Waterworth, WM, Footitt, S, Bray, CM et al. (2 more authors) (2016) DNA damage checkpoint kinase ATM regulates germination and maintains genome stability in seeds. Proceedings of the National Academy of Sciences, 113 (34). pp. 9647-9652. ISSN 0027-8424
Abstract
Genome integrity is crucial for cellular survival and the faithful transmission of genetic information. The eukaryotic cellular response to DNA damage is orchestrated by the DNA damage checkpoint kinases ATAXIA TELANGIECTASIA MUTATED (ATM) and ATM AND RAD3-RELATED (ATR). Here we identify important physiological roles for these sensor kinases in control of seed germination. We demonstrate that double strand breaks (DSBs) are rate-limiting for germination. We identify that desiccation tolerant seeds exhibit a striking transcriptional DSB damage response during germination, indicative of high levels of genotoxic stress, which is induced following maturation drying and quiescence. Mutant atr and atm seeds are highly resistant to ageing, establishing ATM and ATR as determinants of seed viability. In response to ageing, ATM delays germination, while atm mutant seed germinate with extensive chromosomal abnormalities. This reveals ATM as a major factor which controls germination in aged seed, integrating progression through germination with surveillance of genome integrity. Mechanistically ATM functions through control of DNA replication in imbibing seeds. ATM signaling is mediated by transcriptional control of the cell cycle inhibitor SIAMESE-RELATED 5, an essential factor required for the ageing-induced delay to germination. In the soil seed bank, seeds exhibit increased transcript levels of ATM and ATR with changes in dormancy and germination potential, modulated by environmental signals including temperature and soil moisture. Collectively our findings reveal physiological functions for these sensor kinases in linking genome integrity to germination, thereby influencing seed quality, crucial for plant survival in the natural environment and sustainable crop production.
Metadata
Item Type: | Article |
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Authors/Creators: |
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Copyright, Publisher and Additional Information: | (c) 2016, The Authors. This is an author produced version of a paper published in Proceedings of the National Academy of Sciences. Uploaded in accordance with the publisher's self-archiving policy. In order to comply with the publisher requirements the University does not require the author to sign a non-exclusive licence for this paper. |
Keywords: | dormancy cycling, soil seed bank, DNA repair, germination, seed vigor, Arabidopsis, DNA damage response, DNA damage checkpoint |
Dates: |
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Institution: | The University of Leeds |
Academic Units: | The University of Leeds > Faculty of Biological Sciences (Leeds) > School of Biology (Leeds) |
Funding Information: | Funder Grant number BBSRC (Biotechnology & Biological Sciences Research Council) BB/H012346/1 BBSRC (Biotechnology & Biological Sciences Research Council) 24/JF/20608 EU - European Union 311840 |
Depositing User: | Symplectic Publications |
Date Deposited: | 29 Jun 2016 14:27 |
Last Modified: | 06 Oct 2020 13:16 |
Published Version: | http://dx.doi.org/10.1073/pnas.1608829113 |
Status: | Published |
Publisher: | National Academy of Sciences |
Identification Number: | 10.1073/pnas.1608829113 |
Open Archives Initiative ID (OAI ID): | oai:eprints.whiterose.ac.uk:101501 |