Abstract
VERNALIZATION INSENSITIVE 3-LIKE (VIL) proteins are PHD-finger proteins that recruit the repressor complex Polycomb Repressive Complex 2 (PRC2) to the promoters of target genes. Most known VIL targets are flowering repressor genes. Here, we show that the tomato VIL gene CRAWLING ELEPHANT (CREL) promotes differentiation throughout plant development by facilitating the trimethylation of Histone H3 on lysine 27 (H3K27me3). We identified the crel mutant in a screen for suppressors of the simple-leaf phenotype of entire (e), a mutant in the AUX/IAA gene ENTIRE/SlIAA9, involved in compound-leaf development in tomato. crel mutants have increased leaf complexity, and suppress the ectopic blade growth of e mutants. In addition, crel mutants are late flowering, and have delayed and aberrant stem, root and flower development. Consistent with a role for CREL in recruiting PRC2, crel mutants show drastically reduced H3K27me3 enrichment at approximately half of the 14,789 sites enriched in wild-type plants, along with upregulation of many underlying genes. Interestingly, this reduction in H3K27me3 across the genome in crel is also associated with gains in H3K27me3 at a smaller number of sites that normally have modest levels of the mark in wild-type plants, suggesting that PRC2 activity is no longer limiting in the absence of CREL. Our results uncover a wide role for CREL in plant and organ differentiation in tomato and suggest that CREL is required for targeting PRC2 activity to, and thus silencing, a specific subset of polycomb targets.
Highlights
Polycomb Repressive Complex 2 (PRC2) is a conserved complex that represses gene expression by trimethylating lysine 27 of histone H3 proteins (H3K27me3)[1–3]
One of the ways plants regulate the rate of maturation and differentiation is by changing gene expression
We show the importance of CRAWLING ELEPHANT (CREL) in multiple developmental processes and in the expression of multiple genes throughout the tomato genome
Summary
Polycomb Repressive Complex 2 (PRC2) is a conserved complex that represses gene expression by trimethylating lysine 27 of histone H3 proteins (H3K27me3)[1–3]. Some of these subunits are encoded by small gene families, allowing the formation of multiple, distinct complexes. Different plant PRC2 complexes have been shown to regulate specific developmental processes such as endosperm development, flowering time and flower development [2,3]. One of the most characterized PRC2-regulated processes in Arabidopsis is the induction of flowering in response to prolonged cold, termed vernalization. PRC2 promotes flowering by silencing the flowering inhibitor FLC. The vernalizationspecific VRN-PRC2 complex is recruited to FLC by complexing with PHD proteins from the VERNALIZATION INSENSITIVE 3-LIKE (VIL) family [7,11–13]. In Arabidopsis, the VIL family consists of 4 members, including VIN3 and VRN5. VIL proteins repress additional members of the FLC family during vernalization, and VRN5 and VIL2 are involved in other flowering pathways [7,11,14,15]
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