The VIL gene CRAWLING ELEPHANT controls maturation and differentiation in tomato via polycomb silencing

• Type of Material: Article
• Authors: Ido Shwartz, Hebrew University of Jerusalem; Chen Yahav, Hebrew University of Jerusalem; Neta Kovetz, Hebrew University of Jerusalem; Matan Levy, Hebrew University of Jerusalem; Alon Israeli, Hebrew University of Jerusalem; Maya Bar, Hebrew University of Jerusalem; Katherine L Duval, Emory University; Ellen G Krall, Emory University; Naama Teboul, Hebrew University of Jerusalem; José M Jiménez-Gómez, Max Planck Institute for Plant Breeding Research; Roger Deal, Emory University; Naomi Ori, Hebrew University of Jerusalem
• Language: English
• Date: 2022-03-07
• Publisher: PLOS
• Publication Version: Final Published Version
• Copyright Statement: © 2022 Shwartz et al
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1371/journal.pgen.1009633
• Title of Journal or Parent Work: PLoS Genetics
• Volume: 18
• Issue: 3
• Start Page: e1009633
• End Page: e1009633
• Grant/Funding Information: This work was supported by grants from the United States – Israel Binational Science Foundation (BSF, 2015093) to N.O and R.B.D., German-Israel Project Cooperation Foundation (OR309/1-1;FE552/12-1) to N.O. and J.M.J.-and from the U.S. – Israel Binational Agricultural Research and Development Fund (IS4531-12(c) and IS5103-18R) and the Israel Science Foundation (grants number 2407-18 and 248-19) to NO; AI thanks the Azrieli Foundation for the award of an Azrieli fellowship. E.G.K. was supported by NIH training grant 5T32GM008490. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
• Keywords: Histones; Polycomb-Group Proteins; Lycopersicon esculentum; Drosophila Proteins; Polycomb Repressive Complex 2
• Research Categories: Biology, General

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.