The canonical E2Fs together with RETINOBLASTOMA-RELATED are required to establish quiescence during plant development

Magdolna Gombos, Cécile Raynaud, Yuji Nomoto, Eszter Molnár, Rim Brik-Chaouche, Hirotomo Takatsuka, Ahmad Zaki, Dóra Bernula, David Latrasse, Keito Mineta, Fruzsina Nagy, Xiaoning He, Hidekazu Iwakawa, Erika Őszi, Jing An, Takamasa Suzuki, Csaba Papdi, Clara Bergis, Moussa Benhamed, László Bögre, Masaki Ito, Zoltán Magyar

Abstract

Maintaining stable and transient quiescence in differentiated and stem cells, respectively, requires repression of the cell cycle. The plant RETINOBLASTOMA-RELATED (RBR) has been implicated in stem cell maintenance, presumably by forming repressor complexes with E2F transcription factors. Surprisingly we find that mutations in all three canonical E2Fs do not hinder the cell cycle, but similarly to RBR silencing, result in hyperplasia. Contrary to the growth arrest that occurs when exit from proliferation to differentiation is inhibited upon RBR silencing, the e2fabc mutant develops enlarged organs with supernumerary stem and differentiated cells as quiescence is compromised. While E2F, RBR and the M-phase regulatory MYB3Rs are part of the DREAM repressor complexes, and recruited to overlapping groups of targets, they regulate distinct sets of genes. Only the loss of E2Fs but not the MYB3Rs interferes with quiescence, which might be due to the ability of E2Fs to control both G1-S and some key G2-M targets. We conclude that collectively the three canonical E2Fs in complex with RBR have central roles in establishing cellular quiescence during organ development, leading to enhanced plant growth.