SUN Regulates Vegetative and Reproductive Organ Shape by Changing Cell Division Patterns 1[C][W][OA] Shan Wu, Han Xiao 2 , Antonio Cabrera, Tea Meulia, and Esther van der Knaap* Department of Horticulture and Crop Science (S.W., H.X., A.C., E.v.d.K.) and Molecular and Cellular Imaging Center (T.M.), Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 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 retrotrans- poson, Rider . The duplicated gene was placed in a novel genome environment, leading to high expres- sion 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 character- ized by the conserved IQ67 motif that is involved in calmodulin binding (Abel et al., 2005; Levy et al., 2005; Xiao et al., 2008). The function of this family of proteins is poorly understood. Overexpression of the Arabi- dopsis (Arabidopsis thaliana) gene AtIQD1 increases the production of the secondary metabolite glucosinolate (Levy et al., 2005), whereas the high expression of SUN leads to elongated fruit shape. However, the biochem- ical mechanisms by which these phenotypes are real- ized 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 hormone or secondary metabolite that affects the auxin pathway either directly or indirectly (Xiao et al., 2008). It has been hypothesized more than 200 years ago that carpels are modified leaves (Goethe, 1970; Coen, 2001). The notion has gained strong support from studies on flower and fruit development, indicating that floral organs and leaves are partly interchangeable through modifying only a small set of regulatory genes (Honma and Goto, 2001; Pelaz et al., 2001; Alonso- Cantabrana et al., 2007; Østergaard, 2009). Several tomato genes known for their roles in fruit set and growth also exert effects on leaf morphology (Jones 1 This work was supported by the U.S. Department of Agriculture (grant no. 2007–35304–18295) and the National Science Foundation (grant no. DBI 0227541). 2 Present address: Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China. * Corresponding author; e-mail vanderknaap.1@osu.edu. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Esther van der Knaap (vanderknaap.1@osu.edu). [C] Some figures in this article are displayed in color online but in black and white in the print edition. [W] The online version of this article contains Web-only data. [OA] Open Access articles can be viewed online without a sub- scription. www.plantphysiol.org/cgi/doi/10.1104/pp.111.181065 Plant Physiology Ò , November 2011, Vol. 157, pp. 1175–1186, www.plantphysiol.org Ó 2011 American Society of Plant Biologists. All Rights Reserved. 1175 Downloaded from https://academic.oup.com/plphys/article/157/3/1175/6108884 by guest on 08 June 2022