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Basal hsp70 expression levels do not explain adaptive variation of the warm- and cold-climate O3?+?4?+?7 and OST gene arrangements of Drosophila subobscura.

ABSTRACT: BACKGROUND:Drosophila subobscura exhibits a rich inversion polymorphism, with some adaptive inversions showing repeatable spatiotemporal patterns in frequencies related to temperature. Previous studies reported increased basal HSP70 protein levels in homokaryotypic strains for a warm-climate arrangement compared to a cold-climate one. These findings do not match the similar hsp70 genomic organization between arrangements, where gene expression levels are expected to be similar. In order to test this hypothesis and understand the molecular basis for hsp70 expression, we compared basal hsp70 mRNA levels in males and females, and analysed the 5' and 3' regulatory regions of hsp70 genes in warm- and cold-climate isochromosomal O3?+?4?+?7 and OST lines of D. subobscura. RESULTS:We observed comparable mRNA levels between the two arrangements and a sex-biased hsp70 gene expression. The number of heat-shock elements (HSEs) and GAGA sites on the promoters were identical amongst the OST and O3?+?4?+?7 lines analysed. This is also true for 3' AU-rich elements where most A and B copies of hsp70 have, respectively, two and one element in both arrangements. Beyond the regulatory elements, the only notable difference between both arrangements is the presence in 3' UTR of a 14?bp additional fragment after the stop codon in the hsp70A copy in five O3?+?4?+?7 lines, which was not found in any of the six OST lines. CONCLUSIONS:The equivalent hsp70 mRNA amounts in OST and O3?+?4?+?7 arrangements provide the first evidence of a parallelism between gene expression and genetic organization in D. subobscura lines having these arrangements. This is reinforced by the lack of important differential features in the number and structure of regulatory elements between both arrangements, despite the genetic differentiation observed when the complete 5' and 3' regulatory regions were considered. Therefore, the basal levels of hsp70 mRNA cannot account, in principle, for the adaptive variation of the two arrangements studied. Consequently, further studies are necessary to understand the intricate molecular mechanisms of hsp70 gene regulation in D. subobscura.

SUBMITTER: Puig Giribets M

PROVIDER: S-EPMC6995229 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Basal hsp70 expression levels do not explain adaptive variation of the warm- and cold-climate O<sub>3 + 4 + 7</sub> and O<sub>ST</sub> gene arrangements of Drosophila subobscura.

Puig Giribets Marta M Santos Mauro M García Guerreiro María Pilar MP

BMC evolutionary biology 20200131 1

<h4>Background</h4>Drosophila subobscura exhibits a rich inversion polymorphism, with some adaptive inversions showing repeatable spatiotemporal patterns in frequencies related to temperature. Previous studies reported increased basal HSP70 protein levels in homokaryotypic strains for a warm-climate arrangement compared to a cold-climate one. These findings do not match the similar hsp70 genomic organization between arrangements, where gene expression levels are expected to be similar. In order ...[more]

PMID: 32005133

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Project description:BackgroundThe role of chromosomal arrangements in adaptation is supported by the repeatable clinal variation in inversion frequencies across continents in colonizing species such as Drosophila subobscura. However, there is a lack of knowledge on the genetic variation in genes within inversions, possibly targets of climatic selection, across a geographic latitudinal gradient. In the present study we analysed four candidate loci for thermal adaptation, located close to the breakpoints, in two chromosomal arrangements of the sex (A) chromosome of Drosophila subobscura with different thermal preferences. Individual chromosomes with A2 (the inverted arrangement considered warm adapted) or AST (the standard ancestral arrangement considered cold adapted) were sequenced across four European localities at varying latitudes, up to ~ 2500 Kms apart.ResultsImportantly, we found very low differentiation for each specific arrangement across populations as well as no clinal patterns of genomic variation. This suggests wide gene exchange along the cline. Differentiation between the sex chromosome arrangements was significant in the two more proximal regions relative to the AST orientation but not in the distal ones, independently of their location inside or outside the inversion. This can be possibly due to variation in the levels of gene flux and/or selection acting in these regions.ConclusionsGene flow appears to have homogenized the genetic content within-arrangement at a wide geographical scale, despite the expected diverse selective pressures in the specific natural environments of the different populations sampled. It is thus likely that the inversion frequency clines in this species are being maintained by local adaptation in face of gene flow. The differences between arrangements at non-coding regions might be associated with the previously observed differential gene expression in different thermal regimes. Higher resolution genomic scans for individual chromosomal arrangements performed over a large environmental gradient are needed to find the targets of selection and further elucidate the adaptive mechanisms maintaining chromosomal inversion polymorphisms.

Dataset Information

Basal hsp70 expression levels do not explain adaptive variation of the warm- and cold-climate O3?+?4?+?7 and OST gene arrangements of Drosophila subobscura.

Publications

Basal hsp70 expression levels do not explain adaptive variation of the warm- and cold-climate O<sub>3 + 4 + 7</sub> and O<sub>ST</sub> gene arrangements of Drosophila subobscura.

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