ATM-mediated phosphorylation of SOG1 is essential for the DNA damage response in Arabidopsis.

Arabidopsis SOG1 (suppressor of gamma response 1) is a plant-specific 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.

SOG1, a plant-specific master regulator of DNA damage responses, originated from nonvascular land plants.

The suppressor of gamma response 1 (SOG1), a NAM, ATAF1, 2, and CUC2 (NAC)-type transcription factor found in seed plants, is a master regulator of DNA damage responses (DDRs). Upon DNA damage, SOG1 regulates the expression of downstream DDR genes. To know the origin of the DDR network in land plants, we searched for a homolog(s) of SOG1 in a moss Physcomitrium (Physcomitrella) patens and identified PpSOG1a and PpSOG1b. To assess if either or both of them function(s) in DDR, we knocked out the PpSOG1s using CRISPR/Cas9-mediated gene editing and analyzed the responses to DNA-damaging treatments. The double-knockout (KO) sog1a sog1b plants showed resistance to γ-rays, bleomycin, and ultraviolet B (UVB) treatments similarly seen in Arabidopsis sog1 plants. Next, we irradiated wild-type (WT) and KO plants with γ-rays and analyzed the whole transcriptome to examine the effect on the expression of DDR genes. The results revealed that many P. patens genes involved in the checkpoint, DNA repair, replication, and cell cycle-related genes were upregulated after γ-irradiation, which was not seen in sog1a sog1b plant. These results suggest that PpSOG1a and PpSOG1b work redundantly on DDR response in P. patens; in addition, plant-specific DDR systems had been established before the emergence of vascular plants.

The role of SOG1, a plant-specific transcriptional regulator, in the DNA damage response.

Plants are inescapably exposed to environmental stress because of their sessile lifestyle. Such stress induces the production of reactive oxygen species (ROS), which are in turn a source of genotoxic stress. ROS are also generated intrinsically during photosynthesis in the chloroplasts. Furthermore, plants are affected by the UV component of sunlight, which damages their genomes. To protect their genomic integrity from DNA damage, plants activate a DNA damage response (DDR) system that regulates cell cycle arrest, DNA repair, and programmed cell death. Although plants have orthologs of several of the DDR factors that are found in animals, certain critical animal DDR factors, notably the tumor suppressor p53 and the DDR kinases CHK1 and CHK2, have not been found in plants. In this mini-review, we summarize the functions and regulatory mechanism of Arabidopsis thaliana SUPPRESSOR OF GAMMA RESPONSE 1 (SOG1), a plant-specific transcription factor that plays a central role in the DDR. The characteristics of SOG1 are similar to those of animal p53, even though the proteins' amino acid sequences are unrelated. We suggest that plants acquired the central transcriptional factor SOG1 as a functional homolog of p53 during the evolution of their DDR system.