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First published online March 9, 2004; 10.1105/tpc.019158
© 2004 American Society of Plant Biologists Genetic Regulation of Fruit Development and RipeningUnited States Department of Agriculture–Agricultural Research Service Plant, Soil, and Nutrition Laboratory and Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York 14853 1 To whom correspondence should be addressed. E-mail jjg33{at}cornell.edu; fax 1-607-254-2958.
Fruit development and ripening are unique to plants and represent an important component of human and animal diets. Recent discoveries have shed light on the molecular basis of developmental ripening control, suggested common regulators of climacteric and nonclimacteric ripening physiology, and defined a new role for MADS box genes in this late stage of floral development. Analyses of fruit-ripening mutants and ripening-related gene expression suggest higher levels of a developmental regulatory cascade that remain to be defined. Examination of the molecular basis of ethylene signaling in tomato has demonstrated conservation of the basic model defined in Arabidopsis, yet with modifications in gene family composition and expression that may represent adaptations to promote successful fruit development and seed dispersal. The role of light signaling in fruit carotenoid accumulation is being examined and may represent a target for practical manipulation of fruit pigmentation and nutrient content. The continuing development of genomics tools, including ESTs and cDNA microarrays, for important fruit crops should foster accelerated discovery in fruit development and ripening research.
By anatomical definition, the fruit is a mature ovary and therefore typically includes carpel tissues in part or in whole. Many fleshy fruit species important to humans additionally develop mature fruit tissues, including extracarpellary floral components. Examples include strawberry, pineapple, mulberry, and pome fruit (apple, pear), in which the receptacle, bracts, calyx, and floral tube (the fused base of floral organs), respectively, constitute the majority of mature fruit tissue. Even species with fruit derived from carpel tissue exclusively can display a range of developmental programs, spanning the relatively uniform single expanded carpel or drupe of stone fruit to the differentiated carpel tissues giving rise to the peel (flavedo) and multicarpel flesh of citrus and banana. Evolutionary pressures have resulted in a variety of developmental manifestations of fruit tissues, resulting in structures that range in design and function from hardened fruit capsules or pods that forcefully expel seeds at maturation, to forms optimized for seed movement by wind, water, animal fur, or gravity, to those implementing developmental programs that yield succulent and flavorful tissues for organisms that consume and disperse the associated seed. Tanksley (this issue) discusses the impact of domestication on selection for fruit genes that influence size and shape early in fruit development in addition to discoveries regarding their underlying molecular functions. The focus here will be on recent advances in our understanding of developmental and signaling pathways that affect later fruit maturation and ripening.
Although dehiscent and dry fruit types (e.g., cereals) represent the majority of plant species, fruit developmental studies to date have focused primarily on fleshy species because of their importance in the human diet. Particular emphasis has been placed on tomato as an especially tractable system for molecular genetic analysis of fleshy fruit development and ripening (Giovannoni, 2001
Since the initial description of a requirement for the AGAMOUS (AG) protein for carpel and stamen determination (Bowman et al., 1989  ), a large family of Arabidopsis MADS box genes has been reported and in many cases functionally defined (Alvarez-Buylla et al., 2000, and references therein). For example, the redundant SEPALLATA genes (SEP1, SEP2, and SEP3) can be eliminated via mutation individually with minimal impact on floral development, yet the triple mutant results in the conversion of all floral organs to sepals, indicating roles in normal petal, stamen, and carpel development (Pelaz et al., 2000). Spatial constraint of AG expression via negative regulation by the APETALA2 (AP2) EREBP-like protein provided early evidence that additional transcription factors also play important roles in floral and carpel development, in part via the regulation of MADS box genes (Drews et al., 1991).
Additional insight into the molecular basis of carpel determination in the developing flower came through the recent discovery that two previously described MADS box SHATTERPROOF genes (SHP1 and SHP2; Liljegren et al., 2000
Given the diversity of fruit development programs across the plant kingdom and molecular insights developed in Arabidopsis (especially with respect to MADS box genes), it will be important to determine how this family has evolved in number, function, and target genes to facilitate fruit form and development in diverse plant species. Antisense repression of the tomato AG homolog TAG1 caused homeotic conversion of inner floral whorls similar to that observed in Arabidopsis ag mutants, whereas ectopic expression resulted in the development of red fleshy sepals, suggestive of ripe fruit tissues and consistent with a role in carpel determination (Pnueli et al., 1994b
The ripening of fruit organs represents the terminal stage of development in which the matured seeds are released. In the dehiscent fruit of the Arabidopsis silique, this process is facilitated by senescence of the mature carpel tissue followed by separation of the valves at an abscission cell layer (termed the dehiscence zone) that is formed between the valve-replum boundary. The MADS box SHP1 and SHP2 genes were shown originally to regulate the formation of the dehiscence zone (Liljegren et al., 2000 ) under the negative regulation of the FRUITFUL (FUL) and REPLUMLESS gene products, which together limit SHP expression to the dehiscence zone (Ferrandiz et al., 2000; Roeder et al., 2003). The SEEDSTICK MADS box gene was demonstrated recently to be required for the formation of the funiculus/seed abscission zone that allows separation of the seed from the carpel to facilitate seed dispersal at dehiscence (Pinyopich et al., 2003).
In contrast to Arabidopsis, fleshy fruits such as tomato undergo a ripening process in which the biochemistry, physiology, and structure of the organ are developmentally altered to influence appearance, texture, flavor, and aroma in ways designed to attract seed-dispersing organisms (Figure 1) (Seymour et al., 1993
Examples of common climacteric fruits that require ethylene for ripening include tomato, apple, banana, and most stone fruits, whereas nonclimacteric fruits, including grape, citrus, and strawberry, are capable of ripening in the absence of increased ethylene synthesis. Interestingly, climacteric fruit span a wide range of angiosperm evolution, including both dicots (e.g., tomato) and monocots (e.g., banana). Nevertheless, members of the same (e.g., melon) or closely related (e.g., melon and watermelon) species are reported to include both climacteric and nonclimacteric varieties. The molecular distinctions underlying climacteric versus nonclimacteric ripening are poorly understood. Nevertheless, it seems likely that at least in instances of the same or closely related species with examples of both climacteric and nonclimacteric types, that nonclimacteric phenotypes may represent mutations in ethylene synthesis or signaling as opposed to more complex distinctions. Indeed, nonclimacteric melons are notoriously difficult to harvest compared with their climacteric counterparts because of reduced abscission, suggesting a defect in ethylene synthesis or response and a mature phenotype consistent with incomplete ripening (Perin et al., 2002 ). In this regard, it is especially important when selecting a system for the analysis of nonclimacteric ripening to be certain that the ripening physiology of the candidate species is well characterized and consistent with nonclimacteric ripening as opposed to inhibited ripening resulting from reduced ethylene synthesis or response.
Although the specific role of climacteric respiration in fruit ripening remains unclear, the recruitment of ethylene as a coordinator of ripening in climacteric species likely serves to facilitate rapid and coordinated ripening. A great deal is known regarding specific downstream ripening processes in a number of climacteric and nonclimacteric species, yet little is known about the regulation of ripening in nonclimacteric fruit or the upstream regulation of ethylene in their climacteric counterparts. Recent evidence of the MADS box regulation of ripening in both tomato and strawberry suggests common regulatory mechanisms operating early in both climacteric and nonclimacteric species (Vrebalov et al., 2002
Tomato has emerged as the primary model for climacteric fruit ripening for a combination of scientific and agricultural reasons. The importance of tomato as an agricultural commodity has resulted in decades of public and private breeding efforts that have yielded numerous spontaneous and induced mutations, including many that affect fruit development and ripening (tomato germplasm can be viewed and ordered at the following World Wide Web sites: Tomato Genetic Resource Center [http://tgrc.ucdavis.edu/] and Hebrew University [http://zamir.sgn.cornell.edu/mutants/]). Simple diploid genetics, small genome size (0.9 pg per haploid genome [Arumuganathan and Earle, 1991 ]), short generation time, routine transformation technology, and availability of genetic and genomic resources, including mapping populations, mapped DNA markers (Tanksley et al., 1992), extensive EST collections (Van der Hoeven et al., 2002) (Table 1), publicly available microarrays, and a developing physical map, render tomato among the most effective model crop systems (http://www.sgn.cornell.edu/index.html). In addition, numerous single gene mutations that regulate fruit size, shape, development, and ripening (described below and by Tanksley in this issue) combined with dramatic and readily quantifiable ripening phenotypes (ethylene, color index, carotenoids, softening) have enhanced the use of tomato as a model for climacteric ripening (Figure 1).
Strawberry is the most widely studied system for nonclimacteric ripening, resulting in the identification and characterization of numerous ripening-related genes that affect cell wall metabolism, color, and aroma (Wilkinson et al., 1995b ; Manning, 1998; Aharoni and O'Connell, 2002). The octaploid nature of cultivated strawberry has limited genetic analysis in this species, although strawberry is readily transformed (Woolley et al., 2001) and diploid varieties are available. Recent and extensive EST sequencing of grape and to a lesser degree Citrus species (Table 1) suggests the possibility of their greater roles as models for nonclimacteric ripening, although the seasonal nature of these crops will limit their ultimate utilization as basic research systems.
Ethylene production in plant tissues results from Met metabolism (Yang, 1985 ). The rate-limiting steps in fruit ethylene synthesis include the conversion of S-adenosylmethionine to 1-aminocyclopropane-1-carboxylic acid (ACC) via ACC synthase (ACS) and the subsequent metabolism of ACC to ethylene by ACC oxidase (ACO). In tomato and most characterized plants, both steps are encoded by multigene families. At least four ACS genes are expressed in tomato fruit (Rottmann et al., 1991; Barry et al., 2000). LeACS1A and LeACS4 are under developmental control and are responsible for the initiation of ripening ethylene. Both are induced at the onset of ripening, and this induction is impaired by mutation at the ripening-inhibitor (rin) locus (Barry et al., 2000). Fruit homozygous for the rin mutation fail to exhibit the typical ripening-associated increase in ethylene production and do not ripen. Furthermore, although rin fruit are capable of responding to exogenous ethylene, as shown by the induction of ethylene-regulated gene expression, they do not ripen (Lincoln and Fischer, 1988). The rin locus encodes a MADS box transcription factor termed LeMADS-RIN, and the combination of mutant phenotypes described above has been interpreted to reflect a function in ripening control over climacteric ethylene synthesis (presumably via the control of LeACS1A and LeACS4) in addition to a regulatory process operating outside the sphere of ethylene influence (Vrebalov et al., 2002). LeACS4 is under ethylene control and thus facilitates autocatalytic ethylene production (characteristic of climacteric fruits) in response to ethylene resulting from LeACS1A and LeACS2 activity. The fourth tomato fruit ACS gene, LeACS6, is responsible for preripening ethylene synthesis and is repressed in response to ripening ethylene (Barry et al., 2000). Although most plant tissues harbor an excess of ACO activity, two tomato fruit ACO genes also are induced during ripening in response to ethylene and thus contribute to autocatalytic ethylene synthesis (Barry et al., 1996).
A presumed dioxygenase encoded by the E8 gene is upregulated during ripening and is related to members of the ACO family, yet it does not catalyze the conversion of ACC to ethylene (Deikman et al., 1992
Characterization of Arabidopsis ethylene response mutants, tests for epistatic interactions, and isolation of their corresponding genes have resulted in the development of an extensive network of ethylene signal transduction components (reviewed by Bleecker and Kende, 2000 ; Stepanova and Ecker, 2000). Several groups have isolated and characterized homologous genes from tomato in an effort to assess the degree of conservation of the basic signaling structure defined in Arabidopsis and to ascertain any variation (especially related to fruit development, ripening, and senescence) in crop species. The creation of ethylene-insensitive tomato and petunia plants via the introduction of dominant Arabidopsis ethylene receptor alleles demonstrated the functional conservation for this component of ethylene signaling (Wilkinson et al., 1997).
The first ethylene receptor identified in tomato was revealed through the isolation of the Never-ripe (Nr) fruit-ripening locus (Wilkinson et al., 1995a
Ethylene receptors in Arabidopsis have been shown to interact with the CONSTITUTIVE TRIPLE RESPONSE1 (CTR1) mitogen-activated protein kinase kinase kinase (Clark et al., 1998
The Arabidopsis ETHYLENE INSENSITIVE3 (EIN3) and related EIN3-like (EIL) genes encode transcription factors that represent downstream components of ethylene signaling (Chao et al., 1997
Analysis of ethylene signaling components in tomato suggests that at minimum, the early steps of the pathway demonstrate induction during ripening. Because ethylene receptors exhibit exceptionally strong ligand binding (Rodriguez et al., 1999
The molecular basis of ethylene synthesis and regulation has been a focal point of ripening analysis in the past, with more recent emphasis shifting to characterization of ethylene signal transduction (see above). Antisense repression of tomato ACS (Oeller et al., 1991 ) and ACO (Hamilton et al., 1990) genes and similar experiments in melon (Ben-Amor et al., 1999) clarified the role of these genes in regulating climacteric ethylene synthesis. It is well known, however, that ethylene alone is not sufficient for ripening and that a developmental "competence" to respond to ethylene must be achieved (Wilkinson et al., 1995a; Lelievre et al., 1997; Giovannoni, 2001). Consequently, immature fruit typically do not ripen in response to exogenous ethylene. Careful examination of multiple ripening phenotypes, including the production of volatile aroma compounds in ethylene-repressed transgenic melons, demonstrated that aspects of climacteric fruit ripening are regulated by developmental factors that must be properly coordinated with ethylene synthesis (Bauchot et al., 1998).
Developmental mutations that affect all aspects of the tomato fruit-ripening process have been available for decades and include the rin mutation (described above). A second mutation, termed non-ripening (nor), is phenotypically similar to rin in that nor fruit fail to produce climacteric ethylene or ripen yet show responsiveness to ethylene at the molecular level while similarly failing to ripen in response to ethylene (Lincoln and Fischer, 1988
Isolation of the rin locus revealed tandem MADS box genes separated by 2.6 kb of intervening genomic DNA (Vrebalov et al., 2002
Elucidation of the tomato rin locus provided the first molecular insight into the developmental regulation of climacteric ethylene synthesis and fruit ripening. The identification of a fruit-specific strawberry MADS box cDNA homologous with LeMADS-RIN suggests the tantalizing possibility that MADS box proteins may represent a conserved function in the regulation of ripening in both climacteric and nonclimacteric species (Vrebalov et al., 2002 ). Functional analysis of this gene through antisense repression in strawberry is in progress (K. Manning, G. Seymour, and J. Giovannoni, unpublished data). Finally, because MADS box genes have been shown to act as dimers or higher order heterogeneous multimers (Favaro et al., 2003), it is plausible that additional tomato MADS box genes may participate in ripening. More than 30 different members of the tomato MADS box family are available as ESTs (for tomato EST resources, go to http://www.tigr.org/tdb/tgi/lgi/ and http://www.sgn.cornell.edu/), and corresponding cDNA library representation indicates that transcripts for at least six of these genes are expressed in early ripening (breaker) or fully ripe fruit (for tomato gene expression based on EST prevalence, go to http://ted.bti.cornell.edu/digital/). LeMADS-MC, which was shown previously to be expressed in immature and ripe fruit (Vrebalov et al., 2002), in addition to these six genes (TDR4, TDR6, TAG1, TC125359/TM29, TC117868, and TC124330) are thus candidates for genes encoding MADS box proteins that may interact with LeMADS-RIN. TAG1 and SEP29 have been repressed in transgenic tomatoes (Pnueli et al., 1994b; Ampomah-Dwamena et al., 2002), and although it is unclear if additional MADS box genes may have been targeted in these lines, in both instances, ripening of mature carpel tissues did occur.
Phylogenetic analysis of available tomato and Arabidopsis MADS box genes indicates that LeMADS-RIN is most similar to the AGL3 and SEP genes of Arabidopsis (Figure 4) (Vrebalov et al., 2002
The LeMADS-RIN gene itself is induced at the onset of ripening without substantial influence by ethylene, indicating higher order regulatory control (Vrebalov et al., 2002 ). Comparative gene expression analysis in rin and nor fruit suggests an interesting subclass of ethylene-responsive genes, including E8, that respond to developmental signals and ethylene in rin but not nor fruit (DellaPenna et al., 1989). E8 expression has been characterized extensively and is induced to  30% of maximal ripening levels in mature green rin fruit at a time consistent with the onset of ripening and attains normal expression in response to exogenous ethylene (DellaPenna et al., 1989; Giovannoni et al., 1989). The bimodal regulation of E8 expression in rin and the absence of expression in nor, combined with the inability to induce ripening in either mutant via exogenous ethylene, defines a minimal regulatory network that operates during fruit ripening. In this network, ethylene regulates a subset of ripening genes either directly or in concert with developmental signals influenced by LeMADS-RIN and/or the nor gene product. E8 represents a regulatory motif in which nor but not LeMADS-RIN provides developmental control. In this instance, LeMADS-RIN affects E8 gene expression mainly via the activation of autocatalytic ethylene synthesis. Although numerous tomato ripening genes have been assessed for expression changes in rin, relatively few have been characterized in nor. Future characterization of ripening gene expression in nor will facilitate the further definition of developmental regulation during ripening, which is clearly affected by both mutations in ways that do not overlap. The nor locus has been cloned and encodes a putative transcription factor with no relationship to MADS box gene sequences (J. Vrebalov and J. Giovannoni, unpublished data). The availability of this sequence also should promote the refinement of the developmental regulatory network governing fruit ripening (Figure 2).
Additional tomato ripening mutants are available, and the cloning of their corresponding loci should further assist in the expansion of our understanding of ripening (Giovannoni, 2001
Ripening-related cell wall metabolism and associated textural changes have been a major focus of ripening research since the isolation of the tomato fruit POLYGALACTURONASE (PG) gene. PG has been reported to represent 1% of ripening fruit mRNA and results in substantial cell wall pectinase activity, in concert with the induction of ripening and softening (DellaPenna et al., 1989, and references therein). PG expression is inhibited substantially by both the rin and nor mutations, with additional influence by ethylene (DellaPenna et al., 1989). Both antisense repression (Smith et al., 1988) and ectopic expression in unripe fruit (Giovannoni et al., 1989) indicated that PG alone is not sufficient for softening. Nevertheless, a reduction in ripe fruit susceptibility to postharvest pathogenesis in antisense PG fruit led to the commercialization of PG antisense tomatoes.
The collapse of the hypothesis that PG represented the primary determinant of tomato fruit softening caused attention to turn to the isolation and functional analysis of alternative cell wall–associated and/or metabolizing proteins (reviewed by Brummell and Harpster, 2001
In addition to pectin-modifying enzymes, several hemicellulose-metabolizing enzymes have been characterized in ripening fruit. Repression of the ripening-related endo-ß-1,4-glucanases (also known as EGases or cellulases) CEL1 and CEL2 altered pedicel and fruit abscission, respectively, but did not influence fruit softening (Lashbrook et al., 1998 The complexity of cell wall ultrastructure is matched by an equally complex repertoire of cell wall–metabolizing and structural activities, many of which are encoded by multigene families that likely contribute to the difficulty of determining the molecular basis of fruit cell wall metabolism. Although considerable progress has been made in determining the biochemical contribution of specific cell wall proteins during fruit ripening, the molecular basis of fruit softening is still poorly understood and remains an active area of investigation.
Carotenoids, particularly lycopene and ß-carotene, represent the primary components of ripe fruit pigmentation in tomato. Genes encoding enzymes that catalyze carotenoid synthesis have been cloned from tomato and correspond to a number of previously defined pigmentation mutants (Bramley, 2002 ; Isaacson et al., 2002, and references therein). Examples include the yellow-flesh (r) mutation, resulting in deletion of the ethylene-regulated phytoene synthase (PSY) gene (Fray and Grierson, 1993), loss of or reduced expression of the carotenoid isomerase gene, resulting in the prolycopene-accumulating orange fruit of the tangerine mutants (Isaacson et al., 2002), and overexpression and knockout mutations of the lycopene-ß-cyclase gene, resulting in high-ß-carotene Beta (B) and deep-red crimson fruit, respectively (Ronen et al., 1999, 2000). Although a great deal has been learned about the structural components of the carotenoid synthesis pathway in recent years, regulation of flux through the pathway is largely a mystery. It is known that PSY is strongly induced by ethylene during ripening, indicating a major control point for total fruit carotenoid accumulation (Lois et al., 2000). In addition, analysis of quantitative trait loci associated with tomato fruit carotenoid metabolism indicates that multiple loci, in addition to known structural components, contribute to carotenoid flux (Liu et al., 2003).
Light has been shown to affect carotenoid accumulation in a number of species, including tomato. Alba et al. (2000)
The emergence of genomics technologies holds the promise of more rapid and comprehensive strides in elucidating ripening phenomena in coming years. Using a strawberry cDNA microarray, Aharoni et al. (2000) identified an acyl transferase that contributes to flavor development in one of the first demonstrations of large-scale expression analysis in fruit. Although the genome of a major fruit crop remains to be sequenced, review of the public EST collections is an indicator of where developments are likely to occur in the near future. More than 150,000 tomato ESTs have been developed and deposited in public databases, making this the largest EST collection of any fruit crop species (Table 1). Represented are 27 different cDNA libraries defining at least eight tissue types and including >40,000 ESTs from fruit at various stages of development (Van der Hoeven et al., 2002). A similar number of total ESTs are available from grape. In fact, grape is currently the species for which the greatest number of fruit ESTs are publicly available (nearly 50% more fruit ESTs than for tomato). Interestingly, public EST resources are sparse to nonexistent for many of the most important fruit species in terms of worldwide consumption (Table 1).
ESTs derived from nonnormalized and nonsubtracted libraries can be informative in their own right in that the numbers and origins of ESTs within a contig can serve as a reflection of relative gene expression (Ewing et al., 1999
Although digital expression analysis can be useful for characterizing expression in tissues from which ESTs have been developed, this is not a feasible approach for targeted gene expression analysis. A publicly available tomato cDNA array has been developed with National Science Foundation funding that contains >13,000 elements representing 8,700 independent gene sequences (http://bti.cornell.edu/CGEP/CGEP.html). A companion database (http://ted.bti.cornell.edu/) has been developed to allow public deposition and retrieval of raw microarray data resulting from the use of the public tomato array according to MIAME guidelines (Brazma et al., 2001
Special thanks to Ruth White for assisting with technical aspects of the manuscript and Zhangjun Fei for informatics assistance. Thanks to Julia Vrebalov, Zhangjun Fei, and Georgina Aldridge for assistance with figures and to Cornelius Barry for helpful discussions. Research in my laboratory is supported by grants from the National Science Foundation (DBI-9872617 and DBI-0211875), the U.S. Department of Agriculture (00-35300-9356), Initiative for Future Agriculture and Food Systems (2001-52100-11347), the U.S.–Israel Binational Agricultural Research and Development Fund (IS-3333-02), and the U.S. Department of Agriculture–Agricultural Research Service.
Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.019158. Received November 11, 2003; accepted January 14, 2004.
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THE FRUIT ORGAN: DIVERSE...
5)-alpha-L-arabinan in the pericarp of Cnr, a ripening mutant of tomato. Plant Physiol. 126, 210–221.
