Carotenoids

Consumption of tomato products is associated with decreased risk of cardiovascular disease and certain cancers, including prostate and cervical cancer (Gio-vannucci et al. 1995; Gerster 1997; Clinton 1998; Gio-vannucci 1999; Paiva and Russell 1999). P-carotene is well recognized as a pro-vitamin A carotenoid. More recent discussions note the positive association between lycopene and health, but also emphasize that there are a family of beneficial compounds in tomato (Laquatra et al. 2005). Lack of efficacy upon ingestion of purified carotenoid supplements suggests that well-studied carotenoids such as lycopene may act synergistically with other compounds in protecting human health (Ellinger et al. 2006).

Carotene biosynthesis in higher plants has been reviewed extensively (Bartley and Scolnik 1994; Hirschberg 2001). The availability of cDNAs that code for nearly all of the enzymes required for carotenoid biosynthesis in plants has stimulated considerable interest in engineering plants with altered carotenoid content (Cunningham and Gantt 1998). Numerous candidate loci are available for marker-based studies (Table 14). Numerous successful and unsuccessful efforts to alter fruit carotenoid composition by manipulating expression of carotenogenesis transgenes have been reported (Fray et al. 1995; Romer et al. 2000; Rosati et al. 2000; Dharmapuri et al. 2002; Fraser et al. 2002; Mehta et al. 2002). Although transgenic plant development has generally been considered a more expedient route to develop superior cultivars, Zamir (2001) argues that approximately 10 years are required to create a transgenic cultivar for testing and that this time investment is similar to that needed for development and testing of new lines developed in traditional breeding programs using exotic germplasm.

Fruit Color Mutants A large body of genetic data exists for simply inherited genes that influence carotenoid content in tomato. More than 20 genes have been characterized in tomato that influence the type, amount, or distribution of fruit carotenoids. Many of the available color variants were first identified as spontaneous mutants in cultivars of S. lycopersicum, but also occur in wild tomato species. The Beta (B) allele located on chromosome 6 was first characterized in transgressive orange-fruited segre-gants descended from a cross between S. lycopersicum and the green-fruited species S. habrochaites (Lincoln et al. 1943; Kohler et al. 1947). Inheritance studies suggested that high concentrations of P-carotene conditioned by B were controlled by a single gene exhibiting incomplete dominance (Lincoln and Porter 1950). Subsequent studies by Tomes et al. (1954) suggested that B was dominant but subject to influence by a modifier gene, mo-B, which segregated independently of B. Expression of the dominant modifier reduces P-carotene:lycopene ratios resulting in red-orange fruit. Utilizing molecular markers linked to B and mo-B, genotypic evaluations discounted incomplete dominance to explain inheritance of fruit carotene content, but revealed that B and mo-B were linked on chromosome 6 and did not segregate as independent genes (Zhang and Stommel 2000). B encodes a novel lycopene P-cyclase that converts lycopene to P-carotene (Ronen et al. 2000). The introduction of B from accessions of S. galapagense, S. pimpinellifolium, S. chilense, and S. chmielewskii has also been described (Rick 1956; Manuelyan et al. 1975; Chalukova 1988; Stommel and Haynes 1994).

Locus Chromosome Allele synonyms Synonym Description Reference and arma

Carotenoid

Apricot (at)

Beta-carotene (B)

Delta (Del)

Diospyros (dps) Green flesh (gf)

12 S

11 S

High pigment-1 (hp-1) 2L

crimson (c)

Fruit flesh yellow with pinkish blush

Fruit flesh orange; increased P-carotene, reduced lycopene; encodes a chromoplast-specific lycopene P-cyclase Enhanced red color; increased lycopene, reduced P-carotene; phenotype similar to B°S

High P-carotene, low lycopene in ripe fruit Corolla tawny orange; increased fruit lycopene

Orange-red flesh; enhanced S-carotene and a-carotene Fractions; encodes lycopene £-cyclase

Fruit tissue is dusky orange

Chlorophyll retained in ripe fruit, normal lycopene synthesis; fruit reddish-brown

Phytoene synthesis normal, no colored carotenoids; encodes a plastid terminal oxidase

Resembles gf, except that center of fruit turns red

Immature fruit dark green; increased levels of carotenoids and ascorbic acid in mature fruit; encodes the uv-damaged DNA-binding proteinl Similar to hp-1, but more extreme phenotype

Jenkins and McKinney 1955

Lincoln and Porter 1950; Tomes et al. 1954; Ronen et al. 2000

Thompson et al. 1967; Ronen et al. 2000

Chmielewski and Berger 1966 Rick and Smith 1953

Tomes 1963; Ronen et al. 1999

Rick 1967 Kerr 1958a

Rick et al. 1959; Scolnik et al. 1987

Kerr 1958b; Barry et al. 2005

Clayberg et al. 1960; van Tuinen et al. 1997; Liu et al. 2004

Peters et al. 1989; Kerckhoffs and Kendrick 1997

L long; S short

Locus Chromosome Allele synonyms Synonym Description Reference and arma

High pigment-2 (hp-2)

High pigment-3 (hp-3) Intensified pigmentation (Ip) Modifier of B (mo-B)

Yellow (r)

Sherry (sh) Tangerine (t)

10 L

Colorless fruit epidermis (y) IS

Anthocyanin

Anthocyanin fruit (Aft)

Atroviolacium (atv) Aubergine (Abg)

7 10

provisional4 (prov4) provisional (prov5) reddish yellow (y)

virescent (v)

Similar to hpl; encodes deetiolatedl protein

Immature fruit dark green; increased levels of carotenoids in mature fruit Similar to hp2

Increased accumulation of carotenoids Enhanced lycopene synthesis Modifier of B; increases content of P-carotene in presence ofB Reduced polyenes, very low levels of carotenes; fruit flesh yellow; encodes phytoene synthase Fruit flesh yellow

Yellow fruit flesh; lighter yellow flowers Fruit flesh yellow Fruit flesh yellow

Modifier for red color in yellow fruit Fruit flesh yellow with reddish tinge Orange fruit and stamens; colored carotenoids principally prolycopene; encodes carotenoid isomerase Yellowish growing point; light green foliage; resembles t in flower and fruit color Fruit and flower color typical of t; irregular yellowing near growing point Unpigmented fruit epidermis; colorless skin over red flesh results in pink fruit

Variable purple pigmentation; anthocyanin in skin and outer pericarp Excess anthocyanin on fruit, stems and leaves Fruit epidermis purple, particularly on shoulder and where exposed to direct light

Yen et al. 1997; Mustilli et al. 1999

Konsler 1973; Levin et al. 2003

van Tuinen et al. 1997 Chetelat 2005 Rick 1974 Tomes et al. 1954; Zhang and Stommel 2000 Rick and Butler 1956; Fray and Grierson 1993

Stubbe 1963 Stubbe 1960 Chetelat 2005 Chetelat 2005 Young 1956

Zscheile and Lesley 1967 MacArthur 1934; Isaacson et al. 2002

Stubbe 1965

Lesley and Lesley 1956

Rick and Butler 1956

Giorgiev 1972; Jones et al. 2003

Rick 1964; Clayberg 1972 Ricketal. 1994a

Breakage of the linkage between B and sp, the gene for indeterminate growth habit, has eliminated this limitation of B for use in cultivars intended for commercial production (Stommel 2001; Stommel et al. 2005a, b).

In contrast with B, the recessive crimson mutant (c) enhances lycopene content at the expense of P-carotene (Thompson et al. 1967; Lee and Robinson 1980). Ronen et al. (2000) demonstrated that crimson is an allele of B and that null mutations in the B gene are responsible for the crimson phenotype. A second allele of B, og, similarly enhances fruit lycopene content. Crimson cultivars have been developed for their desirable dark red pigmentation. Recognition of health benefits attributable to lycopene in the diet has superseded any negative consequences of the loss in nutrients from reduced levels of P-carotene.

The recessive tangerine (t) mutant also conditions orange fruit color due to the accumulation of poly-cis-lycopene, also referred to as prolycopene (MacArthur 1934; Tomes 1963). Trans-lycopene is the principal form of lycopene in red tomato fruit. Located on chromosome 10, a clone of the tangerine gene, designated CRTISO, was shown to encode a carotenoid isomerase required during carotenoid desaturation (Isaacson et al. 2002). Analysis of two alleles of t demonstrated that in one case, loss of function in CRTISO was attributable to a deletion mutation in CRTISO, and in the second, expression of this gene was impaired. CR-TISO is normally expressed in all green tomato tissues but is up-regulated during fruit ripening and in flowers. Evidence that cis-lycopene is more bioavail-able than trans-lycopene (Boileau etal. 1999; Unlu et al. 2003) has focused considerable interest on this mutant in human nutrition-related studies. Fruit of the tangerine mutant also exhibit elevated phytoene and phytofluene. The dominant delta (Del) allele conditions increased fruit 6-carotene and reduced ly-copene content, resulting in reddish-orange colored fruit (Tomes 1963). Ronen et al. (1999) demonstrated cosegregation of the Crtl-e locus encoding e-cyclase with the Del mutation located on chromosome 12. e-cyclase converts lycopene to 6-carotene. Transcript for Crtl-e was shown to increase 30-fold in ripening fruit of the Del mutant. Additional orange color variants include the diospyros (dps) mutant with dusky orange fruit.

Introgression of the non-allelic high pigment-1 (hp-1) and high pigment-2 (hp-2) (Van Tuinen et al. 1997; Yen et al. 1997) mutant alleles enhances total fruit carotenoid content 30 to 50% without sig nificantly altering the relative percentage of different carotenoid constituents (Cookson etal. 2003). The hp-2 allele encodes the tomato homolog of the nuclear protein DEETIOLATED1 (DET1) from Ara-bidopsis that is involved in light signal transduction (Mustilli et al. 1999). The light hypersensitive dark green (dg) mutant (Konsler 1973) is allelic to hp-2 (Levin et al. 2003). Additional studies demonstrate that hp-1 is a mutation in a tomato UV-DAMAGED DNA-BINDING PROTEIN 1 (DDB1) homolog whose Arabidopsis counterpart interacts with DET1 (Liu et al. 2004). Additional alleles of hp-1 and hp-2, w and j, respectively, have been identified that exhibit varying photoresponsiveness (Kerckhoffs and Kendrick 1997). Studies of these high pigment mutants reveal that light signal transduction regulates the carotenoid pathway in a manner that affects total fruit carotenoid content and that genes encoding components of light signal transduction may provide new genetic tools for manipulating fruit nutritional value (Yen et al. 1997; Liuet al. 2004). Liuet al. (2004) demonstrated that two tomato light signal transduction genes, LeHY5 and LeCOP1LIKE, are positive and negative regulators of fruit pigmentation, respectively. Further studies reported additional putative light responsive genes that modulated carotenoid profiles in fruit of these light hypersensitive tomato mutants (Levin et al. 2004). Mature green fruit of these mutants is characteristically darker green due to elevated chlorophyll content (Baker and Tomes 1964; Palmieri etal. 1978). These high pigment mutations also increase fruit firmness and ascorbic acid levels (Jarret et al. 1984). Plants expressing both crimson and high pigment alleles produce fruit with lycopene levels three to four times that of conventional red-fruited tomatoes. Unfortunately, undesirable pleiotropic effects associated with these mutants have thus far limited their practical use.

The gene Ip, which has effects similar to that of the high pigment mutants, was described in progeny descended from a S. lycopersicum x S. chmielewskii cross (Rick 1974). Fruit expressingIp also exhibit dark green immature fruit and intensified carotenoid pigmentation in ripe fruit. Unlike hp mutants, Ip behaves as a dominant gene and appears to have reduced detrimental effects on seed germination and plant vigor.

A variety of additional fruit color mutants have been characterized. The recessive r gene located on chromosome 3 is responsible for yellow fruit flesh, resulting in greatly reduced levels of polyenes and very low levels of colored carotenoids (Rick and Butler 1956). The r locus is transcriptionally regulated andcorrespondstoanullmutationfor achromoplast-specific phytoene synthase, Psy1 (Fray and Grierson 1993; Fraser et al. 1994). A second phytoene synthase gene, Psy2, has been identified which is also expressed in ripening tomato fruit (Bartley and Scol-nik 1993). However, its transcripts are relatively more abundant in mature leaves. Lois et al. (2000) proposed that a second gene, DXS, encoding the first enzyme of isoprenoid synthesis in plastids, works in concert with Psy1 to control fruit carotenoid synthesis. The variant ry locus is an allele of r eliciting red color in yellow fruit (Young 1956). Variations on the yellow r mutant include the recessive apricot (at) locus on chromosome 5 (Jenkins and Mackinney 1955) and sherry locus on chromosome 10 (sh; Zscheile and Lesley 1967) that result in fruit that are characteristically yellow but with a pinkish/red blush at maturity. Expression of the ghost (gh) allele on chromosome 11 results in fruit that contain only phytoene and no colored carotenoids due to a block in the desaturation of phytoene (Rick et al. 1959; Scolnik et al. 1987). Incorporation of the recessive y allele results in a colorless fruit epidermis lacking normal yellow pigmentation (Rick and Butler 1956). The combination of y plus r results in pale yellow or "white" fruit. Presence ofy in red-fleshed genotypes results in a pink fruit pheno-type.

The recessive green flesh (gf) allele prevents the breakdown of chlorophyll that normally occurs in maturing fruit (Kerr 1958a). Retention of green chlorophylls in combination with lycopene in ripe fruit results in reddish-brown colored fruit. The Green ripe (Gr) mutant elicits green-pigmented flesh in ripe fruit (Kerr 1958b). Berry et al. (2005) mapped Gr to the long arm of chromosome 1 and determined that Gr is an ethylene insensitive mutant that may encode a novel ethylene signaling component.

Fruit Color QTL The described monogenic mutants have a dramatic effect on fruit pigmentation. Nonetheless, they have not contributed widely to enhanced carotenoid pigmentation in commercial cul-tivars. Extensive genetic and molecular characterization of simply inherited tomato pigment mutants has not established a molecular genetic basis for quantitatively inherited variation in fruit pigmentation. Not surprisingly, Liu et al. (2003) concluded that there is more to tomato fruit color than candidate genes involved in carotenoid biosynthesis.

Analogous to fruit firmness, soluble solids, and other fruit quality traits (see Sect. 1.15), QTLs associated with variation in fruit pigmentation have been described that begin to explain dissimilarity in intensity of red pigmentation in modern tomato cul-tivars (Table 15). Numerous QTLs introgressed from S. pimpinellifolium (Tanksley and Nelson 1996; Chen et al. 1999), S. habrochaites (Bernacchi et al. 1998a, b; Monforte etal. 2001; Kabelka etal. 2004; Yates etal. 2004), S. pennellii (Monforte et al. 2001; Liu et al. 2003; Frary et al. 2004), S. peruvianum (Fulton et al. 1997; Monforte et al. 2001; Yates et al. 2004), and S. neorickii (Fulton et al. 2000) have been described that influence fruit color. Analysis of QTLs identified in a S. ly-copersicum cross also revealed loci associated with enhanced fruit color (Saliba-Colombani etal. 2001; Causse et al. 2002). Not surprisingly, these QTLs may have negative or positive effects on ripe fruit color and epistasis as well as pleiotropy may occur. Whereas QTL studies often focus upon the positive effect of loci introgressed from wild relatives of tomato, wild species alleles often have a negative effect on fruit color (Kabelka et al. 2004). Encouragingly, all of these studies identify some QTLs associated with fruit quality attributes that have also been identified by others in different interspecific tomato crosses. Conserved major loci and minor loci with positive epistatic effects will be of great interest in marker-assisted breeding strategies to improve tomato quality and nutritive value.

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