Tomato HAIRY MERISTEM genes are involved in meristem maintenance and compound leaf morphogenesis

The HAIRY MERISTEM (HAM) genes function in meristem maintenance but play minor roles in the morphogenesis of a simple leaf that is determinate. Here, we functionally analyzed HAM genes in tomato and uncovered their involvement in compound leaf morphogenesis. Tomato encodes three HAM homologs, of which SlHAM and SlHAM2 (SlHAMs) are guided for cleavage by microRNA171 and are abundant in the shoot and floral meristems as well as in the compound leaf primordia. We found that SlHAMs silencing led to overproliferation of cells in the periphery of the meristems where SlHAM is localized. As in meristems, leaf-specific silencing of SlHAMs provoked overproliferation of meristematic cells in the organogenic compound leaf rachis. We further demonstrate that the meristematic cell overproliferation in both meristems and leaves was in part due to the misexpression of the stem cell regulator WUSCHEL, previously shown to be induced by cytokinin. Strikingly, reduction of cytokinin levels in SlHAMs-silenced leaves completely suppressed the overproliferation phenotype, suggesting a regulatory link between SlHAMs and cytokinin, a key hormone found to promote indeterminacy in meristems and leaves. Taken together, our data provide evidence that in addition to their conserved function in meristem maintenance, SlHAMs are also required for the proper morphogenesis of the compound leaf.