A Cascade of Arabinosyltransferases Controls Shoot Meristem Size in Tomato

Shoot meristems of plants are composed of stem cells that are continuously replenished through a classical feedback circuit involving the homeobox WUSCHEL (WUS) gene and the CLAVATA (CLV)gene signaling pathway. In CLV signaling, the CLV1 receptor complex is bound by CLV3, a secreted peptide modified with sugars. However, the pathway responsible for modifying CLV3 and its relevance for CLV signaling are unknown. By studying mutants with enlarged meristems and branched inflorescences with extra flowers and floral organs, we show that tomato genes encoding arabinosyltransferases are essential for the CLV-WUS circuit. The most extreme mutant fasciated inflorescence (fin) is disrupted in a hydroxyproline O-arabinosyltransferase and can be rescued with arabinosylated CLV3. Chemically induced and CRISPR/Cas9 engineered mutations in the FASCIATED AND BRANCHED 2 (FAB2) and REDUCED RESIDUAL ARABINOSE 3 (RRA3)genes, encoding arabinosyltransferases predicted to extend arabinose chains, result in plants with fasciated and branched phenotypes, resembling but weaker than fin, indicating that CLV3 must be fully arabinosylated to maintain meristem size. Finally, we show that a mutation in CLV3 increased fruit size during domestication. Our findings uncover a new layer of complexity in the control of plant stem cell proliferation.