Arabidopsis SOG1 (suppressor of gamma response 1) is a plantspecific transcription factor that governs the DNA damage response. Here we report that SOG1 is phosphorylated in response to DNA damage, and that this phosphorylation is mediated by the sensor kinase ataxia telangiectasia mutated (ATM). We show that SOG1 phosphorylation is crucial for the response to DNA damage, including transcriptional induction of downstream genes, transient arrest of cell division and programmed cell death. Although the amino-acid sequences of SOG1 and the mammalian tumour suppressor p53 show no similarity, this study demonstrates that ATM-mediated phosphorylation of a transcription factor has a pivotal role in the DNA damage response in both plants and mammals.

In mammalian cells, the transcription factor p53 plays a crucial role in transmitting DNA damage signals to maintain genome integrity. However, in plants, orthologous genes for p53 and checkpoint proteins are absent. Instead, the plant-specific transcription factor SUPPRESSOR OF GAMMA RESPONSE 1 (SOG1) controls most of the genes induced by gamma irradiation and promotes DNA repair, cell cycle arrest, and stem cell death. To date, the genes directly controlled by SOG1 remain largely unknown, limiting the understanding of DNA damage signaling in plants. Here, we conducted a microarray analysis and chromatin immunoprecipitation (ChIP)-sequencing, and identified 146 Arabidopsis genes as direct targets of SOG1. By using ChIP-sequencing data, we extracted the palindromic motif [CTT(N) AAG] as a consensus SOG1-binding sequence, which mediates target gene induction in response to DNA damage. Furthermore, DNA damage-triggered phosphorylation of SOG1 is required for efficient binding to the SOG1-binding sequence. Comparison between SOG1 and p53 target genes showed that both transcription factors control genes responsible for cell cycle regulation, such as CDK inhibitors, and DNA repair, whereas SOG1 preferentially targets genes involved in homologous recombination. We also found that defense-related genes were enriched in the SOG1 target genes. Consistent with this finding, SOG1 is required for resistance against the hemi-biotrophic fungus Colletotrichum higginsianum, suggesting that SOG1 has a unique function in controlling the immune response.

Cell cycle arrest is an active response to stresses that enables organisms to survive under fluctuating environmental conditions. While signalling pathways that inhibit cell cycle progression have been elucidated, the putative core module orchestrating cell cycle arrest in response to various stresses is still elusive. Here we report that in Arabidopsis, the NAC-type transcription factors ANAC044 and ANAC085 are required for DNA damage-induced G2 arrest. Under genotoxic stress conditions, ANAC044 and ANAC085 enhance protein accumulation of the R1R2R3-type Myb transcription factor (Rep-MYB), which represses G2/M-specific genes. ANAC044/ANAC085-dependent accumulation of Rep-MYB and cell cycle arrest are also observed in the response to heat stress that causes G2 arrest, but not to osmotic stress that retards G1 progression. These results suggest that plants deploy the ANAC044/ANAC085-mediated signalling module as a hub which perceives distinct stress signals and leads to G2 arrest.

19Cell cycle arrest is an active response to stresses that enables organisms to survive under 20 fluctuating environmental conditions. While signalling pathways that inhibit cell cycle 21 progression have been elucidated, the putative core module orchestrating cell cycle arrest 22 in response to various stresses is still elusive. Here we report that in Arabidopsis thaliana, 23 the NAC-type transcription factors ANAC044 and ANAC085 are required for DNA 24 damage-induced G2 arrest. Under genotoxic stress conditions, ANAC044 and ANAC085 25 enhance protein accumulation of the R1R2R3-type Myb transcription factor (Rep-MYB), 26 which represses G2/M-specific genes. ANAC044/ANAC085-dependent accumulation of 27Rep-MYB and cell cycle arrest are also observed in the response to heat stress that causes 28 G2 arrest, but not to osmotic stress that retards G1 progression. These results suggest that 29 plants deploy the ANAC044/ANAC085-mediated signalling module as a hub which 30 perceives distinct stress signals and leads to G2 arrest. 31

Lateral roots (LRs) are an important organ for water and nutrient uptake from soil. Thus, control of LR formation is crucial in the adaptation of plant growth to environmental conditions. However, the underlying mechanism controlling LR formation in response to external factors has remained largely unknown. Here, we found that LR formation was inhibited by DNA damage. Treatment with zeocin, which causes DNA double-strand breaks, up-regulated several DNA repair genes in the LR primordium (LRP) through the signaling pathway mediated by the transcription factor SUPPRESSOR OF GAMMA RESPONSE 1 (SOG1). Cell division was severely inhibited in the LRP of zeocin-treated sog1-1 mutant, which in turn inhibited LR formation. This result suggests that SOG1-mediated maintenance of genome integrity is crucial for proper cell division during LRP development. Furthermore, zeocin induced several cytokinin biosynthesis genes in a SOG1-dependent manner, thereby activating cytokinin signaling in the LRP. LR formation was less inhibited by zeocin in mutants defective in cytokinin biosynthesis or signaling, suggesting that elevated cytokinin signaling is crucial for the inhibition of LR formation in response to DNA damage. We conclude that SOG1 regulates DNA repair and cytokinin signaling separately and plays a key role in controlling LR formation under genotoxic stress.