SOG1 and BRCA1 Interdependently Regulate RAD54 Expression for Repairing Salinity-Induced DNA Double-Strand Breaks in Arabidopsis

Abstract

Abstract As sessile organisms, land plants experience various forms of environmental stresses throughout their life span. Therefore, plants have developed extensive and complicated defense mechanisms, including a robust DNA damage response (DDR) and DNA repair systems for maintaining genome integrity. In Arabidopsis, the NAC [NO APICAL MERISTEM (NAM), ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR (ATAF), CUP-SHAPED COTYLEDON (CUC)] domain family transcription factor SUPPRESSOR OF GAMMA RESPONSE 1 (SOG1) plays an important role in regulating DDR. Here, we show that SOG1 plays a key role in regulating the repair of salinity-induced DNA double-strand breaks (DSBs) via the homologous recombination (HR) pathway in Arabidopsis. The sog1-1 mutant seedlings display a considerably slower rate of repair of salinity-induced DSBs. Accumulation of SOG1 protein increases in wild-type Arabidopsis under salinity stress, and it enhances the expression of HR pathway–related genes, including RAD51, RAD54 and BReast CAncer gene 1 (BRCA1), respectively, as found in SOG1 overexpression lines. SOG1 binds specifically to the AtRAD54 promoter at the 5ʹ-(N)4GTCAA(N)3C-3ʹ consensus sequence and positively regulates its expression under salinity stress. The phenotypic responses of sog1-1/atrad54 double mutants suggest that SOG1 functions upstream of RAD54, and both these genes are essential in regulating DDR under salinity stress. Furthermore, SOG1 interacts directly with BRCA1, an important component of the HR-mediated DSB repair pathway in plants, where BRCA1 appears to facilitate the binding of SOG1 to the RAD54 promoter. At the genetic level, SOG1 and BRCA1 function interdependently in modulating RAD54 expression under salinity-induced DNA damage. Together, our results suggest that SOG1 regulates the repair of salinity-induced DSBs via the HR-mediated pathway through genetic interactions with RAD54 and BRCA1 in Arabidopsis.