Domestication of many plants has correlated with dramatic increases in fruit size. In tomato, one quantitative trait locus (QTL), fw2.2, was responsible for a large step in this process. When transformed into large-fruited cultivars, a cosmid derived from the fw2.2 region of a small-fruited wild species reduced fruit size by the predicted amount and had the gene action expected for fw2.2. The cause of the QTL effect is a single gene, ORFX, that is expressed early in floral development, controls carpel cell number, and has a sequence suggesting structural similarity to the human oncogene c-H-ras p21. Alterations in fruit size, imparted by fw2.2 alleles, are most likely due to changes in regulation rather than in the sequence and structure of the encoded protein.In natural populations, most phenotypic variation is continuous and is effected by alleles at multiple loci. Although this quantitative variation fuels evolutionary change and has been exploited in the domestication and genetic improvement of plants and animals, the identification and isolation of the genes underlying this variation have been difficult.Conspicuous and important quantitative traits in plant agriculture are associated with domestication (1). Dramatic, relatively rapid evolution of fruit size has accompanied the domestication of virtually all fruit-bearing crop species (2). For example, the progenitor of the domesticated tomato (Lycopersicon esculentum) most likely had fruit less than 1 cm in diameter and only a few grams in weight (3). Such fruit was large enough to contain hundreds of seeds and yet small enough to be dispersed by small rodents or birds. In contrast, modern tomatoes can weigh as much as 1000 grams and can exceed 15 cm in diameter (Fig. 1A). Tomato fruit size is quantitatively controlled [for example, (4)]; however, the molecular basis of this transition has been unknown.Most of the loci involved in the evolution and domestication of tomato from small berries to large fruit have been genetically mapped (5, 6). One of these QTLs, fw2.2, changes fruit weight by up to 30% and appears to have been responsible for a key transition during domestication: All wild Lycopersicon species examined thus far contain small-fruit alleles at this locus, whereas modern cultivars have large-fruit alleles (7). By applying a map-based approach, we have cloned and sequenced a 19-kb segment of DNA containing this QTL and have identified the gene responsible for the QTL effect.Genetic complementation with fw2.2. A yeast artificial chromosome (YAC) containing fw2.2 was isolated (8) and used to screen a cDNA library (constructed from the small-fruited genotype, L. pennellii LA716). About 100 positive cDNA clones were identified that represent four unique transcripts (cDNA27, cDNA38, cDNA44, and cDNA70) that were derived from genes in the fw2.2 YAC contig. A high-resolution map was created of the four transcripts on 3472 F 2 individuals derived from a cross between two nearly isogenic lines (NILs) differing for alleles at fw2.2 ( Fig. 2A) (8). The fo...

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.

Plant domestication represents an accelerated form of evolution, resulting in exaggerated changes in the tissues and organs of greatest interest to humans (for example, seeds, roots and tubers). One of the most extreme cases has been the evolution of tomato fruit. Cultivated tomato plants produce fruit as much as 1,000 times larger than those of their wild progenitors. Quantitative trait mapping studies have shown that a relatively small number of genes were involved in this dramatic transition, and these genes control two processes: cell cycle and organ number determination. The key gene in the first process has been isolated and corresponds to fw2.2, a negative regulator of cell division. However, until now, nothing was known about the molecular basis of the second process. Here, we show that the second major step in the evolution of extreme fruit size was the result of a regulatory change of a YABBY-like transcription factor (fasciated) that controls carpel number during flower and/or fruit development.

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fw2.2 is a major quantitative trait locus that accounts for as much as 30% of the difference in fruit size between wild and cultivated tomatoes. Evidence thus far indicates that fw2.2 alleles modulate fruit size through changes in gene regulation rather than in the FW2.2 protein itself. To investigate the nature of these regulatory changes and the manner in which they may affect fruit size, a pair of nearly isogenic lines has been subjected to detailed developmental, transcriptional, mitotic, and in situ hybridization studies. The results indicate that the large-and small-fruited alleles of fw2.2 differ in peak transcript levels by Ϸ1 week. Moreover, this difference in timing of expression is associated with concomitant changes in mitotic activity in the early stage of fruit development. The changes in timing of gene expression (heterochronic allelic variation), combined with overall differences in total transcript levels, are sufficient to account for a large portion phenotypic differences in fruit weight associated with the two alleles. C ell division and expansion are generally considered two distinct phases during tomato fruit development (1). The rate of both cell growth and cell proliferation, which might be coordinated and instructed by cellular mechanisms, is critically important in determining final fruit size (2). Despite the fact that cell expansion may account for the greatest increase in volume, cell division is also an essential factor of fruit organogenesis because it determines the final cell number within the fruit. Therefore, fruit size is, in part, the result of a defined number of cell divisions that occur during development (3). High levels of cell division often take place in the first few weeks after anthesis, but mitotic cells can still be found in later phases of development, even in ripening fruit (4).Recently, increasing knowledge in molecular genetics has allowed the characterization of a number of molecular events that influence cell division or cell expansion. Many genes have been shown to control final organ size in Drosophila via cell division and cell expansion, such as dMYC (5), CyclinD͞Cdk4 (6), RAS (7), TSC1 and TSC2 (8), etc. In plants, recent research has yielded much evidence of the molecular and genetic control of cell division and expansion as well as organ size; for example, AINTEGUMENTA (ANT) (9, 10), ANGUSTIFOLIA and RO-TUNDIFOLIA3 (11), ABP1 (12), CLV and WUS (13), NtKIS1a (14), and CYC1At (15). Despite this recent progress, the precise molecular mechanisms governing organ size by cell division or expansion in plants remain far less clear than in Drosophila. Moreover, most genes characterized to control organ size in plants are associated with the development of leaves, roots, and shoot apical meristems. Less attention has been paid to developmental and molecular mechanisms that regulate fruit weight and size.Recently, molecular marker studies have found 28 quantitative trait loci (QTLs) affecting tomato fruit weight and size in crosses between the domesticated tomato...

We report the cloning of Style2.1, the major quantitative trait locus responsible for a key floral attribute (style length) associated with the evolution of self-pollination in cultivated tomatoes. The gene encodes a putative transcription factor that regulates cell elongation in developing styles. The transition from cross-pollination to self-pollination was accompanied, not by a change in the STYLE2.1 protein, but rather by a mutation in the Style2.1 promoter that results in a down-regulation of Style2.1 expression during flower development.

fw2.2 is one of the few QTLs thus far isolated from plants and the first one known to control fruit size. While it has been established that FW2.2 is a regulator (either directly or indirectly) of cell division, FW2.2 does not share sequence homology to any protein of known function (Frary et al. Science 289:85-88, 2000; Cong et al. Proc Natl Acad Sci USA 99:13606-13611, 2002; Liu et al. Plant Physiol 132:292-299, 2003). Thus, the mechanism by which FW2.2 mediates cell division in developing fruit is currently unknown. In an effort to remedy this situation, a combination of yeast two-hybrid screens, in vitro binding assays and cell bombardment studies were performed. The results provide strong evidence that FW2.2 physically interacts at or near the plasma membrane with the regulatory (beta) subunit of a CKII kinase. CKII kinases are well-studied in both yeast and animals where they form part of cell cycle related signaling pathway. Thus while FW2.2 is a plant-specific protein and regulates cell division in a specialized plant organ (fruit), it appears to participate in a cell-cycle control signal transduction pathway that predates the divergence of single- and multi-cellular organisms. These results thus provide a glimpse into how ancient and conserved regulatory processes can be co-opted in the evolution of novel organs such as fruit.

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