The Genetic, Developmental, and Molecular Bases of Fruit Size and Shape Variation in Tomato
Year: 2004
Type: article
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 the timing of their developmental control is currently unknown (see Table 1). The tomato genus, Lycopersicon, comprises nine species, of which only L. esculentum was domesticated. It is only in this cultivated species that one finds any significant phenotypic variation in fruit size and shape (Figure 1); the other eight wild species all produce fruit that are almost invariably round and small (Figure 1A). Yet, based on estimates made with DNA markers, these wild species are much more variable than their cultivated counterpart at the whole genome level. It is estimated that the genomes of tomato cultivars contain <5% of the genetic variation of their wild counterparts (Miller and Tanksley, 1990). In other words, cultivated tomatoes vary tremendously for fruit size and shape but have little genetic variation elsewhere in their genome. Conversely, wild tomatoes contain tremendous genetic variation in their genomes but show little variation in fruit size and shape. The explanation for this seeming paradox may rest on two factors. In the wild, tomato fruit are adapted for seed dispersal. Ripening fruit, with their soft flesh and ready supply of sugars and other nutrients, attract small rodents and birds. In this regard, small fruit may provide an advantage over large fruit for dispersal because they can be readily removed, carried, and dispersed. With regard to shape, a sphere is a very economical shape for packaging seeds, and it is unlikely that alternative shapes would have provided any benefits to dispersing animals. Also, as will be discussed below, mutations that increase size and/or change shape reduce the seed yield per gram of fruit tissue, something that would likely create a selective disadvantage. Why tomato fruit became progressively larger and more variable in shape during and after domestication is a matter of conjecture. However, the benefits to humans of increased fruit size seem apparent. Less time would be required to harvest a given mass of fruit from a large-fruited genotype than from a small-fruited genotype—a fact the reader can appreciate if given the choice of harvesting a bushel of apples versus a bushel of blueberries. It also seems logical that an increase in fruit size would contribute to an increase in total yield per plant or per unit area. However, although it is true that large-fruited modern varieties yield more than their small-fruited counterparts, to my knowledge there are no experimental data that demonstrate a cause-and-effect relationship between large fruit and higher overall yield. In fact, an experiment in which this was tested directly, using a cloned fruit size quantitative trait locus (QTL), failed to show any relationship between fruit size and total yield (Nesbitt and Tanksley; 2001; see below). Explaining the increase in fruit shape variation is more problematic. There may be several explanations for this phenomenon First, selection for increased fruit size may have led to changes in fruit shape attributable to pleiotropy (e.g., a mutation that increases fruit size may inherently change fruit architecture). There is good supporting evidence for this hypothesis with regard to the mutations that have led to increased fruit size through increases in carpel/locule number (Lippman and Tanksley, 2001; see below). Similarly, mutations that affect fruit shape may have greater phenotypic effects in large-fruited versus small-fruited genetic backgrounds. Several lines of experimental evidence support this notion. For example, a highly significant correlation was found between fruit size and fruit shape, such that larger fruit displayed more extreme shapes than did their small-fruited counterparts (van der Knaap and Tanksley, 2003). Additionally, a dominant allele of the fasciated locus (see below) manifests a very significant change in ovary shape when present in a large-fruited genotype but not in a small-fruited genotype (L. Barrero and S.D. Tanksley, unpublished results). Also, QTL mapping studies have shown that wild tomato species occasionally contain genes/alleles that, when transferred into large-fruited genotypes, change fruit shape from round to elongated or block shapes, despite the fact that the wild species bear small, nearly perfectly round fruit (Tanksley et al., 1996; Grandillo et al., 1999). Thus, selection for larger fruit may have been causally related to increased phenotypic variation in fruit shape by (1) fruit size loci having pleiotropic effects on fruit shape and/or (2) increased fruit size enabling the phenotypic expression of “hidden” fruit shape alleles that have little or no visible effect on fruit shape in small-fruited backgrounds. Another factor that may have contributed to changes in fruit shape are the demands of modern agriculture. For example, processing tomatoes, comprising those varieties used for juice, paste, and sauces, are field grown in large acreages and, on a per unit basis, have less value than do the fresh market tomatoes commonly sold in grocery stores. The high production demand and relatively lower value of processing tomatoes led to the development of machine-harvestable varieties starting in the 1960s. Typical round-fruited tomatoes are too soft for harvest by machines, so selection for firmer-fruited varieties resulted in a shape change from round to elongated or torpedo-shaped tomatoes (often called Roma tomatoes) (Figure 1G). Recent genetic studies have shown that this change in shape and the associated increased firmness were the result of mutations in three genes (ovate, sun, and fs8.1), which effect changes in fruit shape through modulations of early stages of carpel development (Table 1 List of Key Loci Controlling Size and Shape Variation in Tomato Position of the locus on the genetic map based on the most closely linked marker (for map, see http://www.sgn.cornell.edu/). The corresponding gene has been cloned and localized directly on the genetic map. List of Key Loci Controlling Size and Shape Variation in Tomato Position of the locus on the genetic map based on the most closely linked marker (for map, see http://www.sgn.cornell.edu/). The corresponding gene has been cloned and localized directly on the genetic map. As mentioned above, genetic studies, some dating back to the early parts of the last century, have established that tomato fruit size and shape are largely quantitatively inherited. This complexity of inheritance initially hampered efforts to understand the processes that control fruit size and shape at the molecular level. The advent of marker-assisted QTL mapping/cloning techniques has now made this a tractable problem. During the past 15 years, a number of QTL studies have been conducted involving crosses between wild tomatoes and cultivated tomatoes of various sizes and shapes (Grandillo et al., 1999). The conclusion of this research is that ∼30 QTLs account for most of the variation in both tomato fruit size and shape. However, these loci are not equal in the magnitude of their effects. Based on all of the genetic/mapping studies conducted to date, it is estimated that <10 loci, mapping to 7 of the 12 account for the of the changes in size and shape associated with tomato (Grandillo et al., (Table 1). the of these genes and the manner in which mutations in these genes developmental processes is to our understanding of fruit development and Thus, for the of this I on what is known about the developmental and, in some processes that are by these tomato fruit size and shape in loci seem to have been in the small, of wild tomatoes to the extremely large fruit now associated with modern cultivars (Figure Table 1). of our knowledge of these loci loci were as QTLs in crosses between small-fruited wild tomatoes and their large-fruited cultivated counterparts (Grandillo et al., 1999). several in First, they have been by multiple mapping and/or studies of nearly variation at these loci has a on fruit size and can change the fruit mass by as much as the effects of these loci to be largely to fruit mass and not fruit shape, with the of (van der Knaap et al., der Knaap and Tanksley, 2003). date, is the only one of these loci that has been cloned and at the molecular level. The knowledge from molecular studies of is It is that a in the locus on was one of the on the to domestication. genetic variation at this locus can change the size of fruit by to et al., wild tomatoes tested to have alleles at this all cultivated tomatoes tested are for studies with nearly lines have shown that the changes in fruit size associated with are most during the stages of fruit development (Nesbitt and Tanksley, 2001; Cong et al., and Tanksley, 2003). However, studies of the lines the causes of fruit size changes to stages of fruit development. alleles of are associated with a higher in during the after et al., (Figure of has shown that this locus for a of with largely to the of fruit development et al., Cong et al., is with other plant proteins, but of has a known has two a with studies with which show the to be localized to the Cong and S.D. Tanksley, unpublished results). The pathway in which in is currently but the hypothesis is that it is involved in the of of is that the mutations associated with changes from small to large fruit are in the than in the of the changes in the are associated with lower total during the of fruit development as as a in the timing of expression et al., in gene than have been as a of evolutionary concerning In this regard, is one of a number of in which variation associated with changes can be to mutations et al., Cong et al., It also is that, although has a on the of fruit the gene is at very and for only a time et al., In fact, despite the of a tomato many from of fruit no in the for and no has been for this gene Tanksley, unpublished results). with regard to other of the mutations in that changes in fruit size to affect only fruit date, no significant changes in plant fruit shape, or seed or yield are associated with variation at (Nesbitt and Tanksley, 2001; and Tanksley, 2003). such as affect fruit mass and do not effects on the overall or shape of fruit. However, fruit mass can be by changes in the shape and of the the tomato species, and many cultivated produce with a two to carpels. carpel into a in the fruit. However, some varieties produce fruit with more often in fruit (Lippman and Tanksley, 2001; der Knaap and Tanksley, (Figure loci, fasciated and have been as causing changes in fruit size changes in the number of in the (Table of the very fresh market tomatoes tested to mutations in one or both of these genes (Lippman and Tanksley, 2001; L. and S.D. Tanksley, unpublished results). The effect of mutations at the fasciated locus are more that those at the locus. Plants alleles at fasciated can produce locules. one allele of fasciated is associated not only with more but also with unfused (Figure Plants with the fasciated mutation also show increases in the number of other floral including and studies using lines have shown that phenotypic between and fasciated very early in floral development (L. Barrero and S.D. Tanksley, unpublished results). fresh market tomato varieties the fasciated However, the production of the extremely large fruit of some varieties the of not only the fasciated mutation but also the present these mutations to produce fruit with an high number greater (Lippman and Tanksley, 2001; L. Barrero and S.D. Tanksley, unpublished results). fasciated and in one significant Genetic studies have shown that the increase in carpel number associated with mutations at fasciated in a that such mutations a However, alleles in an the that the causing modulations in are than in The nature of the and developmental in which fasciated and genes cannot be both of these loci are As mentioned above, there is not a between the loci fruit size and those fruit shape. The genes fasciated and affect both the size and shape of the fruit. However, the other fruit size loci, and their effects largely on fruit in changes in size with little if any changes in shape. Similarly, there are three loci that fruit shape have a effect on fruit loci are ovate sun and fs8.1 (Table 1). of our current knowledge of of these loci In the early the of a locus tomato fruit by a at the stem end of the fruit and and During this a locus causing to fruit. It was shown that these genes were likely and the corresponding locus was to as ovate before research was conducted on the ovate when et al. nearly lines for ovate and that the locus account for both the pear shape and the elongated fruit shape. The ovate gene was cloned recently and shown to to a of et al., The gene is from the early stages of floral development after through the after et al., (Figure The mutation associated with a change from round to elongated or fruit a in the This mutation is with the of the elongated or allele in genetic studies et al., The of the mutation in ovate is However, a of has shown but a allele of and is to the of with elongated or fruit and S.D. Tanksley, unpublished results). of ovate is that the mutation is not associated with a In some genetic the mutation to elongated fruit with highly constricted neck growth of (Figure 1G). However, in other little or no neck is and the of fruit is not so that the ovate locus with as unknown loci in the genome (Figure 1G). During our genetic studies of the ovate we some processing tomato varieties with elongated fruit shape that did not the ovate QTL mapping with one of these the of a fruit shape locus on this locus was sun after the variety in which the locus was (van der Knaap and Tanksley, variation at both ovate and sun can elongated fruit shape, the two loci in some genetic, and developmental First, sun causes in both such that the fruit a ovate results in such that the stem end of the fruit is more than the Also, neck or pear shape has been associated with this locus (van der Knaap et al., developmental studies have shown that the changes in fruit shape associated with sun after during the of fruit development (van der Knaap and Tanksley, in much during floral development. alleles of sun in an the that mutations that to elongated fruit are than in nature (van der Knaap and Tanksley, The sun locus has been localized to a comprising and it seems likely that the molecular nature of this gene will be der unpublished results). The of the has been for several and is not based on In the early efforts in to harvesting for tomatoes, with on processing tomatoes, which are grown over large of the was that tomato fruit were too soft to harvest with any of the harvesting by a not be that would not the tomato fruit, tomato fruit to be that was what and the results led to machine-harvestable tomato (Figure 1G). early processing tomatoes two changes in fruit shape. First, they were no round but the individual on a more the fruit the of or (Figure 1G). It was this change that the of the fruit during Several QTL mapping studies have shown that a is for both the and elongated of processing tomatoes (Grandillo et al., studies with nearly lines have shown that the change in fruit shape attributed to fs8.1 very early in development et al., a with and the have already the elongated shape that will characterize to the fruit. Thus, it is that fs8.1 or during early floral development and has little if any after et al., (Figure in a variety of sizes and shapes (Figure The size and shape loci can the size and/or shape of tomato fruit. However, it has been these loci can account for the more extreme fruit sizes and For example, some varieties produce fruit of to (Figure 1A). varieties that produce fruit that nearly from fruit (Figure or that are extremely and narrow (Figure It is that several genetic studies involving extreme fruit size or shape varieties have the of two or more of the nine loci in this For example, the variety Giant Heirloom fruit size to the of and fasciated (Figure (Lippman and Tanksley, The most significant loci to the highly elongated fruit of cv Long are ovate and sun (Figure (van der et al., the fruit produced by the variety Yellow can be largely to the effects of and (Figure (van der and Tanksley, 2003). results that the of tomato size and shape from the small, round fruit of wild tomatoes was attributable to mutations at only a loci and that the nine loci were the most significant of this review has been to the question of which loci changes in tomato fruit during domestication. However, a and question is changes that occurred during the domestication of other fruit were attributable to mutations in genes or common developmental As above, a number of plant have been domesticated for the production of edible fruit. in most domestication resulted in both a increase in fruit size and variation in fruit shape. we can the genes and developmental that were to create large edible fruit in these different plant we may to answer this In this regard, there have been QTL mapping studies for fruit size and shape in multiple such as tomato, and et al., 2001; et al., Because these studies used genetic markers, it has been to identify fruit QTLs that are likely attributable to mutations in genes. Other between tomato and fruit size and shape are in Table the most of common is in of tomato and both of which from small-fruited wild QTL mapping involving a large-fruited variety and a small-fruited wild has the of as the most significant locus for increases in fruit size in the of domesticated et al., it is to any about the to which genes and were involved in the control of fruit size and shape in different However, the that than loci account for most of the variation in fruit size and shape in tomato and that at some of these genes to in other plants an underlying in this of plant development and significant progress has been made in identifying the loci involved in the large and variably shaped fruit that are of modern tomatoes, we are to understand how the by these genes fruit size and shape. The two shape and size QTLs cloned and for can be found in other plant species those that do not produce edible fruit, such as and of these has a known The for at the will be not only to the genes that size and shape variation more to the molecular and in which these of this for will be the need to understand the to which these are both and species. most of the to these questions in tomato and other plant species are now in to der and for on the This was by from the the of and the and Development
Source: The Plant Cell
DOI: 10.1105/tpc.018119
Author: S. D. Tanksley
Institution: Cornell University
Language: English
Subfield: Plant Science
Domain: Life Sciences
SDG: Zero hunger
Open Access status: green
Funder: National Science Foundation
OpenAlex ID: W2138891056