A new class of regulatory genes underlying the cause of pear-shaped tomato fruit

Abstract

A common, recurring theme in domesticated plants is the occurrence of pear-shaped fruit. A major quantitative trait locus (termed ovate) controlling the transition from round to pear-shaped fruit has been cloned from tomato. OVATE is expressed early in flower and fruit development and encodes a previously uncharacterized, hydrophilic protein with a putative bipartite nuclear localization signal, Von Willebrand factor type C domains, and an Ϸ70-aa C-terminal domain conserved in tomato, Arabidopsis, and rice. A single mutation, leading to a premature stop codon, causes the transition of tomato fruit from round-to pear-shaped. Moreover, ectopic, transgenic expression of OVATE unevenly reduces the size of floral organs and leaflets, suggesting that OVATE represents a previously uncharacterized class of negative regulatory proteins important in plant development. F ruit-bearing crop plants have been domesticated from a wide range of wild plant species. One of the hallmarks of fruit-crop domestication has been an explosion in fruit shape variation (1, 2), and it is this variation that often determines the market of fruit-bearing crops. Despite its historical and economic importance, the molecular basis for fruit shape variation is largely unknown. Pear-shaped fruit is one of the most common recurring shape themes. Although uncommon in the wild, pearshaped fruit can be found in modern varieties of tomatoes, eggplants, melons, squash, pears, and other fruit-bearing plants. However, little is known about the ontology of pear-shaped fruit, except that the molecular events derailing the normal process of spherical growth apparently occur early in f lower development (3).Pear-shaped fruit possess several phenotypes that differ from those of wild-type fruit: whereas the wild types possess round shaped fruit with seeds distributed around the center of the fruit, pear-shaped fruit are elongated with conspicuous neck constrictions and seeds distributed asymmetrically toward one end of the fruit (4). In early literature on tomato genetics, ovate was described as a single recessive gene on chromosome 2 that is responsible for the pear-shaped tomato fruit traits (5-7). Recent genetic analyses have further identified ovate as a major quantitative trait (QTL) controlling pear-shaped fruit development in both tomato and eggplant (4,8).To shed light on the molecular basis and genetic lesion(s) involved in the creation of pear-shaped fruit, we have cloned the ovate locus from tomato. Protein annotation, overexpression studies, and the recessive nature of ovate indicate that OVATE represents a previously uncharacterized class of negative regulatory proteins important in plant development.

QTL hotspots in eggplant (Solanum melongena) detected with a high resolution map and CIM analysis

“…Colocalization of QTL for correlated traits was common and may suggest the pleiotropic activity of a single structural or regulatory gene. This phenomenon has been previously reported in tomato: fw2.2 and ovate are quantitative regulatory genes (Frary et al 2000;Liu et al 2002) that are most likely responsible for the clustering of fruit size and shape QTL on tomato chromosome 2. Alternatively, clusters of genes influencing related phenomena could arise from gene duplication followed by subfunctionalization such that the duplicate copies evolve slightly different but overlapping functions (for example, tissue-specific expression) (Lynch and Force 2000).…”

Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight

“…For example, TB1, one of these key regulatory genes, controls the morphological transition from wild species to cultivated maize [26], and the major QTLs fw2.2 [27], ovate [28] and qSH1 [29] control tomato fruit size, the transition of tomato fruit from round to pear-shaped and seed shattering, respectively. The identification of GW5 and the earlier reported GW2 as major QTLs that control rice-grain width lends strong support to the notion that "major morphological changes during evolution and domestication can be attributable to a few major regulatory genes of large effects rather than to many genes, each of which contributes a small effect to the changes" [37].…”

“…Regarding the origin of indica and japonica rice subspecies, one school of thought holds that indica and japonica rice originated independently from a wild ancestor [22][23][24]; others favor the notion that the japonica were derived from the indica [25]. Recent functional genomic studies have helped to excavate a number of domestication genes [26][27][28][29]. For example, sh4 and qSH1 are essential for effective field harvest because of their ability to reduce grain shattering [29,30].…”

Population structure and genetic differentiation associated with breeding history and selection in tomato (Solanum lycopersicum L.)

“…This observation suggests that there are 'hot spots' for directional selection through breeding in tomato. Genes on chromosome 2 that were segregating in our collection include the fruit shape gene, ovate (Liu et al, 2002) and loci affecting locule number (Barrero and Tanksley 2004). Chromosome 5 contains multiple bacterial disease-resistance genes including Pto (Martin et al, 1993) and Rx3 (Yang et al, 2005b), and genes that affect plant morphology, which were previously shown to distinguish processing from fresh-market tomatoes (Jones et al, 2007).…”