SUNRegulates Vegetative and Reproductive Organ Shape by Changing Cell Division Patterns      

Abstract

One of the major genes controlling the elongated fruit shape of tomato (Solanum lycopersicum) is SUN. In this study, we explored the roles of SUN in vegetative and reproductive development using near isogenic lines (NILs) that differ at the sun locus, and SUN overexpressors in both the wild species LA1589 (Solanum pimpinellifolium) and the cultivar Sun1642 background. Our results demonstrate that SUN controls tomato shape through redistribution of mass that is mediated by increased cell division in the longitudinal and decreased cell division in the transverse direction of the fruit. The expression of SUN is positively correlated with slender phenotypes in cotyledon, leaflet, and floral organs, an elongated ovary, and negatively correlated with seed weight. Overexpression of SUN leads to more extreme phenotypes than those shown in the NILs and include thinner leaf rachises and stems, twisted leaf rachises, increased serrations of the leaflets, and dramatically increased elongation at the proximal end of the ovary and fruit. In situ hybridizations of the NILs showed that SUN is expressed throughout the ovary and young fruit, particularly in the vascular tissues and placenta surface, and in the ovules and developing seed. The phenotypic effects resulting from high expression of SUN suggest that the gene is involved in several plant developmental processes.Tomato (Solanum lycopersicum) accessions feature a variety of fruit shapes and sizes (Paran and van der Knaap, 2007). Genes controlling fruit morphology offer important insights into the patterning of the organ and mechanisms by which organ shape and size are realized. One of the major tomato fruit shape genes is SUN, which, when expressed at high levels in the fruit, leads to an elongated shape (Xiao et al., 2008). The mutation that led to the identification of SUN was a gene duplication event mediated by the retrotransposon, Rider. The duplicated gene was placed in a novel genome environment, leading to high expression in the fruit (Xiao et al., 2008;Jiang et al., 2009). When overexpressing SUN under the control of the cauliflower mosaic virus 35S promoter in tomato, the transgenic plants produce extremely elongated and often seedless fruits (Xiao et al., 2008). SUN encodes a protein belonging to the IQD family and is characterized by the conserved IQ67 motif that is involved in calmodulin binding Levy et al., 2005;Xiao et al., 2008). The function of this family of proteins is poorly understood. Overexpression of the Arabidopsis (Arabidopsis thaliana) gene AtIQD1 increases the production of the secondary metabolite glucosinolate , whereas the high expression of SUN leads to elongated fruit shape. However, the biochemical mechanisms by which these phenotypes are realized are unknown. Moreover, gene expression studies in tomato did not show dramatic differences in the tomato with or without SUN (Xiao et al., 2009). Yet, the parthenocarpic fruit development associated with SUN overexpression led us to hypothesize that SUN may be involved in the production of a hor...

Regulatory change in cell division activity and genetic mapping of a tomato (Solanum lycopersicum L.) elongated-fruit mutant

“…Histological observation revealed that the elongated ovary shape of Slelf2 at −4 and 0 DAF was due to longitudinal expansion, whereas the Slelf3 ovary was greatly altered in the proximal region ( Figure 4A). Overexpression of SUN reportedly stimulates ovary elongation and is positively correlated with slender phenotypes in cotyledons, leaflets, and floral organs (Wu et al 2011). In addition, the effects of increased SUN expression after pollination can be observed in developing fruit at 5 DAF, which corresponds to the cell division stage of fruit development (van der Knaap and Tanksley 2001;).…”

The IQD Family of Calmodulin-Binding Proteins Links Calcium Signaling to Microtubules, Membrane Subdomains, and the Nucleus

“…Coexpression assays demonstrated that IQD1 colocalizes with CaM2 to MT arrays , which suggests a role for IQD1 in linking Ca 2+ -CaM signaling to the regulation of MT-associated processes . Additional support for IQD functions at MTs is indirectly provided by studies in tomato, which showed that duplication of the IQD12/SUN locus causes elongated fruits, altered cell shape, and twisted stems (Xiao et al, 2008;Wu et al, 2011). These phenotypes are reminiscent of plants with mutations in tubulin subunits (Ishida et al, 2007) and several MAPs (Buschmann et al, 2004;Sedbrook et al, 2004).…”

“…6, A-D), indicating the functionality of the fusion protein. Helical growth aberrations and altered leaf shape were reported for tomato sun lines (Wu et al, 2011) and often are associated with defects in MT functions (Buschmann et al, 2004;Ishida et al, 2007). Moreover, the growth defects are reminiscent of plants overexpressing LONGIFOLIA1/TON1 RECRUITING MOTIF2 (TRM2), which encodes a plant-specific MAP (Lee et al, 2006;Drevensek et al, 2012).…”

Comprehensive Tissue-Specific Transcriptome Analysis Reveals Distinct Regulatory Programs during Early Tomato Fruit Development

“…In situ hybridization was performed using digoxigenin-labeled probes as described by Wu et al (2011) with minor modifications. Gene-specific fragments for probe synthesis were amplified by PCR using primers 59-ATGGCTTCCATGAAGTTGC-39 and 59-TCAGATACGAAGAAAATTATTAGGG-39 for OSP and 59-GAACA-GATACCAAACACAAGCAA-39 and 59-AAACCCCAGTTTTCACATGC-39 for ACO4.…”