Plant somatic cells are generally acknowledged to retain totipotency, the potential to develop into any cell type within an organism. This astonishing plasticity may contribute to a high regenerative capacity on severe damage, but how plants control this potential during normal post-embryonic development remains largely unknown1,2. Here we show that POLYCOMB REPRESSIVE COMPLEX 2 (PRC2), a chromatin regulator that maintains gene repression through histone modification, prevents dedifferentiation of mature somatic cells in Arabidopsis thaliana roots. Loss-of-function mutants in PRC2 subunits initially develop unicellular root hairs indistinguishable from those in wild type but fail to retain the differentiated state, ultimately resulting in the generation of an unorganized cell mass and somatic embryos from a single root hair. Strikingly, mutant root hairs complete the normal endoreduplication programme, increasing their nuclear ploidy, but subsequently reinitiate mitotic division coupled with successive DNA replication. Our data show that the WOUND INDUCED DEDIFFERENTIATION3 (WIND3) and LEAFY COTYLEDON2 (LEC2) genes are among the PRC2 targets involved in this reprogramming, as their ectopic overexpression partly phenocopies the dedifferentiation phenotype of PRC2 mutants. These findings unveil the pivotal role of PRC2-mediated gene repression in preventing unscheduled reprogramming of fully differentiated plant cells.
This work was supported by Grant-in-Aid for Scientific Research on Priority Areas (22119010) and a grant from Scientific Technique Research Promotion Program for Agriculture, Forestry, Fisheries and Food Industry to K.S. M.I. is supported by the RIKEN Special Postdoctoral Researcher Programme. Epigenomic studies were supported by the European Union Seventh Framework Programme Network of Excellence EpiGeneSys and the CNRS to the group of V. Colot (A.K.M. and F.R.). A.K.M. is the recipient of a grant from the French Ministère de la Recherche et de l'Enseignement Supérieur. PRC2 expression studies were supported by a France-Berkeley grant to F.R. and S.M.B., an EMBO LT and Human Frontiers Science Program Postdoctoral Fellowship to M.dL. and a Hellman Junior Faculty Fellowship to S.M.B.