Journal of Experimental Botany, Vol. 53, No.

377,
Fruit Development and Ripening Special Issue, pp. 1995±2000, October 2002
DOI: 10.1093/jxb/erf105

Recent advances in fruit development and ripening: an

overview

Philip J. White1
1
Department of Plant Genetics and Biotechnology, Horticulture Research International, Wellesbourne, Warwick
CV35 9EF, UK

Received 26 July 2002; Accepted 26 July 2002

Abstract improved, so has the ability to improve the organo-

leptic and nutritional qualities of fruits through crop
This article provides an overview of the Journal of management, breeding or biotechnology.
Experimental Botany Special Issue on Fruit
Development and Ripening. It reports that signi®cant Key words: Arabidopsis thaliana, auxin, dehiscence,
progress is being made in identifying genes control- ethylene, Fragaria ananassa, ripening, Solanum
ling the development of dry dehiscent fruits in the lycopersicon, strawberry, tomato, transcription.
model plant species Arabidopsis thaliana. In plants
with ¯eshy fruits, a major focus has been the dissec-
tion of biochemical and genetic regulatory cascades
controlling ripening, using tomato as a model spe- Introduction
cies. Intermediates of the ethylene-signalling cas- Anatomically, fruits are swollen ovaries that may also
cade, potential cross-talk between ethylene and auxin contain associated ¯ower parts. Their development follows
signals, and the role of ethylene-independent signals fertilization, and occurs simultaneously with seed matur-
have all been described in this climacteric fruit. The ation. Initially, fruits enlarge through cell division and then
recent isolation of the NOR and LeMADS-RIN genes, by increasing cell volume. The embryo matures and the
which participate in ethylene-independent signalling seed accumulates storage products, acquires desiccation
in tomato, and the discovery that a homologue of the tolerance, and loses water. The fruit then ripens. Ripening
RIN gene is expressed in strawberry, a non-climac- is accompanied by changes in ¯avour, texture, colour, and
teric fruit, suggests that common regulatory cas- aroma. Fruits can be divided into two groups with
cades may operate in all fruits. Transcriptional contrasting ripening mechanisms. Climacteric fruit (such
pro®ling during the development and ripening of as tomato, avocado, apple, and banana) show a burst of
both climacteric (tomato) and non-climacteric (straw- ethylene biosynthesis and an increase in respiration during
berry) fruit has supported these observations, and ripening, whereas non-climacteric fruits (such as straw-
also identi®ed a number of novel genes involved in berry, grape and citrus) do not. Fruits take many forms that
the biochemistry of fruit development and ripening. have evolved to protect and disperse seeds. Seeds of most
The use of phylogenies based on chloroplast gene ¯eshy fruits are dispersed following consumption by
sequences has allowed an insight into the evolution frugivores, whereas seeds of dry fruits are mainly
of fruit forms and fruit biochemistry, which may be dispersed by the elements. A developmental process
useful for the manipulation of commercial species. termed dehiscence, in which the fruit ruptures in a
Several molecular approaches, including positional predetermined fashion, effects the release of seeds from
cloning, QTL mapping and genetic engineering, are a dry capsule or other fruit form. An attractive combination
helping to de®ne the biochemical and molecular of colour, aroma and ¯avour assist the dispersal of seeds
bases of texture, ¯avour, colour, and aroma. As the from ¯eshy fruits. Fruits are a signi®cant part of the human
understanding of the biology of fruit ripening has diet, providing ®bre, minerals, vitamins, and other bene-
1
Fax: +44 (0)1789 470552. E-mail: philip-j.white@hri.ac.uk

ã Society for Experimental Biology 2002

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 1996 White
®cial compounds such as antioxidants. Hence, in addition isolated species from all clades placental enlargement and
to research programmes directed to understand and expansion, and an increase in locule number, has occurred.
improve the organoleptic qualities of fruit, such as Similarly, berries with stone cells appear to have evolved
palatability, taste and aroma, signi®cant efforts have also several times, but their occurrence may have been selected
been invested in increasing the content in fruits of against in domesticated species. The ancestral fruit colour
compounds that bene®t human health. It is hoped that appears to have been red, with both green and yellow being
the ability to manipulate such traits through crop manage- derived colours, but changes and reversions of fruit colour
ment, breeding or biotechnology will afford better nutri- have occurred frequently during evolution. There is a wide
tion as well as improved fruit quality. variation in the secondary metabolites produced by
different Solanum species, including many compounds
involved in ¯avour. Knapp (2002) suggests that knowledge
Recent advances in fruit development and of how fruit size, colour and biochemistry have evolved
ripening
under natural selection in Solanum could prompt novel
The angiosperms (¯owering plants) are de®ned by the strategies for their manipulation in a commercial context.
possession of fruits and this differentiates them from the The release of seeds from dry fruits can be effected by a
gymnosperms. Fruits are thought to have evolved to developmental process termed dehiscence. This process
protect and disperse seed and, as such, are likely to have involves the differentiation of specialized cell types, and
been, and to be, under strong selective pressure. About 70 the strict co-ordination of both genetic and biochemical
million years ago, during the late Cretaceous or early events that lead to cell separation and pod shatter. Recent
Tertiary period, a great diversi®cation of fruit forms commercial interest in dehiscence has focused on rape
occurred and, although this may be correlated with the rise (Brassica napus), where its manipulation might improve
of animals that disperse seeds, it may also have been driven crop yield. Since dehiscence is similar in both rape and
by changes in climate and vegetation. Arabidopsis thaliana, the model Brassica has been used to
To gain an insight into the evolution of distinct fruit accelerate scienti®c understanding of this process. In
forms, Sandy Knapp from the Natural History Museum, Arabidopsis, the dehiscence zone (DZ) extends the length
London, has reviewed their occurrence within the of the silique and consists of a non-ligni®ed separation
angiosperms, and concludes that the various fruit forms layer (SL) situated between a region of ligni®ed cells in the
have evolved repeatedly in a wide variety of clades valve and the ligni®ed vasculature of the replum. During
(Knapp, 2002). To study this phenomenon further, she has the ®nal stages of silique development, the middle lamella
mapped the ®ve fruit types found in the Solanaceae family of the SL cell wall disintegrates, and the valve and replum
onto a molecular phylogeny founded on chloroplast gene tissues separate. Cristina FerraÂndiz from The Instituto de
sequences. This family contains 9 000 to 10 000 species in BiologõÂa Molecular y Celular de Plantas, Valencia, has
about 105 genera, including several of substantial agricul- reviewed current knowledge of the genes involved in cell
tural (potato, tomato, pepper, aubergine) and medicinal fate speci®cation, in DZ differentiation, and in the
importance (tobacco, mandrake, deadly nightshade, hen- biochemical and physiological changes occurring during
bane). Knapp (2002) observes that the ancestral cell separation in Arabidopsis siliques (FerraÂndiz, 2002).
Solanaceous fruit type was the capsule. This appears to A variety of transcription factors have been implicated
have given rise to both single-seeded drupes and multi- in controlling dehiscence (FerraÂndiz, 2002). The ®rst
seeded pyrenes early in evolution, and to berries later in transcription factors shown to participate in DZ speci®ca-
evolution. Although the juicy, multiseeded berries appear tion were the MADS-box genes SHATTERPROOF1
to have evolved independently from capsules several (SHP1) and SHATTERPROOF2 (SHP2). These function-
times, most belong to a single large, recently-evolved ally redundant genes are expressed speci®cally in the DZ
clade. All berries with stone cells, non-capsular dehiscent where they appear to be upregulated by the AGAMOUS
fruit (found mainly in Solanaceous species from arid (AG) gene product. The expression of both SHP1 and
zones) and mericarps (nutlets found in species of the SHP2 genes is also negatively regulated by the expression
peculiar genus Nolana) appear to have arisen independ- of another MADS-box gene, FRUITFULL (FUL), in the
ently several times from berries. valve tissue. The FUL gene product also appears to
Knapp (2002) has also investigated the evolutionary regulate other factors in the valve involved in specifying
origins of fruit size, colour and biochemistry in the genus DZ fate, including the expression of both YJ161, a putative
Solanum using a phylogenetic approach. This genus zinc ®nger protein, and ALCATRAZ (ALC), a bHLH
contains between 1 000±2 000 species indigenous to transcription factor. The bHLH transcription factor
habitats ranging from rainforest to desert. A few species of INDEHISCENT1 (IND1) is required for DZ differenti-
Solanum occurring in arid environments possess derived, ation. Although little is known of the cis-elements for these
non-capsular dehiscent fruits. All other Solanum species transcription factors, it is likely that the regulatory
possess berries, but their size varies considerably. In cascades they initiate result in the degradation of the

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 Fruit: an overview 1997
middle lamellae of the SL cell walls by increasing the protein that function together. Both AtETR1 and AtERS1
expression and activities of speci®c polygalacturonidases interact with AtCTR1, a Raf-like serine/threonine protein
(PG), b-1,4-glucanases (cellulases), and xyloglucan en- kinase (MAPKKK). Lucy Alexander and Don Grierson
dotransglycosylases (XET). As for the hormonal control of from the University of Nottingham report that tomato
dehiscence, FerraÂndiz (2002) speculates that ethylene ethylene receptors (LeETRs) also interact directly with
plays a minor role, while diverse evidence suggests that members of the LeCTR family of Raf-like protein kinases,
auxin is involved in the co-ordination of this process. which contains at least ®ve genes (Alexander and
Tomatoes are climacteric fruit and their ripening is Grierson, 2002). All LeCTR genes appear to be expressed
initiated by ethylene. As with many hormonal signals, constitutively in tomato fruit with the exception of TCTR1
responses to ethylene can be modulated both by changes in (ER50), which is induced both by ripening and by
ethylene biosynthesis and by the presence (or absence) of exogenous ethylene (Bouzayen, 2002). Using a yeast
cellular perception and signal transduction pathways. Both two-hybrid screen of a cDNA library from tomato fruit, it
genes for ethylene biosynthesis (ACC synthase and ACC has been shown that LeETR1 interacts directly with the N-
oxidase), as well as those encoding ethylene receptors, are terminus of the TCTR2 protein (Alexander and Grierson,
transcriptionally regulated. In tomato, multigene families 2002). However, all ethylene responses do not share a
encode ACC synthases (LeACS) and ACC oxidases common biochemical signal-transduction pathway, since
(LeACO), but LeACS2 and LeACO1 appear to dominate LeETR3 (NR) does not interact with TCTR2. Seven other
climacteric ethylene production. The expression of proteins have been found that interact directly with
LeACO1 increases upon ripening and a recent analysis of LeETR3 (NR), several of which show increased expres-
its promoter has identi®ed both a proximal ethylene- sion during ripening, and a further four proteins have been
independent regulatory motif and several distal ethylene shown to interact with TCTR2 and LeETR1 (Alexander
response motifs (Alexander and Grierson, 2002). This is et al., 2002). Interactions between the other members of
consistent with the notion that an ethylene-independent the ethylene receptor family and all the LeCTRs are
developmental cascade determines the predisposition of currently being investigated. It is likely that the kinase
tomato fruit to ripen. A protein with homology to zinc cascades initiated by the LeETR/LeCTR complex eventu-
®nger proteins may bind to the ethylene-independent ally impact on the expression of the LeEIL1±3 transcrip-
regulatory motif to repress transcription of LeACO1 tion factors (Alexander and Grierson, 2002). These are
(Alexander and Grierson, 2002). To complement these homologues of the Arabidopsis EIN3 gene and have been
observations, Harry Klee from the University of Florida shown to function as positive regulators of many ethylene
has revealed how the transcriptional regulation of the responses, probably through the activation of ERF1
ethylene receptor genes conditions what he terms as transcription factors which upregulate the transcription of
differential sensitivity to ethylene during the development ethylene-responsive genes.
of tomatoes (Klee, 2002). A family of six genes encodes Evidence from biochemical and genetic studies imply
ethylene receptors in tomato (LeETR1±6). These receptors that both ethylene-dependent and ethylene-independent
act as negative regulators of downstream responses by regulatory cascades control the development of tomato
suppressing the expression of ethylene-responsive genes in fruit. Hence, although the non-ripening tomato mutants
the absence of ethylene. Of particular interest is LeETR3, ripening-inhibitor (rin) and non-ripening (nor) do not
which is a homologue of the Arabidopsis AtETR1 gene. A produce autocatalytic ethylene nor ripen in the presence of
semi-dominant mutation in LeETR3 is responsible for the exogenous ethylene, they do display signs of ethylene
Never ripe (Nr) phenotype, whose fruit never ripen. All sensitivity and ethylene-inducible expression of several
LeETR genes are expressed in reproductive tissues (¯owers genes. Thus, it is likely that RIN and NOR participate in
and fruits), the most highly expressed being LeETR4. ethylene-independent regulatory cascades during the early
However, only the expression of LeETR3 (NR) changes stages of fruit ripening. Jim Giovannoni and colleagues
dramatically during fruit ripening. LeETR3 (NR) is initially from the Boyce Thompson Institute for Plant Research at
expressed highly in ovaries at anthesis, then drops until the Cornell have isolated the RIN and NOR genes by positional
onset of ripening when it rises steeply. Since ETRs bind cloning strategies (Moore et al., 2002; Vrebalov et al.,
ethylene so tightly, it appears that the only way to turn off a 2002). LeMADS-RIN encodes a member of the MADS-box
response to ethylene is to make more receptors. Hence, family of transcription factors. Interestingly, homologues
Klee speculates that the increased expression of LeETR3 of LeMADS-RIN are expressed during the ripening of other
(NR) during ripening might reduce ethylene responsive- fruit including strawberry, which might indicate a common
ness, and thereby prevent an excessive induction of (ethylene-independent) function in the ripening of both
ethylene responsive genes. climacteric and non-climacteric fruit. Moore et al. (2002)
The ®ve ethylene receptors of Arabidopsis (AtETR1-5) also describe the development of a tomato cDNA
resemble bacterial two-component receptors, which con- microarray, which they have used to pro®le the expression
sist of a sensor protein plus a separate response regulator of approximately 12 000 genes at ten stages during the

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ripening of wild-type fruit and in fruit of ripening mutants. families in plants (for example there are about 27 genes
In addition to identifying proteins directly effecting the encoding PEL in Arabidopsis) and are expressed through-
physical and biochemical changes during fruit ripening, out the plant including ripening fruit. Fruits of tomato,
such comparative analyses should uncover more key strawberry, grape, and banana all express PEL, where they
transcription factors controlling the ripening process. may play a signi®cant role in fruit softening. Other
Asaph Aharoni and Ann O'Connell from PRI- enzymes involved in modifying cell wall properties
Wageningen have used microarrays based on 1701 clones include pectin esterases (PE) and polygalacturonidases
from a red strawberry fruit cDNA library (i) to pro®le gene (PG). These enzymatic activities are similarly encoded by
expression at various stages during strawberry fruit multi-gene families, in which at least one member shows
ripening, and (ii) to compare gene expression in the ripening-speci®c expression.
achenes and receptacle tissue of ripe fruit (Aharoni and It is thought that knowledge of the identity and role of
O'Connell, 2002). They observed that the abundance of generic ripening-regulatory genes will enable the targeted
441 transcripts differed signi®cantly between the achene manipulation of fruit ripening, fruit quality and shelf life
and receptacle tissues. The most abundant transcripts in the (Moore et al., 2002; Seymour et al., 2002). Indeed, both
achenes were those for components of genetic and the rin and nor mutations are already being used
biochemical regulatory cascades (including transcription commercially to extend shelf-life in tomato. Seymour
factors, protein phosphatases and kinases, and 14-3-3 et al. (2002) have identi®ed a rare dominant mutation in a
proteins), and proteins involved in the accumulation of tomato gene (Cnr, for colourless non-ripening) that results
storage products and in the acquisition of oxidative stress in a non-ripening phenotype with two distinct character-
and desiccation tolerance. Interestingly, the expression istics: (i) ®rm fruit with reduced cell adhesion and (ii) a
pro®les of several genes encoding components of regula- complete absence of carotenoid biosynthesis in the
tory cascades clustered with ABA-regulated genes, and a pericarp. Since the mealy phenotype of Cnr fruit is the
number of putative ethylene-response element binding opposite of the juicy phenotype desired by the consumer,
factors (EREB) and ethylene-responsive genes were up- this mutant might provide an insight to the molecular
regulated in achenes. These observations are consistent biology of juiciness. Microarray analyses indicate that the
with the notion that ABA plays a signi®cant role in seed expression of many genes impacting on many aspects of
maturation, but also suggest a role for ethylene. By ripening is altered in the Cnr mutant, suggesting that Cnr
contrast, proteins related to primary metabolism (mainly may encode a regulatory factor. Several of these genes are
gluconeogenesis), cell-wall modi®cation, pigmentation, themselves transcriptional regulators, including a MADS-
and the amelioration of oxidative stress were expressed box transcription factor (TDR4) homologous to the
highly in receptacle tissues. The expression of these genes Arabidopsis FUL gene that may be linked to the mealy
presumably re¯ects the changes in ¯avour, aroma, texture, phenotype of Cnr fruit.
and colour that occur in this tissue during ripening. Thus, The manipulation of tomato fruit quality through genetic
in addition to discovering the gene products underpinning engineering is reasonably well advanced. In tomato, the
the biochemistry of seed maturation and fruit ripening, the isoprenoid biosynthetic pathway gives rise to carotenoids,
microarray approach is also yielding tissue-speci®c pro- such as b-carotene (the precursor of vitamin A) and
moters and identifying key transcription factors and their lycopene (a potent antioxidant, which gives the fruit its
cis-elements that may be useful for the manipulation of characteristic red colour), gibberellins, quinones, and
strawberry fruit ripening. sterols. This pathway has been well researched since its
Fleshy fruits are frequently harvested prior to ripening manipulation impacts not only on the organoleptic qual-
and, following harvest, they have a relatively short shelf ities of fruit but also their contribution to human health.
life during which they undergo profound changes in Peter Bramley from Royal Holloway College, University
texture, colour and ¯avour. Graham Seymour and of London, is dissecting the regulation of this metabolic
colleagues at HRI-Wellesbourne are investigating the pathway during tomato fruit ripening using transgenic and
biochemistry of fruit texture in order to improve the mutant plants (Bramley, 2002). He notes that although the
palatability and shelf life of produce (MarõÂn-RodrõÂguez control of gene expression is a key regulatory mechanism,
et al., 2002; Seymour et al., 2002). MarõÂn-RodrõÂguez et al. post-transcriptional regulation of enzymes, metabolic
(2002) review the role of pectate lyases in fruit softening. channelling and feedback inhibition by b-carotenoids
Pectate lyases (PEL) catalyse the Ca2+-dependent cleavage also contribute. Through identifying the rate limiting
of de-esteri®ed pectin, which is a major component in the steps of the pathway, he hopes to target appropriate
primary cell walls of many higher plants. Initially, it was transgene expression to achieve an increase in the
thought that these enzymes were produced solely by plant concentrations of carotenoids without changing the levels
pathogens to macerate plant tissues. But, as a result of both of other isoprenoids.
plant genome sequencing and EST programmes, it has Martine Verhoeyen and colleagues at Unilever
become clear that these enzymes are encoded by large gene Research and PRI-Wageningen have applied a similar

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 Fruit: an overview 1999
rationale successfully to increase the levels of bene®cial mapping techniques to determine whether this could be
¯avonoid antioxidants in tomato (Verhoeyen et al., 2002). attributed to speci®c genes conferring pleiotropic pheno-
Flavonoids are a diverse group of polyphenolic secondary types or to fortuitous genetic linkage. Such analyses will
metabolites. The important ¯avonols, kaempferol and accelerate the development of molecular markers for
quercetin, are synthesized from 4-coumaroyl CoA and breeding programmes and facilitate the identi®cation of
malonyl CoA through the concerted action of chalcone candidate genes to improve organoleptic quality.
synthase (CHS), chalcone isomerase (CHI), ¯avanone 3- Richard Watson and colleagues from the University
hydroxylase (F3H), then ¯avanone 3¢-hydroxylase for of Nottingham and ADAS-Rosemaund report that many
quercetin, and ¯avonol synthase (FLS). The most abundant quality traits are strongly in¯uenced by environment
¯avonoid in tomato fruit, naringenin chalcone, is the ®rst (Watson et al., 2002). They note that many volatile
intermediate compound. The major ¯avonol glycosides, and non-volatile compounds give rise to the ¯avour of
quercetin-rutinoside (rutin) and kaempferol-rutinoside, are strawberry fruit. The volatile compounds give the fruit
derived from quercetin and kaempferol. The enzymes its distinctive ¯avour, whereas the non-volatile com-
catalysing these reactions are present solely in the peel of pounds, such as sugars and organic acids, are respon-
tomato fruit, where ¯avonols and ¯avonol glycosides sible for the fruit's sweetness and tartness. Consumers
exclusively accumulate. Verhoeyen et al. (2002) observed desire a reproducible ¯avour for a particular cultivar.
that there was limited natural variation in the ¯avonoid However, Watson et al. (2002) observe that there is
content of tomato fruit and reasoned that genetic engin- often considerable variation in fruit ¯avour even within
eering would be required to increase their levels substan- a single crop. To assess the variability in fruit ¯avour
tially. They found, using transgenic plants, that (i) the arising from management practice, they have used
ectopic overexpression of CHI resulted in up to a 78-fold Atmospheric Pressure Chemical Ionization (APCI) and
increase in the ¯avonol content of the peel (mainly direct liquid-mass spectrometry techniques to determine
quercetin-glycosides), (ii) the ectopic expression of two how harvest date and shading affect the abundance of
maize transcription factors (Lc and C1) resulted in the 13 volatile compounds and three non-volatile com-
accumulation of kaempferol-glycosides in the ¯esh, and pounds (sucrose, glucose and citric acid) implicated in
(iii) the ectopic expression of CHS, CHI and FLS together strawberry fruit ¯avour. They observed that the
was suf®cient to increase the kaempferol- and naringenin- amounts of all the volatile compounds analysed
glycoside content of the ¯esh, and the quercetin-glycoside differed signi®cantly from fruit to fruit (perhaps
content of the peel. None of these genetic manipulations through picking fruits of different maturity) and
had any gross effects on phenotype or adverse effects on between harvests, but could discern no consistent
taste. Such manipulations offer the possibility of develop- trends. Similarly, the concentrations of glucose and
ing new tomato varieties with increased health bene®ts. citric acid varied considerably between fruits and
The organoleptic quality of fruit is a complex charac- between harvests, with no consistent trends. A decline
teristic involving all aspects of ¯avour, texture and aroma. in sucrose concentration occurred across the harvest
To identify the major genetic components impacting on period, which may have been associated with a decline
organoleptic quality Mathilde Causse and colleagues at in solar radiation during the season. The effect of
INRA-Avignon have pursued a QTL approach with a shading was more consistent. A brief period of shading
mapping population of 144 recombinant inbred lines signi®cantly reduced the amounts of volatile ¯avour
(RILs) derived from an intraspeci®c cross between a compounds and the concentrations of sucrose and
cherry tomato (Cervil) of high organoleptic quality and an glucose in the fruit. These observations have direct
inbred line (Levovil) with an unremarkable taste but bigger implications for strawberry growers. In addition,
fruits (Causse et al., 2002). They studied 38 traits using a Watson et al. (2002) suggest that a deeper understand-
variety of physical and biochemical assays, plus a panel of ing of the relationships between photosynthesis and
trained tasters. Many traits were correlated. Sweetness and secondary metabolism may eventually enable straw-
tartness, for example, were well described by sugar content berry growers to manipulate fruit ¯avour through
and titratable acidity, suggesting that laboratory assays environmental management, and to produce fruit of a
could replace a panel of tasters for some sensory traits and more consistent ¯avour and quality both within a crop
also allowing breeders simpler selection criteria. Similarly, and throughout the year.
many QTL overlapped. Indeed, the presence of QTL for
organoleptic qualities was restricted to 14% of the genome,
Perspective
lying on chromosomes 1, 2, 3, 4, 8, 9, 11, and 12. The latter
observation con®rmed and extended previous studies using The papers in this Special Issue describe the recent
other mapping populations. Since small regions of the discoveries in a number of areas. There is much scienti®c
genome in¯uenced several traits, Causse et al. (2002) have interest in identifying the key regulatory mechanisms
used both multitrait QTL analysis and local genetic- involved in fruit development and ripening. Several papers

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 2000 White
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I thank Martin Broadley, Ken Manning, Richard Napier, and Graham 2002. In¯uence of harvest date and light integral on the
Seymour (HRI-Wellesbourne), and all the authors of articles in this development of strawberry ¯avour compounds. Journal of
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