The LFR-SWI/SNF complex: A chromatin wrench safeguarding cellular quiescence in the <i>Arabidopsis</i> root stem cell organizer.

Abstract

The quiescent center (QC) resides in a reversible G₀ 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<i>-</i>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 <i>PLT1</i>, <i>PLT2</i>, and <i>SCR</i> loci to sustain their positive autoregulation, thereby contributing to the prevention of QC cell division. Conversely, LFR compacts <i>WOX5</i> chromatin to enforce negative autoregulation and simultaneously promotes <i>CYCD3;3</i> expression to counteract WOX5-mediated repression, thus ensuring the proliferation competence of the QC. Furthermore, WOX5 throws a wrench into LFR binding at the <i>CYCD3;3</i> promoter, establishing a regulatory circuit that precisely modulates <i>CYCD3;3</i> 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.