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Fruit Development
and Ripening
Graham B. Seymour,1 Lars Østergaard,2
Natalie H. Chapman,1 Sandra Knapp,4
and Cathie Martin3
1
Plant and Crop Science Division, School of Biosciences, University of Nottingham,
Loughborough LE12 5RD, United Kingdom; email: [email protected],
[email protected]
2
Department of Crop Genetics and 3 Department of Metabolic Biology, John Innes Center,
Norwich NR4 7UH, United Kingdom; email: [email protected],
[email protected]
4
Department of Life Sciences, Natural History Museum, London SW7 5BD,
United Kingdom; email: [email protected]
Annu. Rev. Plant Biol. 2013. 64:219–41
Keywords
First published online as a Review in Advance on
February 4, 2013
Arabidopsis, tomato, diet, gene regulation, epigenetics
The Annual Review of Plant Biology is online at
plant.annualreviews.org
Abstract
This article’s doi:
10.1146/annurev-arplant-050312-120057
c 2013 by Annual Reviews.
Copyright All rights reserved
Fruiting structures in the angiosperms range from completely dry to
highly 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 controlling
fruit development has been revealed. Studies on rare nonripening
mutations in tomato, a model for fleshy fruits, have provided new
insights into the networks responsible for the control of ripening. It
is apparent that there are strong similarities between dry and fleshy
fruits in the molecular circuits governing development and maturation.
Translation of information from tomato to other fleshy-fruited
species indicates that regulatory networks are conserved across a wide
spectrum of angiosperm fruit morphologies. Fruits are an essential
part of the human diet, and recent developments in the sequencing of
angiosperm genomes have provided the foundation for a step change
in crop improvement through the understanding and harnessing of
genome-wide genetic and epigenetic variation.
219
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Contents
INTRODUCTION . . . . . . . . . . . . . . . . . .
NOMENCLATURE, EVOLUTION,
DIVERSITY . . . . . . . . . . . . . . . . . . . . . .
FRUIT DEVELOPMENT AND
RIPENING . . . . . . . . . . . . . . . . . . . . . . .
The Fruiting Structure . . . . . . . . . . . . .
Hormonal and Genetic
Regulation. . . . . . . . . . . . . . . . . . . . . .
Fertilization . . . . . . . . . . . . . . . . . . . . . . .
Fruit Development . . . . . . . . . . . . . . . . .
Hormonal and Genetic Regulation
of Maturation and Dehiscence
in Dry Fruits . . . . . . . . . . . . . . . . . . .
Hormonal and Genetic Regulation
of Maturation and Ripening
in Fleshy Fruits . . . . . . . . . . . . . . . . .
FRUITS AND THE HUMAN
DIET . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
CROP IMPROVEMENT . . . . . . . . . . . .
220
220
222
222
223
224
225
227
228
232
233
INTRODUCTION
Gynoecium: the
carpels or female
reproductive organs of
flowering plants,
consisting of an ovary
harboring the ovules,
stigmatic tissue for
pollen reception at the
top, and a gynophore
at the base connecting
the gynoecium to the
plant
Apocarpous: having
free carpels
Syncarpous: having
fused carpels
Nut: indehiscent fruit
with a hard shell
Berry: fleshy fruit
produced from a single
ovary, often with many
seeds
220
True fruits are found only in the angiosperms,
or flowering plants; the name angiosperm
means hidden seed. Flowering plants comprise
some 250,000–400,000 species in four major
clades (10) that are the dominant component
of vegetation in most tropical, subtropical, and
temperate zones worldwide. The angiosperms
comprise tiny herbs to large canopy trees, occupy terrestrial and aquatic (including marine)
habitats, and are the source of all major crop
plants. As such, humans have a long and intimate association with angiosperms, particularly
with their fruits and seeds.
Fruits are often defined as structures derived
from a mature ovary containing seeds (48), but
many structures we might define as fruit are
in fact composed of a variety of tissue types
(Figure 1). Van der Pijl (155) used the concept
of the dispersal unit as his definition of a fruit;
this links fruits to their role in the ecology of
the plant life cycle as the mechanism by which
seeds are dispersed. Dispersal units also occur
Seymour et al.
in land plants other than angiosperms; some
Carboniferous seed ferns had fleshy structures
that are thought to have been eaten by reptiles
(148), and the seed of the “living fossil” Ginkgo
biloba is enveloped in a soft fleshy covering
called the sarcotesta. These propagules are not
considered true fruits despite their functional
similarities. True fruits are derived from the
flower gynoecium (see Fruit Development and
Ripening, below).
NOMENCLATURE, EVOLUTION,
DIVERSITY
The myriad of fruit types recognized in angiosperms can be simplified using combinations
of the following characteristics: dehiscence or
indehiscence, dry or fleshy exterior, and free
(apocarpous) or fused (syncarpous) carpels.
Capsules (Figure 1c) and the siliques of
Arabidopsis relatives (Figure 1a) are dehiscent, dry, and syncarpous; achenes and nuts
(Figure 1e,g,h) are indehiscent, dry, and
unicarpellate; and berries (Figure 1b,d) are
indehiscent, fleshy, and syncarpous. A drupe
is an indehiscent, fleshy, single-seeded fruit
where the seed is enclosed in a hard endocarp,
like a peach pit (Figure 1f ). Syncarpy occurs
in 83% of extant angiosperm species and has
been interpreted as facilitating pollen tube
competition and thus fitness (36); it has arisen
independently in both the monocots and the
eudicots (37). Apocarpy is rarer but can be
seen in the fruits of magnolias, with clusters of
separate carpels termed follicles. Endress (36)
has suggested that syncarpy might facilitate
adaptive radiation in fruit type by increasing
the possibility of developing fleshiness and/or
dehiscence mechanisms.
Darwin thought that the recent origin and
rapid diversification of the angiosperms was
“an abominable mystery” (44). The angiosperm
fossil record extends back to the Early Cretaceous period, and the earliest unambiguous
fossils (65) are dated conservatively to approximately 132 Mya. Angiosperms were common
and diverse by the mid-Cretaceous, indicating
either that their first major diversification and
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a
b
c
d
e
f
g
h
Figure 1
Fruit diversity. (a) Lunaria annua L. (Brassicaceae), cultivated, United Kingdom: dehiscent siliques that dry
and shatter irregularly with age, releasing the seeds. (b) Mandragora officinalis L. (Solanaceae), Andalucı́a,
Spain: indehiscent berries with fleshy, brightly colored mesocarp and many seeds. (c) Nicotiana sylvestris
Speg. & Comes (Solanaceae), Apurı́mac, Peru: dehiscent capsules opening along suture lines. The
seed-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. The
remnants 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-seeded
achenes on the surface of an expanded, brightly colored receptacle. All photos by Sandra Knapp.
ecological radiation occurred over a relatively
short time frame or that they originated and
diversified 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 and
8.3 mm3 (the size of a small cherry) and seed volumes between 0.02 and 6.9 mm3 (39). Diverse
www.annualreviews.org • Fruit Development and Ripening
Drupe: indehiscent
fruit with fleshy outer
pericarp layers
(exocarp and
mesocarp) but a hard
inner pericarp layer
(endocarp)
surrounding the seed
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fruit types are represented in Early Cretaceous
fossils; the vast majority are either indehiscent,
single-seeded nuts or drupes with one or a few
seeds, but some dehiscent, apocarpous fruits
have been found, as have many fruits with fleshy
outer layers (45). One-quarter of all fruits found
at one site were fleshy drupes or berries (40).
Lorts et al. (91) mapped crude fruit type
categories (dry dehiscent, dry indehiscent, and
fleshy) onto the orders of extant angiosperms
and found no association (assessed visually) between fruit type and major clade. This suggests
that there is no phylogenetic constraint on
fruit type evolution across the major lineages
(orders) of angiosperms, with most orders
having all three broadly defined fruit types
(see figure 1 of Reference 91). Fruit and seed
size both increased in the Tertiary (39), with
a drastic change at the Cretaceous–Tertiary
boundary (147, 162). It has been suggested
that the origin of fleshiness was initially related
to defense against pathogens and only later
co-opted for biotic dispersal (93, 149).
Size change in both fruits and seeds through
the fossil record has been attributed to coevolution with seed-dispersing animals (147),
with this mutualistic relationship then driving
the development of closed, forested habitats
(large seeds are characteristic of closed plant
communities). An alternative hypothesis is that
changes in habitat through climate change, perhaps coupled with the demise of large herbivores (e.g., dinosaurs), drove the evolution of
larger fruits and seeds, and the availability of
seed dispersers reinforced this trend (39). Dispersers thus tracked, rather than led, changes
in fruit size and morphology. Distinguishing
between these two hypotheses is difficult owing to bias in the fossil record (39) and uncertainty over ecological dynamics in the past
(149), but a series of studies using both extant and fossil fruits have strongly supported
the latter hypothesis. The significant correlations between fruit type and habitat conditions
in a broad set of extant flowering plants (8) suggest that the evolution of fleshiness is related
to changes in vegetation from open to closed
habitats.
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Seymour et al.
It is tempting to assume that fruit diversity
is the result of adaptation to frugivores; adaptationist scenarios about tight obligate relationships between fruits and their dispersers abound
in the literature, but they have been shown to
be less compelling than originally thought. The
strong role of habitat and climate in the origin and evolution of fruit characteristics such
as fleshiness (39) has been clearly demonstrated
in both the fossil record and through correlation studies with extant angiosperms. Syncarpy
may represent a key innovation for angiosperm
fruits in that it facilitated pollen competition
and pollen tube protection (37). Fruit color is
another characteristic that on its face seems to
be adaptive for frugivore attraction, but studies
examining color as a signal have demonstrated
that, like the evolution of other fruit characteristics, the evolution of fruit color is mediated
through diffuse interactions between plants, antagonists (such as microbial predators), and mutualists (128). Fleshy-fruit evolution has clearly
been an important and continually recurring
theme throughout flowering plant evolution,
and assumptions with respect to the adaptive
value of particular fruit traits must be carefully
examined.
FRUIT DEVELOPMENT AND
RIPENING
The Fruiting Structure
The gynoecium is derived from the fusion of
carpels and forms in the center of the flower.
Many regulators of carpel development identified in Arabidopsis also have roles during leaf development, thereby confirming the evolutionary origin of carpels as modified leaves (41, 129).
The main patterning events of the Arabidopsis
gynoecium take place before fertilization and
occur along three axes: apical-basal, mediolateral, and abaxial-adaxial (dorsoventral). Stigmatic tissue (Figure 2) that mediates pollen
germination develops at the apical (distal) end.
After germination, the pollen tube grows down
through the transmitting tract and enters the
ovules through the micropyle, a small opening
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in the integument layers (90). A solid style with
radial symmetry supports the segment of the
transmitting tract just below the stigma and is
required for efficient fertilization (Figure 2).
The ovary is formed from the carpels as a longitudinal cylinder with mediolateral symmetry
that reflects its origin as two fused leaflike organs (Figure 2). It is composed of two compartments divided by a septum and placenta
from which ovules arise. The carpel walls exhibit abaxial-adaxial asymmetry with an exocarp
layer of large cells interspersed with stomata,
three or four layers of mesocarp cells, and two
innermost layers of endocarp cell layers. The
Arabidopsis gynoecium is connected at its base
to the pedicel and the rest of the plant via a
gynophore.
Hormonal and Genetic Regulation
The plant hormone auxin has been established as an important component for patterning along the different axes of polarity
in the Arabidopsis gynoecium. In the apicalbasal orientation, auxin synthesis at the apex
is required for specification of the style and
stigma (137). Auxin biosynthesis at the apex
is promoted through the activity of transcription factors such as STYLISH1 (STY1), STY2,
and NGATHA3, which induce expression of
YUCCA auxin biosynthesis genes (2, 15, 34,
137, 153). Exogenous application of auxin rescues the split style of the sty1/2 mutant (141).
The basic helix-loop-helix (bHLH) proteins are a large family of transcription factors
found in all eukaryotic organisms (99, 115).
Several members of this family have functions
during gynoecium development or later in
fruit development. For example, mutations
in the SPATULA (SPT ) gene lead to early
defects in the development of carpel marginal
tissues such as the stigma, style, septum, and
transmitting tract (3, 61). SPT activity promoting carpel development was recruited during
the evolution of flowering plants from lightregulated processes such as those involved in
shade-avoidance responses in vegetative organs
(120). Phenotypic defects similar to those
a
b
d
Stigma
Sti
SSt
tig
gma
ma
Sty
Sty
tyle
le
e
Style
Valve
50 µm
Valve
margin
Replum
Septum
c
50 µm
Gynophore
Transmitting
tract
Ovule
200 µm
200 µm
Figure 2
Arabidopsis gynoecium patterning. (a) False-colored scanning electron
micrograph (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 transmitting
tract (orange). (c) Cross section of an ovary with bilateral symmetry. Color
coding 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 spt
double-mutant stage-13 gynoecium that completely lacks the stigmatic tissue
and radial style. The surface of the cells at the very apical part of the valves
suggests that they have retained style identity.
observed in spt mutant gynoecia were observed
in multiple combinations of mutations in the
bHLH-encoding HECATE (HEC) genes, and
protein-protein interactions between SPT and
HEC proteins in yeast two-hybrid experiments
suggest that these factors may jointly regulate
downstream targets (55). Loss-of-function
mutations in the ETTIN (ETT ) gene, which
encodes AUXIN RESPONSE FACTOR3
(ARF3), exhibit enlarged apical and basal
regions at the expense of the ovary (132).
Because ETT negatively regulates SPT/HEC
genes in the ovary, it has been suggested that
ETT regulates ovary size, perhaps in response
to local auxin dynamics (61, 108, 144).
Further connections between gynoecium
patterning and auxin were made when it
appeared that mutations in another bHLHfactor-encoding gene, INDEHISCENT (IND),
strongly enhanced the phenotype of the spt
single mutant (51) (Figure 2d ). IND and SPT
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Parthenocarpic:
producing fruit
without fertilization;
the resulting fruits are
seedless
14:57
heterodimerize in plant cells and regulate a
common set of target genes (51, 139), and a
number of their direct targets are involved in
controlling the direction of auxin transport
(51, 139). IND belongs to the same clade
in the Arabidopsis bHLH family as the three
HEC genes (115). Loss of all three HEC genes
gives rise to a split-style phenotype with no
stigmatic tissue, identical to the ind spt mutant
gynoecium (55), and it is therefore likely that
HEC proteins also interact with SPT in planta.
Tissue identity factor activity and auxin dynamics are at the center of gynoecium patterning control. With the development of tools
to study auxin transport and signaling in Arabidopsis, data are now emerging to provide an
overview of how auxin is distributed during gynoecium development. For example, the auxin
signaling reporter DR5::GFP shows a strong
green fluorescent protein (GFP) signal accumulating in a ring at the distal end of the
gynoecium prior to stigma formation (51). In
the spt single mutant and the ind spt double
mutant, this ring is not formed; instead, the
GFP signal accumulates in two foci at the distal end. Because both IND and SPT are expressed in this distal region, it is likely that they
are responsible for lateral auxin distribution
to create a continuous ring and ensure proper
development.
Fertilization
The developmental switch that turns a gynoecium into a growing fruit depends on the fertilization of ovules that form along the placenta. In
most angiosperms, the gynoecium senesces and
dies if not fertilized. The fruit initiation process has traditionally been thought to involve
phytohormone activities (49). Upon fertilization, a seed-originating auxin signal is generated (32, 104, 126) that is thought to upregulate
biosynthesis of another hormone, gibberellin
(GA). This leads to activation of GA signaling in
the ovules and valves, thereby stimulating fruit
growth (32, 111, 131, 156).
Degradation of the growth-repressing
DELLA proteins is central to GA signaling.
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Seymour et al.
DELLAs are characterized by a conserved
DELLA motif in the N-terminal domain and a
SCARECROW-like C-terminal domain (113,
136). According to the “relief of restraint”
model (58), GA-mediated DELLA degradation
is required to overcome the growth-repressing
DELLA activity. In agreement with their
function as growth repressors, reduction in
DELLA activity can promote parthenocarpic
fruit growth in both dry dehiscent fruits
and fleshy fruits (32, 97). GA treatment of
gynoecia in a della loss-of-function mutant
has revealed the existence of a GA-dependent
but DELLA-independent pathway that contributes to fruit growth in Arabidopsis (46).
This newly identified DELLA-independent
pathway provides additional opportunities for
fine-tuning fruit growth.
ARFs and Aux/IAA proteins also function
during fruit initiation. In Arabidopsis and
tomato, expression of aberrant forms of ARF8
results in parthenocarpic fruit development
(53, 54), as does silencing of IAA9 in tomato
(160). It is not clear by what mechanism ARF8
regulation occurs, but based on the model for
auxin signal transduction, it has been suggested
that ARF8 and the Aux/IAA protein IAA9 may
form a transcriptional repressor complex that is
destabilized by the aberrant forms of ARF8 to
allow transcription of auxin-responsive genes
(53).
In tomato, pollination causes upregulation
of ARF9 and downregulation of ARF7. Silencing of the SlARF7 gene in transgenic plants
(cv. Moneymaker) results in parthenocarpic
fruit development, suggesting that SlARF7
is a negative regulator of fruit set. Silencing
of SlARF7 also results in strong upregulation
of SlGH3, which encodes an IAA–amido
synthetase that may be induced to compensate
for excessive auxin (25, 26). Differences in cell
size between SlARF7-silenced lines and the
wild type become apparent 6 days postanthesis
(DPA), with significant cell size increase in the
mesocarp and endocarp layers, and so it has
been concluded that downregulation of SlARF7
deregulates cell division and upregulates cell
expansion (26). In addition, there is evidence in
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tomato that early photosynthesis is important
for proper seed set (92).
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Fruit Development
Upon fertilization, Arabidopsis fruit enters a
stage in which ovary growth and maturation
are tightly coordinated with seed development. During this process, a number of fruit
tissues develop, including valves (derived from
the carpel walls), a central replum, a false
septum, and valve margins that form at the
valve/replum borders. Late in development,
the valve margins differentiate into dehiscence
zones, where fruit opening will take place.
Although these individual tissues were specified
prior to fertilization, their distinct appearance
becomes more striking after fertilization,
forming sharp boundaries, particularly along
the valve margin (125).
As described above, the valves (carpel walls)
exhibit abaxial-adaxial asymmetry and are composed of an outermost (abaxial) epidermal layer
with long, broad cells interspersed with guard
cells (stomata). Underneath the epidermal
layer, three to six layers of mesophyll cells follow (Figure 3). Two specialized adaxial cell layers form in the valves: The innermost endocarp
A layer (valve margins) is composed of large
cells that undergo cell death before the fruit has
completely matured, whereas cells in the endocarp B layer remain small and develop lignified
cell walls (Figure 3) whose rigidity may assist
in the process of fruit opening by providing significant tension in the mature fruit (140). The
replum is connected to the septum and contains
the main vascular bundles. At the valve margin,
a narrow file of dehiscence zone cells differentiates along the entire length of the fruit late
in development, allowing the valves to detach
from the replum, which causes seed dispersal
to occur by a shattering mechanism. The valve
margins consist of two distinct cell layers: a separation layer, where cell separation will take
place, and a layer of lignified cells, whose rigidity may promote the opening process (140).
Development of fleshy fruit such as tomato
involves cell division and expansion of the ovary
tissues, but without the lignification phase
found in dry fruit. In the miniature tomato
(cv. Micro-Tom) (112), cell division starts at 2
DPA, when the ovary is 1 mm in diameter with
10 cell layers (Figure 3). Cell divisions are both
periclinal and anticlinal, and by 4 DPA the fruit
is 1.5 mm in diameter and has 30 cell layers.
Cell division continues at 7–8 DPA, but then
cell expansion becomes apparent and the cell
layer number increases to 35 at the apex of the
fruit and 20 at the equator. Cell division stops
by 10–13 DPA, and cell expansion progresses
at 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 undergo
division after anthesis are the mesocarp collenchyma. Cell expansion is responsible for
the increase in fleshy-fruit size (Figure 3),
with cell sizes in tomato reaching 0.5 mm in
diameter in the pericarps of some varieties (16).
Fruit size in tomato is controlled by nearly
30 quantitative trait loci. The Fw2.2 gene
is responsible for approximately 30% of the
variation, and encodes a plant-specific and
fruit-specific protein that negatively regulates
mitosis and is possibly part of the cell cycle
signal transduction pathway (20). Pericarp
cell number in tomato is also linked to the
expression of the MADS-box gene TOMATO
AGAMOUS (TAG)–LIKE1 (TAGL1), which
is an ortholog of the Arabidopsis SHATTERPROOF (SHP) genes (158). TAGL1 is expressed
in floral organs and young tomato fruit as well as
during ripening. It is one of the most abundant
MADS-box genes expressed in tissues of young
fruits (100), and in RNAi::TAGL1 tomato fruits
there is a reduction in pericarp thickness from
25 to 15 layers measured at 28 and 38 DPA, respectively, and the inner pericarp appears to be
absent.
Four genes that control shape in tomato
have been cloned: SUN and OVATE, which
control fruit elongation shape; FASCIATED,
which is associated with flat-shaped fruit; and
LOCULE NUMBER, which regulates fruit
locule number. SUN encodes an IQD family
protein that is thought to alter hormone or
secondary metabolite levels (164), whereas
www.annualreviews.org • Fruit Development and Ripening
Quantitative trait
loci: DNA regions
associated with a
phenotype that is
controlled by two or
more genes
MADS-box genes:
transcription factors
detected in nearly all
eukaryotes; in plants,
they are commonly
associated with floral
development
225
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a
b
Exocarp
Exocarp
Mesocarp
Mesocarp
Endocarp
Endocarp
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c
d
Exocarp
Mesocarp
Endocarp
200 µm
500 µm
e
2 DPA
4 DPA
8 DPA
24 DPA
Exocarp
Mesocarp
50 µm
50 µm
Endocarp
240 µm
200 µm
Figure 3
Changes 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 division
and cell expansion phases. Panels a, b, and e courtesy of Pabón-Mora & Litt (112).
OVATE encodes a negative growth regulator,
presumably by acting as a repressor of transcription and thereby reducing fruit length.
FASCIATED encodes a YABBY transcription
factor (19). LOCULE NUMBER was recently
226
Seymour et al.
linked to two single-nucleotide polymorphisms (SNPs) located approximately 1,200
base pairs downstream of the stop codon of a
gene encoding a WUSCHEL homeodomain
protein, members of which regulate plant stem
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cell fate. Alleles of these genes appear to have
played a critical role in forging the shape of
domesticated tomato fruits (123).
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Hormonal and Genetic Regulation
of Maturation and Dehiscence
in Dry Fruits
Formation of the valve margin region depends
on several transcription factor activities.
Upstream in the hierarchy, two closely related
MADS-box transcription factor–encoding
genes, SHP1 and SHP2, positively regulate
the IND gene described above as well as
ALCATRAZ (ALC), which encodes another
bHLH transcription factor (83, 84, 118).
Although none of the shp single mutants have
any detectable phenotype on their own, the
combined shp1 shp2 double mutant produces
indehiscent fruit devoid of valve margin
differentiation (83). Despite the role of IND in
gynoecium formation, the most pronounced
phenotypic defect of ind mutants and loss of
IND function is a loss of valve margin identity
that affects both the lignified and separation
layers (84). In contrast, fruits from alc mutants
produce lignified cells at the valve margin, but
the separation layer cells fail to develop (118).
The FRUITFULL (FUL) gene encodes a
MADS-box transcription factor that is required
for maintaining valve identity (57). The valves
developed in ful mutant fruits adopt a partial
change of identity into valve margin cells with
ectopic lignification. In these mutant valves,
SHP1, SHP2, and IND become ectopically expressed, and the phenotype can be almost entirely rescued by combining the ful mutant with
mutations in valve margin identity genes. FUL
thus specifies valve cell fate at least in part by repressing the expression of valve margin identity
genes in valve tissue (42, 84).
The homeodomain-containing transcription factor REPLUMLESS (RPL) is a key regulator of the replum tissue on the medial side
of the valve margins. As the name implies, rpl
loss-of-function mutants fail to develop a replum. Similar to the activity of FUL, RPL represses valve margin identity gene expression
in the replum, and combining rpl mutants with,
for example, the shp double or ind single mutant
rescues the replum defect (122, 124). Species of
Brassica produce fruits that are morphologically
very similar to those of Arabidopsis, but they lack
an outer replum, suggesting that brassicas have
lost the RPL function in the fruit. Replum tissue was, however, produced in Brassica rapa with
a strong ind mutant allele (52). Lack of RPL
activity in Brassica fruits was demonstrated to
result from reduced RPL gene expression due
to a SNP in a cis-element located ∼3 kb upstream from the RPL-encoding region (5). In
rice, the same SNP in the same cis-element in
an RPL homolog is responsible for preventing
seed shattering in domesticated rice (76), revealing a remarkable example in which the same
nucleotide position in a regulatory element explains developmental variation in seed dispersal
structures in widely diverged species (5).
In recent years more elements of the core
genetic network of Arabidopsis fruit patterning
have been identified, including genes involved
in leaf development, such as ASYMMETRIC LEAVES1, ASYMMETRIC LEAVES2, and
BREVIPEDICELLUS (1). The network has also
expanded upstream to include a combination
of genes, including JAGGED, NUBBIN, FILAMENTOUS FLOWER, and YABBY3 (29, 30).
The floral homeotic gene APETALA2 (AP2)
has been demonstrated to repress replum development (122). A thorough description of all
these interactions is not the purpose of this review and can be obtained at least partly elsewhere (6, 110, 125). Therefore, here we concentrate on the core network and its interaction
with hormonal activities.
The core and extended genetic network of
Arabidopsis fruit development consists entirely
of interactions among transcription factors.
The three genes encoding polygalacturonases
(PGs) required for dehiscence downstream of
IND are functionally redundant (109). This
makes sense, as PGs have cell wall–degrading
activities and secretion of PGs from dehiscence
zone cells has been demonstrated (114).
Hormonal distribution and biosynthesis are
emerging as immediate downstream outputs
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from the core genetic network. In Brassica napus, direct measurements of auxin levels in valve
margin tissue revealed an abrupt decrease in the
auxin content of these cells immediately prior to
fruit opening. This drop correlated exactly with
an increase in the activity of cell wall–degrading
enzymes (14), raising the possibility that auxin
depletion from the valve margin tissue is a requirement for dehiscence. Work in Arabidopsis
confirmed this hypothesis, demonstrating that
IND ensures formation of an auxin minimum in
the valve margins at maturity by regulating the
direction of auxin transport (139); a subsequent
study showed that IND most likely interacts
with SPT to mediate this process (51).
As described earlier, GA promotes fruit
growth in Arabidopsis following fertilization.
This is in line with the general perception of GA
as a growth-promoting hormone, which functions by promoting degradation of the growthrepressing DELLA proteins (58). GA has now
also been identified as having a role in tissue
specification during Arabidopsis fruit development. The GA4 gene is a direct target of IND,
and the ga4 mutant has a defect in specifying
the separation layer of the valve margin similar
to that seen in alc mutants (4). GA4 encodes a
GA3 oxidase, which mediates the last step in the
biosynthesis of active GAs (17, 145). Genetic
analysis demonstrated that GA production at
the valve margin is required to degrade DELLA
proteins. In the absence of GA, DELLA proteins would otherwise interact with ALC proteins to inhibit ALC from regulating its target
genes (4).
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Hormonal and Genetic Regulation
of Maturation and Ripening
in Fleshy Fruits
In tomato and grape, levels of free IAA, the
most abundant auxin, decline prior to the onset of ripening, and at the same time levels of
the “inactive” IAA–amino acid conjugate IAAAsp increase substantially. Similar profiles of
free IAA and IAA conjugates have also been
reported in pepper, banana, muskmelon, and
strawberry (9). The IAA-Asp is generated from
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IAA by IAA–amido synthetase, and this enzyme
is encoded by the GH3 gene. Two GH3 genes
associated with the onset of ripening in tomato
are upregulated (77), and tomato fruits overexpressing the pepper GH3 gene ripen early
(88). These observations are consistent with
a role for endogenous IAA in controlling the
onset of ripening and modulation of its levels
by amino acid conjugation (9). GH3 expression
may be partially under the control of abscisic
acid (ABA), another plant hormone that promotes ripening (9).
There is evidence that ABA acts as a
promoter of ripening in tomato. Suppression of the SlNCED1 gene (encoding 9-cisepoxycarotenoid dioxygenase), which catalyzes
a key step in ABA biosynthesis, results in downregulation in the transcription of several major
ripening-related cell wall enzymes, including
PG and pectin methylesterase; enhanced fruit
shelf life; and slower softening (143). Retardation of ripening is also apparent in strawberry
fruits with reduced levels of NCED (71). ABA is
also 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 elements potentially involved in ABA signaling in
the GH3 promoter (9).
The role of ethylene in fruit ripening has
been reviewed many times (most recently in
References 74 and 56) and is therefore covered
only briefly here. Fleshy fruits have historically
been divided into two classes: climacteric
(e.g., tomato, apples, and banana) and nonclimacteric (e.g., grape, strawberry, and citrus).
Climacteric fruits show a burst of respiration at
the onset of ripening along with a large rise in
ethylene production. Ripening in climacteric
fruits can also be initiated by exposure to
exogenous ethylene. In nonclimacteric fruits,
the respiratory increase is absent and ethylene
does not appear to be critical for the ripening
process. Direct evidence that ethylene is critical
for the induction of ripening in climacteric fruit
came from work with tomato, where antisense
genes were used to suppress the expression of
ACO1 and ACS2, which encode ACC oxidase
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(ACO) and ACC synthase (ACS), respectively,
the major enzymes involved in ethylene
biosynthesis (56). Autocatalytic ethylene
biosynthesis (system-2 ethylene biosynthesis;
see 74) is operational during ripening; this
involves new forms of ACO and ACS that
produce much higher levels of ethylene and
are not subject to autoinhibition. Ethylene is
then perceived by a family of copper-binding
membrane-associated receptors, several of
which—tomato ETHYLENE RESPONSE4
(LeETR4), LeETR6, and NR [which results
in the phenotype of the Never-ripe (Nr)
tomato mutant]—show significantly increased
expression at the onset of ripening (74). The
receptors interact with a Raf kinase–like protein, constitutive triple response1 (CTR1), and
repress ethylene responses. When the receptors bind ethylene, this inhibition is relieved
and a signaling process leads to the ethylene
response (56, 74). This involves activation of
the ETHYLENE INSENSITIVE3 (EIN3)
and EIN3-like (EIL) transcription factors by
EIN2. In the nonclimacteric pepper fruit,
EIL-like genes are induced during ripening
(81), suggesting common systems for downstream signal transduction in climacteric and
nonclimacteric fruits, which in the latter occurs
in the absence of ethylene biosynthesis. In
climacteric fruit, at least, ethylene production
enhances the expression of some regulatory
and structural genes.
Ethylene does not act to regulate ripening
in isolation, but rather acts in concert with
other plant hormones. Lin et al. (85) identified a tetratricopeptide (TPR) repeat protein,
SlTPR1, from tomato that interacts with the
ethylene receptors LeETR1 and NR. Overexpression of SlTPR1 in tomato enhances ethylene responses while causing reduced expression of the early auxin-responsive gene IAA9.
Transcriptional regulators of ripening in
tomato. A major breakthrough in dissecting
the transcriptional control of tomato ripening
was the identification of genes underlying rare
mutations that completely abolish the normal
ripening process, including ripening inhibitor
(rin), nonripening (nor), and Colorless nonripening
(Cnr). These mutant loci all harbor transcription factors. RIN is encoded by a member of
the SEPALLATA4 (SEP4) clade of MADS-box
genes (159), NOR is a member of the NACdomain transcription factor family (50), and
CNR is encoded by an SBP-box gene, targets of
which are likely to include the promoters of the
SQUAMOSA clade of MADS-box genes (95).
The MADS-RIN gene is necessary for ripening in tomato (159) and the rin mutation impacts virtually all ripening pathways, which
supports its role as a master regulator of the
ripening process (96). Chromatin immunoprecipitation experiments indicate that MADSRIN directly controls the expression of a wide
range of other ripening-related genes, targeting the promoters of genes involved in (a) the
biosynthesis and perception of ethylene, such
as LeACS2, LeACS4, NR, and E8; (b) cell wall
metabolism, such as polygalacturonase (PG),
galactanase (TBG4), and expansins (LeEXP1);
(c) carotenoid formation, such as phytoene synthase (PSY1); (d ) aroma biosynthesis, such as
lipoxygenase (Tomlox C), alcohol dehydrogenase (ADH2), and hydroperoxidelyase (HPL);
and (e) the generation of ATP, such as phosphoglycerate kinase (PGK) and the promoter
of MADS-RIN itself (47, 96, 117). MADS-RIN
is also involved in suppressing the expression
of most ARF genes (78) and therefore auxinrelated gene expression.
In tomato, MADS-RIN is involved in
switching on system-2 ethylene through the induction of LeACS2, which encodes ACS (96).
The conversion of ACC to ethylene, however,
requires ACO1. The ACO1 gene does not appear to be under the direct control of MADSRIN, but its expression is governed by LeHB1,
a gene encoding a tomato homeobox protein.
LeHB1 stimulates ethylene synthesis by activating the transcription of ACO1. Inhibition
of LeHB1 using virus-induced gene silencing
(VIGS) inhibits ripening and greatly reduces
ACO1 levels. The LeHB1 gene is expressed at
higher levels in developing fruits, and the levels
of expression decrease at the onset of ripening
(86).
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MADS-RIN binding to promoter targets
occurs throughout ripening (96). The action
of MADS-RIN to induce the transcription of
ripening-related genes is also dependent on the
presence of the CNR gene product or a CNRregulated gene product (96). The promoters of
the NOR, CNR, HB1, and TDR4 genes are also
targets for MADS-RIN, and MADS-RIN can
form heterodimers with other MADS-box transcription factors such as TAGL1 and TAG1 of
the AGAMOUS (AG) clade and TDR4 of the
SQUAMOSA clade (158). This indicates that
MADS-RIN exerts its control over ripening in
cooperation with a range of other regulatory
factors. TAGL1 is upregulated during tomato
ripening, and its suppression inhibits normal
ripening. This occurs partly through inhibition of ethylene biosynthesis, and in TAGL1silenced lines it appears to occur predominantly
through direct ACS2 suppression. Indeed, transient promoter-binding studies indicate direct
interactions with ACS2. TAGL1 needs RIN for
lycopene accumulation, with LYC-B and CYCB upregulated in TAGL1 RNAi lines. Additionally, TAGL1 appears to regulate some cell wall
activities in a RIN-independent manner. It also
appears to be linked to the phenyl propanoid
pathway and activates the flavonoid pathway.
TAGL1 RNAi fruit also have thin pericarps, and
upregulation produces fleshy ripening sepals.
This implicates TAGL1 in not only ripening
but also the development of fleshiness in tomato
(68, 158).
RNAi suppression of AP2—which belongs
to the AP2/ETHYLENE RESPONSE FACTOR (ERF) family of transcription factors (18,
72) and acts downstream of RIN, NOR, and
CNR—results in rapid softening and earlier
ripening. Evidence indicates that AP2 is a negative regulator of ripening in tomato (18) that
operates in a negative-feedback loop with CNR,
as illustrated by the observation that in the
pericarps of AP2 RNAi fruits, mRNA levels of
CNR were elevated. In addition, it has been
demonstrated that CNR can bind to the promoter of AP2 in vitro (72). Interestingly, AP2
RNAi fruits show enhanced GH3 gene expression (72), likely linking AP2 to auxin-related
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gene expression. A study of the expression of
ARF genes during fruit development in the
rin mutant and wild-type fruits indicated that
MADS-RIN normally suppresses the expression of most ARFs (78). These data point to
a control system involving the removal of auxin
by conjugation and then repression of ARFs by
the presence of MADS-RIN.
Unraveling the transcriptome network controlling fruit ripening in tomato has revealed
some striking parallels with the regulatory circuits in dry fruit (Figure 4). Similar MADS-box
transcription factors play a central role in both
fruit types, and in some cases they seem to be directly orthologous (e.g., SHP1/2 and TAGL1).
There are also some major differences between
the molecular events. In dry fruits, lignification
follows cell division, whereas in fleshy fruits,
cell expansion is observed. Also, in Arabidopsis there does not appear to be a fruit-related
MADS-RIN ortholog.
Control of color and texture changes. A
systems biology approach to the tomato transcriptome and metabolome during ripening has
led to the identification of a putative carotenoid
modulator, SlERF6 (80). Reduced expression
of SlERF6 by RNAi enhanced both carotenoid
and ethylene levels during ripening. The
majority of genes substantially influenced by
SlERF6 repression were upregulated, indicating that the primary function of SlERF6 occurs
via negative regulation. SlERF6 was responsive
to ethylene and may be a component of a
feedback restriction in ethylene production
during ripening, similar to SlAP2 (80). A
small number of fruit high-pigment mutants
have been described in tomato, including high
pigment1 (hp1) [a lesion in UV-DAMAGED
DNA BINDING PROTEIN1 (DDB1) (89)] and
hp2 [a mutation in tomato DE-ETIOLATED1
(DET1)] (107). These genes are involved in the
suppression of light responses in the absence
of light, and for DET1, suppression occurs by
a molecular mechanism involving chromatin
remodeling (24). Coordinated upregulation of
core metabolic processes is responsible for the
high-pigment phenotype in the DET1 lines
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a
AP2
TAGL1
(SHP)
TDR4
(FUL)
NOR
CNR
RIN
(SEP4)
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LOXC
EXP
PG
HB1
ACO
PSY1
ACS
Activation
Ethylene
Repression
b
AP2
SHP
RPL
IND
ening. Modulation of genes encoding two
ripening-specific N-glycoprotein-modifying
enzymes—α-mannosidase
and
β-D-Nacetylhexosaminidase—reduces the rate of
softening and enhances fruit shelf life (102).
More than 50 cell wall structure–related genes
show expression changes in ripening tomato
fruits (151), and texture involves complex
quantitative trait loci (13). Shelf life is also
related to water loss from the mature fruits.
Cuticle properties are critical for maintaining fruit integrity postharvest. Delayed Fruit
Deterioration (DFD) mutant tomato fruits
show remarkably prolonged resistance to
postharvest desiccation and remain firm for
many months after harvest (127), and analyses
of cutin-deficient tomato mutants indicate the
importance of waxes (67; see also 64).
FUL
PG
20 µm
Figure 4
Ripening network in fleshy fruits and comparison
with events in the dehiscence of dry fruits. (a) Major
known regulators of ripening in tomato. The blue
circles are transcription factors; the yellow labels are
genes where orthologs are also found in dry
dehiscent fruits. Downstream effectors are shown in
white boxes. Precisely how the gene products of
NOR, CNR, and RIN interact is unknown, so dashed
green lines are shown between those. (b) Brassica pod
and dehiscence zone, illustrating a dry-fruit network
using information obtained in Arabidopsis. Image of
tomato fruit with ripening inhibited by silver
thiosulfate on the left side kindly provided by Don
Grierson and Kevin Davies.
(38). Upregulation of a Golden 2–like transcription factor in tomato has also been shown to
elevate levels of chlorophyll and carotenoids,
and a lesion in this gene is responsible for the
uniform-ripening phenotype (116).
Shelf life is important in tomato and
other fruits. This trait is influenced by many
processes, including the rate of fruit soft-
Tomato as a model for understanding
ripening in other fleshy-fruited species.
In banana—which, like tomato, is a climacteric fruit—SEP3-class MADS-box genes show
ripening-related expression (35) and are probably necessary for normal ripening. In strawberry, a nonclimacteric fruit, a SEP1/2-class
gene is needed for normal development and
ripening (133). VmTDR4, the bilberry ortholog
of the TDR4 gene in tomato, is involved in the
regulation of anthocyanin biosynthesis in the
fruit flesh (69), and in apple, MADS2 expression
is associated with fruit firmness (12). MADSbox and NAC transcription factors are associated with the ripening process in the drupe of
the oil palm (152).
Epigenetics. The lesion responsible for the
Cnr mutation is due to an epigenetic change
leading to hypermethylation of the CNR promoter and inhibition of gene expression and
ripening in the mutant (95). Additionally, in
normal fruit development, at least in the tomato
cultivar Liberto, the promoter of CNR appears
to be demethylated in a specific region just prior
to the onset of ripening.
A further level of regulation controlling fruit
ripening occurs through the presence of small
RNAs (sRNAs). These include microRNAs
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Epigenetics: the
study of heritable
variation involving
mechanisms other
than changes in the
DNA sequence of an
organism
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(miRNAs) and other sRNAs of unknown function. The CNR 3 untranslated-region sequence
contains a miRNA binding site that is complementary to miR156 /157 (23). Deep sequencing
of the sRNAome of developing tomato fruits,
covering the period between closed flowers and
ripened fruits through the profiling of sRNAs
at 10 time points, has revealed that thousands of
non-miRNA sRNAs are differentially expressed
during fruit development and ripening (106).
Some of these sRNAs are derived from transposons, but many map to regions in proteincoding genes, including well-defined areas of
the noncoding regulatory regions (151). Specific classes of sRNAs seem more abundant at
certain stages of development, e.g., 24-mers
during ripening. The function of these changes
in sRNA patterns is not known, but they may
play an important role in the ripening process.
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FRUITS AND THE HUMAN DIET
The human genome evolved in the context
of the diet prevailing before the introduction
of agriculture and animal husbandry approximately 10,000 years ago, when humans were
hunter-gatherers; diets were rich in fruits, vegetables, and protein and low in fats and starches
(33). For primates such as chimpanzees and
orangutans, more than 75% of their diet by
weight is fresh fruit, and the assumption is that
our primate ancestors had similar diets. Fruit
is also common in the diet of modern huntergatherers.
The 10,000 years (∼360 generations) since
the first cultivation of cereals has not been
enough time for humans to adapt to starchier,
cereal-based diets with much higher amounts
of fat and lower amounts of fresh fruit and vegetables, and it has been suggested that many
chronic diseases result from our evolutionary
discordance with modern diets (21). Levels
of phytonutrients—compounds in plant-based
foods that play potentially beneficial roles in
the prevention and treatment of disease—in the
diet have dropped significantly owing to a reduced variety of plants consumed (currently,
just 17 plant species constitute 90% of the
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Seymour et al.
global human diet) and to selective breeding
(161). For these reasons, most modern dietary
recommendations include increased consumption of fresh or whole fruits and vegetables. The
role of plants in human health is the subject of
another review (98), but what is beneficial about
fruit consumption?
Fruits such as eggplant, mango, and okra are
good sources of soluble fiber, which has been
shown experimentally to lower the glycemic
index of foods and to have beneficial effects
on type 2 diabetes, cardiovascular disease, and
obesity (66, 73, 79, 103). Fruits are also rich
in fructose (which constitutes 20–40% of the
available carbohydrates in wild fruit) and intrinsic sugars; these are not subject to restrictions in dietary recommendations because their
concentrations are not high enough to have adverse health outcomes (94). Fruits generally also
contain high levels of phytonutrients, and include carotenoids, polyphenols (flavonoids, stilbenes), plant sterols, vitamins, and polyunsaturated fatty acids.
Some fruits are rich in carotenoids, which
are thought to attract animals as dispersers
through their bright colors (for example,
lycopene in tomato; capsanthin, β-carotene,
lutein, and violaxanthin in red pepper; lycopene and β-carotene in red grapefruit;
and β-carotene, α-carotene, and lutein in
mangoes). Lycopene is a methyl-branched
carotenoid that has no provitamin A activity. It
is a potent lipophilic antioxidant, with greater
antioxidant activity than other carotenoids,
and has been shown to be protective against
cardiovascular disease and prostate cancer (43).
Intervention and epidemiological studies have
linked β-carotene consumption to enhanced
protection against cardiovascular disease,
including cerebral infarction, and resistance
to low-density lipoprotein oxidation, ischemic
stroke, and carotid atherosclerosis (7, 43,
121).
Fruits are rich sources of polyphenols that
have gained significant recognition recently as
being important phytonutrients, reducing the
risk of chronic diseases such as cardiovascular disease, metabolic syndrome, cancer, and
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obesity. Anthocyanins represent a subset of
flavonoids with particularly high antioxidant capacity and strong health-promoting effects. As
part of the human diet, they offer protection
against cancer, inhibiting both the initiation
and progression stages of tumor development
(154), reducing inflammatory inducers of tumor
initiation, suppressing angiogenesis, and minimizing cancer-induced DNA damage in animal disease models. Anthocyanins also protect
against cardiovascular disease and age-related
degenerative diseases associated with metabolic
syndrome (63, 119), have anti-inflammatory activity (134), promote visual acuity (101), and
hinder obesity and diabetes (154). Inverse correlations between consumption of flavonol-rich
diets and the occurrence of cardiovascular disease, certain cancers, and age-related degenerative diseases (62, 75, 105, 130, 138) have been
shown in human epidemiological studies as well
as by data from cell-based assays and feeding
trials with animals.
Another important group of plant-based
bioactive polyphenols is the hydroxycinnamic
acid esters, of which chlorogenic acid is the
major soluble phenolic in solanaceous species
such as potato, tomato, and eggplant as well as
in coffee. Chlorogenic acid is one of the most
abundant polyphenols in the human diet and is
the major antioxidant in the average developedworld diet. It has significant antioxidant activity, and consumption can limit glucose absorption and possibly weight gain (146).
Epicatechins are the major polyphenolic
compounds in green tea, and the most significant active component is thought to be
epigallocatechin gallate. Cell, animal, and human studies have shown that green tea extract/epicatechins prevent cancer development,
particularly prostate cancer (22, 31). Similar effects may be gained by consumption of fleshy
fruits such as cranberry, blueberry, and grape or
by consumption of berry-juice products; these
have relatively high levels of catechins and epicatechins, which also protect against cardiovascular disease (27).
Dietary intervention studies support the
view that consumption of fruit (especially when
replacing calorie-dense food) helps maintain a
healthy weight and reduce the risk of a wide
range of cancers (150, 163) and cardiovascular disease (59, 60, 82). Consequently, dietary
improvement by increasing fruit consumption
or by improving fruit to contain higher levels of fiber or phytonutrients should have a
positive impact on the incidence and progression of chronic disease. Such improvement of
fruit crops could be carried out through genetic
modification (11) or marker-assisted selection
using existing variation.
High-throughput
sequencing
technologies:
methods that involve
producing millions of
sequences from DNA
samples in a parallel
process
CROP IMPROVEMENT
High-throughput sequencing technologies
have provided a powerful new set of tools
to reveal genetic and epigenetic variation
on a genome-wide scale and therefore new
insights into the evolution of genomes and trait
variation. Fruit crop genomes that have been
sequenced include grapevine (Vitis vinifera)
(70), apple (Malus × domestica) (157), diploid
strawberry (Fragaria vesca) (135), tomato
(Solanum lycopersicum) (151), and banana (Musa
acuminata) (28). These resources will underpin
advances in the breeding of fruit crops by (a)
greatly facilitating marker-assisted selection
and allowing efficient cloning of genes underpinning quantitative trait loci, (b) providing
the reference genomes for rapid allele mining
in crop wild relatives (87), (c) providing a
guide for direct sequencing of monogenic
mutants, and (d ) maximizing opportunities
to optimize reverse-genetics tools such as
targeting-induced local lesions in genomes
(TILLING) for gene functional studies (142).
Genome-wide information also allows rapid
analyses of gene structure, binding-site motifs,
and gene regulatory regions.
In the future, high-throughput sequencing
technologies will allow routine screening
of crop epigenomes and therefore permit
detection of epigenetic variation that impacts
phenotypes. Additionally, translational biology
from models to crop species has clear utility
in 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 potentially
useful partial dehiscence phenotype (52).
Harnessing variation in crop wild relatives in
combination with direct genetic modification
provides a powerful route for a massive step
change in crop improvement.
SUMMARY POINTS
1. True fruits are found only in the angiosperms, or flowering plants. They are often defined
as structures derived from a mature ovary containing seeds, but many structures we call
fruit 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.
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2. Recent work on the model plant Arabidopsis and on tomato nonripening mutants has
uncovered the complex high-level regulatory network controlling fruit maturation and
ripening. Striking parallels have been revealed between the molecular circuits in dry
fruits and those in fleshy fruits. In both types, similar MADS-box transcription factors
play 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 controlling ripening in other fleshy fruits. Classes of transcription factors controlling tomato
ripening 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 introduction
of agriculture and animal husbandry approximately 10,000 years ago, when humans were
hunter-gatherers; diets were rich in fruits, vegetables, and protein and low in fats and
starches. Fruits provide vitamins, minerals, and phytochemicals that are essential for
human health.
5. The genomes of a variety of fleshy-fruited species have been sequenced and provide
guides for revealing previously hidden genetic and epigenetic variation that will open a
new frontier for crop improvement.
FUTURE ISSUES
1. Can predictive models of the ripening regulatory network be generated for tomato and
other fleshy- and dry-fruited species? And can major ripening processes—e.g., texture
and 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-fruit
phenotype 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 traits
in crops and crop wild relatives?
DISCLOSURE STATEMENT
C.M. is a director of Norfolk Plant Sciences, an SME for the development of phytonutrientenriched fruits and vegetables.
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ACKNOWLEDGMENTS
We wish to acknowledge the support of the UK Biotechnology and Biological Sciences Research
Council to G.B.S. (BB/G02491X) and the US National Science Foundation Planetary Biodiversity
Initiative to S.K. (DEB-0316614).
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by Universidad Veracruzana on 01/08/14. For personal use only.
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www.annualreviews.org • Fruit Development and Ripening
151. Introduces the
genome sequence for
tomato, an essential
reference for fleshy
fruits.
152. Describes the gene
regulating ripening in
oil palm,
suggesting—along with
other evidence—wide
conservation of
regulatory gene
function in fleshy fruits.
159. Describes the
cloning of the RIN gene,
a master regulator of
ripening in fleshy fruits.
241
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Contents
Annual Review of
Plant Biology
Volume 64, 2013
Annu. Rev. Plant Biol. 2013.64:219-241. Downloaded from www.annualreviews.org
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Benefits of an Inclusive US Education System
Elisabeth Gantt p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Plants, Diet, and Health
Cathie Martin, Yang Zhang, Chiara Tonelli, and Katia Petroni p p p p p p p p p p p p p p p p p p p p p p p p p19
A Bountiful Harvest: Genomic Insights into Crop Domestication
Phenotypes
Kenneth M. Olsen and Jonathan F. Wendel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p47
Progress Toward Understanding Heterosis in Crop Plants
Patrick S. Schnable and Nathan M. Springer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p71
Tapping the Promise of Genomics in Species with Complex,
Nonmodel Genomes
Candice N. Hirsch and C. Robin Buell p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p89
Understanding Reproductive Isolation Based on the Rice Model
Yidan Ouyang and Qifa Zhang p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 111
Classification and Comparison of Small RNAs from Plants
Michael J. Axtell p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 137
Plant Protein Interactomes
Pascal Braun, Sébastien Aubourg, Jelle Van Leene, Geert De Jaeger,
and Claire Lurin p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 161
Seed-Development Programs: A Systems Biology–Based Comparison
Between Dicots and Monocots
Nese Sreenivasulu and Ulrich Wobus p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 189
Fruit Development and Ripening
Graham B. Seymour, Lars Østergaard, Natalie H. Chapman, Sandra Knapp,
and Cathie Martin p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 219
Growth Mechanisms in Tip-Growing Plant Cells
Caleb M. Rounds and Magdalena Bezanilla p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 243
Future Scenarios for Plant Phenotyping
Fabio Fiorani and Ulrich Schurr p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 267
v
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Microgenomics: Genome-Scale, Cell-Specific Monitoring of Multiple
Gene Regulation Tiers
J. Bailey-Serres p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 293
Plant Genome Engineering with Sequence-Specific Nucleases
Daniel F. Voytas p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 327
Smaller, Faster, Brighter: Advances in Optical Imaging
of Living Plant Cells
Sidney L. Shaw and David W. Ehrhardt p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 351
Phytochrome Cytoplasmic Signaling
Jon Hughes p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 377
Annu. Rev. Plant Biol. 2013.64:219-241. Downloaded from www.annualreviews.org
by Universidad Veracruzana on 01/08/14. For personal use only.
Photoreceptor Signaling Networks in Plant Responses to Shade
Jorge J. Casal p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 403
ROS-Mediated Lipid Peroxidation and RES-Activated Signaling
Edward E. Farmer and Martin J. Mueller p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 429
Potassium Transport and Signaling in Higher Plants
Yi Wang and Wei-Hua Wu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 451
Endoplasmic Reticulum Stress Responses in Plants
Stephen H. Howell p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 477
Membrane Microdomains, Rafts, and Detergent-Resistant Membranes
in Plants and Fungi
Jan Malinsky, Miroslava Opekarová, Guido Grossmann, and Widmar Tanner p p p p p p p 501
The Endodermis
Niko Geldner p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 531
Intracellular Signaling from Plastid to Nucleus
Wei Chi, Xuwu Sun, and Lixin Zhang p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 559
The Number, Speed, and Impact of Plastid Endosymbioses in
Eukaryotic Evolution
Patrick J. Keeling p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 583
Photosystem II Assembly: From Cyanobacteria to Plants
Jörg Nickelsen and Birgit Rengstl p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 609
Unraveling the Heater: New Insights into the Structure of the
Alternative Oxidase
Anthony L. Moore, Tomoo Shiba, Luke Young, Shigeharu Harada, Kiyoshi Kita,
and Kikukatsu Ito p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 637
Network Analysis of the MVA and MEP Pathways for Isoprenoid
Synthesis
Eva Vranová, Diana Coman, and Wilhelm Gruissem p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 665
vi
Contents
PP64-frontmatter
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Toward Cool C4 Crops
Stephen P. Long and Ashley K. Spence p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 701
The Spatial Organization of Metabolism Within the Plant Cell
Lee J. Sweetlove and Alisdair R. Fernie p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 723
Evolving Views of Pectin Biosynthesis
Melani A. Atmodjo, Zhangying Hao, and Debra Mohnen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 747
Annu. Rev. Plant Biol. 2013.64:219-241. Downloaded from www.annualreviews.org
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Transport and Metabolism in Legume-Rhizobia Symbioses
Michael Udvardi and Philip S. Poole p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 781
Structure and Functions of the Bacterial Microbiota of Plants
Davide Bulgarelli, Klaus Schlaeppi, Stijn Spaepen, Emiel Ver Loren van Themaat,
and Paul Schulze-Lefert p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 807
Systemic Acquired Resistance: Turning Local Infection
into Global Defense
Zheng Qing Fu and Xinnian Dong p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 839
Indexes
Cumulative Index of Contributing Authors, Volumes 55–64 p p p p p p p p p p p p p p p p p p p p p p p p p p p 865
Cumulative Index of Article Titles, Volumes 55–64 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 871
Errata
An online log of corrections to Annual Review of Plant Biology articles may be found at
http://www.annualreviews.org/errata/arplant
Contents
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