Polycomb Repressive Complex 2 Controls the Embryo-to-Seedling Phase Transition

Justin Goodrich,Arp Schnittger,Maren Heese,Daniel Bouyer,Jean-Pierre Renou,Vincent Colot,Francois Roudier,Paul E. Grini,Delphine Gey,Moritz K. Nowack,Ellen D. Andersen

doi:10.1371/journal.pgen.1002014

Abstract

Polycomb repressive complex 2 (PRC2) is a key regulator of epigenetic states catalyzing histone H3 lysine 27 trimethylation (H3K27me3), a repressive chromatin mark. PRC2 composition is conserved from humans to plants, but the function of PRC2 during the early stage of plant life is unclear beyond the fact that it is required for the development of endosperm, a nutritive tissue that supports embryo growth. Circumventing the requirement of PRC2 in endosperm allowed us to generate viable homozygous null mutants for FERTILIZATION INDEPENDENT ENDOSPERM (FIE), which is the single Arabidopsis homolog of Extra Sex Combs, an indispensable component of Drosophila and mammalian PRC2. Here we show that H3K27me3 deposition is abolished genome-wide in fie mutants demonstrating the essential function of PRC2 in placing this mark in plants as in animals. In contrast to animals, we find that PRC2 function is not required for initial body plan formation in Arabidopsis. Rather, our results show that fie mutant seeds exhibit enhanced dormancy and germination defects, indicating a deficiency in terminating the embryonic phase. After germination, fie mutant seedlings switch to generative development that is not sustained, giving rise to neoplastic, callus-like structures. Further genome-wide studies showed that only a fraction of PRC2 targets are transcriptionally activated in fie seedlings and that this activation is accompanied in only a few cases with deposition of H3K4me3, a mark associated with gene activity and considered to act antagonistically to H3K27me3. Up-regulated PRC2 target genes were found to act at different hierarchical levels from transcriptional master regulators to a wide range of downstream targets. Collectively, our findings demonstrate that PRC2-mediated regulation represents a robust system controlling developmental phase transitions, not only from vegetative phase to flowering but also especially from embryonic phase to the seedling stage.

Highlights

One common principle of flowering plants and probably one of the main reasons for their evolutionary success is the alternation of a dormant seed stage with a growing plant that will eventually reproduce and again generate seeds
We present the development of a genetic system to generate homozygous null mutants of Arabidopsis Polycomb repressive complex 2 (PRC2)
Generation of homozygous fie mutant plants Since the female gametophytic defect of mutants in FIS class genes can be bypassed by fertilization with cdka;1 mutant pollen [24], we asked whether this would allow the generation of homozygous fie mutant plants in crosses of heterozygous fie mutant mother plants with pollen of cdka;1-fie double heterozygous plants

Summary

Introduction

One common principle of flowering plants and probably one of the main reasons for their evolutionary success is the alternation of a dormant seed stage with a growing plant that will eventually reproduce and again generate seeds. Seeds harbor the plant embryo, i.e. the plant generation, but typically contain a nourishing tissue, called the endosperm that supports embryo growth and often provides the nutrients for the germinating seedling. The embryo and the endosperm are protected by a hard shall, the seed coat, that facilitates the distribution of seeds. Many factors have been identified to influence this transition from a dormant embryonic phase to a germinating seedling (for review see [1]). A unifying molecular framework has not been established so far

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