SOG1‐dependent NAC103 modulates the DNA damage response as a transcriptional regulator in Arabidopsis

Abstract

These authors contributed equally to this work. SUMMARYThe plant-specific transcription factor (TF) NAC103 was previously reported to modulate the unfolded protein response in Arabidopsis under endoplasmic reticulum (ER) stress. Alternatively, we report here that NAC103 is involved in downstream signaling of SOG1, a master regulator for expression of DNA damage response (DDR) genes induced by genotoxic stress. Arabidopsis NAC103 expression was strongly induced by genotoxic stress and nac103 mutants displayed substantial inhibition of DDR gene expression after gamma radiation or radiomimetic zeocin treatment. DDR phenotypes, such as true leaf inhibition, root cell death and root growth inhibition, were also suppressed significantly in the nac103 mutants, but to a lesser extent than in the sog1-1 mutant. By contrast, overexpression of NAC103 increased DDR gene expression without genotoxic stress and substantially rescued the phenotypic changes in the sog1-1 mutant after zeocin treatment. The putative promoters of some representative DDR genes, RAD51, PARP1, RPA1E, BRCA1 and At4g22960, were found to partly interact with NAC103. Together with the expected interaction of SOG1 with the promoter of NAC103, our study suggests that NAC103 is a putative SOG1-dependent transcriptional regulator of plant DDR genes, which are responsible for DDR phenotypes under genotoxic stress.

Modulation of plant DNA damage response gene expression during Agrobacterium infection

“…We chose a different approach by following the expression of a series of genes encoding proteins involved in DNA damage repair pathways during early stages of Agrobacterium infection. Indeed, many genes involved in DNA damage response signaling or in DNA repair are induced in Arabidopsis and other plants in response to DNA damage [ 9 – 13 ], consistent with the notion that expression of these genes may be used as marker for activation of DNA damage repair [ 11 – 13 ]. Moreover, biotic stress, such as bacterial infection, can induce DNA damage, which likely represents a general reaction to stress but may also plays a more specific role in the plant defense response [ 14 , 15 ].…”

“…We elected to utilize tobacco (Nicotiana tabacum) as a model plant because, unlike Arabidopsis, it allows harvesting sufficient amounts of tissue uniformly infected with Agrobacterium for reliable and sensitive analyses. Next, we selected a set of 12 genes known to be induced in a dose-dependent manner by DNA damaging treatment in Arabidopsis , which therefore can serve as reliable genetic markers for the DNA damage response [ 11 – 13 ] ( Table 1 ). These genes encode proteins that function in different pathways of DNA damage response and repair (reviewed in Refs.…”

“…[ 20 , 21 ]). Specifically, NAC103 (termed NAC82 in tobacco) is involved in signaling of DNA damage response, acting as a transcription factor that induces expression of several DNA repair genes [ 13 ]. Other selected genes are involved in the actual DNA repair, via HR ( BRCA1, RAD51, RAD17 ), NHEJ ( RAD17, KU70, XRCC1, XRCC4 ), or alt-NHEJ ( PARP1, PARP2 ).…”

Integrative inference of transcriptional networks in Arabidopsis yields novel ROS signalling regulators

“…The remaining 49 identified ROS TFs had previously not been linked to any role in ROS/environmental stress (referred to as ‘NOVEL’ TFs in Table 2), at the time the iGRN was constructed (see Methods). However, five of the 49 novel TFs were validated for a role in environmental stress responses by studies that were published after the iGRN construction (Table 2 and Supplemental Table S5): ANAC102 and BME3 (high light 33-35 ), NAC103 (genotoxic 36 ), ZAT18 (drought 37 ) and ERF019 (drought, bacterial and fungal pathogens 38,39 ).…”

Chromatin Remodeling and Epigenetic Regulation in Plant DNA Damage Repair

“…The active forms of ATM/ATR kinases phosphorylate and/or regulate the secondary downstream transducers H2AX, SUPPRESSOR OF GAMMA RESPONSE1 (SOG1), and RETINOBLASTOMA RELATED1 (RBR1)/E2FA [22,28,29]. The phosphorylated SOG1 plays a pivotal role in plant DDR by inducing transcription of the tertiary downstream transducer NAC103 and the effectors SMR4/5/7, CYCB1, WEE1, ARGONAUTE2 (AGO2), BREAST CANCER1 (BRCA1), RAD17/51/54, PARP1/2, and RPA1E [30,31,32].…”