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.DNA repair | seed vigor | DNA damage response | dormancy cycling | soil seed bank M aintenance of genome integrity is indispensable for cellular survival and transmission of genetic information to the next generation; however, constant exposure of DNA to environmental and cellular oxidative stresses results in damage that can arrest growth and result in mutagenesis or cell death. Consequently, organisms have evolved powerful DNA repair and DNA damage signaling mechanisms. In plants, as in other eukaryotes, the cellular response to DNA damage is orchestrated by the phosphoinositide-3-kinase-related protein kinases (PIKKs) ATAXIA TELANGIECTASIA MUTATED (ATM) and ATM AND RAD3-RELATED (ATR) (1). In response to genotoxic stresses, these checkpoint kinases activate DNA repair factors, delay or halt cell cycle progression, and promote endocycles or programmed cell death (1-4). ATM is activated by double-strand DNA breaks (DSBs), a highly toxic form of DNA damage that results in chromosome fragmentation (1, 5), and plants mutated in ATM display hypersensitivity to DSBs induced by gamma radiation or radiomimetics (6). ATM also mediates a strong transcriptional up-regulation of hundreds of genes, including the SIAMESE/SIAMESE-RELATED cell cycle inhibitors ...

A matter of life and death: Molecular, physiological, and environmental regulation of seed longevity

“…Over the past decades, numerous investigations have identified intrinsic genetic and physiological factors involved in the regulation of seed longevity. For instance, ROS production and elimination (Rajjou et al, ; Rajjou & Debeaujon, ; Wiebach, Nagel, Börner, Altmann, & Riewe, ), the concentrations of plant hormones (Shu et al, ; Shu, Zhou, & Yang, ), repair and maintenance systems for nucleic acids and proteins (Chen et al, ; Fleming, Richards, & Walters, ; Petla et al, ; Waterworth et al, ), and the presence of several storage compounds (Li et al, ; Zhou et al, ) play important roles, via complex pathways or networks, in controlling seed longevity (Figure ).…”

“…In the model plant Arabidopsis thaliana , seed longevity regulatory networks have been identified, including the roles of biochemical pathways, seed developmental conditions, and phytohormones (Righetti et al, ). Recently, several studies have suggested that the mechanisms underlying seed longevity may be associated with DNA repair, the level of reactive oxygen species (ROS) production and scavenging and glucose metabolism (Lee et al, ; Waterworth, Footitt, Bray, Finch‐Savage, & West, ). In this review, we principally focus on the regulatory factors involved in seed longevity, including the physical structure of the seed coat, environmental cues, and genetic and phytohormonal factors.…”

SUPPRESSOR OF GAMMA RESPONSE1 Links DNA Damage Response to Organ Regeneration

“…In this scenario, the preferential growth of lateral roots (rather than a futile cycle of primary root DDR-induced PCD and regeneration) could successfully redirect root growth away from the chronic DNA-damaging agent. In contrast, the restoration of primary root tip growth seems most cost beneficial (and evolutionarily favorable) in the case of an acute and transient exposure to DNA damage, which is the case for seeds upon imbibition, where they acutely experience the DNA damage they accumulated during aging (Waterworth et al, 2015(Waterworth et al, , 2016. Regeneration of the embryonic root in response to DNA damage is critical for the viability of a germinating seed, as the linear-growing embryonic root carries no additional root primordia (Van Norman et al, 2013).…”

“…These arrest and repair processes, together with programmed cell death (Curtis and Hays, 2007) and the early induction of the endoreduplicative cell cycle (Adachi et al, 2011), are collectively known as the DNA damage response (DDR), which safeguards the genomic integrity of the organism as a whole (Yoshiyama, 2016). In plants, DDR has a key role in the germination of seeds that have accumulated DNA damage during aging from desiccation/rehydration cycles, as repair is limited in the desiccated state (Waterworth et al, 2015(Waterworth et al, , 2016. Here, we demonstrate the role of DDR genes in seedling recovery from growth-disruptive levels of DNA damage, which we have artificially induced by exposure to ionizing radiation (IR).…”

PLATINUM SENSITIVE 2 LIKE impacts growth, root morphology, seed set, and stress responses

“…Interestingly, it was recently also reported that genotoxic stress induced DNA repair signaling and delayed germination in a SMR5 dependent manner [53]. …”