SOG1: a master regulator of the DNA damage response in plants

Abstract

The DNA damage response (DDR) is a critical mechanism to maintain the genome stability of an organism upon exposure to endogenous and exogenous DNA-damaging factors. The DDR system is particularly important for plants as these organisms, owing to their intrinsic immobility, are inevitably exposed to environmental stress factors, some of which induce DNA damage. Arabidopsis thaliana has orthologs of several DDR factors that are present in animals; however, some of the important animal regulators, such as the tumor suppressor p53 and the DDR kinases CHK1 and CHK2, have not been found in plants. These observations imply a unique DDR system in plants. The present review focuses on recent advances in our understanding of the DDR in A. thaliana and, in particular, on the function and role of SUPPRESSOR OF GAMMA RESPONSE 1 (SOG1), a plant-specific transcription factor that regulates the DDR. The most obvious response to DNA damage in A. thaliana is a rapid and robust change in the transcriptional regulation of numerous genes, in which SOG1 is an essential regulatory factor. Mutation of SOG1 causes various defects in the activation of cell cycle arrest, programmed cell death, and endoreduplication in response to DNA damage. These observations indicate that SOG1 is a master regulator of the DDR. Phylogenetic analyses of SOG1 reveal that orthologs of this crucial transcription factor are present not only in angiosperms but also in gymnosperms, suggesting that the SOG1 system is conserved across spermatophytes. Finally, future prospects for SOG1 research are also discussed.

SUPPRESSOR OF GAMMA RESPONSE1 Links DNA Damage Response to Organ Regeneration

“…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). We propose that SOG1, a gene unique to seed-bearing plants (Yoshiyama, 2016), may have evolved to salvage the overall mitotic competency (prevent permanent mitotic arrest) of the embryonic root during the germination of aged seeds.…”

“…DSBs are also potent inducers of checkpoint response, where cell cycle progression is transiently inhibited to allow for DNA repair before mitotic M phase (Hu et al, 2016). 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.…”

“…We also demonstrate that the regeneration response, which involves a partial loss of cellular identities and the induction of regenerative (periclinal) cell divisions, facilitates the rebuilding of a functional stem cell niche able to resume proliferative cell division (and thus root growth). As SOG1 is unique to seed-bearing plants (Yoshiyama, 2016), this developmental response may have evolved to rescue the growth of seed-borne embryos from DNA damage accumulated during aging (Waterworth et al, 2015).…”

Phosphoproteomic analysis reveals plant DNA damage signalling pathways with a functional role for histone H2AX phosphorylation in plant growth under genotoxic stress

“…Notably, plants lack clear homologues of many of these downstream factors, including p53, the effector kinases CHK1, CHK2, and apoptotic factors, indicating that signalling downstream of ATM and ATR may have evolved independently in the plant lineage (Hu et al ., ). Some functionality of p53 is performed by the SUPPRESSOR OF GAMMA 1 (SOG1) transcription factor, which is required for the transcriptional DNA damage response, programmed cell death, endoreduplication and cell‐cycle arrest (Yoshiyama et al ., ; Yoshiyama, ).…”

Alternative Splicing and DNA Damage Response in Plants

“…Neither orthologs of CHK1 and CHK2, nor of p53, have been identified in plants so far. However, a functional homolog of p53, SUPPRESSOR OF GAMMA RESPONSE 1 (SOG1), transcriptionally regulating DDR downstream of ATM and ATR was found (Preuss and Britt, 2003;Yoshiyama et al, 2009;Yoshiyama, 2016). Indeed, SOG1 was identified as a master regulator transcription factor of the plant DDR, influencing expression of genes related to the cell cycle and DNA repair (Ogita et al, 2018).…”