title: DNA damage checkpoint kinase ATM regulates germination and maintains genome stability in seeds.
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 aging, establishing ATM and ATR as determinants of seed viability. In response to aging, ATM delays germination, whereas atm mutant seeds germinate with extensive chromosomal abnormalities. This identifies ATM as a major factor that controls germination in aged seeds, 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 aging-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.
authors: Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom;
authors: Wanda M
authors: WM
authors: Waterworth
authors: School of Life Sciences, University of Warwick, Warwickshire CV35 9EF, United Kingdom;
authors: Steven
authors: S
authors: Footitt
authors: Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, United Kingdom.
authors: Clifford M
authors: CM
authors: Bray
authors: School of Life Sciences, University of Warwick, Warwickshire CV35 9EF, United Kingdom;
authors: William E
authors: WE
authors: Finch-Savage
authors: Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom; c.e.west@leeds.ac.uk.
authors: Christopher E
authors: CE
authors: West
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics; D017360:Arabidopsis / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D064007:Ataxia Telangiectasia Mutated Proteins / Q000235:genetics* / Q000378:metabolism; D059447:Cell Cycle Checkpoints / Q000235:genetics; D018797:Cell Cycle Proteins / Q000235:genetics / Q000378:metabolism; D053903:DNA Breaks, Double-Stranded; D018744:DNA, Plant / Q000235:genetics; D003890:Desiccation; D018506:Gene Expression Regulation, Plant; D018745:Genome, Plant; D042822:Genomic Instability; D018525:Germination / Q000235:genetics*; D009154:Mutation; D012639:Seeds / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D015398:Signal Transduction; D013312:Stress, Physiological; D013997:Time Factors
chemical_list: C576589:ATM protein, Arabidopsis; D029681:Arabidopsis Proteins; D018797:Cell Cycle Proteins; D018744:DNA, Plant; C000592968:SMR5 protein, Arabidopsis; C576892:ATR protein, Arabidopsis; D064007:Ataxia Telangiectasia Mutated Proteins
keywords: DNA damage response; DNA repair; dormancy cycling; seed vigor; soil seed bank