Network Analyses Reveal Shifts in Transcript Profiles and Metabolites That Accompany the Expression of SUN and an Elongated Tomato Fruit

SUN controls elongated tomato (Solanum lycopersicum) shape early in development through changes in cell number along the different axes of growth. The gene encodes a member of the IQD family characterized by a calmodulin-binding motif. To gain insights into the role of SUN in regulating organ shape, we characterized genome-wide transcriptional changes, and metabolite and hormone accumulation following pollination and fertilization in wild type (WT) and SUN fruit tissues. Pericarp, seed/placenta and columella tissues were collected at 4, 7 and 10 days after anthesis. Pairwise comparisons between SUN and WT identified 3,154 significant differentially expressed genes that cluster in distinct Gene Regulatory Networks (GRN). GRNs that were enriched for cell division, calcium/transport, lipid/hormone, cell wall, secondary metabolism and patterning processes contributed to profound shifts in gene expression in the different fruit tissues as a consequence of high expression of SUN. Promoter motif searches identified putative cis-elements recognized by known transcription factors and motifs related to Mitotic Specific Activator sequences. Hormone levels did not change dramatically, but some metabolite levels were significantly altered, namely participants in glycolysis and the TCA cycle. Also, hormone and primary metabolite networks shifted in SUN compared to WT fruit. Our findings imply that SUN indirectly leads to changes in gene expression most strongly of those involved in cell division, cell wall and patterning-related processes. When evaluating global co-regulation in SUN fruit, the main node represented genes involved in calcium-regulated processes, suggesting that SUN and its calmodulin-binding domain impact fruit shape through calcium signaling.