NAC1 regulates root ground tissue maturation by coordinating with the SCR/SHR–CYCD6;1 module in Arabidopsis.

Precise spatiotemporal control of the timing and extent of asymmetric cell divisions (ACDs) is essential for plant development. In the Arabidopsis root, ground tissue maturation involves an additional ACD of the endodermis that maintains the inner cell layer as the endodermis and generates the middle cortex to the outside. Through regulation of the cell cycle regulator CYCLIND6;1 (CYCD6;1), the transcription factors SCARECROW (SCR) and SHORT-ROOT (SHR) play critical roles in this process. In the present study, we found that loss of function of NAC1 , a NAC transcription factor family gene, causes markedly increased periclinal cell divisions in the root endodermis. Importantly, NAC1 directly represses the transcription of CYCD6;1 by recruiting the co-repressor TOPLESS (TPL), creating a fine-tuned mechanism to maintain proper root ground tissue patterning by limiting production of middle cortex cells. Biochemical and genetic analyses further showed that NAC1 physically interacts with SCR and SHR to restrict excessive periclinal cell divisions in the endodermis during root middle cortex formation. Although NAC1–TPL is recruited to the CYCD6;1 promoter and represses its transcription in an SCR-dependent manner, NAC1 and SHR antagonize each other to regulate the expression of CYCD6;1. Collectively, our study provides mechanistic insights into how the NAC1–TPL module integrates with the master transcriptional regulators SCR and SHR to control root ground tissue patterning by fine-tuning spatiotemporal expression of CYCD6;1 in Arabidopsis. The SCR/SHR-CYCD6;1 module is essential for root ground tissue maturation. This study reveals that NAC1 restricts excessive periclinal cell divisions in root endodermis to control ground tissue maturation. Mechanistically, NAC1 interacts with TOPLESS and fine-tunes the expression of CYCD6;1 through coordination with SCR and SHR. [ABSTRACT FROM AUTHOR]