The locus sun on the short arm of tomato chromosome 7 controls morphology of the fruit. Alleles from wild relatives impart a round shape, while alleles from certain cultivated varieties impart an oval shape typical of roma-type tomatoes. We fine mapped the locus in two populations and investigated the genome organization of the region spanning and flanking sun. The first high-resolution genetic map of the sun locus was constructed using a nearly isogenic F(2) population derived from a cross between Lycopersicon pennellii introgression line IL7-4 and L. esculentum cv Sun1642. The mapping combined with results from pachytene FISH experiments demonstrated that the top of chromosome 7 is inverted in L. pennellii accession LA716. sun was located close to the chromosomal breakpoint and within the inversion, thereby precluding map-based cloning of the gene using this population. The fruit-shape locus was subsequently fine mapped in a population derived from a cross between L. esculentum Sun1642 and L. pimpinellifolium LA1589. Chromosome walking using clones identified from several large genomic insert libraries resulted in two noncontiguous contigs flanking sun. Fiber-FISH analysis showed that distance between the two contigs measured 68 kb in L. esculentum Sun1642 and 38 kb in L. pimpinellifolium LA1589, respectively. The sun locus mapped between the two contigs, suggesting that allelic variation at this locus may be due to an insertion/deletion event. The results demonstrate that sun is located in a highly dynamic region of the tomato genome.

Variation in fruit morphology is a prevalent characteristic among cultivated tomato. The genetic and developmental mechanisms underlying similarities and differences in shape between the fruit of two elongated tomato varieties were investigated. Fruit from two F2 populations constructed from either Solanum lycopersicum cv. Howard German or cv. Banana Legs crossed with S. pimpinellifolium accession LA1589, and one BC1 population constructed with S. lycopersicum Howard German as the recurrent parent, were analysed for shape by using a new software program Tomato Analyzer. Quantitative trait loci (QTLs) controlling 15 individual shape attributes were mapped by both single and multitrait composite interval mapping in each population. In addition, principal components analysis and canonical discriminant analysis were conducted on these shape attributes to determine the greatest sources of variation among and between the populations. Individual principal components and canonical variates were subjected to QTL analysis to map regions of the genome influencing fruit shape in the cultivars. Common and unique regions, as well as previously known and novel QTLs, underlying fruit morphology in tomato were identified. Four major loci were found to control multiple fruit shape traits, principal components, and canonical variates in the populations. In addition, QTLs associated with the principal components better revealed regions of the genome that varied among populations than did the QTL associated with canonical variates. The QTL identified can be compared across additional populations of tomato and other fruit-bearing crop species.

Fruit shape is a quantitatively inherited character. In tomato, two major loci, sun and ovate, control fruit shape index, which is the ratio of fruit height over width. In this study, we measured many additional fruit shape features in three inter-specific F(2) populations using the software application Tomato Analyzer. These populations were derived from varieties carrying elongated fruit but for which the major shape loci differed. We compared the effect of the major fruit shape loci with overall shape, as well as with the distal and proximal end shape features in each population. sun and ovate represented the largest effect on fruit shape in the Howard German and Sausage F(2) populations, respectively. The largest effect QTL in the Rio Grande population carrying neither sun nor ovate, were fs8.1 on chromosome 8 and tri2.1/dblk2.1 on chromosome 2. These latter loci were also segregating in the other two populations, thus indicating common regions that control shape across the three populations. The phenotypic analyses showed that sun and ovate contributed to almost all aspects of shape such as the distal and proximal end features. In Rio Grande however, the largest effect QTL did not control all aspects of shape and the distal and proximal features were distinctly controlled in that population. Combined, our results implied that within the cultivated tomato germplasm pool the largest effect on elongated fruit shape was controlled by a combination of the loci sun, ovate, fs8.1 and tri2.1/dblk2.1.

Edible fruits, such as that of the tomato plant and other vegetable crops, are markedly diverse in shape and size. SUN, one of the major genes controlling the elongated fruit shape of tomato, was positionally cloned and found to encode a member of the IQ67 domain-containing family. We show that the locus arose as a result of an unusual 24.7-kilobase gene duplication event mediated by the long terminal repeat retrotransposon Rider. This event resulted in a new genomic context that increased SUN expression relative to that of the ancestral copy, culminating in an elongated fruit shape. Our discovery demonstrates that retrotransposons may be a major driving force in genome evolution and gene duplication, resulting in phenotypic change in plants.

Summary DNA sequences provide useful insights into genome structure and organization as well as evolution of species. We report on a detailed analysis of the locus surrounding the tomato (Solanum lycopersicum) fruit-shape gene SUN to determine the driving force and genome environment that foster the appearance of novel phenotypes. The gene density at the sun locus is similar to that described in other euchromatic portions of the tomato genome despite the relatively high number of transposable elements. Genes at the sun locus include protein-coding as well as RNA genes, are small in size, and belong to families that were duplicated at the locus an estimated 5-74 million years ago. In general, the DNA transposons at the sun locus are older than the RNA transposons, and their insertion pre-dates the speciation of S. lycopersicum and S. pimpinellifolium. Gene redundancy and large intergenic regions may explain the tolerance of the sun locus to frequent rearrangements and transpositions. The most recent transposition event at the sun locus involved Rider, a recently discovered high-copy retrotransposon. Rider probably arose early during the speciation of tomato. The element inserts into or near to genes and may still be active, which are unusual features for a high-copy element. Rider full-length and read-through transcripts past the typical transcription termination stop are detected, and the latter are required for mobilizing nearby sequences. Rider activity has resulted in an altered phenotype in three known cases, and may therefore have played an important role in tomato evolution and domestication.

Phenotypic diversity within cultivated tomato (Solanum lycopersicum) is particularly evident for fruit shape and size. Four genes that control tomato fruit shape have been cloned. SUN and OVATE control elongated shape whereas FASCIATED (FAS) and LOCULE NUMBER (LC) control fruit locule number and flat shape. We investigated the distribution of the fruit shape alleles in the tomato germplasm and evaluated their contribution to morphology in a diverse collection of 368 predominantly tomato and tomato var. cerasiforme accessions. Fruits were visually classified into eight shape categories that were supported by objective measurements obtained from image analysis using the Tomato Analyzer software. The allele distribution of SUN, OVATE, LC, and FAS in all accessions was strongly associated with fruit shape classification. We also genotyped 116 representative accessions with additional 25 markers distributed evenly across the genome. Through a model-based clustering we demonstrated that shape categories, germplasm classes, and the shape genes were nonrandomly distributed among five genetic clusters (P < 0.001), implying that selection for fruit shape genes was critical to subpopulation differentiation within cultivated tomato. Our data suggested that the LC, FAS, and SUN mutations arose in the same ancestral population while the OVATE mutation arose in a separate lineage. Furthermore, LC, OVATE, and FAS mutations may have arisen prior to domestication or early during the selection of cultivated tomato whereas the SUN mutation appeared to be a postdomestication event arising in Europe.

Members of the plant-specific gene families IQD/SUN, OFP and YABBY are thought to play important roles in plant growth and development. YABBY family members are involved in lateral organ polarity and growth; OFP members encode transcriptional repressors, whereas the role of IQD/SUN members is less clear. The tomato fruit shape genes SUN, OVATE, and FASCIATED belong to IQD/SUN, OFP and the YABBY gene family, respectively. A gene duplication resulting in high expression of SUN leads to elongated fruit, whereas a premature stop codon in OVATE and a large inversion within FASCIATED control fruit elongation and a flat fruit shape, respectively. In this study, we identified 34 SlSUN, 31 SlOFP and 9 SlYABBY genes in tomato and identified their position on 12 chromosomes. Genome mapping analysis showed that the SlSUN, SlOFP, and SlYABBY genes were enriched on the top and bottom segments of several chromosomes. In particular, on chromosome 10, a cluster of SlOFPs were found to originate from tandem duplication events. We also constructed three phylogenetic trees based on the protein sequences of the IQ67, OVATE and YABBY domains, respectively, from members of these families in Arabidopsis and tomato. The closest putative orthologs of the Arabidopsis and tomato genes were determined by the position on the phylogenetic tree and sequence similarity. Furthermore, expression analysis showed that some family members exhibited tissue-specific expression, whereas others were more ubiquitously expressed. Also, certain family members overlapped with known QTLs controlling fruit shape in Solanaceous plants. Combined, these results may help elucidate the roles of SUN, OFP and YABBY family members in plant growth and development.