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Experimentally heat‐induced transposition increases drought tolerance in Arabidopsis thaliana


Thieme, Michael; Brêchet, Arthur; Bourgeois, Yann; Keller, Bettina; Bucher, Etienne; Roulin, Anne C (2022). Experimentally heat‐induced transposition increases drought tolerance in Arabidopsis thaliana. New Phytologist, 236(1):182-194.

Abstract

Eukaryotic genomes contain a vast diversity of transposable elements (TEs). Formerly often described as selfish and parasitic DNA sequences, TEs are now recognized as a source of genetic diversity and powerful drivers of evolution. Yet, because their mobility is tightly controlled by the host, studies experimentally assessing how fast TEs may mediate the emergence of adaptive traits are scare. We exposed Arabidopsis thaliana high-copy TE lines (hcLines) with up to ~8 fold increased copy numbers of the heat-responsive ONSEN TE to drought as a straightforward and ecologically highly relevant selection pressure. We provide evidence for increased drought tolerance in five out of the 23 tested hcLines and further pinpoint one of the causative mutations to an exonic insertion of ONSEN in the ribose-5-phosphate-isomerase 2 gene. The resulting loss-of-function mutation caused a decreased rate of photosynthesis, plant size and water consumption. Overall, we show that the heat-induced transposition of a low-copy TE increases phenotypic diversity and leads to the emergence of drought-tolerant individuals in Arabidopsis thaliana. This is one of the rare empirical examples substantiating the adaptive potential of mobilized stress-responsive TEs in eukaryotes. Our work demonstrates the potential of TE-mediated loss-of-function mutations in stress adaptation.

Abstract

Eukaryotic genomes contain a vast diversity of transposable elements (TEs). Formerly often described as selfish and parasitic DNA sequences, TEs are now recognized as a source of genetic diversity and powerful drivers of evolution. Yet, because their mobility is tightly controlled by the host, studies experimentally assessing how fast TEs may mediate the emergence of adaptive traits are scare. We exposed Arabidopsis thaliana high-copy TE lines (hcLines) with up to ~8 fold increased copy numbers of the heat-responsive ONSEN TE to drought as a straightforward and ecologically highly relevant selection pressure. We provide evidence for increased drought tolerance in five out of the 23 tested hcLines and further pinpoint one of the causative mutations to an exonic insertion of ONSEN in the ribose-5-phosphate-isomerase 2 gene. The resulting loss-of-function mutation caused a decreased rate of photosynthesis, plant size and water consumption. Overall, we show that the heat-induced transposition of a low-copy TE increases phenotypic diversity and leads to the emergence of drought-tolerant individuals in Arabidopsis thaliana. This is one of the rare empirical examples substantiating the adaptive potential of mobilized stress-responsive TEs in eukaryotes. Our work demonstrates the potential of TE-mediated loss-of-function mutations in stress adaptation.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Department of Plant and Microbial Biology
07 Faculty of Science > Zurich-Basel Plant Science Center
08 Research Priority Programs > Evolution in Action: From Genomes to Ecosystems
Dewey Decimal Classification:580 Plants (Botany)
Scopus Subject Areas:Life Sciences > Physiology
Life Sciences > Plant Science
Uncontrolled Keywords:Plant Science, Physiology
Language:English
Date:1 October 2022
Deposited On:30 Aug 2022 12:27
Last Modified:29 Jan 2024 02:43
Publisher:Wiley-Blackwell Publishing, Inc.
ISSN:0028-646X
OA Status:Hybrid
Free access at:PubMed ID. An embargo period may apply.
Publisher DOI:https://doi.org/10.1111/nph.18322
PubMed ID:35715973
Project Information:
  • : FunderSNSF
  • : Grant ID31003A_182785
  • : Project TitleImpact of transposable elements on plant population evolution: insight from the model grass species brachypodium distachyon
  • : FunderFreiwillige Akademische Gesellschaft
  • : Grant ID
  • : Project Title
  • Content: Published Version
  • Licence: Creative Commons: Attribution 4.0 International (CC BY 4.0)