Annals of Botany 87: 101±108, 2001
doi:10.1006/anbo.2000.1309, available online at http://www.idealibrary.com on
Within-bunch Variability in Banana Fruit Weight: Importance of Developmental Lag
Between Fruits
A L E X A N D R A JU L L I E N *{, E R I C M A L EÂ Z I E U X {, N I CO L E MI C H A U X - F E R R I EÁ R E },
M A R C C H I L L E T { and B E R T R A N D N E Y k
{CIRAD-FLHOR, station de Neufchateau 97130 Capesterre Belle Eau, Guadeloupe (FWI), {CIRAD DS AGER,
Av Agropolis (Bat 1) BP5035 34032 Montpellier Cedex 1, France, }CIRAD-BIOTROP, Av Agropolis (Bat 3)
BP5035 34032 Montpellier Cedex 1, France and kINRA INA-PG±Laboratoire d'Agronomie,
F-78850 Thiverval-Grignon, France
Received: 8 June 2000
Returned for revision: 14 August 2000
Accepted: 26 September 2000
Within-bunch (in¯orescence) variability in banana fruit weight is of great importance: distal fruits (at the bottom of
the bunch) are 30 to 40 % smaller than basal fruits at the top. We hypothesize that this variability is related to a
developmental lag between fruits. To validate this hypothesis, histological studies (evolution in number of cells along
the fruit radius, starch granule number and size) associated with physiological measurements ( pulp dry weight, dry
matter and starch concentration) were carried out. Fruit development stages were dated in cumulative degree-days
(dd) from ¯ower emergence to 3 weeks after the harvest stage (1300 dd). For a fruit located at the top of the bunch,
cell divisions ceased around 350 dd and cells began to ®ll with starch as soon as they appeared. A developmental lag
between fruits at the top and bottom of the bunch was observed: cell divisions started and stopped approx. 70 dd later
in bottom (distal) compared to top (basal) fruits. At the end of cell divisions, basal fruits had a higher number of cells
along the fruit radius. This di€erence in cell number may be due to increased competition for assimilates between
fruits when cell division occurs in distal fruits. Variability in cell number may be related to variability in pulp dry
weight. We conclude that within-bunch variability in banana fruit weight is related to a di€erence in cell number
# 2001 Annals of Botany Company
and age.
Key words: Musa acuminata, banana, fruit development, fruit growth, cell number, starch accumulation, fruit
quality, fruit green-life, fruit-fruit competition.
I N T RO D U C T I O N
Within-bunch (in¯orescence) variability in banana fruit
weight is due to a negative gradient in fruit weight from the
top (basal) to the bottom (distal) of the bunch (LassoudieÁre
and Maubert, 1971; LassoudieÁre, 1972). Fruit at the bottom
of the bunch is 30 to 40 % smaller than that at the top
(Robinson, 1996), and this gradient contributes to yield
variability as the whole bunch is harvested at the same time.
This variability is a disadvantage for banana growers
because fruit weight and size are important commercial
criteria for exported bananas. To reduce this variability we
®rst need to understand and explain its causes. The bunch is
a raceme on which fruits are organized in clusters called
`hands'. Hands are arranged helicoidally around a central
axis called the `stalk'. Our ®rst hypothesis to explain the
fruit weight gradient is that the upper (basal) hands are in a
favoured position in the photosynthetic pathway [assimilates pass through the central stalk from top (basal) to
bottom (apex)] and, consequently, the growth of the lower
fruits is limited by carbon supply. Another hypothesis is
that the basal hands that are initiated ®rst in the reproductive meristem (Ganry, 1980) maintain their lead over the
lower hands throughout development and growth. The
* For correspondence. Fax: 05 90 86 80 77, e-mail [email protected]
0305-7364/01/010101+08 $35.00/00
objective of this paper is to test this second hypothesis by
studying the chronology and duration of fruit development
phases in relation to their position on the bunch.
Cell division intensity and duration are important
processes in yield determination as they determine cell
number. Coombe (1976) emphasized the importance of the
cell multiplication stage in weight increase for ¯eshy fruits.
In legumes like soybean, seed ®lling rate is correlated with
seed cell number that is ®xed before the beginning of seed
®lling (Munier-Jolain, 1994; Munier-Jolain and Ney, 1998).
Gleadow et al. (1982) and Jones et al. (1985) have shown
that, in wheat and maize, respectively, endosperm cell
number and also starch granule number per cell are
important variables in grain weight. In our study, banana
fruit development was characterized by changes in pulp cell
number, starch granule number per cell (SGN) and starch
granule length (SGL). These histological observations were
supported by physiological measurements ( pulp dry matter,
starch and total sugar concentration and green-life) to
characterize fruit quality and maturity at harvest.
The dessert banana is a parthenocarpic fruit. Histological
studies [Ram et al. (1962) on the Musa spp AAA group
`Gros Michel' (Cavendish subgroup) and Fahn and Kotler
(1972) on `Grande Naine'] showed that cell division takes
place in the innermost portion of the pericarp between the
second and fourth week after bunch (in¯orescence)
# 2001 Annals of Botany Company
102
Jullien et al.ÐWithin-bunch Variability in Banana Fruit Weight
emergence (ABE). According to Ram et al. (1962), starch
synthesis begins around the fourth week ABE. Studies on
fruit development and growth were also carried out by
LassoudieÁre and Maubert (1971) on Musa spp AAA group
`Poyo' (Cavendish subgroup) in the Ivory Coast and by
Barnell (1940) on `Gros Michel'. In broad terms (Robinson,
1996), fruit growth is due to cell multiplication from ÿ20 to
‡30 d ABE, then to cell elongation and ®lling from 30 to
85 d ABE. Fruit maturation begins 85 d after ABE.
In this study, the development of a reference fruit in the
bunch and the possible developmental lag between basal
and distal fruits on the same bunch were analysed.
Development stages were de®ned in cumulative degreedays from in¯orescence emergence.
M AT E R I A L S A N D M E T H O D S
Growing conditions
Field experiments were conducted with Musa spp AAA
group `Grande Naine'. Three plots (NEUF1, NEUF2 and
NEUF3) were planted in the Neufchateau area, Guadeloupe, French West Indies (168 N, 628 W, altitude 250 m,
annual rainfall 3500 mm). Plants raised from tissue culture
were planted on 15 Jun. 1997 (NEUF1), 22 Jun. 1998
(NEUF2) and 3 Jul. 1999 (NEUF3). Plant population
density was 1800 plants ha ÿ1 in NEUF1 and NEUF2 and
2240 plants ha ÿ1 in NEUF3. A ®rst group of plants at the
same developmental stage (in¯orescence emergence) was
selected in February 1998 (NEUF1), February 1999
(NEUF2) and March 2000 (NEUF3). Of these plants,
only those with eight hands and an equivalent number of
fruit per hand were retained after the bracts covering the
hands had lifted. Hands were numbered from top to
bottom (hand 1: top of the bunch, hand 8: bottom of the
bunch).
Daily thermal time was calculated using 148C as a base
temperature (Ganry and Meyer, 1975). The mean daily air
temperature was calculated by averaging the hourly
temperature recorded by a meteorological station located
on the experimental site. Fruit age was expressed in thermal
time calculated from in¯orescence emergence and expressed
in degree-days (dd).
Fruit sampling
Fruits of the same bunch were all harvested at the same
time on each sampling date. Fruits on a hand are organized
in two rows: an internal row (nearest the stalk) and an
external row. Samples were always taken from the external
row of the hand. In NEUF1, fruits were sampled at regular
intervals from in¯orescence emergence (week 1) to 3 weeks
after the `harvest stage'. The harvest stage is when a
diameter of 34 mm is reached by the reference fruit in the
bunch (the fruit located in the middle of the external row of
hand 4). Samplings were made weekly at the beginning
(weeks 1±4) and end (weeks 14±18) of the cycle. In between,
fruits were sampled every 2 weeks. Each sampling was made
on a di€erent group of ®ve bunches or replicates. In
NEUF2, fruit age was measured in degree-days for sample
fruits at a developmental stage corresponding to weeks 5, 6
and 7 of the NEUF1 experiment. In NEUF3, fruits were
sampled in week 1, then twice a week from weeks 2 to 4 and
®nally once a week until week 8.
Changes in pulp fruit weight (NEUF1)
At each sampling date, a reference fruit (the middle fruit
of the external row) was harvested on hands 1 and 7 of each
bunch and the fresh and dry weight of peel and pulp were
measured. Fruits were dried in a ventilated drying room at
808C (+18C).
Histological observations (NEUF1, NEUF2 and NEUF3)
In NEUF1, the fruit adjacent to the reference fruit was
harvested on hands 1 and 7 on one of the ®ve bunches.
Fruit sections were made in weeks 1±5, 8, 14 and 18 of the
experiment. Transverse sections were taken from the middle
of the fruit for weeks 1 to 8, and longitudinal sections for
weeks 14 and 18. The portion excised was placed in 25 %
glutaraldehyde : 10 % paraformaldehyde ®xative solution
with a phosphate bu€er ( pH 6.8), kept for 20 min in a
vacuum ¯ask and then for 48 h at 48C. Samples were then
stored in 70 % ethyl alcohol. After dehydration in a series
of alcohol baths (70 to 100 %) and ®xation in KLB resin,
samples were cut into 3 mm slices with a microtome. Slides
were then treated with double colouration PAS-Naphtol
Blue Black. The PAS reaction stains polysaccharides red
(walls and reserve starch) and Naphtol Blue Black
speci®cally stains soluble and reserve proteins blue. In
NEUF2 and NEUF3, transverse sections were taken from
the reference fruit of hands 1 and 7 at each sampling date
using the same method.
The pulp initiating cells described by Ram et al. (1962)
could be seen in transverse sections in our experiment
(Fig. 1). This tissue surrounds the carpel cavity and is made
up of the inner epidermis of the carpel and the three to ®ve
adjacent cell layers (Fig. 1A). We counted the number of
new cell layers initiated by this tissue from weeks 1 to 8
(NEUF1, NEUF2 and NEUF3), henceforth termed `cell
number along the fruit radius' (CNFR). We also determined the mitotic index of the pulp (NEUF1 and NEUF2),
de®ned as the ratio of dividing nuclei to the total number of
nuclei observed in the pulp section. Mitotic ®gures were
observed and counted. The total number of nuclei was
estimated by the number of nuclei counted on ten clusters
of 20 cells displayed on the whole pulp. Counts were
repeated on three successive sections of the same sample.
To characterize cell ®lling, starch granule number per cell
(SGN), starch granule length (SGL) and width were
measured on all sections (NEUF1 and NEUF2). SGN
and SGL were always determined on the peripheral pulp
cells. Cell counting and SGN and SGL determinations were
made on fruit sections for hands 1 and 7 with ®ve
replications at three di€erent points in the pulp of a given
section and repeated on three successive sections of the
same pulp sample.
NEUF1 and NEUF2 plots had the same plant population density (1800 plants ha ÿ1) and in¯orescence emergence
Jullien et al.ÐWithin-bunch Variability in Banana Fruit Weight
103
F I G . 1. Transverse section of a banana carpel of hand 1 (most basal) at in¯orescence emergence. A, The peel. vb, Vascular bundle; lc, latex cells.
B, The aerenchyma. C, The carpel cavity and pulp initiating cells. cc, Carpel cavity; o, ovule; vb, vascular bundle; a, aerenchyma; pic, pulp
initiating cells.
Changes in pulp composition and fruit maturity at harvest
(NEUF1)
At each sampling date in NEUF1, a third fruit was also
harvested on hands 1 and 7 for pulp composition analysis.
The pulp was lyophilized. Starch and total sugar content
were determined in the CIRAD-AMIS laboratory at
Montpellier, France. During weeks 14±18, a fourth fruit
per hand was sampled to determine green-life (GL). GL is
the number of days from fruit harvest to the beginning of
the climacteric rise, characterized by a large increase in fruit
respiration rate. GL is an indicator of the degree of fruit
immaturity at harvest and of its storage potential (Peacock
and Blake, 1970) and was measured using the method
described by Chillet and de Lapeyre de Bellaire (1996).
Statistical analysis
To compare means, Newman-Keuls tests at the 0.05
probability level were performed using STATITCF software
(STAT-ITCF5.0, 1991). Gompertz curves were ®tted to the
data using the Least Squares method.
R E S U LT S
Characterization of the within-bunch variability in pulp dry
weight
Pulp dry weight (PDW) increased from 200 dd for hand 1
and followed an S-shaped curve against thermal time
(Fig. 2). From 0 to 350 dd the dry matter accumulation rate
was low. By 350 dd, PDW had reached 9 % of its maximum
value. From 350 dd to the harvest stage (1030 dd), the
PDW increase curve can be considered linear. After the
harvest stage, PDW still increased, but the rate of increase
slowed. The increase in PDW started at the same time for
hands 1 and 7, but the rate was greater for hand 1. At the
50
45
40
35
PDW (g)
date (February). We thus considered that fruit development
in these two plots was equivalent. The plant population
density for NEUF3 was 2240 plants ha ÿ1 and in¯orescences
emerged in March. As fruit development may be di€erent,
results from NEUF3 are treated separately from those of
NEUF1 and NEUF2.
30
25
20
15
10
5
0
0
350
700
1050
1400
dd since inflorescence emergence
F I G . 2. Time course of changes in pulp dry weight (PDW, NEUF1) in
hand 1 (j) and hand 7 (h). The S-shaped curves of PDW changes are
those of the ®tted Gompertz equations: y ˆ Mexpfÿexp‰ÿa…x ÿ b†Šg
where M is the maximal value of y and b the abscissa at in¯exion point.
For hand 1: M ˆ 48, a ˆ 0.0025, b ˆ 753. For hand 7: M ˆ 37,
a ˆ 0.0022, b ˆ 771. Points are the mean + s.e. of ®ve fruits. dd,
Degree days. Error bars represent standard deviation.
harvest stage the di€erence in PDW between hands 1 and 7
was 8 g (P 5 0.05).
Changes in cell number along the fruit radius
As expected, changes in cell number along the fruit
radius (CNFR) followed the same pattern in NEUF1 and
NEUF2 (Fig. 3). On the other hand, changes in CNFR in
NEUF3 had a di€erent pattern. For hand 1 in NEUF1 and
NEUF2, CNFR remained constant and equal to 5 from 0
to 70 dd. Then CNFR increased signi®cantly (P 5 0.05)
from 70 to 350 dd. After 350 dd, no signi®cant increase in
CNFR occurred. In NEUF3, the increase in CNFR started
later (140 dd) but was again not signi®cant after 350 dd.
The maximal CNFR reached in NEUF3 was lower (55 + 7)
than in NEUF1 and NEUF2 (72 + 5). For hand 7, changes
in CNFR followed the same pattern as for hand 1 but still
increased signi®cantly after 350 dd in NEUF1, NEUF2 and
NEUF3. In NEUF3, the increase in CNFR was not
signi®cant after 420 dd. CNFR was signi®cantly lower in
104
Jullien et al.ÐWithin-bunch Variability in Banana Fruit Weight
60
CNFR
50
40
30
20
10
0
0
70
140
210 280 350
420 490
560
80
CNFR
60
40
Cell ®lling (Fig. 3)
20
0
0
350
700
1050
1400
0
350
700
1050
1400
20
SGN
16
12
8
4
0
60
Three phases of development could be distinguished for
SGN: (1) from 0 to 70 dd there was no change in SGN; (2)
from 70 to 350 dd SGN increased, reaching a mean value of
11 + 3 granules per cell in hand 1; and (3) from 350 dd
SGN was constant. For hand 7, the pattern of change in
SGN was the same but the maximal value reached was
higher (15 + 3).
For SGL, the three phases of development observed for
hand 1 were (Fig. 3): (1) from 0 to 200 dd there was no
change in SGL; (2) from 200 to approx. 600 dd SGL
increased rapidly; and (3) after 600 dd SGL stabilized at
approx. 50 + 2 mm. For hand 7, the pattern of change in
SGL was the same. In NEUF2, there was no signi®cant
di€erence in SGL between hands 1 and 7. In NEUF1, SGL
was signi®cantly lower in hand 7 than in hand 1 until
1000 dd. After this time, SGL was equivalent for hands 1
and 7. It seems that cells in hand 1 stopped ®lling at approx.
600 dd and cells in hand 7 reached their maximal SGL
later.
Variation in within-fruit ®lling (Fig. 4)
Not all the cells in the fruit were ®lled the same way. At
500 dd (middle of ®lling phase), we observed a gradient in
starch content between the periphery and the centre of the
pulp: for hand 1, peripheral cells contained a few big starch
SGL (µm)
40
20
0
hand 7 than in hand 1 after 150 dd in NEUF1 and NEUF2
and after 200 dd in NEUF3.
Gompertz equations were ®tted to the data (Fig. 3).
According to these equations, the delay between curves of
CNFR changes was estimated to be 50 dd in NEUF1 and
NEUF2 and 20 dd in NEUF3. Cell division rate was
calculated by di€erentiation of the Gompertz equation.
Maximal cell division rate was found to be higher in hand 1
(0.26 in NEUF1 and NEUF2, and 0.28 in NEUF3) than in
hand 7 (0.18 in NEUF1 and NEUF2, and 0.22 in NEUF3).
Changes in the mitotic index con®rmed (1) the existence
of a lag between hand 1 and 7 at the start of cell division,
and (2) the di€erence in cell division rate between hands 1
and 7. At 70 dd the mitotic index was zero for both hands.
At 140 dd, the mitotic index was 0.015 + 0.004 for hand 1
and zero for hand 7. At 200 dd, the index was close to zero
for hand 7 (0.01 + 0.005) and signi®cantly lower for hand 1
(0.027 + 0.013). After 280 dd, the mitotic indexes were
equivalent in hands 1 and 7.
0
350
700
1050
dd since inflorescence emergence
1400
F I G . 3. Quantitative histological changes in banana pulp: time courses
of changes in cell number along the fruit radius (CNFR), starch
granule number (SGN) and starch granule length (SGL). Hand 1
NEUF1 (j); Hand 7 NEUF1 (h); Hand 1 NEUF2 (d); Hand 7
NEUF2 (s); Hand 1 NEUF3 (m); Hand 7 NEUF3 (n). NEUF 1:
1997 experiment; NEUF2: 1998 experiment; NEUF3: 1999 experiment.
The S-shaped curves of cell number changes are those of the ®tted
Gompertz equations: y ˆ 5 ‡ Mexpfÿexp‰ÿa…x ÿ b†Šg: NEUF1 and
NEUF2: Hand 1: M ˆ 72, a ˆ 0.0099, b ˆ 233. Hand 7: M ˆ 67,
a ˆ 0.0074, b ˆ 282. NEUF3: Hand 1: M ˆ 50, a ˆ 0.015, b ˆ 220.
Hand 7: M ˆ 38, a ˆ 0.016, b ˆ 240. Error bars represent standard
deviation of the population. dd, Degree days.
Jullien et al.ÐWithin-bunch Variability in Banana Fruit Weight
50
19
45
17
30
25
13
20
11
15
10
9
5
Fruit
centre
Middle
Fruit
periphery
0
Pulp dry matter concentration
(g g–1)
35
SGL (µm)
SGN
0.4
40
15
7
105
0.25
0.2
0.15
0.1
0.05
Fruit
centre
Fruit
middle
Fruit
periphery
Hand 1
Mean starch volume per cell
s.e.
554
591
2434
1305
26 868
18 440
Hand 2
Mean starch volume per cell
s.e.
90
96
2074
1171
8260
3407
Pulp physiological composition and fruit maturity at harvest
(Fig. 5)
Changes in pulp dry matter concentration (PDMC) over
time followed an S-shaped curve. For hand 1, changes in
PDMC followed the same pattern as SGL: from 0 to 200 dd
700
1050
1400
0
350
700
1050
1400
350
700
1050
1400
70
60
50
40
30
20
10
3.5
Pulp total sugar content
(% of lyophilized pulp weight)
T A B L E 1. Heterogeneity in cell starch volume (mm3) in
banana fruit pulp at 500 dd (NEUFI)
350
80
0
where w represents starch granule width. It appeared
(Table 1) that starch volume per cell was more important
(P 5 0.05) in peripheral cells than in central cells for both
hands. By 500 dd, peripheral cells, but not central cells, in
hand 1 fruits had reached their maximal starch volume.
0
90
Pulp starch concentration
(% of lyophilized pulp weight)
SGL 2 w 2pSGN
2
3
2
0.3
0
F I G . 4. Heterogeneity in cell starch content in the fruit pulp at 500 dd
(NEUF1). SGN hand 1 (j); SGL hand 1 (d); SGN hand 7 (h); SGL
hand 7 (s). Error bars represent standard deviation of the population.
SGL, Starch grain length on a section; SGN, starch grain number per
cell.
granules (9 + 3 granules, 41 + 4 mm long) whereas central
cells contained many small granules (16 + 1 granules,
10 + 5 mm long). The same gradient was observed for
hand 7.
These data suggest that there may be a trade-o€ between
SGL and SGN in the fruit. Assuming that starch granules
are spheroids, we calculated the mean starch granule
volume per cell using the equation:
0.35
3
2.5
2
1.5
1
0.5
0
0
dd since inflorescence emergence
F I G . 5. Changes in pulp physiological characteristics (NEUF1):
time courses of changes in pulp dry matter concentration (PDMC),
pulp starch concentration and pulp total sugar concentration. Hand 1
(j); hand 7 (h). The S-shaped curves of PDMC changes are those of
®tted Gompertz equations: y ˆ 0.08 ‡ Mexp{ÿexp[ÿa(xÿb)]}. For
Hand 1: M ˆ 0.22, a ˆ 0.0086, b ˆ 315. For Hand 7: M ˆ 0.22,
a ˆ 0.0073, b ˆ 345. Error bars represent standard deviation. dd,
degree days.
106
Jullien et al.ÐWithin-bunch Variability in Banana Fruit Weight
there was only a small increase in PDMC. From 200 to
500 dd PDMC increased rapidly. After 500 dd the rate of
PDMC increase slowed and PDMC stabilized after approx.
700 dd. After the harvest stage (1030 dd), PDMC
decreased. Changes in PDMC followed the same pattern
for hand 7. At 350 dd there was a signi®cant di€erence in
PDMC between the two hands, but from 500 dd to the
harvest stage (1030 dd) it was no longer signi®cant.
Gompertz equations were ®tted to the data.
Pulp starch concentration (PSC) started to increase
rapidly from 70 until 350 dd, in accordance with histological observations of changes in SGN. From 350 until
600 dd, the rate of PSC increase slowed down and PSC
stabilized at approx. 700 dd. The di€erence between hands
1 and 7 was signi®cant at 140 and 200 dd but not from
350 dd to the harvest stage. The fall in pulp sugar
concentration corresponded with the increase in starch
concentration. Pulp sugar concentration increased from 0
to 70 dd then decreased and stabilized at 0.5 % of
lyophilized matter at around 700 dd.
There was no signi®cant di€erence in fruit GL between
hands 1 and 7 from 1030 to 1300 dd. After 1030 dd, fruit
GL decreased with fruit age according to an exponential
relation: GL ˆ 348.17exp(ÿ0.0022x), r2 ˆ 0.96, where x is
the fruit age at harvest expressed in cumulative degree-days
from in¯orescence emergence. At 1030 dd, the mean GL
was 34 d, at 1300 dd mean GL was 20 d.
DISCUSSION
Within-bunch (in¯orescence) variability in banana fruit
development
We hypothesized that the di€erence in age between fruits
observed at the initiation stage was maintained throughout
development and growth. Our data con®rm this hypothesis.
Di€erent developmental phases were distinguished and
described for a hand 1 fruit (Table 2); until approx. 350 dd,
pulp cell number increased. Each cell produced follows the
same developmental pattern as described for hand 1 fruit
peripheral cells: from 70 to 350 dd, SGN increases; from
200 to approx. 600 dd, starch is accumulated and SGL
increases. According to our results, cell division began and
stopped later in hand 7 than in hand 1. The developmental
lag between hands 1 and 7 was estimated to be approx. 20
to 70 dd at the beginning of cell division and was observed
at each stage of development: there was a lag between hands
1 and 7 for SGN, SGL, PSC and PDMC curves. At a given
date: (1) fruit pulp in hand 1 contains more cells than that
of hand 7; and (2) the oldest cells in hand 1 are in a more
advanced stage of development than those of hand 7. At
T A B L E 2. Chronology and duration of di€erent development phases of a peripheral pulp cell in hands 1 and 7 in relation to
changes in pulp composition (SGN and SGL)
Fruit age (dd from in¯orescence emergence)
Variable
PDW
Hand
1
0
70
200
350
500
600
1030
Result at harvest
PDW1 4 PDW7
7
CNFR
1
CNFR1 4 CNFR7
7
SGN
1
SGN1 5 SGN7
7
SGL
1
SGL1 ˆ SGL7
7
PDMC
1
PDMC1 ˆ PDMC7
7
PSC
1
PSC1 ˆ PSC7
7
CNFR, Cell number on a fruit radius; SGL, starch grain length on a section; SGN, starch grain number per cell; PDMC, pulp dry matter
content; PSC, pulp starch concentration; PDW, pulp dry matter.
Jullien et al.ÐWithin-bunch Variability in Banana Fruit Weight
600 dd, the oldest cells at the periphery of the pulp of hand
1 are ®lled. From 600 to 1030 dd, SGL still increases in
younger cells and homogenization in cell ®lling occurs
progressively. At harvest, pulp dry matter and starch
concentration are the same in hands 1 and 7. There was
also no signi®cant di€erence in fruit green-life between
hands 1 and 7 from 1030 to 1300 dd. The possible
di€erence in green-life between fruits before 1030 dd was
not evaluated but this result corroborates the fact that the
di€erence in age between fruits is reduced during growth.
Turner and Rippon (1973) have shown that the relationship between green-life and fruit age at harvest expressed in
number of days varies with the season and year. According
to our results, fruit green-life correlates well with bunch age
expressed in degree-days accumulated since in¯orescence
emergence. This is an interesting indicator as it allows us to
take into account variations in air temperature. This
indicator was calibrated for fruits older than 1030 dd. It
should be also tested for fruits younger than 1030 dd and
for di€erent growing conditions.
At harvest, the number of cells along the fruit radius was
higher in hand 1 than in hand 7. This di€erence may be
explained by a di€erence in assimilate availability during
cell divisions. When cell division starts in fruits on hand 1,
competition for assimilates is low as only hand 1 fruits are
undergoing cell division. On the other hand, when cell
division starts in fruits on hand 7, all fruits in the bunch are
in the cell division phase, hence competition for assimilates
is increased and cell division may be limited by assimilate
availability. Such a scheme was shown for maize by Reddy
and Daynard (1983): tip kernels had a reduced number of
cells because of the domination of basal kernels that started
cell division earlier and became stronger sinks. The e€ect of
assimilate availability on cell division was also shown for
wheat by Brocklehurst (1977).
Intra-fruit variability in cell ®lling
Cell division and cell ®lling with starch occur simultaneously in the same fruit. Each cell, once initiated, begins
to ®ll with starch. During fruit growth, this cell is pushed to
the pulp periphery (cell division is centrifugal). Peripheral
cells, that are also the older ones, start accumulating starch
(cell ®lling is centripetal). During starch accumulation,
starch granules grow and may fuse. Peripheral cells will thus
contain fewer, but larger, starch granules. Starch granule
number per cell and starch granule size depend on the
distance of the cell from the centre of the fruit. At approx.
600 dd, the oldest cells at the pulp periphery of hand 1 have
maximal SGL. At this time, younger cells continue to
develop and ®ll with starch. In fact, physiological changes
in pulp composition result from the developmental lag of
cells of di€erent ages. Maximal values of PDMC and PSC
are reached at approx. 700 dd and remain constant until
1030 dd. At this time there is a fall in PDMC. This decrease
in PDMC was also observed by Barnell (1940) 100 d after
¯ower emergence. This decrease was shown to be related to
fruit maturation processes. Our data do not show an
increase in pulp sugar nor a decrease in pulp starch
concentration observed by that author at this stage. Barnell
107
(1940) also observed starch hydrolysis from 85 d after
¯ower emergence. We did not identify starch hydrolysis in
our histological study and could not determine a time of
`beginning of starch hydrolysis' in the oldest cells. We thus
could not relate the fall in PDMC or the changes in fruit
green-life to histological changes such as starch hydrolysis.
Relationship between fruit development and within-bunch
variability in fruit weight
According to our results, fruit from hand 1 has a higher
pulp dry weight, a larger number of cells, an equal starch
granule length and a lower starch granule number per cell
than fruit from hand 7 (Table 2). This indicates that pulp
dry weight and cell number are positively related. The
importance of cell number in ®nal weight determination has
been demonstrated for other fruit such as apple (Denne,
1960; Westwood et al., 1967), apricot (Jackson and
Coombe, 1966) and grape (Harris et al., 1968). In peach,
Scorza et al. (1991) showed that the di€erence between
large- and small-fruited peaches is related more to a
di€erence in number than size of mesocarp cells. Our
study con®rms the role of pulp cell number in fruit weight
determination for banana. In other studies by Gleadow
et al. (1982) and Jones et al. (1985) on wheat and maize,
respectively, the number of starch granules per cell was
shown to be positively related to grain weight. For banana
fruit, number of starch granules per cell may not be a good
estimator of fruit weight because granules seem to fuse
during fruit growth.
We conclude that the di€erence in weight between upper
(basal) and lower (distal) banana fruits within the bunch
may be due to a di€erence in cell number and age. Ablation
experiments, where only lower hands are left on the bunch
either at the beginning of cell division or after the end of cell
division would allow us to con®rm this scheme and to
better characterize source-sink relationships in the bunch.
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