Shuge Wang, Jiayu Li, Mengmeng Li, Qionglei Fang, Xiaolei Shi, Yan Long, Qiang Chen, Xiaoyun Li, Muhammad Ans Aslam, Hao Zhang, Xigang Liu, Wenqiang Tang, Sujuan Cui, Hongtao Zhao
The quiescent center (QC) resides in a reversible G 0 state in which cells are not actively dividing and yet retain their proliferation competence upon stimulation. How this quiescent state is molecularly defined and stably maintained is a fascinating question. Here, we uncover a dual role for LEAF AND FLOWER RELATED (LFR), a component of the SWITCH/SUCROSE NONFERMENTABLE (SWI/SNF) chromatin-remodeling complex, in maintaining quiescence of the QC. We demonstrate that LFR is recruited to the chromatin of core transcription factors (TFs) PLETHORA 1 (PLT1), PLT2, SCARECROW (SCR), and WUSCHEL - RELATED HOMEOBOX (WOX5) via physical interactions with them. Moreover, the autoregulatory binding of these TFs reciprocally requires LFR. Functioning as a chromatin wrench, LFR relaxes the chromatin at PLT1 , PLT2 , and SCR loci to sustain their positive autoregulation, thereby contributing to the prevention of QC cell division. Conversely, LFR compacts WOX5 chromatin to enforce negative autoregulation and simultaneously promotes CYCD3;3 expression to counteract WOX5-mediated repression, thus ensuring the proliferation competence of the QC. Furthermore, WOX5 throws a wrench into LFR binding at the CYCD3;3 promoter, establishing a regulatory circuit that precisely modulates CYCD3;3 expression, a D-type cyclin whose appropriate level is critical for QC quiescence. Consequently, the QC is maintained in a proliferation-competent but arrested state. Our findings establish the LFR-containing SWI/SNF complex as a key regulatory node that coordinates TF autoregulation with cell-cycle control to maintain QC quiescence.