Cell Expansion and Endoreduplication Show a Large
Genetic Variability in Pericarp and Contribute Strongly
to Tomato Fruit Growth1
Catherine Cheniclet, Wen Ying Rong, Mathilde Causse, Nathalie Frangne, Laurence Bolling,
Jean-Pierre Carde, and Jean-Pierre Renaudin*
Unité Mixte de Recherche 619 Physiologie et Biotechnologies Végétales, Institut National de la Recherche
Agronomique, Université Bordeaux 1, Université Victor Segalen Bordeaux 2, 33883 Villenave d’Ornon, France
(C.C., W.Y.R., N.F., L.B., J.-P.C., J.-P.R.); and Unité de Recherche Génétique et Amélioration des Fruits et
Légumes, Institut National de la Recherche Agronomique, 84143 Montfavet, France (M.C.)
Postanthesis growth of tomato (Solanum lycopersicon) as of many types of fruit relies on cell division and cell expansion, so that
some of the largest cells to be found in plants occur in fleshy fruit. Endoreduplication is known to occur in such materials,
which suggests its involvement in cell expansion, although no data have demonstrated this hypothesis as yet. We have
analyzed pattern formation, cell size, and ploidy in tomato fruit pericarp. A first set of data was collected in one cherry tomato
line throughout fruit development. A second set of data was obtained from 20 tomato lines displaying a large weight range in
fruit, which were compared as ovaries at anthesis and as fully grown fruit at breaker stage. A remarkable conservation of
pericarp pattern, including cell layer number and cell size, is observed in all of the 20 tomato lines at anthesis, whereas large
variations of growth occur afterward. A strong, positive correlation, combining development and genetic diversity, is
demonstrated between mean cell size and ploidy, which holds for mean cell diameters from 10 to 350 mm (i.e. a 32,000-times
volume variation) and for mean ploidy levels from 3 to 80 C. Fruit weight appears also significantly correlated with cell size
and ploidy. These data provide a framework of pericarp patterning and growth. They strongly suggest the quantitative
importance of polyploidy-associated cell expansion as a determinant of fruit weight in tomato.
In Angiosperms, fruit typically develops from ovary
after flower pollination and fertilization. In fleshy
fruits, cells in the ovary wall undergo a long series of
divisions and expansion, which give the fruit its final
size before the onset of ripening (Esau, 1962; Coombe,
1976; Gillaspy et al., 1993; Giovannoni, 2004). Knowledge of these mechanisms associated with fruit growth
and of their relationship with environmental factors
increases our basic understanding of fruit development as well as paving the way for potential applications in agriculture (Giovannoni, 2004; Tanksley, 2004).
The tomato (Solanum lycopersicon) berry is one of
the most studied fleshy fruits. The extensive genetic
resources available for tomato and related species are
illustrated by a wide variability of many characters of
tomato fruit (Causse et al., 2002). The characterization
of many mutant lines with specific alterations in fruit
development is currently under way in various laboratories to unravel the mechanisms underlying fruit
1
This work was supported by Région Aquitaine (contract no.
2004 0307002A).
* Corresponding author; e-mail jean-pierre.renaudin@bordeaux.
inra.fr; fax 335–557–125–541.
The author responsible for distribution of materials integral to the
findings presented in this article in accordance with the policy
described in the Instructions for Authors (www.plantphysiol.org) is:
Jean-Pierre Renaudin ([email protected]).
Article, publication date, and citation information can be found at
www.plantphysiol.org/cgi/doi/10.1104/pp.105.068767.
1984
development (Mazzucato et al., 1998; Giovannoni,
2004; Tanksley, 2004). As far as growth is concerned,
these studies require a detailed knowledge of fruit
patterning. Few studies to date have given quantitative details of the kinetics and localization of cell division and of cell expansion in pericarp, a prominent
tissue of tomato fruit formed from ovary wall (Smith,
1935; Gillaspy et al., 1993). In addition, although many
studies have compared fruit growth in mutants and
various wild-type tomato lines (Bohner and Bangerth,
1988; Mazzucato et al., 1998; Cong et al., 2002; Bertin
et al., 2003; Liu et al., 2003), data from such varying
genetic backgrounds remain difficult to reconcile into
an integrated model of pericarp formation.
Pericarp becomes polyploid in several fleshy fruit
species (Coombe, 1976), including tomato, where C
values span from 2 to 256 C at the end of growth
(Bergervoet et al., 1996; Joubès et al., 1999). In addition,
Joubès et al. (1999) showed that another fruit tissue,
the locular gel, which develops from the placenta after
fertilization, is also polyploid, but not the epidermis.
Endoreduplication is a frequent, somatic event in
many plant organs and tissues (Kondorosi et al.,
2000; Larkins et al., 2001; Barow and Meister, 2003;
Sugimoto-Shirasu and Roberts, 2003). Its wide occurrence in plant and animal cells is largely assumed to be
associated with metabolic activity and with cell expansion (Edgar and Orr-Weaver, 2001; Storchova and
Pellman, 2004). This latter phenomenon is especially
important in plants as compared with animals, as the
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Cell Size and Ploidy in Tomato Pericarp
volume of plant cells may increase by several orders of
magnitude. In this way, cell expansion plays a critical
role in the control of plant organ size as well as cell
division (Dolan and Davies, 2004). One role of endoreduplication in the fruit could be to trigger the huge
cell expansion that takes place in these organs
(Coombe, 1976), but to our knowledge no data have
demonstrated this hypothesis as yet. Although some
studies have shown the importance of cell number for
fruit size in tomato (Bohner and Bangerth, 1988; Frary
et al., 2000), so far there is very little data dealing with
the relationship between cell expansion and fruit size
in this material (Tanksley, 2004), as well as in other
species.
This study considers the variability of tomato fruit
size to address the question of its dependence on cell
size and polyploidy. It includes a kinetic analysis of
pericarp development in a cherry tomato line, and
a comparative analysis of pericarp in 20 tomato lines
displaying a wide range of fruit size and genetic
origins. Both approaches emphasize a significant correlation between polyploidy and cell size for this
material. The contribution of cell size to final fruit
weight is demonstrated, and the putative role of endoreduplication in this phenomenon is strongly suggested. These data provide a framework for the
analysis of specific mutant lines. Moreover, they set
the basis for a genetic approach to cell expansion and
endoreduplication in tomato fruit.
RESULTS
Fruit Characteristics of 20 Tomato Lines
Twenty tomato lines were selected in the Institut
National de la Recherche Agronomique collection of
tomato genetic resources in Avignon (Table I). All lines
are from S. lycopersicon, except cherry tomato Wva700
from S. pimpinellifolium. All lines have indeterminate
growth, except Caline. These lines were chosen because of the very different fruit sizes and various
genetic backgrounds. Mean fruit weights ranged from
3.8 to 431 g (Table I). Part of this variability was related
to the number of carpellar locules, which varied from
two to 22 (Table I). A set of 12 lines displayed fruit
weights from 3.8 to 130 g while keeping two or three
carpellar locules (exceptionally four; lines 1–12 in
Table I).
Organization of Pericarp at Anthesis, and
Growth Initiation
In tomato, fertilization occurs within 20 h after
anthesis (Picken, 1984). At that time, the carpellar
wall of Wva106, a cherry tomato line, displays eight to
nine cell layers, in which all cells have a roughly cubic
shape and have nearly the same size, except for
vascular bundles (Fig. 1A). The characteristics of
ovaries at anthesis were compared in the 20 tomato
lines (Fig. 2). Ovary diameter varied from 1.3 to
Table I. Properties of the 20 tomato lines
The number before the name of each line identifies it in Figures 2 and
10. Fruit weight of ripe fruit (mean 6 SD, n 5 5–7) and locule number
(n 5 9–17; when more than one number is indicated, a bold character
shows the most frequent locule number) were measured in fruit grown
in Avignon, spring 2003, as detailed in ‘‘Materials and Methods.’’
Tomato Line
Fruit Weight
Locule No.
g
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
Wva700
Cervil
Red Cherry Small
Wva 106
Sweetie
Gardener’s Delight
Bubjekosoko
Montfavet 133-5
Chemin
Ailsa Craig
Kondine Red
Ferum 26
Sucrée à Gros Fruits
Montfavet 136-11
Caline
Montfavet 315
Jaune Grosse Lisse
Saint-Pierre Clause
Marmandaise
Grosse de Gros
3.8
5.6
9.8
9.9
13.8
25
42
44
66
81
82
130
92
102
105
127
195
198
201
431
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
0.2
0.4
0.3
0.8
0.8
1
6
2
8
13
11
14
20
27
42
22
46
28
55
71
2
2, 3
2, 3
2, 3
2, 3
2, 3
3, 2, 4
2
2, 3
2, 3
2, 3
2, 3
7–12
3–5
4–7
3, 5
6–18
3–8
4–13
11–22
4.7 mm among the 20 lines, and from 1.3 to 2.4 mm
between the 12 lines with only two to three locules per
fruit (data not shown). Yet, pericarp pattern was found
to be dramatically conserved between the 20 lines, as
inter-line SDs of pericarp thickness (Fig. 2A), mean
cross-sectional pericarp cell area (Fig. 2B), and number
of cell layers across pericarp (Fig. 2C) were less than
10% of the mean values of these parameters. The
conserved structure of pericarp at anthesis is illustrated in Figure 1 for Wva 106 (Fig. 1A); for Ferum 26,
which has the largest fruits with only two to three
locules (Fig. 1B; Table I); and for Grosse de Gros, which
shows the largest fruits among the 20 lines (Fig. 1C;
Table I).
The increase in pericarp thickness became detectable at 4 DPA in Wva106 (Figs. 1, A and D, and 3B).
This was due both to cell division and to cell expansion. After anthesis, mitoses occurred at the highest
rate in the two outer epidermal and subepidermal
layers (Fig. 1, D and E), as well as in the two inner
epidermal and subepidermal ones, but to a lower
extent (Fig. 1D). In epidermal layers, only anticlinal
cell divisions were detected, whereas they were mostly
periclinal in the two subepidermal layers. Thus, the
outer subepidermal layer, and to a lesser degree the
inner subepidermal one, are the major sources of new
cell layers during pericarp growth. Mitotic activity
also occurred in more central cells, but to a much lesser
extent and with various division planes. In Wva106,
new cell layers arise very early, between 3 and 5 DPA
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Cheniclet et al.
Figure 1. Structure and development of pericarp after anthesis. A to C,
Cross sections of ovary wall at anthesis for Wva106 (A), Ferum 26 (B),
and Grosse de Gros (C) lines. D, Pericarp cross section of 4-DPA
Wva106 fruit, showing anticlinal (vertical arrows), periclinal (horizontal arrows), and randomly oriented (arrowheads) cell divisions in inner
epidermal and subepidermal layers and in central cells. E, Enlarged
portion of the outer pericarp of the same fruit as in D showing anticlinal
divisions (vertical arrows) in outer epidermal layer and periclinal
divisions (horizontal arrows) in outer subepidermal layer. oe, Outer
epidermis; ie, inner epidermis; vb, vascular bundle. Scale bars: 50 mm
(A–D) or 20 mm (E).
between nine and 12. New cell layers originated
predominantly from the outer subepidermis layer
and less from the inner one, as suggested by mitotic
activity in both layers and by counting cell layers
above and below vascular bundles (data not shown).
Examples of fruit structure and pericarp pattern at
breaker stage are shown in Figure 4. Most pericarp
cells expanded a lot during fruit growth, to reach
diameters of 200 mm and beyond (Fig. 4, A–C, right).
In contrast, outer epidermal and subepidermal cells
kept a size close to the one they had at anthesis (Figs.
1E and 4D). The mean size of pericarp cells was
determined in cross sections of parenchymatous (not
vascular) parts of the mesocarp (see the location of
these measurements in Fig. 4C, right). The most outer
and inner layers of pericarp and the vascular bundles
were excluded from these measurements.
In Wva106, pericarp cell expansion followed a twostep increase very similar to the kinetics of pericarp
thickness (Fig. 3, B and C). In a first step, from anthesis
to green mature stage, the mean cellular cross section
(Fig. 3D). Cell expansion also resumed very early, as it
was detectable at 4 DPA (Figs. 1 and 3C).
Pericarp Growth and Pericarp Structure at
Breaker Stage
Fruit diameter and pericarp thickness of Wva106
fruits increased steadily from anthesis, and both
parameters leveled off at green mature stage (Fig. 3,
A and B). Then, a secondary increase of pericarp
thickness by 1.5 times was evident at the transition
between green mature and breaker stage, at the time
when chlorophyll is degraded and carotenoids accumulate (Fig. 3B). In contrast, no increase of fruit diameter was detected at that time (Fig. 3A). When the
pericarp thickness of the 20 tomato lines was compared at breaker stage, dramatically contrasted values
were found (Fig. 2A). The increase of pericarp thickness from anthesis to breaker stage ranged from 10
times for cherry tomato lines as Wva106 to more than
50 times for Ferum 26. These variations were accounted
for by generation of new cell layers and by cell expansion, as detailed below.
The production of new cell layers after anthesis
varied from five in two cherry tomato lines, Wva700
and Wva106, to 17 in three larger fruit lines, Ferum 26,
Montfavet 315, and Grosse de Gros (Fig. 2C). In 13
lines, the average number of new cell layers was
Figure 2. Cellular parameters of pericarp at anthesis and breaker
stages. Tomato plants from 20 lines were grown in a greenhouse
(Avignon). For each line, three to seven fruits were sampled for
structural and cytological analyses at the time of anthesis (white
columns) and at the beginning of breaker stage (gray columns). A,
Pericarp thickness at anthesis (mm, left) and breaker (mm, right) stages.
B, Mean cross-sectional area of one pericarp cell at anthesis (mm2, left)
and breaker (mm2, right) stages. C, Number of cell layers across
pericarp. D, MCV of pericarp cells at breaker stage.
1986
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Cell Size and Ploidy in Tomato Pericarp
values (256 C) in pericarp. Sepals become also polyploid during fruit growth, but to a lower extent, with C
values from 2 to 32 C (Fig. 5G).
Ploidy histograms and mean C value (MCV) are
fairly reproducible, as relative SD of MCV is lower than
15% between similar fruits, except for columella (Fig.
5, B, D, F, and H). Pericarp and locular gel have a
similar MCV of 35 to 40, larger than columella (MCV 5
18) and sepals (MCV 5 8). MCVs as well as ploidy
profiles can usually be reproduced in pericarp of
similar fruit of the same line, grown in different conditions (Fig. 5B). Very similar data were obtained with
the Wva106 line (data not shown).
The kinetics of pericarp MCV during fruit development was investigated in the Wva106 line. At anthesis,
Figure 3. Kinetics of pericarp growth in the Wva106 line. Six Wva106
plants were grown in a greenhouse (Bordeaux). At each developmental
stage, three to five fruits (total no. 102) were selected for measurement
(mean 6 SD). A, Fruit diameter. B, Pericarp thickness. C, Mean crosssectional area of one pericarp cell. D, Number of cell layers across
pericarp. E, MCV of pericarp cells, as described in Figure 5. Insets in C
and E show enlarged kinetics for the 0 to 8 DPA period. Arrows show
the breaker stage.
area increased from 150 to 18,000 mm2. After a transient
stationary level, cell expansion resumed rapidly at the
transition with breaker stage, and mean cross section
cell area attained 34,000 mm2 in ripening fruits. Quantitative differences in the extent of cell expansion were
obvious between tomato lines at the breaker stage (Fig.
4, A–C, right). At that time, the mean cross-sectional
area of mesocarp cells varied from 20,000 mm2 in
Wva700 cherry tomato line to 100,000 mm2 in Ferum
26, Montfavet 133-5, and Montfavet 135-11 (Fig. 2B). It
should be noted that the smallest mean cell sizes,
below 40,000 mm2, were encountered both in cherry
tomato lines and in some lines with the largest fruit,
such as Grosse de Gros and Jaune Grosse Lisse (Figs.
2B and 4, A–C).
Ploidy Analysis in Tomato Fruit
Ploidy of cells from pericarp, locular gel, and central
columella was analyzed in Bubjekosoko fruits at
breaker stage (Fig. 5, A, C, and E). The three tissues
display different ploidy profiles, with the largest C
Figure 4. Pericarp structure at breaker stage. A to C, Cross sections of
fruit (left) and pericarp (right) at breaker stage are shown for Grosse de
Gros (A), Ferum 26 (B), and Wva106 (C) lines. D, Enlargement of
Wva106 outer pericarp at the same magnification as Figure 1E; these
show that epidermal and subepidermal cells have mainly enlarged
tangentially since anthesis. The rectangle in A, right, is an example of
an area within which mean cell size has been estimated, as detailed in
‘‘Materials and Methods.’’ Bars: 1 cm (A–C, left sections), 1 mm (A–C,
right sections), and 20 mm (D).
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Cheniclet et al.
a significant decrease of nuclei with lower C values
(Fig. 7). In nine lines, 256- 1 512-C nuclei represented
more than 5% of all nuclei. The highest MCVs were
found in the three lines Montfavet 136-11, Ferum 26,
and Saint-Pierre Clause in which 512-C nuclei have
a frequency above 1% (Fig. 7).
Evidence for Correlation between Ploidy,
Cell Size, and Fruit Size
Figure 5. Endoreduplication in tomato fruit. Ploidy has been analyzed
by flow cytometry in pericarp (A and B), locular gel (C and D),
columella (E and F), and sepals (G and H) of Bubjekosoko fruit grown in
Bordeaux and harvested at breaker stage. Left sections show histograms
of one representative fruit. Right sections (gray bars) show the frequency
of each C value class as calculated from measurements performed on
29, 20, 19, and 12 fruits for B, D, F, and H, respectively. In B, the results
from another set of three fruits from plants of the same line grown in
Avignon are also shown (white bars, MCV’).
the whole ovary contains mostly 2- and 4-C, and few
8-C nuclei (MCV 5 3.2; Figs. 3E and 6A). In pericarp,
MCV increased slightly to 7 within 10 DPA (Fig. 3E)
because of the disappearance of 2-C (from anthesis),
the increase of 8-C (from 3 DPA), and the appearance
of 16-C nuclei (from 6 DPA). Then, it increased more
steadily up to 32 at the breaker stage (Fig. 3E), owing to
the successive appearance of 32-C (from 10 DPA), 64-C
(from 13 DPA), 128-C (from 20 DPA), and 256-C (from
33 DPA) nuclei (Fig. 6B). Very similar data were
obtained with the Bubjekosoko line (data not shown).
The pericarp ploidy of the 20 tomato lines was
analyzed at breaker stage (Fig. 2D). MCVs varied from
24 to 68 according to the line. Ploidy profiles of two
lines with a low MCV and two lines with a high MCV
are shown in Figure 7. C values from 4 to 128 C were
systematically encountered in all lines. Interestingly,
the lowest MCVs were encountered both in cherry
tomato lines and in some lines with very large fruits,
such as Jaune Grosse Lisse, Marmandaise, and Grosse
de Gros. High MCVs were due to relatively high
frequencies of 128-, 256-, and 512-C nuclei, but not to
The two sets of measurements of cell size and ploidy
during fruit development in Wva106 (Fig. 3, C and E)
and at breaker stage in 20 tomato lines (Fig. 2, B and D)
were used to investigate the relationship between
these two parameters. For this purpose, cell size was
expressed as cell diameter, calculated from crosssectional areas by assuming round-shaped cells.
Figure 8A shows that there is a significant correlation between ploidy and cell size in pericarp of
102 Wva106 single fruits collected at various developmental stages. Figure 8B shows that ploidy and cell
diameter are also significantly correlated in fruit
pericarp of 20 tomato lines at breaker stage. Although
the correlation is somewhat weaker than in Figure 8A,
because of more dispersed individual values, the most
suitable regression is polynomial as in Figure 8A.
The combination of both sets of data in Figure 8, A
and B, reveals a unique relationship between ploidy
and cell size in tomato pericarp (Fig. 8C). Cell diameter
is positively correlated with ploidy by a polynomial,
Figure 6. Developmental kinetics of C-value classes in Wva106
pericarp. Data are from the same experiment as in Figure 3. A,
Evolution of 2-C (white triangles, dashed line), 4-C (white squares,
dashed line), 8-C (black triangles, solid line), and 16-C (black squares,
solid line) classes in fruit pericarp. B, Evolution of 32-C (white circles,
dashed line), 64-C (white diamonds, dashed line), 128-C (black circles,
solid line), and 256 C (black diamonds, solid line) classes in fruit
pericarp.
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Cell Size and Ploidy in Tomato Pericarp
Figure 7. Ploidy distribution in pericarp of four tomato lines. Data are
mean 6 SD of the frequency of each C-value class of three to seven fruits
at breaker stage for four selected tomato lines, two lines with a low
MCV value, Wva106 (white bars) and Grosse de Gros (light-gray bars),
and two lines with a high MCV, Montfavet 136-11 (dark-gray bars) and
Ferum 26 (black bars). Growth conditions and line characteristics are
detailed in Figure 2.
almost linear, over a wide range of variation: 35-fold
for cell diameter and 27-fold for MCV.
As cell size is obviously one of the regulators of fruit
size, we investigated the quantitative relationship
between these two parameters. During Wva106 fruit
growth, fruit weight increases from 3 to 4 mg at
anthesis to 8 to 9 g at the late mature stage, having
a close, positive correlation with the increase of mean
pericarp cell diameter (Fig. 9A). No correlation was
found between fruit weight and pericarp cell size
when fruit from all 20 lines were analyzed at the
breaker stage (Fig. 9B, white and black symbols).
Because fruit weight is also dependent on the number
of carpellar locules, the relationship between cell size
and fruit weight was investigated for fruits with only
two to three carpellar locules, and a significant correlation was found (Fig. 9B, black symbols). The combination of both sets of data in Figure 9, A and B, again
reveals a unique correlation between fruit weight and
mean pericarp cell diameter in tomato fruit with only
two to three carpellar locules, whatever their developmental stage. As expected, fruit weight is approximately a cubic function of cell diameter (Fig. 9C).
The relationship of endoreduplication with fruit size
is illustrated in Figure 10, which shows mean pericarp
ploidy and fruit weight of each of the 20 tomato lines.
As mentioned for cell size, ploidy is not correlated
with fruit size when the 20 lines are compared (black
and white symbols in Fig. 10), but a positive correlation becomes prominent when the 12 lines with two to
three carpellar locules are considered (black symbols
in Fig. 10).
DISCUSSION
The Ovary Wall Structure Is Highly Conserved in
Several Tomato Lines, and Different Mechanisms
Control Pericarp Growth
This study shows that the pattern of ovary wall,
including the number of cell layers and cell size, is
dramatically conserved at the time of anthesis in 20
tomato lines, including 19 S. lycopersicon lines and one
wild relative, S. pimpinellifolium. This phenomenon is
remarkable with respect to the large variability among
the 20 lines in ovary size and locule number on one
hand, and in overall fruit growth and final pericarp
pattern and thickness on the other hand (Table I; Fig. 2).
Our data indicate the cooccurrence of two distinct
mechanisms of cell division in tomato pericarp after
anthesis, as previously reported in grape (Vitis vinifera;
Considine and Knox, 1981). Periclinal cell divisions,
located mostly in the outer subepidermal cell layer
and, to a lesser extent, in the inner one, generate five to
17 new cell layers according to the line. These will be
referred to as histogenic cell divisions. In addition,
randomly oriented cell divisions occur in many cell
layers to accommodate pericarp growth with fruit
growth; we refer to these as growth-related cell divisions. Several lines of evidence point to different
Figure 8. Relationship between cell size and ploidy. Each point shows
the MCV and cell diameter in pericarp of a single fruit. The mean cell
diameter was calculated from mean cross-sectional cell areas estimated as described in ‘‘Materials and Methods,’’ by approximating
cells as spheres. White symbols in A and C report data from the same
experiment as in Figure 3, where fruit development was analyzed in
Wva106 line from anthesis to ripening (n 5 102 fruits). Black symbols
in B and C report data from the same experiment as in Figure 2, where
20 tomato lines were compared at breaker stage (all lines are
represented by the same symbol; n 5 81 fruits). Dashed lines show
the polynomial regression curves for each set of data. R2 5 0.93 and
0.69 for A and B, respectively. The equation in C is y 5 0.05x2 1 8.9x 2
7.0, R2 5 0.96, n 5 183.
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Cheniclet et al.
Figure 9. Relationship between cell size and fruit size. Each point
shows the weight of one fruit as a function of its mean pericarp cell
diameter. Mean cell diameters were calculated from mean crosssectional cell areas estimated as described in ‘‘Materials and Methods,’’
by approximating cells as spheres. Note the log scale of fruit weight in
all panels. A, Same experiment as in Figure 3, where fruit development
was analyzed in Wva106 line from anthesis to ripening. The dashed
line is the regression curve (R2 5 0.96, n 5 107). B, Same experiment as
in Figure 2, where fruit from 20 tomato lines was compared at the
breaker stage. Black symbols in B represent fruits with only two to three
carpellar locules and the dashed line is the regression curve (R2 5 0.85,
n 5 41). White symbols in B show 40 fruits with four or more carpellar
locules. C, Combination of all data from A (white symbols) and of data
from fruits with only two to three carpellar locules in B (black symbols).
The dashed line is the regression curve (y 5 3.1026x2.79, R2 5 0.96, n 5
148).
controls for histogenic and growth-related cell divisions in tomato pericarp. Our data show that histogenic cell divisions proceed rapidly in the Wva106
line, as they are completed within 5 DPA, whereas
mitotic activity remains significant in the pericarp up
to 20 DPA. Similar data were reported in other lines
(Joubès et al., 1999; Cong et al., 2002). The major
quantitative trait locus fw2.2 has been shown to control
fruit size directly through cell division, but not cell
expansion (Cong et al., 2002; Liu et al., 2003). The
authors showed that cell layer production is not
regulated by fw2.2, which argues for different genetic
controls of the two modes of division in pericarp. The
variation between lines of the number of cell layers
generated after anthesis suggests a genetic determi-
nant for histogenic cell division. To which extent this
pericarp-located genetic mechanism also operates in
more central parts of the tomato fruit remains unknown.
The accumulation of some metabolites is heterogeneous throughout pericarp. For instance, starch predominantly accumulates in inner pericarp cells, and
carotenoid synthesis during ripening is often more
intense in outer pericarp (Smith, 1935). Variation in
pericarp patterning, such as number and location of
new cell layers, may thus modify the balance between
metabolic pathways related to fruit quality. Cell layers
are only defined here according to their position, and
no assumption is made as to their homogeneity with
regard to cell size and cell content.
Confocal analysis has revealed the volume and shape
of inner mesocarp cells in grape berry (Gray et al., 1999).
As in grape lines with almost round-shaped fruits,
tomato pericarp cells are roughly isodiametric or egg
shaped (C. Cheniclet, unpublished data). Thus, convenient approximations of cell diameters and volumes can
be extrapolated from cross-sectioned cell areas. However, single-cell size measurements cannot be simply
compared, e.g. as histograms, because of variability in
the location of cross section planes. For this reason, we
have only estimated the mean size of mesocarp parenchymatous cells. The large variation in this parameter
during fruit growth and between different lines has
added significant new data on the process of cell
expansion in tomato pericarp.
Our data point to the rapid increase of cell size as
early as at 4 DPA, i.e. before the end of histogenic and
growth-related cell divisions (Figs. 1, A and D, and 3C).
Cell expansion then occurs during 3 to 4 weeks up to
the green mature stage and may be accompanied by cell
division during 2 to 3 weeks. At the mature green stage,
as compared with anthesis, the mean extrapolated
Figure 10. Relationship between fruit size and ploidy. Fruit weight is
shown as a function of MCV in pericarp. Each point represents one
tomato line (mean of three to seven fruits per line, 20 tomato lines).
Data are the same as in Figure 2. The number beside each symbol is the
line number shown in Table I. Black symbols represent lines with only
two to three carpellar locules, and the associated dashed line shows
the polynomial regression curve (y 5 0.0264x2 1 0.2622x 2 21.758,
R2 5 0.87, n 5 12). White symbols show eight lines with four or
more carpellar locules.
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Cell Size and Ploidy in Tomato Pericarp
pericarp cell volume has increased between 2,000
times in three cherry tomato lines, Wva700, Wva106,
and Cervil, and 22,000 times in four lines, Montfavet
133-5, Kondine Red, Ferum 26, and Montfavet 136-11
(Fig. 2B). These data are in good agreement with the
small amount of data available elsewhere concerning
tomato pericarp (Bohner and Bangerth, 1988; Cong
et al., 2002) and other fleshy fruits (Coombe, 1976;
Gray et al., 1999; Higashi et al., 1999; Harada et al.,
2005). They also indicate that the 20 tomato genotypes
display a broad range of values, from 1 to 14, for their
mean pericarp cell volume at the end of fruit growth.
These results provide a solid basis for further genetic
analysis of cell size regulation in tomato fruit.
A detailed time-course analysis of pericarp thickness and cell size reveals a rapid and transient step of
cell enlargement at the transition between green mature and breaker stages (Fig. 3C). To our knowledge,
this phenomenon has not yet been reported. It is not
related to environmental changes of growth conditions, and it is reproducible (data not shown). It
appears to be confined only to pericarp, as fruit size
does not increase significantly at the same time. A
decrease in tomato pericarp cell turgor has been
reported at the beginning of ripening (Shackel et al.,
1991). It is tempting to make this event the consequence of cell expansion at the same time. Although
the underlying mechanism has not yet been explored,
it could be related to cell wall alterations at the onset of
ripening (Giovannoni, 2004).
Besides some results showing the importance of cell
number for fruit size in tomato (Bohner and Bangerth,
1988; Frary et al., 2000), very few studies have addressed the quantitative contribution of cell expansion
to the growth of fleshy fruit (Coombe, 1976; Tanksley,
2004). This study shows that the dramatic increase in
pericarp cell size during tomato fruit development
correlates nicely with the increase in fruit weight (Fig.
9A). This same correlation holds true when those lines
that share a similar number of carpellar locules, so that
there is no effect of locule number on fruit weight, are
compared at the breaker stage (Fig. 9, B and C). This
suggests that cell expansion in other tissues, such as
locular gel and central columella, parallels that of
pericarp cells. Indeed, cell expansion also occurs in
these two tissues to a large extent, with columella cells
remaining smaller than pericarp or locular gel cells (C.
Cheniclet, unpublished data). These data demonstrate
that the huge potential of plant cells for expansion is
actually a strong determinant of fruit size in tomato.
of C values in a given tissue may relate partly to the
presence of various cell types, as is the case for
pericarp. Five C value classes were found in locular
gel, despite the apparent lower heterogeneity of cell
types in this tissue. A similar result was reported for
maize (Zea mays) endosperm (Larkins et al., 2001;
Dilkes et al., 2002) and in older reports (Buvat, 1965).
The complexity of ploidy profiles in given tissues
suggests discrete endogenous regulations within tissues, with cell age probably playing an influential role
(List, 1963; Melaragno et al., 1993).
The tomato ovary comprises an equal number of 2
and 4 C cells at anthesis. Because 4-C ploidy can be
attributed both to G2 or to the first endocycle, the
unambiguous detection of polyploidy is only by 8-C
nuclei, due to the second endocycle. This event has
already started to a limited extent at anthesis, and it
resumes at 3 DPA in tomato pericarp. These data agree
with those of Bertin et al. (2003) to suggest that the first
and second endocycles begin prior to anthesis in ovary
cells. Then, the third, fourth, and fifth endocycles occur successively every 3 d up to 13 DPA (Fig. 6), which
suggests that the mean endocycle duration in this
material is 3 d. To our knowledge, such a value has not
yet been reported for plant materials. The sixth (to
128 C) and seventh (to 256 C) endocycles appear much
later, at 20 and 33 DPA, respectively, and only concern
a small number of nuclei. This suggests a decrease in
the efficiency of these endocycles, rather than the
disappearance of a polyploidy-inductive signal after
13 DPA, as a significant increase of 32- and 64-C nuclei
still occurs up to 40 DPA. As a whole, pericarp MCV increases steadily from anthesis to ripening in a way that
confirms and extends previous reports (Bergervoet
et al., 1996; Bertin et al., 2003). Notably, no significant
change of ploidy occurs during the second phase of
cell expansion at the end of the green mature stage
(Fig. 3, C and E).
Significant variations in pericarp MCV were found
between the 20 tomato lines at the breaker stage (Fig.
2D). They originated from variations in the largest
C values, namely 128, 256, and 512 C. The large variation of MCV between lines suggests that a genetic component regulates the ability of each line to proceed
through high levels of polyploidy in pericarp, i.e.
through the sixth to eighth endocycles. A similar
situation has recently been demonstrated in maize
endosperm, with a 2-fold variation of MCVs between
most Midwestern dent types and maize popcorns
(Dilkes et al., 2002).
Endoreduplication Occurs to Various Extents in
Different Fruit Tissues and in Different Tomato Lines
Endoreduplication Could Be a Regulator of Cell
and Fruit Size
Pericarp, locular gel, central columella, and sepals
display significant differences in ploidy profiles with
respect to distribution, highest value, mean, and mode
of C values (Fig. 5). These data extend previous results
on the same material (Bergervoet et al., 1996; Joubès
et al., 1999; Bertin et al., 2003). The broad distribution
A positive correlation between cell size and ploidy
has been demonstrated in numerous instances in
a wide range of organisms (Day and Lawrence, 2000;
Kondorosi et al., 2000; Edgar and Orr-Weaver, 2001;
Sugimoto-Shirasu and Roberts, 2003; Storchova and
Pellman, 2004). We have combined kinetic and genetic
Plant Physiol. Vol. 139, 2005
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Cheniclet et al.
variations to demonstrate that such a correlation also
occurs in developing tomato pericarp. The data of
Figure 8C show a striking quantitative agreement with
many data from different plant species, such as developing xylem cells of monocotyledonous roots (List,
1963), pea (Pisum sativum) cotyledon cells (Lemontey
et al., 2000), Arabidopsis (Arabidopsis thaliana) epidermal pavement cells (Melaragno et al., 1993), and maize
endosperm cells (Leiva-Neto et al., 2004). In these
studies, the reported cell size and MCV values fit with
the first part (MCV below 20) of the regression curve of
Figure 8C (data not shown), which strongly supports
the relevance of the correlation between ploidy and
cell size. Tomato fruit offer the opportunity to extend
this correlation to much larger ploidy values. In situ
analysis of ploidy and cell size in tomato pericarp are
under way to assess the location of polyploid cells in
this tissue.
Although widely assumed, the correlation between
cell size and ploidy is not systematic. Cell size is tissue
specific, in a way unrelated to ploidy. In Arabidopsis,
the ploidy of cortical root cells is not related to their
size in ecotypes differing by organ size (Beemster et al.,
2002), and the ploidy of hypocotyl cells can be uncoupled from cell expansion during seed germination
(Gendreau et al., 1998). Ploidy and cell size of maize
endosperm cells have also been shown to vary separately (Vilhar et al., 2002; Leiva-Neto et al., 2004). We
have found only diploid nuclei in grape fleshy tissues
(J.P. Renaudin, unpublished data), as already suggested (Ojeda et al., 1999), but grape mesocarp cells
become almost as large as in ripe tomato pericarp
(Gray et al., 1999; J.P. Carde, unpublished data). Large
and exclusively diploid cells have also been reported
in apple fruit (Malus sp.; Harada et al., 2005). In tomato
fruits of varying size, pericarp ploidy was not modified because of their position in a truss, but a 30%
variation of pericarp cell size was found (Bertin et al.,
2003). An increase of cell volume by 50% to 100%
occurs in tomato pericarp at the breaker stage in the
absence of any ploidy increase (Fig. 3, C and E).
Endoreduplication appears to start a few days prior
to cell expansion in tomato ovary, in a manner similar
to that which occurs in Arabidopsis hypocotyls cells
during germination (Gendreau et al., 1998) and in
Arabidopsis trichomes (Hulskamp, 2004). This and the
previous data are consistent with the hypothesis that
endoreduplication is likely to be a driving regulator
of cell expansion in these materials, although direct
evidence awaits further demonstration. It appears also
clearly that, alternatively, other phenomena are also
able to promote cell expansion. Moreover, one additional function of endoreduplication, notably in fleshy
fruits, could be to enhance cell growth rate, so as to
shorten the duration of fruit growth, or to increase
fruit size.
The contribution of polyploidy to the control of
organ size has long been assumed from the observation of many constitutively polyploid plants (Day and
Lawrence, 2000; Sugimoto-Shirasu and Roberts, 2003),
and much less from developmentally controlled endoreduplication (Lemontey et al., 2000). This study
shows that, in addition to well known parameters
regulating fruit size in tomato, such as carpellar locule
number, the mean ploidy level achieved in pericarp
also correlates with fruit size. This suggests that the
variation of the mean ploidy of the whole fruit
parallels that of the pericarp. Quantitative trait loci
analysis of fruit size in tomato (Causse et al., 2002;
Tanksley, 2004) would be a valuable approach for
identifying some genetic determinants of endoreduplication in this material.
This study provides a framework of pericarp patterning and growth for forthcoming genetic and functional genomic analyses of processes involved in
tomato fruit development and quality. In particular,
we reveal the dramatic extent of cell expansion, and
we propose endoreduplication to play a driving role in
this process in tomato.
MATERIALS AND METHODS
Plant Material
In a first set of experiments, seeds from 20 tomato lines (Solanum
lycopersicon; Table I) were sown in January 2003. Five to eight plants per line
were picked out and grown in the soil of a greenhouse in Avignon. In a second
set of experiments, seeds from Wva106 and Bubjekosoko lines were sown in
pots in January 2004. Five plants from each line were picked out in 25-cm pots
with vermiculite and grown in a greenhouse in Bordeaux. In both experiments, the plants were grown under greenhouse conditions, with average
daily minimal, medium, and maximal temperatures, respectively, of 15°C,
20°C, and 24°C from anthesis (March) to ripening (May). Air relative humidity
was stable at 80% in both places. The plants were watered daily with a nutrient
solution (Algospeed 1 g L21, containing 13N-13P-24K-3Mg 1 oligoelements).
Lateral shoots were removed regularly. Flowers were pollinated with an
electrical bee. In the Avignon experiment, three to seven ovaries at anthesis or
fruits at the transition between green mature and breaker stages were taken
from position two to five of second to fourth truss for each line to perform
cytology and ploidy analyses. In the Bordeaux experiment, three to six ovaries
or fruits were taken at various stages from 0 to 72 DPA, from position two to
five of first to seventh truss for cytology and ploidy analyses.
Cytological Analyses
Ovaries from the 20 lines sampled at anthesis and young fruits of the
Wva106 line were prepared for cytological analysis by a resin-embedding
method. After removal of floral organs, ovaries were cut at equatorial level
and the two halves immersed in 2.5% glutaraldehyde in a phosphate buffer
(0.1 M pH 7.2) for 2 h at room temperature. For the young fruit, an equatorial
slice was excised and cut into fragments less than 4-mm wide before
immersion in the fixative. During fixation, a partial vacuum was applied to
extract intercellular gas. Samples were rinsed, dehydrated through an ethanol
series, and embedded in Technovit 7100 (Kulzer) in 0.5-mL microtubes.
Sections (1–3 mm thick) were made with glass knives on a Reichert 2040
microtome, stained with toluidine blue, and photographed on a Zeiss Axiophot microscope with a Spot digital color camera (Diagnostic Instruments).
In most of the 20 lines, the pericarp thickness of developed fruits exceeded
the width of glass knives. Additionally, since embedding methods are time
consuming and have low throughput, we developed a quick method for
pericarp cytological analysis. Thin pericarp slices (0.3–0.6 mm thick, 1–2 cm
long) were handmade with a razor blade in the fruit equatorial plane, by
avoiding septa, and placed on the surface of a drop of 0.04% toluidine blue.
After 10 to 15 min staining, they were rinsed briefly in water and immersed,
with the colored face turned upside, into a small layer of water in a petri dish.
Pericarp fragments were observed with a Leica FLIII stereomicroscope with
1992
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Copyright © 2005 American Society of Plant Biologists. All rights reserved.
Cell Size and Ploidy in Tomato Pericarp
illumination from above. Images were acquired with a Leica DC300F color
digital camera.
Images acquired with both methods were analyzed with ImagePro-Plus
software (Media Cybernetics). For each fruit, three to 10 portions of pericarp
were analyzed. The number of cell layers from the outer epidermis to the inner
epidermis was estimated in pericarp areas devoid of vascular bundles. The mean
pericarp cell size was estimated using a method similar to that of Cong et al.
(2002). A rectangular area (width 5 1.5 mm, height 5 pericarp thickness 3
80%) was drawn between outer and inner pericarp epidermis and centered in
a zone containing no vascular bundles, as shown in Figure 4C. The mean
pericarp cell size, excluding peripheral zones and vascular bundles, was
calculated by dividing the rectangle area by the number of cells included in it.
Ploidy Analysis
Nuclei were prepared from whole ovaries at anthesis, and from various
tissues of developing fruits by gentle chopping with a razor blade of 0.1–0.2 g
fresh weight in 0.5 mL of Cystain UV ploidy solution (Partec). The suspension
was filtered through a 100 mm nylon mesh and the remaining sample was
reextracted with 0.5 mL of the same solution. The combined filtrates were
analyzed on a Partec PAS-II flow cytometer. Data were plotted on a semilogarithmic scale. Calibration of C values was made with nuclei from young
leaves and ovaries at anthesis, and from the observation of endosperm triploid
nuclei when young seeds were analyzed (data not shown).
Ploidy histograms were quantitatively analyzed with DPAC software
(Partec), after manual treatment to exclude noise. The MCV of each histogram
was calculated as the sum of each C value class weighed by its frequency.
Although this parameter overemphasizes high ploidy levels because of the
exponential increase of DNA content during endoreduplication (Barow and
Meister, 2003), it was retained for comparison with cell size, because
calculation of mean cell size has shown also the same bias toward the largest
cells. Moreover, calculation of cycle value, defined as the mean number of
endoreduplication cycles per nucleus (Barow and Meister, 2003), gave very
similar results (data not shown).
ACKNOWLEDGMENTS
The technical assistance of A.M. Cassalter, J. Leonetti, and V. Rouyère in
growing tomato plants is acknowledged.
Received July 24, 2005; revised September 25, 2005; accepted September 28,
2005; published November 25, 2005.
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