Control of plant maturation and differentiation by VIL genes in tomato

Polycomb Repressive Complex 2 (PRC2) is a conserved complex that represses gene expression by trimethylating lysine 27 of histone H3 proteins (H3K27me3). In Arabidopsis, several discrete PRC2 complexes regulate different developmental processes, including flowering. The VERNALIZATION INSENSITIVE 3-LIKE (VIL) gene family recruit PRC2 to flowering repressor genes to promote flowering. The tomato crawling elephant (crel) mutation, affected in a tomato VIL gene, was isolated in a screen for modulators of leaf shape. In addition to being late flowering, crel affected many aspects of plant maturation and differentiation. crel mutants have delayed and impaired stem and root vasculature development, leading to a sprawling growth habit. Their leaves developed slower and were more complex than wild-type leaves, and their flowers did not reach full maturation and were sterile. Using genome editing, we generated mutations in the two additional tomato VIL genes, one of which also led to pleotropic effects on plant development. We found a genome-wide effect of crel on H3K27me3 methylation, and identified a set of genes that lost the methylation and were upregulated in crel in comparison to the wild type, representing putative CREL targets. These results show that CREL and other VIL proteins regulate diverse developmental processes via the modulation of H3K27me3 modifications of many genes throughout the tomato genome, likely by recruiting PRC2 complexes to a subset of their target genes. They further suggest that the role of VIL genes in plant development extends beyond flowering time.