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Evolution of fruit size in tomato

Domesticated tomatoes can be up to 1000 times larger than their wild relatives. How did they get so big? In general, domesticated food plants have larger fruits, heads of grain, tubers, etc, because this is one of the characteristics that early hunter-gatherers chose when foraging for food. In addition to size, tomatoes have been bred for shape, texture, flavor, shelf-life, and nutrient composition, but it has been difficult to study these traits in tomatoes, because many of them are the result of many genes acting together. These genes are often located in close proximity on chromosomal regions called loci, and regions with groups of genes that influence a particular trait are called quantitative trait loci (QTLs). When a trait is influenced by one gene, it is much simpler to study, but quantitative traits, like skin and eye color in humans or fruit size in tomatoes, cannot be easily defined just by crossing different individuals. Now, with genome sequencing and genomics tools, chromosomal regions with QTLs can be mapped and cloned more easily than in the past. These genomic maps can also be compared across plant genomes to identify similar genes in other species. With this knowledge, breeders can improve tomato varieties as well as other less well known food plants in the family Solanaceae.

Dr. Steven D. Tanksley and his colleagues, Bin Cong and Luz S. Barrero, are studying QTLs that influence fruit size. Dr. Barrero, of the Corporacin Colombiana de Investigacin Agropecuaria (CORPOICA), Colombia, will be presenting this work at a symposium on the Biology of Solanaceous Species at the annual meeting of the American Society of Plant Biologists in Mrida, Mexico (June 29, 8:30 AM).

Tomato (Solanum lycopersicum) is a member of the Solanaceae or nightshade family, which also includes potato, eggplant, tobacco, and chili peppers. The center of origin and diversity of tomato and other solanaceous species is in the northern Andes, where endemic wild populations of these species still grow. Tanksley and his colleagues have been employing the data emerging from the International Tomato Genome Sequencing Project as well as the tools of structural genomics to clone and characterize the major gene and QTL responsible for extreme fruit size during tomato domesticationfas.

The first QTL, fw2.2, was the first ever cloned in plants and may have been the site of one of the earliest mutations in tomato that led to its selection by humans and subsequent domestication. The size of tomato fruit can vary up to 30% as a result of variation at this locus alone. Cloning and sequencing of this locus reveals that the wild type protein codes for a repressor of cell division. When the control sequence is mutated, the repressor protein is not expressed or only very little, leading to higher cell division during fruit development and, consequently, larger fruits.

However, fw2.2 and associated genes related to cell-cycle control and cell division are not solely responsible for extreme fruit size. Two other loci-- locule-number and fasciated (fas)-- influence fruit size indirectly by affecting the number of carpels, the female parts of the flower that will become seed chambers in the fruit. Most wild tomatoes have only 2-4 locules (ovary chambers) while domesticated varieties can have 8 or more, and it appears that increase in locule number can increase fruit size by 50%. The data indicate that, of the two loci, fas has the larger effect. Tanksley and his colleagues used positional cloning to isolate the fas locus.

Sequencing suggested that the fas gene encodes a protein (YABBY-like transcription factor) that controls transcription of DNA into RNA as the first step of gene expression. It also revealed that there were no changes in the protein coding region of the gene but rather the mutation consisted of an insertion in the first intron, which is a non-coding sequence embedded within the protein coding sequence. Although introns are not part of a gene's protein code and are removed from the RNA sequence before translation into proteins, they are nevertheless structurally and functionally important, as demonstrated in this locus. The presence of an insertion in this intron reduces expression of the fas gene. The scientists looked at where and when the gene is expressed and found it dramatically reduced in developing flower buds in plants with high locule numbers.

Further comparisons of this locus across different tomato cultivars, including wild varieties, which turned out not to contain the mutation, suggests the mutation occurred relatively recently in tomato domestication and spread rapidly throughout modern tomatoes as a result of selection for extreme fruit size. Comparative genomics tools are being applied in both well-known and obscure solanaceous species. Conservation of genes and loci across a number of these species suggests that the knowledge gained from these efforts can also be applied in crop and yield improvement for other members of the Solanaceae.


Contact: Dr. Luz Barrero
American Society of Plant Biologists

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