The Genetic, Developmental, and Molecular Bases of Fruit Size and Shape Variation in Tomato

Abstract

Fruit, corresponding to the plant's ovary (or ovaries), protect seed development and serve as the vehicle for seed dispersal to different habitats for species propagation. Fruit also provide humans with a source of nutrition, culinary diversity, and often great pleasure. Humans consume fruit from a wide range of plants, including members of the Rutaceae (citrus), Rosaceae (stone fruits, apples, pears), Solanaceae (eggplant, pepper, tomato, husk tomato), Cucurbitaceae (melons, squash, cucumbers), Ribaceae (berries), Vitaceae (grapes), and a multitude of additional species. Collage depicting wide variation in size and shape of tomato fruit. (A) The large-fruited tomato cv Giant Heirloom common to modern agriculture (right), and the typical fruit of a related wild species (L. pimpinellifolium). (B) The range of fruit size and shape variation in tomato. (C) Cross-section of the fruit from a plant homozygous for a mutation at the fasciated locus causing multiple locules. (D) Alternate allele of fasciated associated with unfused carpels. (E) Fruit from cv Long John, which carries mutations at both the sun and ovate loci causing extremely long, narrow fruit. (F) Bell pepper–type fruit produced by cv Yellow Stuffer. (G) Fruit from two different cultivars homozygous for a mutation at the ovate locus. In the variety at left, the ovate mutation results in the production of fruit that are both elongated and constricted at the stem end of the fruit (hence, the pear shape). However, in the processing variety at right, the ovate mutation causes elongated fruit but has a much reduced effect on neck constriction. The angular or square shape of the variety at left can be attributed to the fs8.1 locus. The topic of fruit growth and development can be approached with several questions in mind. From a global perspective, one can ask, What are the genes, proteins, and processes that specify or affect the formation of fruit? Of course, the answer to this question is that many if not most plant genes/proteins/processes influence fruit development. Plants compromised in photosynthesis, phloem transport, floral initiation/development, or male or female fertility either cannot produce fruit or are abnormal in their fruit production (e.g., parthenocarpic fruit, reduced fruit size, or reduced fruit load). As a result, many if not most tomato mutants have some alteration in their fruit phenotypes (Balbi and Lomax, 2003). Another question regarding fruit growth and development is, What are the underlying genetic, molecular, and developmental changes that permitted wild progenitors to produce the large, highly variable edible fruit associated with modern agriculture? Because this question is more narrowly defined, it is more likely to yield specific answers concerning processes unique to fruit development and relevant to agriculture. Thus, this review is focused on the question of how tomato fruit were changed by domestication. In approaching this topic, I try to summarize what is known about the alteration of fruit development during tomato domestication and to set forth a series of questions that need to be answered before we can claim any general understanding of this topic. L. esculentum was domesticated by native Americans, possibly in Mexico, and by the time Europeans arrived, large fruited types already were in existence (Jenkins, 1948; Rick, 1995). Because domestication occurred in prehistoric times, no one knows the actual evolutionary pathway by which wild species gave rise to plants with larger and variably shaped fruit. The most likely scenario is that early humans selected for mutations associated with larger fruit, and gradually, enough “large-fruited” mutations accumulated to give rise to our present-day cultivars. Genetic analysis of crosses between cultivated species and their wild relatives supports this idea, because progeny from these crosses almost always segregate in a continuous manner with respect to fruit size, indicating that the domestication process involved mutations at a number of different genetic loci (MacArthur and Butler, 1938; Banerjee and Kalloo, 1989). The quantitative nature of fruit size variation has severely inhibited the use of classic Mendelian techniques to identify and characterize the individual gene mutations associated with fruit domestication. Only recently has significant progress been made in identifying and cloning the underlying genes. The goal of this review is to both summarize our current knowledge of this topic and to frame some of the unanswered questions concerning the developmental and genetic control of fruit size and shape. However, before launching into a detailed discussion of this topic, it is worthwhile to summarize what is known about tomato fruit development. Stages of Tomato Fruit Development Based on Cong et al. (2002). The developmental timing of genes known to affect tomato fruit size and shape is shown at top. Other genes are known to affect fruit size and shape, but