The roles of OVATE and other elongation genes in regulating proximal-distal patterning of tomato fruit

Domestication of tomato (Solanum lycopersicum) has resulted in a variety of fruit shapes from flat to very elongated. The elongated shape is a common feature that distinguishes many cultivated tomatoes from the undomesticated types, and it is mainly controlled by three loci, ovate, sun and fs8.1. We performed detailed morphological analyses of the reproductive and vegetative organs, which demonstrated that ovate, sun and fs8.1 regulate unique aspects of ovary and fruit elongation and in different temporal manners. The synergistic interaction between sun and ovate or fs8.1 suggested that the pathways involving SUN, OVATE and the gene(s) underlying fs8.1 may converge at a common node. We also conducted a transcriptome comparison analysis between the triple mutant sun/ovate/fs8.1 and wild type by RNA-seq using reproductive meristems and young flower buds. This study revealed changes in the transcription profile possibly caused by the combined effects of the three mutations. To gain insights into the role of OVATE in regulating fruit shape, we searched for its genetic and protein interactors. A synergistic interaction was found between ovate and suppressor of ovate 1 (sov1) in controlling ovary and fruit elongation. Tomato OVATE family protein 20 ( SlOFP20) was identified as a candidate gene underlying the sov1 locus. Yeast two-hybrid (Y2H) experiments showed that OVATE interacted with Tonneau1 Recruiting Motif (TRM) proteins, which are a part of a protein complex regulating the formation of preprophase band and organization of cortical microtubule (MT) array. Transient co-expression of OVATE or SlOFP20 with putative MT-associated SlTRMs in N. benthamiana resulted in relocalizations of SlOFPs and SlTRMs. Our findings have shed new light on the roles of OFPs in proximal-distal fruit patterning and provided insights into fundamental aspects of plant organ growth.