Journal of Experimental Botany, Vol. 53, No. 377, pp. 1995-2000,
October 1, 2002
© 2002 Oxford University Press
Recent advances in fruit development and ripening: an overview
Received 26 July 2002; Accepted 26 July 2002
Department of Plant Genetics and Biotechnology, Horticulture Research International, Wellesbourne, Warwick CV35 9EF, UK
1 Fax: +44 (0)1789 470552. E-mail: philip-j.white{at}hri.ac.uk
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This article provides an overview of the Journal of Experimental Botany Special Issue on Fruit Development and Ripening. It reports that significant progress is being made in identifying genes controlling the development of dry dehiscent fruits in the model plant species Arabidopsis thaliana. In plants with fleshy fruits, a major focus has been the dissection of biochemical and genetic regulatory cascades controlling ripening, using tomato as a model species. Intermediates of the ethylene-signalling cascade, potential cross-talk between ethylene and auxin signals, and the role of ethylene-independent signals have all been described in this climacteric fruit. The recent isolation of the NOR and LeMADS-RIN genes, which participate in ethylene-independent signalling in tomato, and the discovery that a homologue of the RIN gene is expressed in strawberry, a non-climacteric fruit, suggests that common regulatory cascades may operate in all fruits. Transcriptional profiling during the development and ripening of both climacteric (tomato) and non-climacteric (strawberry) fruit has supported these observations, and also identified a number of novel genes involved in the biochemistry of fruit development and ripening. The use of phylogenies based on chloroplast gene sequences has allowed an insight into the evolution of fruit forms and fruit biochemistry, which may be useful for the manipulation of commercial species. Several molecular approaches, including positional cloning, QTL mapping and genetic engineering, are helping to define the biochemical and molecular bases of texture, flavour, colour, and aroma. As the understanding of the biology of fruit ripening has improved, so has the ability to improve the organoleptic and nutritional qualities of fruits through crop management, breeding or biotechnology.
Key words: Key words: Arabidopsis thaliana, auxin, dehiscence, ethylene, Fragaria ananassa, ripening, Solanum lycopersicon, strawberry, tomato, transcription.
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Anatomically, fruits are swollen ovaries that may also contain associated flower parts. Their development follows fertilization, and occurs simultaneously with seed maturation. Initially, fruits enlarge through cell division and then by increasing cell volume. The embryo matures and the seed accumulates storage products, acquires desiccation tolerance, and loses water. The fruit then ripens. Ripening is accompanied by changes in flavour, texture, colour, and aroma. Fruits can be divided into two groups with contrasting ripening mechanisms. Climacteric fruit (such as tomato, avocado, apple, and banana) show a burst of ethylene biosynthesis and an increase in respiration during ripening, whereas non-climacteric fruits (such as strawberry, grape and citrus) do not. Fruits take many forms that have evolved to protect and disperse seeds. Seeds of most fleshy fruits are dispersed following consumption by frugivores, whereas seeds of dry fruits are mainly dispersed by the elements. A developmental process termed dehiscence, in which the fruit ruptures in a predetermined fashion, effects the release of seeds from a dry capsule or other fruit form. An attractive combination of colour, aroma and flavour assist the dispersal of seeds from fleshy fruits. Fruits are a significant part of the human diet, providing fibre, minerals, vitamins, and other beneficial compounds such as antioxidants. Hence, in addition to research programmes directed to understand and improve the organoleptic qualities of fruit, such as palatability, taste and aroma, significant efforts have also been invested in increasing the content in fruits of compounds that benefit human health. It is hoped that the ability to manipulate such traits through crop management, breeding or biotechnology will afford better nutrition as well as improved fruit quality.
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Recent advances in fruit development and ripening |
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The angiosperms (flowering plants) are defined by the possession of fruits and this differentiates them from the gymnosperms. Fruits are thought to have evolved to protect and disperse seed and, as such, are likely to have been, and to be, under strong selective pressure. About 70 million years ago, during the late Cretaceous or early Tertiary period, a great diversification of fruit forms occurred and, although this may be correlated with the rise of animals that disperse seeds, it may also have been driven by changes in climate and vegetation.
To gain an insight into the evolution of distinct fruit forms, Sandy Knapp from the Natural History Museum, London, has reviewed their occurrence within the angiosperms, and concludes that the various fruit forms have evolved repeatedly in a wide variety of clades (Knapp, 2002). To study this phenomenon further, she has mapped the five fruit types found in the Solanaceae family onto a molecular phylogeny founded on chloroplast gene sequences. This family contains 9 000 to 10 000 species in about 105 genera, including several of substantial agricultural (potato, tomato, pepper, aubergine) and medicinal importance (tobacco, mandrake, deadly nightshade, henbane). Knapp (2002) observes that the ancestral Solanaceous fruit type was the capsule. This appears to have given rise to both single-seeded drupes and multi-seeded pyrenes early in evolution, and to berries later in evolution. Although the juicy, multiseeded berries appear to have evolved independently from capsules several times, most belong to a single large, recently-evolved clade. All berries with stone cells, non-capsular dehiscent fruit (found mainly in Solanaceous species from arid zones) and mericarps (nutlets found in species of the peculiar genus Nolana) appear to have arisen independently several times from berries.
Knapp (2002) has also investigated the evolutionary origins of fruit size, colour and biochemistry in the genus Solanum using a phylogenetic approach. This genus contains between 1 000–2 000 species indigenous to habitats ranging from rainforest to desert. A few species of Solanum occurring in arid environments possess derived, non-capsular dehiscent fruits. All other Solanum species possess berries, but their size varies considerably. In isolated species from all clades placental enlargement and expansion, and an increase in locule number, has occurred. Similarly, berries with stone cells appear to have evolved several times, but their occurrence may have been selected against in domesticated species. The ancestral fruit colour appears to have been red, with both green and yellow being derived colours, but changes and reversions of fruit colour have occurred frequently during evolution. There is a wide variation in the secondary metabolites produced by different Solanum species, including many compounds involved in flavour. Knapp (2002) suggests that knowledge of how fruit size, colour and biochemistry have evolved under natural selection in Solanum could prompt novel strategies for their manipulation in a commercial context.
The release of seeds from dry fruits can be effected by a developmental process termed dehiscence. This process involves the differentiation of specialized cell types, and the strict co-ordination of both genetic and biochemical events that lead to cell separation and pod shatter. Recent commercial interest in dehiscence has focused on rape (Brassica napus), where its manipulation might improve crop yield. Since dehiscence is similar in both rape and Arabidopsis thaliana, the model Brassica has been used to accelerate scientific understanding of this process. In Arabidopsis, the dehiscence zone (DZ) extends the length of the silique and consists of a non-lignified separation layer (SL) situated between a region of lignified cells in the valve and the lignified vasculature of the replum. During the final stages of silique development, the middle lamella of the SL cell wall disintegrates, and the valve and replum tissues separate. Cristina Ferrándiz from The Instituto de Biología Molecular y Celular de Plantas, Valencia, has reviewed current knowledge of the genes involved in cell fate specification, in DZ differentiation, and in the biochemical and physiological changes occurring during cell separation in Arabidopsis siliques (Ferrándiz, 2002).
A variety of transcription factors have been implicated in controlling dehiscence (Ferrándiz, 2002). The first transcription factors shown to participate in DZ specification were the MADS-box genes SHATTERPROOF1 (SHP1) and SHATTERPROOF2 (SHP2). These functionally redundant genes are expressed specifically in the DZ where they appear to be upregulated by the AGAMOUS (AG) gene product. The expression of both SHP1 and SHP2 genes is also negatively regulated by the expression of another MADS-box gene, FRUITFULL (FUL), in the valve tissue. The FUL gene product also appears to regulate other factors in the valve involved in specifying DZ fate, including the expression of both YJ161, a putative zinc finger protein, and ALCATRAZ (ALC), a bHLH transcription factor. The bHLH transcription factor INDEHISCENT1 (IND1) is required for DZ differentiation. Although little is known of the cis-elements for these transcription factors, it is likely that the regulatory cascades they initiate result in the degradation of the middle lamellae of the SL cell walls by increasing the expression and activities of specific polygalacturonidases (PG), ß-1,4-glucanases (cellulases), and xyloglucan endotransglycosylases (XET). As for the hormonal control of dehiscence, Ferrándiz (2002) speculates that ethylene plays a minor role, while diverse evidence suggests that auxin is involved in the co-ordination of this process.
Tomatoes are climacteric fruit and their ripening is initiated by ethylene. As with many hormonal signals, responses to ethylene can be modulated both by changes in ethylene biosynthesis and by the presence (or absence) of cellular perception and signal transduction pathways. Both genes for ethylene biosynthesis (ACC synthase and ACC oxidase), as well as those encoding ethylene receptors, are transcriptionally regulated. In tomato, multigene families encode ACC synthases (LeACS) and ACC oxidases (LeACO), but LeACS2 and LeACO1 appear to dominate climacteric ethylene production. The expression of LeACO1 increases upon ripening and a recent analysis of its promoter has identified both a proximal ethylene-independent regulatory motif and several distal ethylene response motifs (Alexander and Grierson, 2002). This is consistent with the notion that an ethylene-independent developmental cascade determines the predisposition of tomato fruit to ripen. A protein with homology to zinc finger proteins may bind to the ethylene-independent regulatory motif to repress transcription of LeACO1 (Alexander and Grierson, 2002). To complement these observations, Harry Klee from the University of Florida has revealed how the transcriptional regulation of the ethylene receptor genes conditions what he terms as differential sensitivity to ethylene during the development of tomatoes (Klee, 2002). A family of six genes encodes ethylene receptors in tomato (LeETR1–6). These receptors act as negative regulators of downstream responses by suppressing the expression of ethylene-responsive genes in the absence of ethylene. Of particular interest is LeETR3, which is a homologue of the Arabidopsis AtETR1 gene. A semi-dominant mutation in LeETR3 is responsible for the Never ripe (Nr) phenotype, whose fruit never ripen. All LeETR genes are expressed in reproductive tissues (flowers and fruits), the most highly expressed being LeETR4. However, only the expression of LeETR3 (NR) changes dramatically during fruit ripening. LeETR3 (NR) is initially expressed highly in ovaries at anthesis, then drops until the onset of ripening when it rises steeply. Since ETRs bind ethylene so tightly, it appears that the only way to turn off a response to ethylene is to make more receptors. Hence, Klee speculates that the increased expression of LeETR3 (NR) during ripening might reduce ethylene responsiveness, and thereby prevent an excessive induction of ethylene responsive genes.
The five ethylene receptors of Arabidopsis (AtETR1-5) resemble bacterial two-component receptors, which consist of a sensor protein plus a separate response regulator protein that function together. Both AtETR1 and AtERS1 interact with AtCTR1, a Raf-like serine/threonine protein kinase (MAPKKK). Lucy Alexander and Don Grierson from the University of Nottingham report that tomato ethylene receptors (LeETRs) also interact directly with members of the LeCTR family of Raf-like protein kinases, which contains at least five genes (Alexander and Grierson, 2002). All LeCTR genes appear to be expressed constitutively in tomato fruit with the exception of TCTR1 (ER50), which is induced both by ripening and by exogenous ethylene (Bouzayen, 2002). Using a yeast two-hybrid screen of a cDNA library from tomato fruit, it has been shown that LeETR1 interacts directly with the N-terminus of the TCTR2 protein (Alexander and Grierson, 2002). However, all ethylene responses do not share a common biochemical signal-transduction pathway, since LeETR3 (NR) does not interact with TCTR2. Seven other proteins have been found that interact directly with LeETR3 (NR), several of which show increased expression during ripening, and a further four proteins have been shown to interact with TCTR2 and LeETR1 (Alexander et al., 2002). Interactions between the other members of the ethylene receptor family and all the LeCTRs are currently being investigated. It is likely that the kinase cascades initiated by the LeETR/LeCTR complex eventually impact on the expression of the LeEIL1–3 transcription factors (Alexander and Grierson, 2002). These are homologues of the Arabidopsis EIN3 gene and have been shown to function as positive regulators of many ethylene responses, probably through the activation of ERF1 transcription factors which upregulate the transcription of ethylene-responsive genes.
Evidence from biochemical and genetic studies imply that both ethylene-dependent and ethylene-independent regulatory cascades control the development of tomato fruit. Hence, although the non-ripening tomato mutants ripening-inhibitor (rin) and non-ripening (nor) do not produce autocatalytic ethylene nor ripen in the presence of exogenous ethylene, they do display signs of ethylene sensitivity and ethylene-inducible expression of several genes. Thus, it is likely that RIN and NOR participate in ethylene-independent regulatory cascades during the early stages of fruit ripening. Jim Giovannoni and colleagues from the Boyce Thompson Institute for Plant Research at Cornell have isolated the RIN and NOR genes by positional cloning strategies (Moore et al., 2002; Vrebalov et al., 2002). LeMADS-RIN encodes a member of the MADS-box family of transcription factors. Interestingly, homologues of LeMADS-RIN are expressed during the ripening of other fruit including strawberry, which might indicate a common (ethylene-independent) function in the ripening of both climacteric and non-climacteric fruit. Moore et al. (2002) also describe the development of a tomato cDNA microarray, which they have used to profile the expression of approximately 12 000 genes at ten stages during the ripening of wild-type fruit and in fruit of ripening mutants. In addition to identifying proteins directly effecting the physical and biochemical changes during fruit ripening, such comparative analyses should uncover more key transcription factors controlling the ripening process.
Asaph Aharoni and Ann O’Connell from PRI-Wageningen have used microarrays based on 1701 clones from a red strawberry fruit cDNA library (i) to profile gene expression at various stages during strawberry fruit ripening, and (ii) to compare gene expression in the achenes and receptacle tissue of ripe fruit (Aharoni and O’Connell, 2002). They observed that the abundance of 441 transcripts differed significantly between the achene and receptacle tissues. The most abundant transcripts in the achenes were those for components of genetic and biochemical regulatory cascades (including transcription factors, protein phosphatases and kinases, and 14-3-3 proteins), and proteins involved in the accumulation of storage products and in the acquisition of oxidative stress and desiccation tolerance. Interestingly, the expression profiles of several genes encoding components of regulatory cascades clustered with ABA-regulated genes, and a number of putative ethylene-response element binding factors (EREB) and ethylene-responsive genes were up-regulated in achenes. These observations are consistent with the notion that ABA plays a significant role in seed maturation, but also suggest a role for ethylene. By contrast, proteins related to primary metabolism (mainly gluconeogenesis), cell-wall modification, pigmentation, and the amelioration of oxidative stress were expressed highly in receptacle tissues. The expression of these genes presumably reflects the changes in flavour, aroma, texture, and colour that occur in this tissue during ripening. Thus, in addition to discovering the gene products underpinning the biochemistry of seed maturation and fruit ripening, the microarray approach is also yielding tissue-specific promoters and identifying key transcription factors and their cis-elements that may be useful for the manipulation of strawberry fruit ripening.
Fleshy fruits are frequently harvested prior to ripening and, following harvest, they have a relatively short shelf life during which they undergo profound changes in texture, colour and flavour. Graham Seymour and colleagues at HRI-Wellesbourne are investigating the biochemistry of fruit texture in order to improve the palatability and shelf life of produce (Marín-Rodríguez et al., 2002; Seymour et al., 2002). Marín-Rodríguez et al. (2002) review the role of pectate lyases in fruit softening. Pectate lyases (PEL) catalyse the Ca2+-dependent cleavage of de-esterified pectin, which is a major component in the primary cell walls of many higher plants. Initially, it was thought that these enzymes were produced solely by plant pathogens to macerate plant tissues. But, as a result of both plant genome sequencing and EST programmes, it has become clear that these enzymes are encoded by large gene families in plants (for example there are about 27 genes encoding PEL in Arabidopsis) and are expressed throughout the plant including ripening fruit. Fruits of tomato, strawberry, grape, and banana all express PEL, where they may play a significant role in fruit softening. Other enzymes involved in modifying cell wall properties include pectin esterases (PE) and polygalacturonidases (PG). These enzymatic activities are similarly encoded by multi-gene families, in which at least one member shows ripening-specific expression.
It is thought that knowledge of the identity and role of generic ripening-regulatory genes will enable the targeted manipulation of fruit ripening, fruit quality and shelf life (Moore et al., 2002; Seymour et al., 2002). Indeed, both the rin and nor mutations are already being used commercially to extend shelf-life in tomato. Seymour et al. (2002) have identified a rare dominant mutation in a tomato gene (Cnr, for colourless non-ripening) that results in a non-ripening phenotype with two distinct characteristics: (i) firm fruit with reduced cell adhesion and (ii) a complete absence of carotenoid biosynthesis in the pericarp. Since the mealy phenotype of Cnr fruit is the opposite of the juicy phenotype desired by the consumer, this mutant might provide an insight to the molecular biology of juiciness. Microarray analyses indicate that the expression of many genes impacting on many aspects of ripening is altered in the Cnr mutant, suggesting that Cnr may encode a regulatory factor. Several of these genes are themselves transcriptional regulators, including a MADS-box transcription factor (TDR4) homologous to the Arabidopsis FUL gene that may be linked to the mealy phenotype of Cnr fruit.
The manipulation of tomato fruit quality through genetic engineering is reasonably well advanced. In tomato, the isoprenoid biosynthetic pathway gives rise to carotenoids, such as ß-carotene (the precursor of vitamin A) and lycopene (a potent antioxidant, which gives the fruit its characteristic red colour), gibberellins, quinones, and sterols. This pathway has been well researched since its manipulation impacts not only on the organoleptic qualities of fruit but also their contribution to human health. Peter Bramley from Royal Holloway College, University of London, is dissecting the regulation of this metabolic pathway during tomato fruit ripening using transgenic and mutant plants (Bramley, 2002). He notes that although the control of gene expression is a key regulatory mechanism, post-transcriptional regulation of enzymes, metabolic channelling and feedback inhibition by ß-carotenoids also contribute. Through identifying the rate limiting steps of the pathway, he hopes to target appropriate transgene expression to achieve an increase in the concentrations of carotenoids without changing the levels of other isoprenoids.
Martine Verhoeyen and colleagues at Unilever Research and PRI-Wageningen have applied a similar rationale successfully to increase the levels of beneficial flavonoid antioxidants in tomato (Verhoeyen et al., 2002). Flavonoids are a diverse group of polyphenolic secondary metabolites. The important flavonols, kaempferol and quercetin, are synthesized from 4-coumaroyl CoA and malonyl CoA through the concerted action of chalcone synthase (CHS), chalcone isomerase (CHI), flavanone 3-hydroxylase (F3H), then flavanone 3'-hydroxylase for quercetin, and flavonol synthase (FLS). The most abundant flavonoid in tomato fruit, naringenin chalcone, is the first intermediate compound. The major flavonol glycosides, quercetin-rutinoside (rutin) and kaempferol-rutinoside, are derived from quercetin and kaempferol. The enzymes catalysing these reactions are present solely in the peel of tomato fruit, where flavonols and flavonol glycosides exclusively accumulate. Verhoeyen et al. (2002) observed that there was limited natural variation in the flavonoid content of tomato fruit and reasoned that genetic engineering would be required to increase their levels substantially. They found, using transgenic plants, that (i) the ectopic overexpression of CHI resulted in up to a 78-fold increase in the flavonol content of the peel (mainly quercetin-glycosides), (ii) the ectopic expression of two maize transcription factors (Lc and C1) resulted in the accumulation of kaempferol-glycosides in the flesh, and (iii) the ectopic expression of CHS, CHI and FLS together was sufficient to increase the kaempferol- and naringenin-glycoside content of the flesh, and the quercetin-glycoside content of the peel. None of these genetic manipulations had any gross effects on phenotype or adverse effects on taste. Such manipulations offer the possibility of developing new tomato varieties with increased health benefits.
The organoleptic quality of fruit is a complex characteristic involving all aspects of flavour, texture and aroma. To identify the major genetic components impacting on organoleptic quality Mathilde Causse and colleagues at INRA-Avignon have pursued a QTL approach with a mapping population of 144 recombinant inbred lines (RILs) derived from an intraspecific cross between a cherry tomato (Cervil) of high organoleptic quality and an inbred line (Levovil) with an unremarkable taste but bigger fruits (Causse et al., 2002). They studied 38 traits using a variety of physical and biochemical assays, plus a panel of trained tasters. Many traits were correlated. Sweetness and tartness, for example, were well described by sugar content and titratable acidity, suggesting that laboratory assays could replace a panel of tasters for some sensory traits and also allowing breeders simpler selection criteria. Similarly, many QTL overlapped. Indeed, the presence of QTL for organoleptic qualities was restricted to 14% of the genome, lying on chromosomes 1, 2, 3, 4, 8, 9, 11, and 12. The latter observation confirmed and extended previous studies using other mapping populations. Since small regions of the genome influenced several traits, Causse et al. (2002) have used both multitrait QTL analysis and local genetic-mapping techniques to determine whether this could be attributed to specific genes conferring pleiotropic phenotypes or to fortuitous genetic linkage. Such analyses will accelerate the development of molecular markers for breeding programmes and facilitate the identification of candidate genes to improve organoleptic quality.
Richard Watson and colleagues from the University of Nottingham and ADAS-Rosemaund report that many quality traits are strongly influenced by environment (Watson et al., 2002). They note that many volatile and non-volatile compounds give rise to the flavour of strawberry fruit. The volatile compounds give the fruit its distinctive flavour, whereas the non-volatile compounds, such as sugars and organic acids, are responsible for the fruit’s sweetness and tartness. Consumers desire a reproducible flavour for a particular cultivar. However, Watson et al. (2002) observe that there is often considerable variation in fruit flavour even within a single crop. To assess the variability in fruit flavour arising from management practice, they have used Atmospheric Pressure Chemical Ionization (APCI) and direct liquid-mass spectrometry techniques to determine how harvest date and shading affect the abundance of 13 volatile compounds and three non-volatile compounds (sucrose, glucose and citric acid) implicated in strawberry fruit flavour. They observed that the amounts of all the volatile compounds analysed differed significantly from fruit to fruit (perhaps through picking fruits of different maturity) and between harvests, but could discern no consistent trends. Similarly, the concentrations of glucose and citric acid varied considerably between fruits and between harvests, with no consistent trends. A decline in sucrose concentration occurred across the harvest period, which may have been associated with a decline in solar radiation during the season. The effect of shading was more consistent. A brief period of shading significantly reduced the amounts of volatile flavour compounds and the concentrations of sucrose and glucose in the fruit. These observations have direct implications for strawberry growers. In addition, Watson et al. (2002) suggest that a deeper understanding of the relationships between photosynthesis and secondary metabolism may eventually enable strawberry growers to manipulate fruit flavour through environmental management, and to produce fruit of a more consistent flavour and quality both within a crop and throughout the year.
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The papers in this Special Issue describe the recent discoveries in a number of areas. There is much scientific interest in identifying the key regulatory mechanisms involved in fruit development and ripening. Several papers describe the role of ethylene in the ripening of climacteric fruit (Alexander and Grierson, 2002; Klee, 2002; Moore et al., 2002). These concentrate on the elucidation of biochemical and genetic signalling cascades that impact on the development and ripening of tomato fruit. The recent isolation of the transcription factors NOR and LeMADS-RIN, which participate in ethylene-independent signalling in tomato, and the discovery that a homologue of the RIN gene is expressed in non-climacteric fruit, has suggested that common regulatory cascades may operate in all fruits. This knowledge could enable generic strategies to manipulate the ripening of any fruit. Such work has been complemented by transcriptional profiling during the development and ripening of both climacteric and non-climacteric fruit (Aharoni and O’Connell, 2002; Moore et al., 2002; Seymour et al., 2002), which may disclose more common regulatory elements.
The use of molecular phylogenies has revealed moments in the evolution of fruit forms and fruit biochemistry, which may be used to inform the manipulation of commercial species (Knapp, 2002). In addition, genomics tools have also been immensely useful in identifying and confirming the genes involved in fruit quality, and in defining the biochemical and molecular bases of texture, flavour, colour, and aroma. Key enzymes involved in fruit softening, and the genetic regulatory factors that influence fruit texture and shelf-life in tomato are being characterised (Marín-Rodríguez et al., 2002; Seymour et al., 2002). Molecular-markers for use in breeding programmes to improve the organoleptic qualities of tomato fruit have been developed using QTL approaches (Causse et al., 2002). Strategies for the manipulation of tomato fruit quality through genetic engineering to increase the levels of the carotenoids ß-carotene (the precursor of vitamin A) and lycopene (Bramley, 2002), and the flavonoid antioxidants quercetin and flavonol-glycosides (Verhoeyen et al., 2002), have been described. Hence, as the understanding of the biology of fruit ripening has improved, so has the ability to manipulate fruits for improved nutritional and organoleptic quality. Long may this vital trend continue.
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Acknowledgements |
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I thank Martin Broadley, Ken Manning, Richard Napier, and Graham Seymour (HRI-Wellesbourne), and all the authors of articles in this Special Issue, who commented on my original manuscript.
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Aharoni A, O’Connell AP. 2002. Gene expression analysis of strawberry achene and receptacle maturation using DNA microarrays. Journal of Experimental Botany 53, 2073–2087.
Alexander L, Grierson D. 2002. Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. Journal of Experimental Botany 53, 2039–2055.
Alexander L, Lin Z, Chen G, Kim S, Hackett R, Wilson I, Grierson D. 2002. Ethylene signalling in ripening tomato fruit. Comparative Biochemistry and Physiology, Part A: Molecular and Integrative Physiology 132, S97.
Bramley PM. 2002. Regulation of carotenoid formation during tomato fruit ripening and development. Journal of Experimental Botany 53, 2107–2113.
Bouzayen M. 2002. Ripening-associated transcriptional regulation in the tomato. A case of cross-talk between ethylene and auxin? Comparative Biochemistry and Physiology, Part A: Molecular and Integrative Physiology 132, S97.
Causse M, Saliba-Colombani V, Lecomte L, Duffé P, Rousselle P, Buret M. 2002. QTL analysis of fruit quality in fresh market tomato: a few chromosome regions control the variation of sensory and instrumental traits. Journal of Experimental Botany 53, 2089–2098.
Ferrándiz C. 2002. Regulation of fruit dehiscence in Arabidopsis. Journal of Experimental Botany 53, 2031–2038.
Klee HJ. 2002. Control of ethylene-mediated processes in tomato at the level of receptors. Journal of Experimental Botany 53, 2057–2063.
Knapp S. 2002. Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. Journal of Experimental Botany 53, 2001–2022.
Marín-Rodríguez MC, Orchard J, Seymour GB. 2002. Pectate lyases, cell wall degradation and fruit softening. Journal of Experimental Botany 53, 2115–2119.
Moore S, Vrebalov J, Payton P, Giovannoni J. 2002. Use of genomics tools to isolate key ripening genes and analyse fruit maturation in tomato. Journal of Experimental Botany 53, 2023–2030.
Seymour GB, Manning K, Eriksson EM, Popovich AH, King GJ. 2002. Genetic identification and genomic organization of factors affecting fruit texture. Journal of Experimental Botany 53, 2065–2071.
Verhoeyen ME, Bovy A, Collins G, Muir S, Robinson S, de Vos CHR, Colliver S. 2002. Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. Journal of Experimental Botany 53, 2099–2106.
Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J. 2002. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296, 343–346.
Watson R, Wright CJ, McBurney T, Taylor AJ, Linforth RST. 2002. Influence of harvest date and light integral on the development of strawberry flavour compounds. Journal of Experimental Botany 53, 2121–2129.
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