Journal of Experimental Botany Advance Access published January 7, 2015

Journal of Experimental Botany

doi:10.1093/jxb/eru527

Review Paper

Fruit growth-related genes in tomato

Lamia Azzi1,*, Cynthia Deluche1,*, Frédéric Gévaudant1, Nathalie Frangne1, Frédéric Delmas1, Michel Hernould1
and Christian Chevalier2,†
1 
University of Bordeaux, UMR1332 Biologie du Fruit et Pathologie, INRA Bordeaux Aquitaine, CS20032, F-33882 Villenave d’Ornon
cedex, France
2 
INRA, UMR1332 Biologie du Fruit et Pathologie, INRA Bordeaux Aquitaine, CS20032, F-33882, Villenave d’Ornon cedex, France

*  These authors contributed equally to this work.

† 
To whom correspondence should be addressed. E-mail: [email protected]

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Received 1 October 2014; Revised 5 December 2014; Accepted 10 December 2014

Abstract
Tomato (Solanum lycopersicum Mill.) represents a model species for all fleshy fruits due to its biological cycle and the
availability of numerous genetic and molecular resources. Its importance in human nutrition has made it one of the
most valuable worldwide commodities. Tomato fruit size results from the combination of cell number and cell size,
which are determined by both cell division and expansion. As fruit growth is mainly driven by cell expansion, cells
from the (fleshy) pericarp tissue become highly polyploid according to the endoreduplication process, reaching a DNA
content rarely encountered in other plant species (between 2C and 512C). Both cell division and cell expansion are
under the control of complex interactions between hormone signalling and carbon partitioning, which establish cru-
cial determinants of the quality of ripe fruit, such as the final size, weight, and shape, and organoleptic and nutritional
traits. This review describes the genes known to contribute to fruit growth in tomato.

Key words:  Cell cycle, cell division, cell expansion, development, endoreduplication, fruit, genetic control, growth, metabolic
control, hormones, tomato.

Introduction
The fruit is a plant organ specific to angiosperms that protects In general, the term fruit refers to the fleshy, edible portion
the ovule and seed during embryo development and ensures that is the major component of fruits, such as grape, banana,
seed dispersal after maturation. At the botanical level, most apple, citrus, peach, strawberry, melon, and tomato. All of
fruits develop from mature ovaries and, therefore, include these species are produced worldwide, and continue to rely
carpellar tissues. The physiological function of seed disper- on breeding schemes for agronomic traits. Particular traits of
sal accounts for a significant part of the adaptive success of interest are enhanced yield and quality, increased time of fruit
angiosperms on Earth. Indeed, a wide diversity of fruit size, storage and longer shelf-life, optimized cultural practices, and
form, and composition, as well as a variety of fruit dispersion pest and pathogen resistance. The common feature of fleshy
mechanisms, have emerged as the result of strong environ- fruits is the fine balance between sugars and organic acids,
mental selective pressures. For example, the Solanaceae fam- and the accumulation of water, minerals, pigments, aromatic
ily, which encompasses nearly 10 000 species, has very diverse compounds, and vitamins that confer upon the fruit its juici-
types of fruits, with capsules, drupes, pyrenes, berries, and ness and attractiveness. Consequently, fleshy fruits represent
several types of dehiscent non-capsular fruits occurring in a major source of vitamins, fibre, carbohydrates, and phyto-
>90 genera (Knapp, 2002). nutrient compounds essential for human nutrition.

© The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.
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Page 2 of 12 | Azzi et al.

Tomato (Solanum lycopersicum Mill.) fruit, a multicarpel- ~17–20 rounds of cell divisions that occur during a pre-anthe-
lar berry, has arisen as the model species for fleshy fruits, due sis period located within the L3 layer of the floral meristem,
to certain advantages for use in both agronomical and funda- but which involve virtually no cell expansion (Coombe, 1976;
mental research (Gillaspy et  al., 1993; Tanksley, 2004; Klee Ho, 1992). Obviously, the number of cells formed in the ovary
and Giovannoni, 2011). These advantages include a short before anthesis is critical for the final size of fruit, and such
life cycle, high multiplication rate, self-pollination, and ease a positive correlation is frequently observed (Tanksley, 2004).
of mechanical crossing. This highly favourable biology has From flower initiation to the double fertilization occurring in
been widely exploited to generate segregating populations ovules (Gillaspy et al., 1993; Brukhin et al., 2003), the mor-
such as recombinant inbred lines (RILs) or near isogenic lines phogenesis and growth of carpels and ovules require the spa-
(NILs). Tomato has proven amenable for marker-assisted tial and temporal synthesis and action of auxin, cytokinin,
mapping using crosses between small and round, wild toma- and gibberellins (GAs). In order to keep the ovary in a tem-
toes and domesticated varieties of various sizes and shapes porally protected and dormant state, abscisic acid (ABA) and
that has enriched our knowledge of the genetic control of ethylene work to stop growth within the ovary shortly before
fruit development (Grandillo et  al., 1999; Causse et  al., anthesis when the ovary has reached its mature size (Vriezen
2007; Muños et  al., 2011; Rodriguez et  al., 2011). A  large et al., 2008). Growth resumes only after successful pollination
spectrum of mutants is now available (Menda et  al., 2004; and fertilization of ovules triggers fruit set—the first phase of
Watanabe et al., 2007; Just et al., 2013) for screening and gene fruit development—through the action of ovary-synthesized

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identification by reverse genetic tools, such as the powerful auxins and GAs (Ruan et al., 2012, and references therein).
technology of Tilling (Targeting Induced Local Lesions In Fruit growth is the longest phase of fruit development,
Genomes; Okabe et  al., 2011). Functional analyses of can- as it ranges from 5 to 8 weeks depending on the genotype.
didate genes are routinely conducted, since tomato is highly Growth proceeds first by a period of intense mitotic activity
suitable to stable transformation via Agrobacterium tumefa- according to a spatially and temporally organized pattern of
ciens, and susceptible to transient gene expression via agroin- cell division. Active cell division within the pericarp is usu-
jection (Orzaez et al., 2006). Additionally, the repression of ally restricted to an initial period of 1–2 weeks after fruit set
target genes can be obtained by virus-induced gene silencing (Fig. 1). Remarkably, cell division occurs within discrete cell
(VIGS) (Orzaez et  al., 2009) or by a genome-editing strat- layers with well-defined planes of division fulfilling specific
egy using the RNA-guided DNA endonuclease system called purposes. For instance, the two subepidermal layers of the
the clustered regularly interspaced short palindromic repeats pericarp undergo several rounds of periclinal divisions, thus
(CRISPR)/CRISPR-associated9 (Cas9) system (Brooks leading to an increase in the number of pericarp cell layers,
et  al., 2014). Finally, the release in 2012 of the full tomato whereas the two epidermal cell layers undergo anticlinal divi-
genome sequence represented an extraordinary breakthrough sions in response to the resulting increase in fruit volume
for developmental studies in fleshy fruits (Tomato Genome (Cheniclet et al., 2005). These various types of cell divisions
Consortium, 2012). are differently regulated, because cell divisions promoting
The development of plant organs requires mechanisms of cell layer formation occur only within 5–8  days post-anthe-
differentiation by which tissue identity is imposed on cells as sis (dpa), whereas randomly oriented cell divisions occur for
well as mechanisms regulating growth that dictate final organ longer periods up to 10–18 dpa (Cheniclet et al., 2005). Cell
size. The determination of organ size thus relies on the fine divisions in growing fruit account for as much as 80–97% of
regulation of the number and size of cells that is determined newly formed cells present after anthesis. How this spatio-
by the cell division and cell expansion processes, respectively. temporal pattern of development is related to gene expres-
These processes respond to spatial and temporal controls that sion, metabolic profiles, and cellular characteristics remains
come under the influence of internal (genotypic) and external poorly understood (Lemaire-Chamley et al., 2005; Bourdon
(environmental) cues. As a general feature of angiosperms, et  al., 2011, 2012), primarily due to the complex nature of
cell expansion is frequently ascribed to nuclear endopoly- fruit in relation to differing cell type.
ploidization in several plant organs, according to the pro- It has been reported that a second phase of growth related
cess of endoreduplication (Chevalier et  al., 2011, 2014; De to cell expansion occurs separately after the cell division
Veylder et al., 2011). phase (Gillaspy et  al., 1993). In fact, cell expansion starts
This review addresses the current knowledge on fruit devel- within very few days after fruit set, concomitantly with cell
opment in tomato, in particular describing those genes that division (Cheniclet et al., 2005), and lasts for the entire period
are involved in the developmental processes governing fruit of fruit growth (Fig.  1). At the end of the cell expansion
growth. phase, individual cells in the fleshy part (mesocarp tissue)
of the fruit have reached spectacular volumes, exhibiting a
>30 000-fold increase from initial cell volume, and can cor-
Tomato fruit development and the respond to a >0.5 mm increase in diameter (Cheniclet et al.,
contribution of endopolyploidization to 2005). This cell enlargement mostly occurs through dramatic
increases in the vacuolar compartment and cell vacuola-
fruit growth
tion index. Remarkably, this spectacular cell hypertrophy is
Fruits typically develop from pre-existing organs, such as closely correlated to an increase in nuclear DNA levels due to
carpels inside flowers. In tomato, carpels are formed by endopolyploidization.
 Tomato fruit growth  |  Page 3 of 12

Fruit Development

Cell expansion

Fruit set Cell division Ripening

Anthesis 3 5 8 12 15 20 25 35 40 dpa

35 dpa

8 dpa

0 dpa

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7-8
Cell layers
14
Cell layers 14
Cell layers

Fig. 1.  Fruit development in tomato. The fruit originates from the development of the ovary. Following fertilization (concomitant with anthesis) and fruit
set, fruit growth starts with a period of very active cell division inside the ovary that lasts for 8–10 days post-anthesis (dpa). After anthesis and in <8–10 d,
the number of cell layers across the pericarp has doubled compared with that at anthesis and becomes fixed until the end of development. Fruit growth
then proceeds into the cell expansion phase and continues until ripening (~35 dpa). Cell enlargement starts concomitantly with cell division as early as 1
or 2 dpa and contributes to the increase in fruit size.

Endopolyploidy is the occurrence of different ploidy levels 1996; Joubès et al., 1999; Cheniclet et al., 2005; Bertin et al.,
within an organism. In plants, it results mostly from endore- 2007). Ploidy levels as high as 512C (where C is the haploid
duplication that is estimated to occur in >90% of angiosperms DNA content) have been observed to occur in a large array
(Nagl, 1976; D’Amato, 1984). Endoreduplication occurs in of tomato genotypes. This extraordinary extent of endore-
the absence of any obvious DNA condensation and decon- duplication occurring in tomato fruit is unmatched by any
densation steps that lead to the production of chromosomes other plant species and makes tomato an excellent model
with 2n chromatids or without any change in chromosome to study the role of endoreduplication as a determinant of
number (Joubès and Chevalier, 2000; Edgar and Orr-Weaver, fruit size. Cheniclet et al. (2005) demonstrated that the mean
2001). As a consequence, hypertrophic nuclei arise from suc- ploidy level achieved in pericarp cells correlates not only with
cessive cycles of DNA replication without segregation of the large variation in the fruit weight that can be encoun-
sister chromatids, thereby resulting in the production of poly- tered in the various genotypes, but also with the mean cell
tene chromosomes (Bourdon et al., 2012). The physiological size inside the pericarp. The endoreduplication-associated
and developmental importance of endoreduplication is still a cell expansion in fruit is characterized by profound cellular
matter of debate. However, the frequent observation that cell modifications. It is evident that the formation of polytene
size and ploidy levels are highly and positively correlated in chromosomes impacts on nuclear, nucleolar, and chroma-
many different plant species, organs, and cell types (Chevalier tin organization within hypertrophied nuclei delimited by a
et al., 2011) suggests a role for endoreduplication in the con- highly invaginated nuclear envelope (Bourdon et  al., 2012).
trol of cell size, according to the ‘karyoplasmic ratio theory’. These profound nuclear grooves are filled with numerous
This theory, which was formulated as early as the beginning mitochondria, whose number increases according to nuclear
of the 20th century, states that there is a causal relationship DNA content. Apparently, endoreduplication triggers effi-
between nuclear and cytoplasmic growth to maintain a con- cient communication between the nucleus and the cytoplasm,
stant ratio of nucleus to cell volume (Sugimoto-Shirasu and despite the increase in nuclear volume. The cytoplasmic vol-
Roberts, 2003; Chevalier et al., 2014). ume of cells also correlates with ploidy levels, which indicates
In the course of tomato fruit development, endoreduplica- that the maintenance of the nuclear to cytoplasmic ratio to
tion produces high levels of nuclear DNA ploidy within the drive cell growth is consistent with the ‘karyoplasmic ratio’
mesocarp and the locular jelly-like tissue (Bergervoet et  al., theory. In addition, Bourdon et al. (2012) provided evidence
Page 4 of 12 | Azzi et al.

for the existence of a strong relationship between endoredu- complex activity as it confers its stability, its localization, and
plication and rRNA and mRNA transcription. its substrate specificity (Inzé and De Veylder, 2006). Specific
As a morphogenetic factor, endoreduplication thus con- CDK–CYC complexes operate at the boundaries between the
tributes to maintain homeostasis of cytoplasmic components various phases of the cell cycle in order to phosphorylate tar-
through the establishment of a highly structured cellular sys- get proteins. These post-translational modifications which can
tem, where multiple physiological functions are integrated to be either inhibitory or activating, are essential for the progres-
support cell growth during fruit development. sion through cell cycle boundaries (De Veylder et al., 2007). To
allow a subtle regulation of cell cycle progression, the kinase
activities of the CDK–CYC complexes are regulated in sev-
Modifying fruit growth with cell cycle and eral ways: (i) CDK activity is finely tuned by phosphorylation
and dephosphorylation of the CDK on conserved residues by
endocycle regulatory genes
specific kinases and phosphatases; (ii) the proteolytic destruc-
Cell division and cell expansion associated with endoredu- tion of the cyclin subunit by the ubiquitin–proteasome system
plication provide, respectively, the building blocks for the (UPS) is sufficient to abolish activity of the complex, as CDK
fruit organ and the growth-driving force that contribute to alone does not display kinase activity without its cyclin part-
establish the final fruit weight/size. Therefore, modifying fruit ner; and (iii) the CDK–CYC complexes are inactivated by the
growth by targeting genes involved in mitosis and endoredu- specific binding of CDK inhibitors (Churchmann et al., 2006;

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plication has been considered for tomato (Fig. 2). Torres Acosta et al., 2011).
In Eukaryotes, the cell cycle is composed of four distinct The endoreduplication cycle (endocyle) consists of succes-
phases: an undifferentiated DNA pre-synthesis phase with a sive rounds of DNA synthesis (S phases) in the absence of
2C nuclear DNA content, termed the G1 phase; the S phase mitosis, and thus represents a partial and modified cell cycle.
during which DNA is synthesized, with a nuclear DNA con- Consequently, cell cycle and endocycle progression involves
tent intermediate between 2C and 4C; a second undifferenti- control of CDK–CYC activity levels by common regulatory
ated phase (a DNA post-synthetic phase) with a 4C nuclear mechanisms on the molecular level, such as those mentioned
DNA content, termed the G2 phase; and the M phase, or above (De Veylder et al., 2011). Central to this regulation is
mitotic phase. Progression of the cell cycle is ensured by the the maintenance of a certain threshold of CDK–CYC activ-
activity of core regulators consisting of conserved heterodi- ity to allow the commitment to mitosis. When mitotic CDK
meric protein complexes. These complexes are formed by complexes do not form or their activity is suppressed, this
a catalytic subunit referred to as cyclin-dependent kinase threshold is not exceeded and the level of CDK–CYC activ-
(CDK) and a regulatory cyclin (CYC) subunit. The pres- ity is insufficient to drive cells into mitosis; endoreduplication
ence of the regulatory CYC is essential for the CDK–CYC can then take place.

Anthesis
A B C 3 5 8
Cell division
Ovary Dev.

Fruit set

Carpel identity and Auxin signaling: Cell cycle control:

Cell division control: SlPIN4, SlTIR1, SlARF7, SlCDKA;1, SlCDKB1, SlCDKB2
TAGL1, SlARF8, SlIAA9
FAS, LC, Cell division control:
SlWUS, GA signaling: FW2.2, SlKLUH/FW3.2, FW11.3,
SlIMA SlGA20ox1, SlDELLA1 OVATE, SUN, SlIMA

Auxin signaling:
SlPIN4

D 3 5 8 12 15 20 25 35
Cell expansion

Endocycle control: Primary metabolism:

SlCCS52A, SlWEE1, SlKRP1 HXK1, SuSY, LIN5, TIV1
mMDH, cpFBP
Auxin signaling:
SlIAA17 Regulation of primary metabolism:
SPA
ABA biosynthesis:
NOTABILIS/NCED1, FLACCA Ascorbate biosythesis:
Gal-LDH, GME

Fig. 2.  Genes involved in tomato fruit growth. Mapping of QTLs, cloning of the associated genes, in planta functional analyses, and characterization of
mutants have identified genes that impact fruit growth both positively and negatively. Theses genes are reported according to the respective stages of
fruit development in which they are involved: (A) ovary development; (B) fruit set; (C) phase of cell division; and (D) phase of cell expansion.
 Tomato fruit growth  |  Page 5 of 12

In tomato, several functional analyses have attempted to complex activity, which is necessary to permit the youngest
modulate the CDK–CYC complex activity during fruit devel- cells of the outermost layers of pericarp (namely the exo-
opment, either through direct targeting of CDK gene expres- carp) to enter into the phase of endoreduplication-driven cell
sion or through post-translational regulation of the complex expansion. In a similar manner, overexpression of CDKA;1
(Fig. 2C). Czerednik et al. (2012) generated transgenic plants induced mitosis across the pericarp and altered the endore-
aimed at down-regulating the canonical CDKA;1, the key duplication index (Czerednik et  al., 2014), thus supporting
player in cell cycle progression, in a fruit-specific manner the idea that CDKA plays an important part in the onset of
using an artificial microRNA (amiCDKA) and the TPRP endoreduplication and subsequent cell and fruit growth.
promoter (Fernandez et al., 2009). The amiCDKA plants pro- The inhibitory effect of phosphorylating CDKA on the
duced smaller fruits than those of the wild type, and which Tyr15 residue through the action of the WEE1 kinase rep-
had a thinner pericarp due to an overall decreased number resents a good example of a post-translational regulatory
of cell layers within the exocarp (displaying the smallest mechanism impairing the cell cycle, and potentially trigger-
cells). In contrast, the mesocarp displayed normal, enlarged ing the endocycle (Fig. 2D). Gonzalez et al. (2007) generated
cells without any significant difference in ploidy levels. transgenic tomato plants in which WEE1 was ectopically
A  similar phenotype was obtained with fruit-specific over- repressed. Smaller fruits were produced displaying a thin-
expression of either mitosis-associated CDKB1 or CDKB2 ner pericarp composed of smaller cells. There was a strong
(Czerednik et  al., 2012). Interestingly, the expression of reduction in endoreduplication as a result of impaired WEE1

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CDKA;1 was greatly repressed in overexpressing CDKB1 kinase activity leading to an enhanced CDK–CYC activ-
and CDKB2 lines in accordance with the phenotype of the ity. The WEE1 phosphorylation activity on its CDK targets
amiCDKA line. More recently, tomato fruits overexpress- appears to be an important mode of regulation for the pro-
ing CDKA;1 have been reported (Czerednik et  al., 2014). motion of endoreduplication during fruit development, and
CDKA1-overexpressing fruits were visually indistinguishable contributes to cell size determination, which ultimately influ-
from those of the wild type, with similar fruit weights and ences final fruit size (Chevalier et al., 2011, 2014).
diameters. However, they exhibited a larger placental area, The completion of mitosis and progression from mitosis
a thicker pericarp, and a reduced number of seeds. Across back into interphase requires the loss of CDK–CYC com-
the pericarp, the number of constituting cell layers was sig- plex activity, which occurs through proteolytic destruction of
nificantly increased, as well as the number of cells per mm2, the cyclin moiety by the UPS. This process involves a spe-
which was also observed in the placenta. Overall, the observa- cific E3-type ubiquitin ligase named the anaphase-promoting
tions showed that mean cell size was smaller, and was accom- complex/cyclosome (APC/C), which is activated through its
panied by a decrease in endoreduplication levels in cells from association with CDH1/FZR-type proteins (Heyman and De
the mesocarp, placenta, and jelly-like tissues. These data pro- Veylder, 2012). In plants, the commitment towards endoredu-
vided another example of the relationship between endore- plication involves the selective destruction of mitotic cyclins,
duplication and final cell size, suggesting a pivotal role for thereby preventing the formation of a proper mitotic CDK–
CDKA1 in the regulation of mitotic activities during fruit CYC complex, and thus impairing the associated kinase
development. Additionally, CDKA1 overexpression affected activity. This process is achieved by the CCS52A-mediated
the production of seeds in developing fruits that indirectly activation of the APC/C (Cebolla et al., 1999). The ectopic
affected pericarp cell expansion, which is normally driven by loss of function of CCS52A in transgenic tomato plants led
seed-produced phytohormones. to the production of smaller fruits, when compared with the
Altering CDKA or CDKB1/B2 gene expression in tomato wild type (Mathieu-Rivet et al., 2010) (Fig. 2D). The DNA
fruits produced phenotypes that highlighted differential ploidy levels in these fruits were shifted towards lower levels,
effects on cell division, cell expansion, and endoreduplica- which corresponded to a decrease in mean cell size and an
tion (Czerednik et al., 2012, 2014). In general, the observed increase in cell number. Conversely, the ectopic overexpres-
data are difficult to interpret, most probably because they are sion of SlCCS52A in tomato plants resulted in fruits slightly
associated with the specific tissular and developmental pat- smaller than those of the wild type. The cytological analyses
tern of expression of the TPRP promoter, which was used of these fruits revealed that the overexpression of SlCCS52A
to drive gene misexpression. The TPRP promoter is a fruit- first slowed down early fruit growth, which then resumed
specific promoter whose expression starts early in the ovary as highly endoreduplicated nuclei, and consequently larger
and reaches a maximum during the cell expansion phase of cells, were generated. The resulting accelerated fruit growth
fruit development (Fernandez et al., 2009). As a consequence, (Mathieu-Rivet et  al., 2010) was in agreement with the
CDKB1 and CDKB2 were overexpressed outside their natu- expected involvement of SlCCS52A in endoreduplication-
ral timing of expression (Joubès et  al., 1999, 2001), which driven cell expansion.
may have greatly affected the availability of regulatory cyc- The last example in modulating the CDK–CYC complex
lins for proper composition of CDK–CYC complexes, and/ activity during tomato fruit development refers to the work
or created an artificial competition for regulatory cyclins of Nafati et al. (2011). SlKRP1 (Fig. 2D), encoding a tomato
among the misexpressed CDKs. In the absence of measured CDK-specific inhibitor, was overexpressed in a fruit- and
CDK activity, we speculate that the phenotypes observed by cell expansion-specific manner using the PEPC2 promoter
down-regulating CDKA genes, or up-regulating CDKB genes (Fernandez et  al. 2009). Increasing SlKRP1 significantly
are caused by the lack of endocycle-specific CDKA–CYC reduced the extent of endoreduplication within the mesocarp,
Page 6 of 12 | Azzi et al.

as already described for a strong overexpression of KRP and its orthologues in relation to ion transport remains to be
genes in other plant tissues or organs (De Veylder et al., 2001; established, and how this could interfere with the control of
Jasinski et  al., 2002; Zhou et  al., 2003). However, the same cell proliferation is an intriguing question.
construct was ineffective during the phase of cell expansion fw3.2 is only the second major QTL for fruit size/weight
and did not alter the final size of fruits, in contrast to pre- to be fine mapped and cloned in tomato (Chakrabarti et al.,
vious reports describing plant dwarfism. The mean cell size 2013) (Fig.  2C). The gene underlying this QTL encodes a
within the pericarp was unaffected, demonstrating that cell P450 enzyme of the CYP78A subfamily, previously identified
size was, at least partially, uncoupled from DNA ploidy levels. as KLUH (Anastasiou et  al., 2007). The effect of SlKLUH
Nevetheless, endoreduplication occurred in these transgenic is to enlarge fruit volume through an increase in cell number
fruit, but to a far lesser extent than in the wild type. This sug- within the pericarp and septum tissues. Repressing SlKLUH
gests that DNA ploidy levels were sufficient to support cell using an RNA interference (RNAi) strategy led to decreased
growth, which is in agreement with the ‘karyoplasmic ratio fruit and seed size and, consequently, plant architecture was
theory’ (Schnittger et al., 2003; Chevalier et al., 2014). modified with a higher number and length of side shoots
(Chakrabarti et  al., 2013). The cloning of the gene and its
function characterization will be an important step towards
Modifying fruit growth by genes controlling elucidating the biological function of FW3.2.
fw11.3 is another important locus governing fruit weight in
fruit size and shape

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tomato (Van der Knaap and Tanksley, 2003) (Fig. 2C). The
Since its introduction in Europe in the 16th century, the fine mapping of fw11.3 demonstrated that it overlaps with
domestication and extensive breeding of tomato led to the fasciated (fas) which is a locus governing fruit shape on chro-
creation of cultivated varieties bearing enlarged fruits com- mosome 11, but fw11.3 and fas are not allelic (Huang and van
pared with the wild ancestors (Paran and van der Knaap, der Knaap, 2011). Unlike fw2.2 and fas, the large-fruit allele
2007). The diversity of fruit size in tomato has been attrib- of fw11.3 is partially dominant. The anticipated cloning of
uted to nearly 30 quantitative trait loci (QTLs; Grandillo FW11.3 will yield a third example of a cloned QTL regulating
et al., 1999). fruit weight.
The Fruit Weight QTL of chromosome 2, number 2 (fw2.2) Besides increasing fruit size, the domestication of tomato
was the first QTL-associated gene that was identified and resulted in a high diversity in fruit shape. From the invari-
cloned (Alpert et al., 1995; Alpert and Tanksley, 1996; Frary able, round-shaped fruits of wild species, cultivated tomato
et al., 2000). As a major QTL, fw2.2 accounts for as much as has diversified into round, flat, rectangular, ellipsoid, obovoid
a 30% difference in fruit fresh weight between the domesti- (pear-shaped), heart, oxheart, and long (bell pepper-shaped)
cated tomato and its wild relatives. FW2.2 acts as a negative fruits (Monforte et al., 2014). This diversity in tomato fruit
regulator of cell proliferation (Fig.  2C), thus explaining its shape originates from only four mutated genes, OVATE,
major effect on fruit size in tomato. In addition, the role of SUN, FASCIATED (FAS), and LOCULE NUMBER (LC)
fw2.2 in the determination of organ size is conserved within (Rodríguez et al., 2011). Both OVATE and SUN control fruit
the plant kingdom, in both monocotyledonous and dicotyle- elongation, OVATE is a negative regulator of growth lead-
donous species, such as avocado, maize, soybean, and cherry ing to shorter fruit, whereas SUN is a positive regulator of
(Dahan et al., 2010; Guo et al., 2010; Libault et al., 2010; De growth resulting in elongated fruit (Fig.  2C). FAS and LC
Franceschi et al., 2013). Unfortunately, no clear biochemical control the number of fruit locules, which ultimately influ-
function has been attributed so far to FW2.2 and its ortho- ences both fruit shape and fruit size (Fig. 2A).
logues, especially in relation to the regulation of the cell cycle/ OVATE was the first gene associated with fruit shape to be
cell division. identified by positional cloning (Liu et al., 2002). It belongs
FW2.2 belongs to a multigene family encompassing 17 to the ovate family protein (OFP) family of as yet unclear
homologues in tomato (hereafter referred to as FW2.2-Like function (Liu et al., 2002; Wang et al., 2011). The effects of
or FWL genes). FW2.2 and FWL proteins all contain the the ovate mutation on fruit shape vary from elongated fruits
uncharacterized PLAC8 motif, which was originally identi- to pear- or round-shaped fruits depending on the genetic
fied in proteins from mammalian placenta (Guo et al., 2010). background carrying the ovate mutation (Gonzalo and van
The PLAC8 motif contains two conserved cysteine-rich der Knaap, 2008). This suggests that OVATE is not respon-
domains separated by a variable region that are predicted to sible for the observed phenotype and probably interacts with
be transmembrane segments. The original tomato FW2.2 pro- other genes in an epistatic manner. The ovate pear-shaped
tein possesses these two transmembrane-spanning domains fruit phenotype was complemented both by a genomic DNA
that fix the protein to the plasmalemma (Cong and Tanksley, fragment covering the OVATE gene and by its ectopic over-
2006). From previous reports, it appears that the cysteine-rich expression to revert to round-shaped fruits (Liu et al., 2002).
domains may be involvled in the transport of heavy metals As a result, the ovate mutation is likely to be a loss-of-func-
such as cadmium and zinc, as identified in the plant cadmium tion mutation of a negative regulator of plant growth whose
resistance proteins from Arabidopsis (Song et al., 2010). This function remains to be elucidated. Interestingly, it has been
type of protein may multimerize into a homopentamer to shown in Arabidopsis that OVATE-like proteins act as tran-
form a transmembrane pore, thereby facilitating metal cation scriptional repressors that affect, in particular, the expression
transport (Guo et al., 2010). The association between FW2.2 of AtGA20ox1, a key player in the GA biosynthetic pathway,
 Tomato fruit growth  |  Page 7 of 12

thus resulting in reduced cell elongation (Hackbusch et  al., seeds occur concomitantly according to a precise, genetically
2005; Wang et  al., 2007, 2011). The indirect influence of controlled process mediated by phytohormones (Gillaspy
OVATE on fruit shape through regulation of GA biosynthe- et al., 1993).
sis in tomato remains to be demonstrated. Recent reviews have highlighted the role of plant hormones
The sun mutation causes an elongated-fruit phenotype. and their interplay in the control of fruit development (Ruan
A  gene duplication event mediated by a retrotransposon et al., 2012; Kumar et al., 2014). Here, we focus on the most
placed the SUN gene under the control of the defensin relevant genes, whose functional characterization in tomato
gene DEFL1 promoter, thus leading to high expression in revealed an involvement in the growth period of fruit devel-
fruit (Xiao et al., 2008; Jiang et al., 2009). The SUN protein opment. Auxin and GA appear to be the predominant hor-
belongs to the IQ67 domain-containing plant protein family mones required for fruit initiation in response to fertilization,
(Xiao et al., 2008) of unknown function. SUN overexpression since exogenous applications of both hormones lead to fruit
results in increased cell number in the longitudinal direction initiation and parthenocarpic development (de Jong et  al.,
and reduced cell number in the transverse direction of the 2009). A role for cytokinin, ethylene, and ABA in fruit for-
fruit, thus leading to fruit elongation (Wu et al., 2011). mation has been demonstrated, but is less well documented
The number of fruit locules is determined by the number of thus far (Kumar et al., 2014).
carpels within the flower. Wild species of tomato produce fruits Early fruit development is governed by the allocation of
with 2–4 locules, whereas cultivated varieties can develop >15 auxin to tissues and cells in order to initiate signal transduc-

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locules. As a result, not only can the shape of such fruits be tion pathways (Fig. 2B). Recent evidence has indicated that
greatly impacted, but this can also account for a tremendous the PIN-FORMED (PIN) auxin efflux transport proteins are
increase in fruit size by as much as 50% (Tanksley, 2004). The involved in the processes of fruit set and early fruit develop-
QTL fas was identified as a trait governing extreme fruit size ment in tomato (Pattison and Catala, 2012). Silencing of the
that increases the number of locules from two to more than tomato SlPIN4 gene, which is predominantly expressed in
seven, whereas the QTL lc has a weaker effect (Lippman and flower buds and young developing fruit, produced seedless
Tanksley, 2001; Barrero et al., 2006). FAS codes for a YABBY- (parthenocarpic) fruits of reduced size exhibiting precocious
like transcription factor (Cong et  al., 2008), whereas LC has development (Mounet et  al., 2012). The auxin signalling
been located in a non-coding region between two putative can- pathway involves an auxin receptor called the TRANSPORT
didate genes, WUSCHEL, which is a member of the plant-spe- INHIBITOR RESPONSE1 (TIR1) protein. In the presence
cific WUS homeobox (WOX) transcription factor family, and of auxin, TIR1 recruits the AUXIN/INDOLE-3-ACETIC
a gene encoding a WD40 repeat protein (Muños et al., 2011). ACID (Aux/IAA) transcriptional repressors and triggers
The function of most of the WOX genes studied so far can their degradation by the 26S proteasome. The degradation
be ascribed to promotion of cell division and/or prevention of of Aux/IAA repressor proteins releases the Aux/IAA-bound
premature differentiation (van der Graaff et al., 2009). More auxin response factors (ARFs), thereby initiating the auxin
specifically, WUS is involved in maintaining stem cell fate and response through auxin responsive element-mediated gene
meristem size, and, therefore, it is possible that the function of transcription. The misexpression in tomato of the auxin
WUSCHEL is affected in lc. FAS and LC can interact epistati- receptor TIR1 gene, as well as specific members of the Aux/
cally to produce fruits with an extremely high locule number IAA and ARF gene family, alters the normal flower-to-fruit
(Barrero and Tanksley, 2004). Both FAS and LC control floral transition and results in uncoupling fruit set from pollina-
meristem size and ultimately the development of supernumer- tion and fertilization and gives rise to parthenocarpic fruits
ary carpels (locules) leading to larger fruits (Cong et al., 2008; (Wang et  al., 2005; de Jong et  al., 2009; Ren et  al., 2011).
Muños et al., 2011). In this context, the link between fruit size, Recently, Su et al. (2014) reported that tomato plants silenced
as influenced by FAS and LC, and the activities regulating mer- for the Aux/IAA transcriptional repressor SlIAA17 displayed
istem size and cell division have been clearly established. larger fruits with thicker pericarp tissue (Fig. 2D). This phe-
Functional analyses using TOMATO AGAMOUS- notype stemmed from enhanced cell expansion due to high
LIKE1 (TAGL1), which is the orthologue of the duplicated ploidy levels. This suggests an enhancement of the endore-
SHATTERPROOF (SHP) MADS box gene of Arabidopsis duplication process in the absence of the optimal quantity of
thaliana, demonstrated the involvement of this transcrip- SlIAA17 during fruit development.
tion factor in the regulation of fruit development (Vrebalov In tomato, fruit set is partly mediated by GAs accord-
et al., 2009) (Fig. 2A). Tomato plants repressing TAGL1 by ing to a complex hormonal cross-talk with auxin (Serrani
RNAi produced smaller fruits with a thinner pericarp which et al., 2008) (Fig. 2B). Auxin synthesized both in the ovary
displayed fewer cell layers, and altered ripening-related fruit and in the apical shoot prevents unpollinated ovaries from
pigmentation, indicating that TAGL1 is important for regu- developing by reducing transcript levels of genes encoding
lating both fruit growth and the ripening process. GA biosynthetic enzymes, in particular the GA 20-oxidases
(Serrani et  al., 2007). Pollination then triggers the up-regu-
Hormonal regulation of fruit growth lation of transcripts for GA 20-oxidases that successively
synthesize active GA1 and GA4. The GA 20-oxidase activ-
After successful flower pollination and ovule fertilization, the ity thus appears as the limiting factor for active GA biosyn-
fruit and seed initiation, a stage that is commonly referred to thesis and, consequently, for fruit set. Functional analyses in
as fruit set, and subsequent development of both fruit and tomato aimed at the constitutive repression of SlGA20ox1
Page 8 of 12 | Azzi et al.

during fruit initiation and growth resulted in plants severely plants, whereas they were enlarged in RNAi-silenced plants.
affected in vegetative development and reduced pollen viabil- The cell number within the carpel was reduced, leading to a
ity (Olimpieri et  al., 2011). Ovaries from these SlGA20ox1- smaller carpel, thus suggesting that IMA encodes an inhibi-
silenced plants remained fertile and developed normally tor of cell division. Consequently, plants overexpressing IMA
after cross-pollination with wild-type pollen, but remained produced smaller flowers and fruits, whereas RNAi-silenced
parthenocarpic. The individual silencing of SlGA20ox1, plants produced fruits composed of supernumerary ovaries.
SlGA20ox2, and SlGA20ox3 genes confirmed the effects on In addition, IMA repressed the expression of WUS which
vegetative development but, again, no effects on fruit set were controls the meristem organizing centre and the determinacy
observed (Xiao et al., 2006). Altogether, these data confirmed of the nucellus during ovule development (Sicard et al., 2008)
the pleiotropic developmental role of GAs, but suggested that (Fig. 2A).
the expression of more than one GA20ox gene is required to
control fruit set in tomato. Interestingly, the heterologous
Metabolic control of fruit development
overexpression in tomato of CgGA20ox1 from citrus clearly
demonstrated the expected influence of GA and GA20ox The early stages of fruit development represent a critical
activity on fruit set and development (Garcia-Hurtado et al., period whereby traits, such as organoleptic composition,
2012). The overexpression of CgGA20ox1 resulted in elevated are established and ultimately dictate the final quality of the
GA4 content and boosted vegetative development, as shown fruit. Water, organic acids (primarily citrate and malate), and

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by longer hypocotyls and roots and increased plant height. minerals accumulate inside the vacuole of expanding cells
In addition, flowers from the the transgenic plants exhibited (Coombe, 1976) while starch accumulates transiently and
a protruding stigma due to a longer style and fruit displayed is converted subsequently to reducing sugars (Wang et  al.,
parthenocarpic development. 1993). Fruit softening, colouring, and sweetening then occur
The GA signal transduction pathway requires the rec- during the ripening phase (Giovannoni, 2004; Gapper et al.,
ognition of GA by its receptor called GA INSENSITIVE 2013). Fruit development and fruit weight are intimately con-
DWARF1 (GID1). The GID1–GA complex interacts with the nected to its composition of primary and secondary metabo-
nuclear repressor DELLA to target it for ubiquitin-depend- lites (Carrari and Fernie, 2006; Tohge et al., 2014). Therefore,
ent proteolytic degradation by the 26S proteasome. The modifying the expression of metabolism-associated genes
repression of GA-responsive genes is then released to initi- has been investigated as a means to induce variations in fruit
ate GA signal transduction. Silencing of the SlDELLA1 gene composition and size.
in tomato produced very similar vegetative and reproductive The development of fruit as a sink organ is more dependent
phenotypes to those described for GA20ox1-overexpressing upon the allocation of photo-assimilates than on the fruit’s
plants (Marti et al., 2007), as fruits were facultative parthe- own photosynthetic capacity. Modification of photo-assim-
nocarpic, smaller in size, and elongated in shape (Fig. 2B). ilate supply substantially affects fruit development and size
A number of ABA-deficient mutants have proven valuable through the modulation of cell number and cell size (Bohner
toward elucidating the role of ABA in fruit growth. Three and Bangerth, 1988; Bertin et al., 2002). When tomato plants
ABA biosynthetic mutants have been described: sitiens (sit), were submitted to extended darkness, fruit growth was
flacca (flc), and notabilis (not) that lack, respectively, an severely impaired as the result of a strong repression of cell
ABA-aldehyde oxidase (Harrison et  al., 2011), a molybde- cycle genes inside fruit tissues (Baldet et al., 2002). Conversely,
num-cofactor sulphurase (Sagi et al., 2002), and 9-cis epoxy- increasing photo-assimilate availability within the fruit by
carotenoid dioxygenase1 (NCED1) (Burbidge et  al., 1999) reducing the number of fruit per truss led to an enhancement
(Fig. 2D). Although the mutants have been characterized on in both flower and fruit growth rates. This corresponded to a
the molecular level, unfortunately little was reported on the greater cell number inside the carpel, due to an enhancement
effects of these mutations on fruit growth. Nitsch et al. (2012) of mitotic activities (Baldet et al., 2006). The percentage vari-
reported the phenotypic characterization of not/flc double ation observed in fruit fresh weight resulting from modulat-
mutant lines. The fruits of these double mutants have con- ing fruit load is even as high as that which can be achieved by
siderably reduced ABA levels, and displayed smaller fruit size genetic modification (Prudent et al., 2009). Hence, the modi-
and cell size, especially within the pericarp. The consequence fication of carbon metabolism and photo-assimilate parti-
of increasing ethylene levels, while lowering ABA, suggested tioning by the manipulation of key enzymatic activities, such
that ABA stimulates fruit growth by restricting ethylene levels as those involved in primary carbon metabolism and photo-
in normal fruits. synthesis, was expected to have an impact on fruit growth.
The INHIBITOR OF MERISTEM ACTIVITY (IMA) In order to investigate this, the Arabidopsis Hexokinase 1
protein is a mini zinc finger (MIF) protein harbouring an unu- (AtHXK1) gene was constitutively overexpressed in tomato
sual zinc-finger domain that was identified as an important plants (Menu et  al., 2004) (Fig.  2D). Overexpressing lines
effector of a signalling pathway involving multiple hormones exhibited marked phenotypic and biochemical changes in
that links cell division, cell differentiation, and hormonal con- developing fruits, such as reduced fruit size and a decrease in
trol of development in tomato (Sicard et al., 2008) (Fig. 2A, cell expansion. The carbon supply required to support these
C). IMA regulates the meristem activity and the processes of processes was lower throughout development, most probably
flower and ovule development. Carpel primordia within the due to decreased photosynthesis. Consequently, any sucrose
floral meristem were much smaller in IMA-overexpressing provided to these fruits would be used to fuel cell metabolism
 Tomato fruit growth  |  Page 9 of 12

at the expense of starch storage. Fruit displayed reduced res- central enzyme in ascorbate biosynthesis, exhibited defects
piratory rates, which were accompanied by lower ATP levels in cell expansion and the biosynthesis of non-cellulosic cell
and ATP/ADP ratios in fruit extracts, indicating profound wall polysaccharides (Gilbert et  al., 2009) (Fig.  2D). Taken
metabolic perturbations. together, these findings indicate an ascorbate-mediated link
The role of sucrose synthase (SuSy) in tomato fruit devel- among the energy-generating processes of respiration and
opment has been studied by silencing a fruit-specific isoform photosynthesis, primary metabolism, and developmental
(D’Aoust et al., 1999) (Fig. 2D). The inhibition of SuSy activ- processes, all of which are crucial for fruit growth in tomato.
ity affected fruit set and very early fruit development related Another example of a gene potentially modifying pri-
to the reduced unloading capacity for sucrose. This led the mary carbon metabolism and photosynthesis in fruit is the
authors to propose that SuSy participates in the control of chloroplastic isoform of fructose 1,6-bisphosphatase (cp-
sucrose import capacity of young tomato fruit and, conse- FBPase), an important enzyme in control of the Calvin cycle.
quently, influences fruit set and development. Unfortunately, Obiadalla-Ali et  al. (2004) generated tomato plants where
independent trials using equivalent transgenic plants failed the activity of this isoform was repressed specifically in fruit
to reproduce these results, and the lack of reports associating (Fig.  2D). Although overall carbohydrate metabolism was
SuSy isoforms and QTLs for fruit weight or sugar content only slightly altered, fruit growth and final fruit size were sig-
raised doubts about the validity of these conclusions (Carrari nificantly reduced, suggesting that cp-FBPase contributes to
and Fernie, 2006). fruit photosynthesis in providing carbon for fruit growth.

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The QTL Lin5 has been identified as a major QTL control- More recently, the search for genomic regions spanning
ling fruit weight and sugar content (Fridman et  al., 2000), QTLs connected to yield-associated traits identified nine can-
and the associated gene was found to code for a cell wall- didate genes located to tomato chromosome 4 (Bermúdez
bound invertase (Fridman et al., 2004). When Lin5 was RNAi et  al., 2008). Among these genes, a DnaJ chaperone-like-
silenced, fruit yield was greatly reduced, as well as fruit size, encoding gene was isolated and appeared to be associated
seed size, and seed number (Zanor et al., 2009) (Fig. 2D). In with changes in primary metabolites across tomato fruit devel-
these transgenic plants, metabolic changes were largely con- opment. The in planta functional analysis aimed at silencing
fined to sugar metabolism, since sucrose content increased this gene, subsequently named SPA for Sugar Partitioning-
while glucose and fructose contents decreased, as observed Affecting (Fig.  2D), showed that the ripe fruit weight, the
at the red ripe stage. Silencing of the vacuolar invertase TIV1 number of fruits per plant, and the harvest index were signifi-
gene by an antisense strategy in tomato gave overall similar cantly higher in transgenic than in wild-type plants (Bermúdez
results. Production of smaller fruits corresponded to high et al., 2014). SPA as a putative chaperone protein was shown
rates of sucrose accumulation and decreased hexose sugar to act through a mechanism involving the regulation of phos-
concentrations during the last stage of development (Klann phoglucomutase, sugar kinase, and invertase enzyme activities
et al., 1996) (Fig. 2D). Interestingly, changes in the concentra- during tomato fruit growth, thus regulating the harvest index
tion of osmotically active soluble sugars occurred during the by affecting the source–sink carbon distribution.
phase of cell expansion of fruit growth and affected fruit size.
This suggests that the concentration of osmotically active
sugars is tied to water influx, which is an important determi- Conclusion
nant of fruit enlargement.
In order to establish a link between glycolysis, synthesis of In this review, we focused mainly on developmental and cel-
hexose phosphates, and their conversion into organic acids, lular processes that relate to the determination of growth-
transgenic tomato plants were silenced for the mitochondrial related traits in tomato fruit, and we described various genetic
tricarboxylic acid (TCA) cycle-associated malate dehydro- and functional analyses that provide insight into factors mod-
genase (mMDH) gene (Nunes-Nesi et  al., 2005) (Fig.  2D). ifying fruit size. Although studies aimed at deciphering the
RNAi-mMDH plants showed not only enhanced chloro- genetic control of fruit size and shape have provided intrigu-
plastic electron transport rates and photosynthetic activity, ing results, many questions remain unanswered from the
but also increased fruit dry matter, indicating that the repres- available data. Association genetics and functional genom-
sion of mMDH improves carbon assimilation. Interestingly, ics approaches have allowed the localization of major QTLs,
transgenic fruit accumulated the redox-related compound and the genes controlling these traits have subsequently been
ascorbate and displayed an increased capacity to use l-galac- identified. Since we are still far from understanding the influ-
tono-lactone which is the immediate precursor of ascorbate ence of genes, such as FW2.2, FW3.2, FW11.3, or OVATE,
biosynthesis, as a respiratory substrate. Correspondingly, SUN, and LC, on the process of fruit development, such as
silencing of the tomato l-galactono-1,4-lactone dehydroge- cell proliferation, in-depth functional analyses are required
nase (Gal-LDH), which converts l-galactono-lactone into to unravel the molecular bases of their respective regulatory
ascorbate, substantially modified mitochondrial function, properties.
including alteration of the ascorbate redox state and the TCA
cycle (Alhagdow et al., 2007) (Fig. 2D). Consequently, plant
and fruit growth were greatly reduced, since cell expansion Acknowledgements
was affected. Additionally, fruit from tomato plants silenced The authors wish to express their deepest thanks to Professor Mark Hooks
for the GDP-d-mannose 3,5-epimerase (GME), which is the (University of Bordeaux) for reading and editing the manuscript.
Page 10 of 12 | Azzi et al.

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