4584-b5d1-85194514ce31
date added to LUP
2019-07-16 10:44:26
date last changed
2019-08-06 03:24:25
@article{09ef97a1-55c0-4584-b5d1-85194514ce31,
  abstract     = {<p>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.</p>},
  author       = {Sørensen, Jesper Givskov and Giribets, Marta Puig and Tarrío, Rosa and Rodríguez-Trelles, Francisco and Schou, Mads Fristrup and Loeschcke, Volker},
  issn         = {0306-4565},
  keyword      = {Drosophila melanogaster,Drosophila subobscura,Gene expression,Heat tolerance,Hsp,Plasticity},
  language     = {eng},
  pages        = {200--207},
  publisher    = {Elsevier},
  series       = {Journal of Thermal Biology},
  title        = {Expression of thermal tolerance genes in two Drosophila species with different acclimation capacities},
  url          = {http://dx.doi.org/10.1016/j.jtherbio.2019.07.005},
  volume       = {84},
  year         = {2019},
}