development and ripening

PP64CH10-Seymour ARI 23 March 2013 14:57

Fruit Developmentand RipeningGraham B. Seymour,1 Lars Østergaard,2

Natalie H. Chapman,1 Sandra Knapp,4

and Cathie Martin3

1Plant and Crop Science Division, School of Biosciences, University of Nottingham,Loughborough LE12 5RD, United Kingdom; email: [email protected],[email protected] of Crop Genetics and 3Department of Metabolic Biology, John Innes Center,Norwich NR4 7UH, United Kingdom; email: [email protected],[email protected] of Life Sciences, Natural History Museum, London SW7 5BD,United Kingdom; email: [email protected]

Annu. Rev. Plant Biol. 2013. 64:219–41

First published online as a Review in Advance onFebruary 4, 2013

The Annual Review of Plant Biology is online atplant.annualreviews.org

This article’s doi:10.1146/annurev-arplant-050312-120057

Copyright c© 2013 by Annual Reviews.All rights reserved

Keywords

Arabidopsis, tomato, diet, gene regulation, epigenetics

Abstract

Fruiting structures in the angiosperms range from completely dry tohighly fleshy organs and provide many of our major crop products,including grains. In the model plant Arabidopsis, which has dry fruits,a high-level regulatory network of transcription factors controllingfruit development has been revealed. Studies on rare nonripeningmutations in tomato, a model for fleshy fruits, have provided newinsights into the networks responsible for the control of ripening. Itis apparent that there are strong similarities between dry and fleshyfruits in the molecular circuits governing development and maturation.Translation of information from tomato to other fleshy-fruitedspecies indicates that regulatory networks are conserved across a widespectrum of angiosperm fruit morphologies. Fruits are an essentialpart of the human diet, and recent developments in the sequencing ofangiosperm genomes have provided the foundation for a step changein crop improvement through the understanding and harnessing ofgenome-wide genetic and epigenetic variation.

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Gynoecium: thecarpels or femalereproductive organs offlowering plants,consisting of an ovaryharboring the ovules,stigmatic tissue forpollen reception at thetop, and a gynophoreat the base connectingthe gynoecium to theplant

Apocarpous: havingfree carpels

Syncarpous: havingfused carpels

Nut: indehiscent fruitwith a hard shell

Berry: fleshy fruitproduced from a singleovary, often with manyseeds

Contents

INTRODUCTION . . . . . . . . . . . . . . . . . . 220NOMENCLATURE, EVOLUTION,

DIVERSITY . . . . . . . . . . . . . . . . . . . . . . 220FRUIT DEVELOPMENT AND

RIPENING . . . . . . . . . . . . . . . . . . . . . . . 222The Fruiting Structure . . . . . . . . . . . . . 222Hormonal and Genetic

Regulation. . . . . . . . . . . . . . . . . . . . . . 223Fertilization . . . . . . . . . . . . . . . . . . . . . . . 224Fruit Development. . . . . . . . . . . . . . . . . 225Hormonal and Genetic Regulation

of Maturation and Dehiscencein Dry Fruits . . . . . . . . . . . . . . . . . . . 227

Hormonal and Genetic Regulationof Maturation and Ripeningin Fleshy Fruits . . . . . . . . . . . . . . . . . 228

FRUITS AND THE HUMANDIET . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 232

CROP IMPROVEMENT . . . . . . . . . . . . 233

INTRODUCTION

True fruits are found only in the angiosperms,or flowering plants; the name angiospermmeans hidden seed. Flowering plants comprisesome 250,000–400,000 species in four majorclades (10) that are the dominant componentof vegetation in most tropical, subtropical, andtemperate zones worldwide. The angiospermscomprise tiny herbs to large canopy trees, oc-cupy terrestrial and aquatic (including marine)habitats, and are the source of all major cropplants. As such, humans have a long and inti-mate association with angiosperms, particularlywith their fruits and seeds.

Fruits are often defined as structures derivedfrom a mature ovary containing seeds (48), butmany structures we might define as fruit arein fact composed of a variety of tissue types(Figure 1). Van der Pijl (155) used the conceptof the dispersal unit as his definition of a fruit;this links fruits to their role in the ecology ofthe plant life cycle as the mechanism by whichseeds are dispersed. Dispersal units also occur

in land plants other than angiosperms; someCarboniferous seed ferns had fleshy structuresthat are thought to have been eaten by reptiles(148), and the seed of the “living fossil” Ginkgobiloba is enveloped in a soft fleshy coveringcalled the sarcotesta. These propagules are notconsidered true fruits despite their functionalsimilarities. True fruits are derived from theflower gynoecium (see Fruit Development andRipening, below).

NOMENCLATURE, EVOLUTION,DIVERSITY

The myriad of fruit types recognized in an-giosperms can be simplified using combinationsof the following characteristics: dehiscence orindehiscence, dry or fleshy exterior, and free(apocarpous) or fused (syncarpous) carpels.Capsules (Figure 1c) and the siliques ofArabidopsis relatives (Figure 1a) are dehis-cent, dry, and syncarpous; achenes and nuts(Figure 1e,g,h) are indehiscent, dry, andunicarpellate; and berries (Figure 1b,d) areindehiscent, fleshy, and syncarpous. A drupeis an indehiscent, fleshy, single-seeded fruitwhere the seed is enclosed in a hard endocarp,like a peach pit (Figure 1f ). Syncarpy occursin 83% of extant angiosperm species and hasbeen interpreted as facilitating pollen tubecompetition and thus fitness (36); it has arisenindependently in both the monocots and theeudicots (37). Apocarpy is rarer but can beseen in the fruits of magnolias, with clusters ofseparate carpels termed follicles. Endress (36)has suggested that syncarpy might facilitateadaptive radiation in fruit type by increasingthe possibility of developing fleshiness and/ordehiscence mechanisms.

Darwin thought that the recent origin andrapid diversification of the angiosperms was“an abominable mystery” (44). The angiospermfossil record extends back to the Early Cre-taceous period, and the earliest unambiguousfossils (65) are dated conservatively to approx-imately 132 Mya. Angiosperms were commonand diverse by the mid-Cretaceous, indicatingeither that their first major diversification and

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a b

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Figure 1Fruit diversity. (a) Lunaria annua L. (Brassicaceae), cultivated, United Kingdom: dehiscent siliques that dryand shatter irregularly with age, releasing the seeds. (b) Mandragora officinalis L. (Solanaceae), Andalucıa,Spain: indehiscent berries with fleshy, brightly colored mesocarp and many seeds. (c) Nicotiana sylvestrisSpeg. & Comes (Solanaceae), Apurımac, Peru: dehiscent capsules opening along suture lines. Theseed-bearing placentae are visible as columns in the center of the capsule. (d ) Ribes cereum Douglas(Grossulariaceae), New Mexico, United States: indehiscent berries from an inferior gynoecium. Theremnants of the flower are clearly visible. (e) Corylus sp. (Betulaceae), cultivated, United Kingdom:indehiscent, single-seeded nuts. ( f ) Rhus trilobata Nutt. (Anacardiaceae), New Mexico, United States:indehiscent, single-seeded drupes with fleshy mesocarp. ( g) Fallugia paradoxa (D. Don) Endl. (Rosaceae),New Mexico, United States: indehiscent, single-seeded achenes with long plumes to aid dispersal.(h) Fragaria × ananassa Duchesne ex Rozier (Rosaceae), cultivated, United Kingdom: tiny, single-seededachenes on the surface of an expanded, brightly colored receptacle. All photos by Sandra Knapp.

Drupe: indehiscentfruit with fleshy outerpericarp layers(exocarp andmesocarp) but a hardinner pericarp layer(endocarp)surrounding the seed

ecological radiation occurred over a relativelyshort time frame or that they originated anddiversified earlier than was previously thought.The reproductive structures of these Early Cre-

taceous angiosperms were mostly very small(45), with fruit volumes between 0.1 and8.3 mm3 (the size of a small cherry) and seed vol-umes between 0.02 and 6.9 mm3 (39). Diverse

www.annualreviews.org • Fruit Development and Ripening 221

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fruit types are represented in Early Cretaceousfossils; the vast majority are either indehiscent,single-seeded nuts or drupes with one or a fewseeds, but some dehiscent, apocarpous fruitshave been found, as have many fruits with fleshyouter layers (45). One-quarter of all fruits foundat one site were fleshy drupes or berries (40).

Lorts et al. (91) mapped crude fruit typecategories (dry dehiscent, dry indehiscent, andfleshy) onto the orders of extant angiospermsand found no association (assessed visually) be-tween fruit type and major clade. This suggeststhat there is no phylogenetic constraint onfruit type evolution across the major lineages(orders) of angiosperms, with most ordershaving all three broadly defined fruit types(see figure 1 of Reference 91). Fruit and seedsize both increased in the Tertiary (39), witha drastic change at the Cretaceous–Tertiaryboundary (147, 162). It has been suggestedthat the origin of fleshiness was initially relatedto defense against pathogens and only laterco-opted for biotic dispersal (93, 149).

Size change in both fruits and seeds throughthe fossil record has been attributed to co-evolution with seed-dispersing animals (147),with this mutualistic relationship then drivingthe development of closed, forested habitats(large seeds are characteristic of closed plantcommunities). An alternative hypothesis is thatchanges in habitat through climate change, per-haps coupled with the demise of large herbi-vores (e.g., dinosaurs), drove the evolution oflarger fruits and seeds, and the availability ofseed dispersers reinforced this trend (39). Dis-persers thus tracked, rather than led, changesin fruit size and morphology. Distinguishingbetween these two hypotheses is difficult ow-ing to bias in the fossil record (39) and un-certainty over ecological dynamics in the past(149), but a series of studies using both ex-tant and fossil fruits have strongly supportedthe latter hypothesis. The significant correla-tions between fruit type and habitat conditionsin a broad set of extant flowering plants (8) sug-gest that the evolution of fleshiness is relatedto changes in vegetation from open to closedhabitats.

It is tempting to assume that fruit diversityis the result of adaptation to frugivores; adapta-tionist scenarios about tight obligate relation-ships between fruits and their dispersers aboundin the literature, but they have been shown tobe less compelling than originally thought. Thestrong role of habitat and climate in the ori-gin and evolution of fruit characteristics suchas fleshiness (39) has been clearly demonstratedin both the fossil record and through correla-tion studies with extant angiosperms. Syncarpymay represent a key innovation for angiospermfruits in that it facilitated pollen competitionand pollen tube protection (37). Fruit color isanother characteristic that on its face seems tobe adaptive for frugivore attraction, but studiesexamining color as a signal have demonstratedthat, like the evolution of other fruit character-istics, the evolution of fruit color is mediatedthrough diffuse interactions between plants, an-tagonists (such as microbial predators), and mu-tualists (128). Fleshy-fruit evolution has clearlybeen an important and continually recurringtheme throughout flowering plant evolution,and assumptions with respect to the adaptivevalue of particular fruit traits must be carefullyexamined.

FRUIT DEVELOPMENT ANDRIPENING

The Fruiting Structure

The gynoecium is derived from the fusion ofcarpels and forms in the center of the flower.Many regulators of carpel development identi-fied in Arabidopsis also have roles during leaf de-velopment, thereby confirming the evolution-ary origin of carpels as modified leaves (41, 129).The main patterning events of the Arabidopsisgynoecium take place before fertilization andoccur along three axes: apical-basal, mediolat-eral, and abaxial-adaxial (dorsoventral). Stig-matic tissue (Figure 2) that mediates pollengermination develops at the apical (distal) end.After germination, the pollen tube grows downthrough the transmitting tract and enters theovules through the micropyle, a small opening

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in the integument layers (90). A solid style withradial symmetry supports the segment of thetransmitting tract just below the stigma and isrequired for efficient fertilization (Figure 2).The ovary is formed from the carpels as a lon-gitudinal cylinder with mediolateral symmetrythat reflects its origin as two fused leaflike or-gans (Figure 2). It is composed of two com-partments divided by a septum and placentafrom which ovules arise. The carpel walls ex-hibit abaxial-adaxial asymmetry with an exocarplayer of large cells interspersed with stomata,three or four layers of mesocarp cells, and twoinnermost layers of endocarp cell layers. TheArabidopsis gynoecium is connected at its baseto the pedicel and the rest of the plant via agynophore.

Hormonal and Genetic Regulation

The plant hormone auxin has been estab-lished as an important component for pat-terning along the different axes of polarityin the Arabidopsis gynoecium. In the apical-basal orientation, auxin synthesis at the apexis required for specification of the style andstigma (137). Auxin biosynthesis at the apexis promoted through the activity of transcrip-tion factors such as STYLISH1 (STY1), STY2,and NGATHA3, which induce expression ofYUCCA auxin biosynthesis genes (2, 15, 34,137, 153). Exogenous application of auxin res-cues the split style of the sty1/2 mutant (141).

The basic helix-loop-helix (bHLH) pro-teins are a large family of transcription factorsfound in all eukaryotic organisms (99, 115).Several members of this family have functionsduring gynoecium development or later infruit development. For example, mutationsin the SPATULA (SPT ) gene lead to earlydefects in the development of carpel marginaltissues such as the stigma, style, septum, andtransmitting tract (3, 61). SPT activity promot-ing carpel development was recruited duringthe evolution of flowering plants from light-regulated processes such as those involved inshade-avoidance responses in vegetative organs(120). Phenotypic defects similar to those

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SStiStiStiStitiStStiStitiSStiS gggggmagmagmamaggggggggg

StyStyStyStyStyStyStyStyStyStyStyStyStySStyStytyStyStyStytyleleleleeeeleeleleleeleeeeleeee

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Figure 2Arabidopsis gynoecium patterning. (a) False-colored scanning electronmicrograph (SEM) of a stage-13 gynoecium, showing the stigma ( yellow), style(blue), valves ( green), replum (red ), valve margins (turquoise), and gynophore( purple). (b) Cross section of a radial symmetric style with a transmittingtract (orange). (c) Cross section of an ovary with bilateral symmetry. Colorcoding is identical to that in panels a and b, with the addition of the septum(dark blue) and ovules ( gray). (d ) False-colored SEM of an ind sptdouble-mutant stage-13 gynoecium that completely lacks the stigmatic tissueand radial style. The surface of the cells at the very apical part of the valvessuggests that they have retained style identity.

observed in spt mutant gynoecia were observedin multiple combinations of mutations in thebHLH-encoding HECATE (HEC) genes, andprotein-protein interactions between SPT andHEC proteins in yeast two-hybrid experimentssuggest that these factors may jointly regulatedownstream targets (55). Loss-of-functionmutations in the ETTIN (ETT ) gene, whichencodes AUXIN RESPONSE FACTOR3(ARF3), exhibit enlarged apical and basalregions at the expense of the ovary (132).Because ETT negatively regulates SPT/HECgenes in the ovary, it has been suggested thatETT regulates ovary size, perhaps in responseto local auxin dynamics (61, 108, 144).

Further connections between gynoeciumpatterning and auxin were made when itappeared that mutations in another bHLH-factor-encoding gene, INDEHISCENT (IND),strongly enhanced the phenotype of the sptsingle mutant (51) (Figure 2d ). IND and SPT


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Parthenocarpic:producing fruitwithout fertilization;the resulting fruits areseedless

heterodimerize in plant cells and regulate acommon set of target genes (51, 139), and anumber of their direct targets are involved incontrolling the direction of auxin transport(51, 139). IND belongs to the same cladein the Arabidopsis bHLH family as the threeHEC genes (115). Loss of all three HEC genesgives rise to a split-style phenotype with nostigmatic tissue, identical to the ind spt mutantgynoecium (55), and it is therefore likely thatHEC proteins also interact with SPT in planta.

Tissue identity factor activity and auxin dy-namics are at the center of gynoecium pat-terning control. With the development of toolsto study auxin transport and signaling in Ara-bidopsis, data are now emerging to provide anoverview of how auxin is distributed during gy-noecium development. For example, the auxinsignaling reporter DR5::GFP shows a stronggreen fluorescent protein (GFP) signal accu-mulating in a ring at the distal end of thegynoecium prior to stigma formation (51). Inthe spt single mutant and the ind spt doublemutant, this ring is not formed; instead, theGFP signal accumulates in two foci at the dis-tal end. Because both IND and SPT are ex-pressed in this distal region, it is likely that theyare responsible for lateral auxin distributionto create a continuous ring and ensure properdevelopment.

Fertilization

The developmental switch that turns a gynoe-cium into a growing fruit depends on the fertil-ization of ovules that form along the placenta. Inmost angiosperms, the gynoecium senesces anddies if not fertilized. The fruit initiation pro-cess has traditionally been thought to involvephytohormone activities (49). Upon fertiliza-tion, a seed-originating auxin signal is gener-ated (32, 104, 126) that is thought to upregulatebiosynthesis of another hormone, gibberellin(GA). This leads to activation of GA signaling inthe ovules and valves, thereby stimulating fruitgrowth (32, 111, 131, 156).

Degradation of the growth-repressingDELLA proteins is central to GA signaling.

DELLAs are characterized by a conservedDELLA motif in the N-terminal domain and aSCARECROW-like C-terminal domain (113,136). According to the “relief of restraint”model (58), GA-mediated DELLA degradationis required to overcome the growth-repressingDELLA activity. In agreement with theirfunction as growth repressors, reduction inDELLA activity can promote parthenocarpicfruit growth in both dry dehiscent fruitsand fleshy fruits (32, 97). GA treatment ofgynoecia in a della loss-of-function mutanthas revealed the existence of a GA-dependentbut DELLA-independent pathway that con-tributes to fruit growth in Arabidopsis (46).This newly identified DELLA-independentpathway provides additional opportunities forfine-tuning fruit growth.

ARFs and Aux/IAA proteins also functionduring fruit initiation. In Arabidopsis andtomato, expression of aberrant forms of ARF8results in parthenocarpic fruit development(53, 54), as does silencing of IAA9 in tomato(160). It is not clear by what mechanism ARF8regulation occurs, but based on the model forauxin signal transduction, it has been suggestedthat ARF8 and the Aux/IAA protein IAA9 mayform a transcriptional repressor complex that isdestabilized by the aberrant forms of ARF8 toallow transcription of auxin-responsive genes(53).

In tomato, pollination causes upregulationof ARF9 and downregulation of ARF7. Silenc-ing of the SlARF7 gene in transgenic plants(cv. Moneymaker) results in parthenocarpicfruit development, suggesting that SlARF7is a negative regulator of fruit set. Silencingof SlARF7 also results in strong upregulationof SlGH3, which encodes an IAA–amidosynthetase that may be induced to compensatefor excessive auxin (25, 26). Differences in cellsize between SlARF7-silenced lines and thewild type become apparent 6 days postanthesis(DPA), with significant cell size increase in themesocarp and endocarp layers, and so it hasbeen concluded that downregulation of SlARF7deregulates cell division and upregulates cellexpansion (26). In addition, there is evidence in

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Quantitative traitloci: DNA regionsassociated with aphenotype that iscontrolled by two ormore genes

MADS-box genes:transcription factorsdetected in nearly alleukaryotes; in plants,they are commonlyassociated with floraldevelopment

tomato that early photosynthesis is importantfor proper seed set (92).

Fruit Development

Upon fertilization, Arabidopsis fruit enters astage in which ovary growth and maturationare tightly coordinated with seed develop-ment. During this process, a number of fruittissues develop, including valves (derived fromthe carpel walls), a central replum, a falseseptum, and valve margins that form at thevalve/replum borders. Late in development,the valve margins differentiate into dehiscencezones, where fruit opening will take place.Although these individual tissues were specifiedprior to fertilization, their distinct appearancebecomes more striking after fertilization,forming sharp boundaries, particularly alongthe valve margin (125).

As described above, the valves (carpel walls)exhibit abaxial-adaxial asymmetry and are com-posed of an outermost (abaxial) epidermal layerwith long, broad cells interspersed with guardcells (stomata). Underneath the epidermallayer, three to six layers of mesophyll cells fol-low (Figure 3). Two specialized adaxial cell lay-ers form in the valves: The innermost endocarpA layer (valve margins) is composed of largecells that undergo cell death before the fruit hascompletely matured, whereas cells in the endo-carp B layer remain small and develop lignifiedcell walls (Figure 3) whose rigidity may assistin the process of fruit opening by providing sig-nificant tension in the mature fruit (140). Thereplum is connected to the septum and containsthe main vascular bundles. At the valve margin,a narrow file of dehiscence zone cells differen-tiates along the entire length of the fruit latein development, allowing the valves to detachfrom the replum, which causes seed dispersalto occur by a shattering mechanism. The valvemargins consist of two distinct cell layers: a sep-aration layer, where cell separation will takeplace, and a layer of lignified cells, whose rigid-ity may promote the opening process (140).

Development of fleshy fruit such as tomatoinvolves cell division and expansion of the ovary

tissues, but without the lignification phasefound in dry fruit. In the miniature tomato(cv. Micro-Tom) (112), cell division starts at 2DPA, when the ovary is 1 mm in diameter with10 cell layers (Figure 3). Cell divisions are bothpericlinal and anticlinal, and by 4 DPA the fruitis 1.5 mm in diameter and has 30 cell layers.Cell division continues at 7–8 DPA, but thencell expansion becomes apparent and the celllayer number increases to 35 at the apex of thefruit and 20 at the equator. Cell division stopsby 10–13 DPA, and cell expansion progressesat a dramatic rate until approximately 30 DPA,when the fruit reaches a diameter of 1.5–2 cm(Figure 3). The layers of cells that undergodivision after anthesis are the mesocarp col-lenchyma. Cell expansion is responsible forthe increase in fleshy-fruit size (Figure 3),with cell sizes in tomato reaching 0.5 mm indiameter in the pericarps of some varieties (16).

Fruit size in tomato is controlled by nearly30 quantitative trait loci. The Fw2.2 geneis responsible for approximately 30% of thevariation, and encodes a plant-specific andfruit-specific protein that negatively regulatesmitosis and is possibly part of the cell cyclesignal transduction pathway (20). Pericarpcell number in tomato is also linked to theexpression of the MADS-box gene TOMATOAGAMOUS (TAG)–LIKE1 (TAGL1), whichis an ortholog of the Arabidopsis SHATTER-PROOF (SHP) genes (158). TAGL1 is expressedin floral organs and young tomato fruit as well asduring ripening. It is one of the most abundantMADS-box genes expressed in tissues of youngfruits (100), and in RNAi::TAGL1 tomato fruitsthere is a reduction in pericarp thickness from25 to 15 layers measured at 28 and 38 DPA, re-spectively, and the inner pericarp appears to beabsent.

Four genes that control shape in tomatohave been cloned: SUN and OVATE, whichcontrol fruit elongation shape; FASCIATED,which is associated with flat-shaped fruit; andLOCULE NUMBER, which regulates fruitlocule number. SUN encodes an IQD familyprotein that is thought to alter hormone orsecondary metabolite levels (164), whereas


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Exocarp

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Figure 3Changes in fruit anatomy during development. (a) Pericarp layers characteristic of dry fruits (e.g., capsules).(b) Pericarp layers characteristic of fleshy fruits. (c) Transverse section of entire mature Brassica pod.(d ) Transverse section of Brassica pod valve wall. (e) Transverse section of Solanum lycopersicum cv.Micro-Tom fruit at different days postanthesis (DPA), showing pericarp layers and illustrating cell divisionand cell expansion phases. Panels a, b, and e courtesy of Pabon-Mora & Litt (112).

OVATE encodes a negative growth regulator,presumably by acting as a repressor of tran-scription and thereby reducing fruit length.FASCIATED encodes a YABBY transcriptionfactor (19). LOCULE NUMBER was recently

linked to two single-nucleotide polymor-phisms (SNPs) located approximately 1,200base pairs downstream of the stop codon of agene encoding a WUSCHEL homeodomainprotein, members of which regulate plant stem

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cell fate. Alleles of these genes appear to haveplayed a critical role in forging the shape ofdomesticated tomato fruits (123).

Hormonal and Genetic Regulationof Maturation and Dehiscencein Dry Fruits

Formation of the valve margin region dependson several transcription factor activities.Upstream in the hierarchy, two closely relatedMADS-box transcription factor–encodinggenes, SHP1 and SHP2, positively regulatethe IND gene described above as well asALCATRAZ (ALC), which encodes anotherbHLH transcription factor (83, 84, 118).Although none of the shp single mutants haveany detectable phenotype on their own, thecombined shp1 shp2 double mutant producesindehiscent fruit devoid of valve margindifferentiation (83). Despite the role of IND ingynoecium formation, the most pronouncedphenotypic defect of ind mutants and loss ofIND function is a loss of valve margin identitythat affects both the lignified and separationlayers (84). In contrast, fruits from alc mutantsproduce lignified cells at the valve margin, butthe separation layer cells fail to develop (118).

The FRUITFULL (FUL) gene encodes aMADS-box transcription factor that is requiredfor maintaining valve identity (57). The valvesdeveloped in ful mutant fruits adopt a partialchange of identity into valve margin cells withectopic lignification. In these mutant valves,SHP1, SHP2, and IND become ectopically ex-pressed, and the phenotype can be almost en-tirely rescued by combining the ful mutant withmutations in valve margin identity genes. FULthus specifies valve cell fate at least in part by re-pressing the expression of valve margin identitygenes in valve tissue (42, 84).

The homeodomain-containing transcrip-tion factor REPLUMLESS (RPL) is a key reg-ulator of the replum tissue on the medial sideof the valve margins. As the name implies, rplloss-of-function mutants fail to develop a re-plum. Similar to the activity of FUL, RPL re-presses valve margin identity gene expression

in the replum, and combining rpl mutants with,for example, the shp double or ind single mutantrescues the replum defect (122, 124). Species ofBrassica produce fruits that are morphologicallyvery similar to those of Arabidopsis, but they lackan outer replum, suggesting that brassicas havelost the RPL function in the fruit. Replum tis-sue was, however, produced in Brassica rapa witha strong ind mutant allele (52). Lack of RPLactivity in Brassica fruits was demonstrated toresult from reduced RPL gene expression dueto a SNP in a cis-element located ∼3 kb up-stream from the RPL-encoding region (5). Inrice, the same SNP in the same cis-element inan RPL homolog is responsible for preventingseed shattering in domesticated rice (76), re-vealing a remarkable example in which the samenucleotide position in a regulatory element ex-plains developmental variation in seed dispersalstructures in widely diverged species (5).

In recent years more elements of the coregenetic network of Arabidopsis fruit patterninghave been identified, including genes involvedin leaf development, such as ASYMMET-RIC LEAVES1, ASYMMETRIC LEAVES2, andBREVIPEDICELLUS (1). The network has alsoexpanded upstream to include a combinationof genes, including JAGGED, NUBBIN, FILA-MENTOUS FLOWER, and YABBY3 (29, 30).The floral homeotic gene APETALA2 (AP2)has been demonstrated to repress replum de-velopment (122). A thorough description of allthese interactions is not the purpose of this re-view and can be obtained at least partly else-where (6, 110, 125). Therefore, here we con-centrate on the core network and its interactionwith hormonal activities.

The core and extended genetic network ofArabidopsis fruit development consists entirelyof interactions among transcription factors.The three genes encoding polygalacturonases(PGs) required for dehiscence downstream ofIND are functionally redundant (109). Thismakes sense, as PGs have cell wall–degradingactivities and secretion of PGs from dehiscencezone cells has been demonstrated (114).

Hormonal distribution and biosynthesis areemerging as immediate downstream outputs


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from the core genetic network. In Brassica na-pus, direct measurements of auxin levels in valvemargin tissue revealed an abrupt decrease in theauxin content of these cells immediately prior tofruit opening. This drop correlated exactly withan increase in the activity of cell wall–degradingenzymes (14), raising the possibility that auxindepletion from the valve margin tissue is a re-quirement for dehiscence. Work in Arabidopsisconfirmed this hypothesis, demonstrating thatIND ensures formation of an auxin minimum inthe valve margins at maturity by regulating thedirection of auxin transport (139); a subsequentstudy showed that IND most likely interactswith SPT to mediate this process (51).

As described earlier, GA promotes fruitgrowth in Arabidopsis following fertilization.This is in line with the general perception of GAas a growth-promoting hormone, which func-tions by promoting degradation of the growth-repressing DELLA proteins (58). GA has nowalso been identified as having a role in tissuespecification during Arabidopsis fruit develop-ment. The GA4 gene is a direct target of IND,and the ga4 mutant has a defect in specifyingthe separation layer of the valve margin similarto that seen in alc mutants (4). GA4 encodes aGA3 oxidase, which mediates the last step in thebiosynthesis of active GAs (17, 145). Geneticanalysis demonstrated that GA production atthe valve margin is required to degrade DELLAproteins. In the absence of GA, DELLA pro-teins would otherwise interact with ALC pro-teins to inhibit ALC from regulating its targetgenes (4).

Hormonal and Genetic Regulationof Maturation and Ripeningin Fleshy Fruits

In tomato and grape, levels of free IAA, themost abundant auxin, decline prior to the on-set of ripening, and at the same time levels ofthe “inactive” IAA–amino acid conjugate IAA-Asp increase substantially. Similar profiles offree IAA and IAA conjugates have also beenreported in pepper, banana, muskmelon, andstrawberry (9). The IAA-Asp is generated from

IAA by IAA–amido synthetase, and this enzymeis encoded by the GH3 gene. Two GH3 genesassociated with the onset of ripening in tomatoare upregulated (77), and tomato fruits over-expressing the pepper GH3 gene ripen early(88). These observations are consistent witha role for endogenous IAA in controlling theonset of ripening and modulation of its levelsby amino acid conjugation (9). GH3 expressionmay be partially under the control of abscisicacid (ABA), another plant hormone that pro-motes ripening (9).

There is evidence that ABA acts as apromoter of ripening in tomato. Suppres-sion of the SlNCED1 gene (encoding 9-cis-epoxycarotenoid dioxygenase), which catalyzesa key step in ABA biosynthesis, results in down-regulation in the transcription of several majorripening-related cell wall enzymes, includingPG and pectin methylesterase; enhanced fruitshelf life; and slower softening (143). Retarda-tion of ripening is also apparent in strawberryfruits with reduced levels of NCED (71). ABA isalso a positive regulator of ripening in grape (9).The mechanism of ABA action is not known,but in grape it can increase GH3 expression,and a promoter scan identified ABRE-like ele-ments potentially involved in ABA signaling inthe GH3 promoter (9).

The role of ethylene in fruit ripening hasbeen reviewed many times (most recently inReferences 74 and 56) and is therefore coveredonly briefly here. Fleshy fruits have historicallybeen divided into two classes: climacteric(e.g., tomato, apples, and banana) and noncli-macteric (e.g., grape, strawberry, and citrus).Climacteric fruits show a burst of respiration atthe onset of ripening along with a large rise inethylene production. Ripening in climactericfruits can also be initiated by exposure toexogenous ethylene. In nonclimacteric fruits,the respiratory increase is absent and ethylenedoes not appear to be critical for the ripeningprocess. Direct evidence that ethylene is criticalfor the induction of ripening in climacteric fruitcame from work with tomato, where antisensegenes were used to suppress the expression ofACO1 and ACS2, which encode ACC oxidase

228 Seymour et al.

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(ACO) and ACC synthase (ACS), respectively,the major enzymes involved in ethylenebiosynthesis (56). Autocatalytic ethylenebiosynthesis (system-2 ethylene biosynthesis;see 74) is operational during ripening; thisinvolves new forms of ACO and ACS thatproduce much higher levels of ethylene andare not subject to autoinhibition. Ethylene isthen perceived by a family of copper-bindingmembrane-associated receptors, several ofwhich—tomato ETHYLENE RESPONSE4(LeETR4), LeETR6, and NR [which resultsin the phenotype of the Never-ripe (Nr)tomato mutant]—show significantly increasedexpression at the onset of ripening (74). Thereceptors interact with a Raf kinase–like pro-tein, constitutive triple response1 (CTR1), andrepress ethylene responses. When the recep-tors bind ethylene, this inhibition is relievedand a signaling process leads to the ethyleneresponse (56, 74). This involves activation ofthe ETHYLENE INSENSITIVE3 (EIN3)and EIN3-like (EIL) transcription factors byEIN2. In the nonclimacteric pepper fruit,EIL-like genes are induced during ripening(81), suggesting common systems for down-stream signal transduction in climacteric andnonclimacteric fruits, which in the latter occursin the absence of ethylene biosynthesis. Inclimacteric fruit, at least, ethylene productionenhances the expression of some regulatoryand structural genes.

Ethylene does not act to regulate ripeningin isolation, but rather acts in concert withother plant hormones. Lin et al. (85) identi-fied a tetratricopeptide (TPR) repeat protein,SlTPR1, from tomato that interacts with theethylene receptors LeETR1 and NR. Overex-pression of SlTPR1 in tomato enhances ethy-lene responses while causing reduced expres-sion of the early auxin-responsive gene IAA9.

Transcriptional regulators of ripening intomato. A major breakthrough in dissectingthe transcriptional control of tomato ripeningwas the identification of genes underlying raremutations that completely abolish the normalripening process, including ripening inhibitor

(rin), nonripening (nor), and Colorless nonripening(Cnr). These mutant loci all harbor transcrip-tion factors. RIN is encoded by a member ofthe SEPALLATA4 (SEP4) clade of MADS-boxgenes (159), NOR is a member of the NAC-domain transcription factor family (50), andCNR is encoded by an SBP-box gene, targets ofwhich are likely to include the promoters of theSQUAMOSA clade of MADS-box genes (95).

The MADS-RIN gene is necessary for ripen-ing in tomato (159) and the rin mutation im-pacts virtually all ripening pathways, whichsupports its role as a master regulator of theripening process (96). Chromatin immunopre-cipitation experiments indicate that MADS-RIN directly controls the expression of a widerange of other ripening-related genes, target-ing the promoters of genes involved in (a) thebiosynthesis and perception of ethylene, suchas LeACS2, LeACS4, NR, and E8; (b) cell wallmetabolism, such as polygalacturonase (PG),galactanase (TBG4), and expansins (LeEXP1);(c) carotenoid formation, such as phytoene syn-thase (PSY1); (d ) aroma biosynthesis, such aslipoxygenase (Tomlox C), alcohol dehydroge-nase (ADH2), and hydroperoxidelyase (HPL);and (e) the generation of ATP, such as phos-phoglycerate kinase (PGK) and the promoterof MADS-RIN itself (47, 96, 117). MADS-RINis also involved in suppressing the expressionof most ARF genes (78) and therefore auxin-related gene expression.

In tomato, MADS-RIN is involved inswitching on system-2 ethylene through the in-duction of LeACS2, which encodes ACS (96).The conversion of ACC to ethylene, however,requires ACO1. The ACO1 gene does not ap-pear to be under the direct control of MADS-RIN, but its expression is governed by LeHB1,a gene encoding a tomato homeobox protein.LeHB1 stimulates ethylene synthesis by acti-vating the transcription of ACO1. Inhibitionof LeHB1 using virus-induced gene silencing(VIGS) inhibits ripening and greatly reducesACO1 levels. The LeHB1 gene is expressed athigher levels in developing fruits, and the levelsof expression decrease at the onset of ripening(86).


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MADS-RIN binding to promoter targetsoccurs throughout ripening (96). The actionof MADS-RIN to induce the transcription ofripening-related genes is also dependent on thepresence of the CNR gene product or a CNR-regulated gene product (96). The promoters ofthe NOR, CNR, HB1, and TDR4 genes are alsotargets for MADS-RIN, and MADS-RIN canform heterodimers with other MADS-box tran-scription factors such as TAGL1 and TAG1 ofthe AGAMOUS (AG) clade and TDR4 of theSQUAMOSA clade (158). This indicates thatMADS-RIN exerts its control over ripening incooperation with a range of other regulatoryfactors. TAGL1 is upregulated during tomatoripening, and its suppression inhibits normalripening. This occurs partly through inhibi-tion of ethylene biosynthesis, and in TAGL1-silenced lines it appears to occur predominantlythrough direct ACS2 suppression. Indeed, tran-sient promoter-binding studies indicate directinteractions with ACS2. TAGL1 needs RIN forlycopene accumulation, with LYC-B and CYC-B upregulated in TAGL1 RNAi lines. Addition-ally, TAGL1 appears to regulate some cell wallactivities in a RIN-independent manner. It alsoappears to be linked to the phenyl propanoidpathway and activates the flavonoid pathway.TAGL1 RNAi fruit also have thin pericarps, andupregulation produces fleshy ripening sepals.This implicates TAGL1 in not only ripeningbut also the development of fleshiness in tomato(68, 158).

RNAi suppression of AP2—which belongsto the AP2/ETHYLENE RESPONSE FAC-TOR (ERF) family of transcription factors (18,72) and acts downstream of RIN, NOR, andCNR—results in rapid softening and earlierripening. Evidence indicates that AP2 is a neg-ative regulator of ripening in tomato (18) thatoperates in a negative-feedback loop with CNR,as illustrated by the observation that in thepericarps of AP2 RNAi fruits, mRNA levels ofCNR were elevated. In addition, it has beendemonstrated that CNR can bind to the pro-moter of AP2 in vitro (72). Interestingly, AP2RNAi fruits show enhanced GH3 gene expres-sion (72), likely linking AP2 to auxin-related

gene expression. A study of the expression ofARF genes during fruit development in therin mutant and wild-type fruits indicated thatMADS-RIN normally suppresses the expres-sion of most ARFs (78). These data point toa control system involving the removal of auxinby conjugation and then repression of ARFs bythe presence of MADS-RIN.

Unraveling the transcriptome network con-trolling fruit ripening in tomato has revealedsome striking parallels with the regulatory cir-cuits in dry fruit (Figure 4). Similar MADS-boxtranscription factors play a central role in bothfruit types, and in some cases they seem to be di-rectly orthologous (e.g., SHP1/2 and TAGL1).There are also some major differences betweenthe molecular events. In dry fruits, lignificationfollows cell division, whereas in fleshy fruits,cell expansion is observed. Also, in Arabidop-sis there does not appear to be a fruit-relatedMADS-RIN ortholog.

Control of color and texture changes. Asystems biology approach to the tomato tran-scriptome and metabolome during ripening hasled to the identification of a putative carotenoidmodulator, SlERF6 (80). Reduced expressionof SlERF6 by RNAi enhanced both carotenoidand ethylene levels during ripening. Themajority of genes substantially influenced bySlERF6 repression were upregulated, indicat-ing that the primary function of SlERF6 occursvia negative regulation. SlERF6 was responsiveto ethylene and may be a component of afeedback restriction in ethylene productionduring ripening, similar to SlAP2 (80). Asmall number of fruit high-pigment mutantshave been described in tomato, including highpigment1 (hp1) [a lesion in UV-DAMAGEDDNA BINDING PROTEIN1 (DDB1) (89)] andhp2 [a mutation in tomato DE-ETIOLATED1(DET1)] (107). These genes are involved in thesuppression of light responses in the absenceof light, and for DET1, suppression occurs bya molecular mechanism involving chromatinremodeling (24). Coordinated upregulation ofcore metabolic processes is responsible for thehigh-pigment phenotype in the DET1 lines

230 Seymour et al.

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a

b

20 µm

AP2 SHP

INDRPL

FUL

PG

ACO Ethylene

PG

PSY1AP2

NOR EXP

ACS

LOXC

TDR4(FUL)

TAGL1(SHP)

CNRRIN

(SEP4)

HB1

RepressionActivation

Figure 4Ripening network in fleshy fruits and comparisonwith events in the dehiscence of dry fruits. (a) Majorknown regulators of ripening in tomato. The bluecircles are transcription factors; the yellow labels aregenes where orthologs are also found in drydehiscent fruits. Downstream effectors are shown inwhite boxes. Precisely how the gene products ofNOR, CNR, and RIN interact is unknown, so dashedgreen lines are shown between those. (b) Brassica podand dehiscence zone, illustrating a dry-fruit networkusing information obtained in Arabidopsis. Image oftomato fruit with ripening inhibited by silverthiosulfate on the left side kindly provided by DonGrierson and Kevin Davies.

Epigenetics: thestudy of heritablevariation involvingmechanisms otherthan changes in theDNA sequence of anorganism

(38). Upregulation of a Golden 2–like transcrip-tion factor in tomato has also been shown toelevate levels of chlorophyll and carotenoids,and a lesion in this gene is responsible for theuniform-ripening phenotype (116).

Shelf life is important in tomato andother fruits. This trait is influenced by manyprocesses, including the rate of fruit soft-

ening. Modulation of genes encoding tworipening-specific N-glycoprotein-modifyingenzymes—α-mannosidase and β-D-N-acetylhexosaminidase—reduces the rate ofsoftening and enhances fruit shelf life (102).More than 50 cell wall structure–related genesshow expression changes in ripening tomatofruits (151), and texture involves complexquantitative trait loci (13). Shelf life is alsorelated to water loss from the mature fruits.Cuticle properties are critical for maintain-ing fruit integrity postharvest. Delayed FruitDeterioration (DFD) mutant tomato fruitsshow remarkably prolonged resistance topostharvest desiccation and remain firm formany months after harvest (127), and analysesof cutin-deficient tomato mutants indicate theimportance of waxes (67; see also 64).

Tomato as a model for understandingripening in other fleshy-fruited species.In banana—which, like tomato, is a climac-teric fruit—SEP3-class MADS-box genes showripening-related expression (35) and are prob-ably necessary for normal ripening. In straw-berry, a nonclimacteric fruit, a SEP1/2-classgene is needed for normal development andripening (133). VmTDR4, the bilberry orthologof the TDR4 gene in tomato, is involved in theregulation of anthocyanin biosynthesis in thefruit flesh (69), and in apple, MADS2 expressionis associated with fruit firmness (12). MADS-box and NAC transcription factors are associ-ated with the ripening process in the drupe ofthe oil palm (152).

Epigenetics. The lesion responsible for theCnr mutation is due to an epigenetic changeleading to hypermethylation of the CNR pro-moter and inhibition of gene expression andripening in the mutant (95). Additionally, innormal fruit development, at least in the tomatocultivar Liberto, the promoter of CNR appearsto be demethylated in a specific region just priorto the onset of ripening.

A further level of regulation controlling fruitripening occurs through the presence of smallRNAs (sRNAs). These include microRNAs


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(miRNAs) and other sRNAs of unknown func-tion. The CNR 3′ untranslated-region sequencecontains a miRNA binding site that is comple-mentary to miR156 /157 (23). Deep sequencingof the sRNAome of developing tomato fruits,covering the period between closed flowers andripened fruits through the profiling of sRNAsat 10 time points, has revealed that thousands ofnon-miRNA sRNAs are differentially expressedduring fruit development and ripening (106).Some of these sRNAs are derived from trans-posons, but many map to regions in protein-coding genes, including well-defined areas ofthe noncoding regulatory regions (151). Spe-cific classes of sRNAs seem more abundant atcertain stages of development, e.g., 24-mersduring ripening. The function of these changesin sRNA patterns is not known, but they mayplay an important role in the ripening process.

FRUITS AND THE HUMAN DIET

The human genome evolved in the contextof the diet prevailing before the introductionof agriculture and animal husbandry approxi-mately 10,000 years ago, when humans werehunter-gatherers; diets were rich in fruits, veg-etables, and protein and low in fats and starches(33). For primates such as chimpanzees andorangutans, more than 75% of their diet byweight is fresh fruit, and the assumption is thatour primate ancestors had similar diets. Fruitis also common in the diet of modern hunter-gatherers.

The 10,000 years (∼360 generations) sincethe first cultivation of cereals has not beenenough time for humans to adapt to starchier,cereal-based diets with much higher amountsof fat and lower amounts of fresh fruit and veg-etables, and it has been suggested that manychronic diseases result from our evolutionarydiscordance with modern diets (21). Levelsof phytonutrients—compounds in plant-basedfoods that play potentially beneficial roles inthe prevention and treatment of disease—in thediet have dropped significantly owing to a re-duced variety of plants consumed (currently,just 17 plant species constitute 90% of the

global human diet) and to selective breeding(161). For these reasons, most modern dietaryrecommendations include increased consump-tion of fresh or whole fruits and vegetables. Therole of plants in human health is the subject ofanother review (98), but what is beneficial aboutfruit consumption?

Fruits such as eggplant, mango, and okra aregood sources of soluble fiber, which has beenshown experimentally to lower the glycemicindex of foods and to have beneficial effectson type 2 diabetes, cardiovascular disease, andobesity (66, 73, 79, 103). Fruits are also richin fructose (which constitutes 20–40% of theavailable carbohydrates in wild fruit) and in-trinsic sugars; these are not subject to restric-tions in dietary recommendations because theirconcentrations are not high enough to have ad-verse health outcomes (94). Fruits generally alsocontain high levels of phytonutrients, and in-clude carotenoids, polyphenols (flavonoids, stil-benes), plant sterols, vitamins, and polyunsatu-rated fatty acids.

Some fruits are rich in carotenoids, whichare thought to attract animals as dispersersthrough their bright colors (for example,lycopene in tomato; capsanthin, β-carotene,lutein, and violaxanthin in red pepper; ly-copene and β-carotene in red grapefruit;and β-carotene, α-carotene, and lutein inmangoes). Lycopene is a methyl-branchedcarotenoid that has no provitamin A activity. Itis a potent lipophilic antioxidant, with greaterantioxidant activity than other carotenoids,and has been shown to be protective againstcardiovascular disease and prostate cancer (43).Intervention and epidemiological studies havelinked β-carotene consumption to enhancedprotection against cardiovascular disease,including cerebral infarction, and resistanceto low-density lipoprotein oxidation, ischemicstroke, and carotid atherosclerosis (7, 43,121).

Fruits are rich sources of polyphenols thathave gained significant recognition recently asbeing important phytonutrients, reducing therisk of chronic diseases such as cardiovascu-lar disease, metabolic syndrome, cancer, and

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High-throughputsequencingtechnologies:methods that involveproducing millions ofsequences from DNAsamples in a parallelprocess

obesity. Anthocyanins represent a subset offlavonoids with particularly high antioxidant ca-pacity and strong health-promoting effects. Aspart of the human diet, they offer protectionagainst cancer, inhibiting both the initiationand progression stages of tumor development(154), reducing inflammatory inducers of tumorinitiation, suppressing angiogenesis, and min-imizing cancer-induced DNA damage in ani-mal disease models. Anthocyanins also protectagainst cardiovascular disease and age-relateddegenerative diseases associated with metabolicsyndrome (63, 119), have anti-inflammatory ac-tivity (134), promote visual acuity (101), andhinder obesity and diabetes (154). Inverse cor-relations between consumption of flavonol-richdiets and the occurrence of cardiovascular dis-ease, certain cancers, and age-related degener-ative diseases (62, 75, 105, 130, 138) have beenshown in human epidemiological studies as wellas by data from cell-based assays and feedingtrials with animals.

Another important group of plant-basedbioactive polyphenols is the hydroxycinnamicacid esters, of which chlorogenic acid is themajor soluble phenolic in solanaceous speciessuch as potato, tomato, and eggplant as well asin coffee. Chlorogenic acid is one of the mostabundant polyphenols in the human diet and isthe major antioxidant in the average developed-world diet. It has significant antioxidant activ-ity, and consumption can limit glucose absorp-tion and possibly weight gain (146).

Epicatechins are the major polyphenoliccompounds in green tea, and the most sig-nificant active component is thought to beepigallocatechin gallate. Cell, animal, and hu-man studies have shown that green tea ex-tract/epicatechins prevent cancer development,particularly prostate cancer (22, 31). Similar ef-fects may be gained by consumption of fleshyfruits such as cranberry, blueberry, and grape orby consumption of berry-juice products; thesehave relatively high levels of catechins and epi-catechins, which also protect against cardiovas-cular disease (27).

Dietary intervention studies support theview that consumption of fruit (especially when

replacing calorie-dense food) helps maintain ahealthy weight and reduce the risk of a widerange of cancers (150, 163) and cardiovascu-lar disease (59, 60, 82). Consequently, dietaryimprovement by increasing fruit consumptionor by improving fruit to contain higher lev-els of fiber or phytonutrients should have apositive impact on the incidence and progres-sion of chronic disease. Such improvement offruit crops could be carried out through geneticmodification (11) or marker-assisted selectionusing existing variation.

CROP IMPROVEMENT

High-throughput sequencing technologieshave provided a powerful new set of toolsto reveal genetic and epigenetic variationon a genome-wide scale and therefore newinsights into the evolution of genomes and traitvariation. Fruit crop genomes that have beensequenced include grapevine (Vitis vinifera)(70), apple (Malus × domestica) (157), diploidstrawberry (Fragaria vesca) (135), tomato(Solanum lycopersicum) (151), and banana (Musaacuminata) (28). These resources will underpinadvances in the breeding of fruit crops by (a)greatly facilitating marker-assisted selectionand allowing efficient cloning of genes under-pinning quantitative trait loci, (b) providingthe reference genomes for rapid allele miningin crop wild relatives (87), (c) providing aguide for direct sequencing of monogenicmutants, and (d ) maximizing opportunitiesto optimize reverse-genetics tools such astargeting-induced local lesions in genomes(TILLING) for gene functional studies (142).Genome-wide information also allows rapidanalyses of gene structure, binding-site motifs,and gene regulatory regions.

In the future, high-throughput sequencingtechnologies will allow routine screeningof crop epigenomes and therefore permitdetection of epigenetic variation that impactsphenotypes. Additionally, translational biologyfrom models to crop species has clear utilityin enhancing important crop traits; e.g.,fine-tuning the expression of the value margin


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identity gene IND in Brassica gives a potentiallyuseful partial dehiscence phenotype (52).Harnessing variation in crop wild relatives in

combination with direct genetic modificationprovides a powerful route for a massive stepchange in crop improvement.

SUMMARY POINTS

1. True fruits are found only in the angiosperms, or flowering plants. They are often definedas structures derived from a mature ovary containing seeds, but many structures we callfruit are composed of a variety of tissues. Fruit structures can be dehiscent or indehiscent,can have a dry or fleshy exterior, and include grains, nuts, capsules, and berries.

2. Recent work on the model plant Arabidopsis and on tomato nonripening mutants hasuncovered the complex high-level regulatory network controlling fruit maturation andripening. Striking parallels have been revealed between the molecular circuits in dryfruits and those in fleshy fruits. In both types, similar MADS-box transcription factorsplay a central role, and in some cases they seem to be directly orthologous.

3. Tomato is a good model for understanding aspects of the molecular framework control-ling ripening in other fleshy fruits. Classes of transcription factors controlling tomatoripening have been shown to govern this process in other fleshy-fruit-bearing species.

4. The human genome evolved in the context of the diet prevailing before the introductionof agriculture and animal husbandry approximately 10,000 years ago, when humans werehunter-gatherers; diets were rich in fruits, vegetables, and protein and low in fats andstarches. Fruits provide vitamins, minerals, and phytochemicals that are essential forhuman health.

5. The genomes of a variety of fleshy-fruited species have been sequenced and provideguides for revealing previously hidden genetic and epigenetic variation that will open anew frontier for crop improvement.

FUTURE ISSUES

1. Can predictive models of the ripening regulatory network be generated for tomato andother fleshy- and dry-fruited species? And can major ripening processes—e.g., textureand color development—be separated to allow better control over the process?

2. Is it possible to modify regulatory networks to easily transition from a dry- to fleshy-fruitphenotype or vice versa?

3. One of the best-characterized natural epigenetic mutations was discovered in tomato.To what extent is epigenetic variation responsible for controlling important quality traitsin crops and crop wild relatives?

DISCLOSURE STATEMENT

C.M. is a director of Norfolk Plant Sciences, an SME for the development of phytonutrient-enriched fruits and vegetables.

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ACKNOWLEDGMENTS

We wish to acknowledge the support of the UK Biotechnology and Biological Sciences ResearchCouncil to G.B.S. (BB/G02491X) and the US National Science Foundation Planetary BiodiversityInitiative to S.K. (DEB-0316614).

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PP64-frontmatter ARI 25 March 2013 10:21

Annual Review ofPlant Biology

Volume 64, 2013Contents

Benefits of an Inclusive US Education SystemElisabeth Gantt � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Plants, Diet, and HealthCathie Martin, Yang Zhang, Chiara Tonelli, and Katia Petroni � � � � � � � � � � � � � � � � � � � � � � � � �19

A Bountiful Harvest: Genomic Insights into Crop DomesticationPhenotypesKenneth M. Olsen and Jonathan F. Wendel � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �47

Progress Toward Understanding Heterosis in Crop PlantsPatrick S. Schnable and Nathan M. Springer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �71

Tapping the Promise of Genomics in Species with Complex,Nonmodel GenomesCandice N. Hirsch and C. Robin Buell � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �89

Understanding Reproductive Isolation Based on the Rice ModelYidan Ouyang and Qifa Zhang � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 111

Classification and Comparison of Small RNAs from PlantsMichael J. Axtell � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 137

Plant Protein InteractomesPascal Braun, Sebastien Aubourg, Jelle Van Leene, Geert De Jaeger,

and Claire Lurin � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 161

Seed-Development Programs: A Systems Biology–Based ComparisonBetween Dicots and MonocotsNese Sreenivasulu and Ulrich Wobus � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 189

Fruit Development and RipeningGraham B. Seymour, Lars Østergaard, Natalie H. Chapman, Sandra Knapp,

and Cathie Martin � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 219

Growth Mechanisms in Tip-Growing Plant CellsCaleb M. Rounds and Magdalena Bezanilla � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 243

Future Scenarios for Plant PhenotypingFabio Fiorani and Ulrich Schurr � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 267

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Microgenomics: Genome-Scale, Cell-Specific Monitoring of MultipleGene Regulation TiersJ. Bailey-Serres � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 293

Plant Genome Engineering with Sequence-Specific NucleasesDaniel F. Voytas � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 327

Smaller, Faster, Brighter: Advances in Optical Imagingof Living Plant CellsSidney L. Shaw and David W. Ehrhardt � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 351

Phytochrome Cytoplasmic SignalingJon Hughes � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 377

Photoreceptor Signaling Networks in Plant Responses to ShadeJorge J. Casal � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 403

ROS-Mediated Lipid Peroxidation and RES-Activated SignalingEdward E. Farmer and Martin J. Mueller � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 429

Potassium Transport and Signaling in Higher PlantsYi Wang and Wei-Hua Wu � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 451

Endoplasmic Reticulum Stress Responses in PlantsStephen H. Howell � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 477

Membrane Microdomains, Rafts, and Detergent-Resistant Membranesin Plants and FungiJan Malinsky, Miroslava Opekarova, Guido Grossmann, and Widmar Tanner � � � � � � � 501

The EndodermisNiko Geldner � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 531

Intracellular Signaling from Plastid to NucleusWei Chi, Xuwu Sun, and Lixin Zhang � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 559

The Number, Speed, and Impact of Plastid Endosymbioses inEukaryotic EvolutionPatrick J. Keeling � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 583

Photosystem II Assembly: From Cyanobacteria to PlantsJorg Nickelsen and Birgit Rengstl � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 609

Unraveling the Heater: New Insights into the Structure of theAlternative OxidaseAnthony L. Moore, Tomoo Shiba, Luke Young, Shigeharu Harada, Kiyoshi Kita,

and Kikukatsu Ito � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 637

Network Analysis of the MVA and MEP Pathways for IsoprenoidSynthesisEva Vranova, Diana Coman, and Wilhelm Gruissem � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 665

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Toward Cool C4 CropsStephen P. Long and Ashley K. Spence � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 701

The Spatial Organization of Metabolism Within the Plant CellLee J. Sweetlove and Alisdair R. Fernie � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 723

Evolving Views of Pectin BiosynthesisMelani A. Atmodjo, Zhangying Hao, and Debra Mohnen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 747

Transport and Metabolism in Legume-Rhizobia SymbiosesMichael Udvardi and Philip S. Poole � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 781

Structure and Functions of the Bacterial Microbiota of PlantsDavide Bulgarelli, Klaus Schlaeppi, Stijn Spaepen, Emiel Ver Loren van Themaat,

and Paul Schulze-Lefert � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 807

Systemic Acquired Resistance: Turning Local Infectioninto Global DefenseZheng Qing Fu and Xinnian Dong � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 839

Indexes

Cumulative Index of Contributing Authors, Volumes 55–64 � � � � � � � � � � � � � � � � � � � � � � � � � � � 865

Cumulative Index of Article Titles, Volumes 55–64 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 871

Errata

An online log of corrections to Annual Review of Plant Biology articles may be found athttp://www.annualreviews.org/errata/arplant

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Technology