Gene expression differences consistent with water loss reduction underlie desiccation tolerance of natural Drosophila populations.


Journal

BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720

Informations de publication

Date de publication:
16 02 2023
Historique:
received: 23 05 2022
accepted: 27 01 2023
entrez: 16 2 2023
pubmed: 17 2 2023
medline: 22 2 2023
Statut: epublish

Résumé

Climate change is one of the main factors shaping the distribution and biodiversity of organisms, among others by greatly altering water availability, thus exposing species and ecosystems to harsh desiccation conditions. However, most of the studies so far have focused on the effects of increased temperature. Integrating transcriptomics and physiology is key to advancing our knowledge on how species cope with desiccation stress, and these studies are still best accomplished in model organisms. Here, we characterized the natural variation of European D. melanogaster populations across climate zones and found that strains from arid regions were similar or more tolerant to desiccation compared with strains from temperate regions. Tolerant and sensitive strains differed not only in their transcriptomic response to stress but also in their basal expression levels. We further showed that gene expression changes in tolerant strains correlated with their physiological response to desiccation stress and with their cuticular hydrocarbon composition, and functionally validated three of the candidate genes identified. Transposable elements, which are known to influence stress response across organisms, were not found to be enriched nearby differentially expressed genes. Finally, we identified several tRNA-derived small RNA fragments that differentially targeted genes in response to desiccation stress. Overall, our results showed that basal gene expression differences across individuals should be analyzed if we are to understand the genetic basis of differential stress survival. Moreover, tRNA-derived small RNA fragments appear to be relevant across stress responses and allow for the identification of stress-response genes not detected at the transcriptional level.

Sections du résumé

BACKGROUND
Climate change is one of the main factors shaping the distribution and biodiversity of organisms, among others by greatly altering water availability, thus exposing species and ecosystems to harsh desiccation conditions. However, most of the studies so far have focused on the effects of increased temperature. Integrating transcriptomics and physiology is key to advancing our knowledge on how species cope with desiccation stress, and these studies are still best accomplished in model organisms.
RESULTS
Here, we characterized the natural variation of European D. melanogaster populations across climate zones and found that strains from arid regions were similar or more tolerant to desiccation compared with strains from temperate regions. Tolerant and sensitive strains differed not only in their transcriptomic response to stress but also in their basal expression levels. We further showed that gene expression changes in tolerant strains correlated with their physiological response to desiccation stress and with their cuticular hydrocarbon composition, and functionally validated three of the candidate genes identified. Transposable elements, which are known to influence stress response across organisms, were not found to be enriched nearby differentially expressed genes. Finally, we identified several tRNA-derived small RNA fragments that differentially targeted genes in response to desiccation stress.
CONCLUSIONS
Overall, our results showed that basal gene expression differences across individuals should be analyzed if we are to understand the genetic basis of differential stress survival. Moreover, tRNA-derived small RNA fragments appear to be relevant across stress responses and allow for the identification of stress-response genes not detected at the transcriptional level.

Identifiants

pubmed: 36797754
doi: 10.1186/s12915-023-01530-4
pii: 10.1186/s12915-023-01530-4
pmc: PMC9933328
doi:

Substances chimiques

Water 059QF0KO0R

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

35

Subventions

Organisme : European Research Council
ID : H2020-ERC-2014-CoG-647900
Pays : International

Informations de copyright

© 2023. The Author(s).

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Auteurs

Vivien Horváth (V)

Institute of Evolutionary Biology, CSIC, UPF, Barcelona, Spain.

Sara Guirao-Rico (S)

Institute of Evolutionary Biology, CSIC, UPF, Barcelona, Spain.

Judit Salces-Ortiz (J)

Institute of Evolutionary Biology, CSIC, UPF, Barcelona, Spain.

Gabriel E Rech (GE)

Institute of Evolutionary Biology, CSIC, UPF, Barcelona, Spain.

Llewellyn Green (L)

Institute of Evolutionary Biology, CSIC, UPF, Barcelona, Spain.

Eugenio Aprea (E)

Agriculture Food Environment Centre (C3A), University of Trento, San Michele All'adige (TN), Italy.
Research and Innovation Centre, Fondazione Edmund Mach, San Michele All'adige (TN), Italy.

Mirco Rodeghiero (M)

Agriculture Food Environment Centre (C3A), University of Trento, San Michele All'adige (TN), Italy.
Research and Innovation Centre, Fondazione Edmund Mach, San Michele All'adige (TN), Italy.

Gianfranco Anfora (G)

Agriculture Food Environment Centre (C3A), University of Trento, San Michele All'adige (TN), Italy.
Research and Innovation Centre, Fondazione Edmund Mach, San Michele All'adige (TN), Italy.

Josefa González (J)

Institute of Evolutionary Biology, CSIC, UPF, Barcelona, Spain. josefa.gonzalez@csic.es.

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