Annals of Botany 80 : 533–538, 1997
The Development of Tomato Root System in Relation to the Carbohydrate Status
of the Whole Plant
E. P R E S S M AN*†, A. B A R-T A L‡, R A C H E L S H A K ED* and K A T E R I N A R O S E N F E LD*
* Department of Vegetable Crops and ‡ Department of Soils and Water, ARO, The Volcani Center,
Bet Dagan 50250, Israel
Received : 17 September 1996
Accepted : 27 June 1997
The decrease in growth rate of the root system or complete cessation of its growth in developed, fruit-bearing tomato
plants are known phenomena. It has been suggested that a limited supply of carbohydrates to this organ, due to its
relative weakness in competition with the flowers and developing fruitlets is the main cause for these disorders. This
theory was tested in the present study with plants grown in an aerohydroponic system up to the appearance of 12–13
trusses per plant, 172 d after transplanting. The changes in the contents of carbohydrates in the various organs during
this period were monitored. The concentrations of soluble sugars and starch in the leaves increased with the increase
in truss number. The upper stem was found to contain more carbohydrates than the lower stem, while no significant
changes in the concentration of these compounds could be detected in the roots throughout the experiment.
Nevertheless, 120–130 d after transplanting, the roots of the plants, bearing five to six trusses and two to three
inflorescences, ceased growing and remained at the same or a slightly reduced size for another 40–50 d. Calculations
show that at the stage of five to six trusses, 38 g total soluble sugars and 35 g starch were stored in the vegetative
organs. Therefore, it seems unlikely that carbon deficiency caused by the competition with the reproductive organs
(mainly developing fruits), affected the root growth. Instead, it is suggested that some other factor is responsible.
# 1997 Annals of Botany Company
Key words : Lycopersicon esculentum Mill, carbohydrates, root growth rate, sink-source relationship, soluble sugars,
starch.
INTRODUCTION
The development of tomato roots is characterized by linear
growth during the vegetative phase. Upon flowering, and
especially during fruit set and development, the root
extension rate has been found to decline (Gasim and Hurd,
1986). Hurd, Gay and Mountfield (1979) observed root
growth cessation and some root death 4 weeks after anthesis ;
they suggested that the fruit grows in competition with the
vegetative organs, and that root growth was affected to a
greater extent. Leonard and Head (1958) showed that a
reduction in total length, caused by rapid death and
disappearance of roots, occurred when the plants bore
50–75 fruits per plant. Ho (1988) concluded that the sink
strength of the inflorescence increases from the flowering to
the fruiting stage, and that during fruiting of the tomato
plant the fruits have the highest sink strength and the roots
have the lowest. On the other hand, Hocking and Steer
(1994) reported that the importance of the root as a strong
sink declined as early as the time when the plant reached the
nine-leaf stage. Moreover, growing tomato plants of several
genotypes under high CO caused a marked increase in
#
starch content of the leaves (Tripp et al., 1991 a) ; but even
under these conditions of a CO -enriched atmosphere, a
#
reduction in root mass was detected in plants of all genotypes
(Tripp et al., 1991 b).
Therefore, in the present work changes in root devel† For correspondence.
0305-7364}97}100533­06 $25.00}0
opment during vegetative and reproductive phases were
monitored and were correlated with changes in carbohydrate
contents in the main vegetative organs. Calculations of the
total carbon pool show that it exceeded the demand by the
developing fruits.
MATERIALS AND METHODS
Plant material
Tomato plants (Lycopersicon esculentum Mill., cv. F121)
were grown in an aerohydroponic system in a unheated
glasshouse at Bet Dagan (Feigin et al., 1984). The minimum
and maximum temperatures throughout the experiment
(November 1992 to April 1993) were 10³2 and 21³2 °C,
respectively. The aerohydroponic system consisted of two
separate polystyrene, 50¬29¬20-cm boxes, mounted on a
140 l covered container. Roots were continuously exposed
to nutrient solutions which were circulated by a pump and
plastic tubes with small holes through which the solution
was ejected. The nutrient solution composition has been
described previously (Bar-Tal et al., 1994). The plant main
stems were supported by vertical threads and the side shoots
were removed.
Analysis of carbohydrates
Carbohydrate measurements were performed according
to Schaffer et al. (1987). A leaflet was sampled from the first
bo970485
# 1997 Annals of Botany Company
Pressman et al.—Carbon Content and Tomato Root DeŠelopment
Root measurements
Root volume was determined using a calibrated cylinder
into which the entire root system was placed and to which
water was added to the height of a mark. The difference
between the water quantity required to fill the cylinder up to
the mark and the cylinder volume below the mark equalled
the root system volume.
Growth curŠe
A Gompertz function was fitted to the root growth data
(for details see Bar-Tal et al., 1994).
RESULTS
Root growth
Three major phases in the root development are shown in
Fig. 1. The initial phase, lasting about 40 d, with a relatively
small increase in volume, despite a high relative growth rate
2000
0.80
1500
0.60
1000
0.40
500
0.20
0
40
80
120
160
Days after transplanting
RGR (d–1)
3
leaf above each of the trusses numbered 2, 5, 8 and 11. Each
leaf was sampled three times : first at the stage of flowering
and beginning of fruit set of the truss next to it ; then,
concomitantly with the first sampling of the leaf above the
next indicated truss, when that was at the same stage of
development ; and again together with the leaf above to the
subsequent indicated truss. All samplings were carried out
at noon. Roots (1 g per sample) were sampled concomitantly
with the first sampling of each leaf and were patted dry on
tissue paper. Samples from four locations along the stem,
next to trusses 2, 5, 8 and 11, were taken at the termination
of the experiment, 172 d after transplanting. The sampled
tissues were extracted five times in 80 % EtOH and, after
evaporation, reducing sugars and sucrose were measured in
the soluble fraction. Reducing sugars were measured using
dinitrosalicylic acid, according to Miller (1959). Sucrose
was measured using anthrone according to Van Handel
(1968) and, after amyloglucosidase treatment, starch was
measured with anthrone in the insoluble fraction (Schaffer
et al., 1985). Diurnal cycles in soluble sugar and starch
contents were detected in discs, 1 cm in diameter, sampled
from the leaves indicated in Fig. 5, and at the times
indicated. The uppermost truss (number 10) was at the stage
of anthesis and early stages of fruit set.
To study the carbohydrate status in the leaves next to the
upper trusses and in the stems of the side shoots, plants of
two cultivars (522 and 144) were grown in 101 buckets
containing volcanic ash (tuff). When the thirteenth inflorescence began to flower, truss number 11 was at the stage of
fruit set or fruitlet development. At that stage, in half of the
plants, two out of three leaves of the main stem were
removed, leaving the leaf above the truss. Two or three side
shoots were left on the upper part of the plant, of which one
third of the leaves were left. At various dates after the
treatments, leaflets of the leaf next to truss number 11 were
sampled for analysis of carbohydrates. On the last sampling
date, the stems of the side shoots were also sampled for the
same purpose.
Root volume (cm )
534
0.00
200
F. 1. The calculated (solid line), measured (E), and relative (broken
line) growth rates (RGR) of a tomato root system grown in an
aerohydroponic system.
(RGR), was followed by a second phase of 100 d, with a
rapid increase in volume, and a third phase, starting 138 d
after transplanting which was characterized by zero growth
and even some reduction in the root volume. The relative
growth rate was derived from the calculated growth curve.
Content of carbohydrates
Data in Fig. 2 show a constant increase in total sugars
and starch concentration with increasing truss number at
the first sampling of each leaf. This sampling took place at
anthesis and the beginning of fruit set in the relevant truss.
Lower carbohydrate contents were found in the following
two samplings of each leaf, which took place during fruit
growth and maturation.
Root samples were taken concomitantly with the first
sampling of each leaf to analyse carbohydrate concentrations. Except for a small increase in carbohydrate content
from the first sampling to the second, no significant changes
in either total sugars or starch content could be detected in
the roots throughout the experiment (Fig. 3).
The differences in the total sugar content at different
points along the stem resembled those of the leaves. Figure
4 shows that the total sugar content was inversely related to
the stem age. Thus, younger (upper) parts contained more
sugars than older parts of the stem. On the other hand,
similar concentrations of starch were detected at different
points along the stem.
Significant diurnal changes in total sugars (Fig. 5 A) and
starch (Fig. 5 B) content could be detected mainly in the
younger leaves next to the upper trusses. In these leaves, the
sugars accumulated towards noon, while starch accumulation took place in the afternoon. During the night, these
leaves lost approximately one third of their daytime maximal
sugar and starch contents.
Calculations of the amounts of either total sugars or
starch in the leaves next to the succeeding trusses along the
Carbohydrates content (mg g–1 f.wt)
Pressman et al.—Carbon Content and Tomato Root DeŠelopment
535
40
35
30
25
20
15
10
5
0
1
2
2
3
1
2
3
1
5
Truss number
2
8
3
1
11
2
0.8
7
6
Total sugars content (mg cm2)
Carbohydrates content (mg g–1 f.wt)
F. 2. The concentration of total sugars (*) and starch (+) in tomato leaves positioned next to the indicated trusses along the plant. Each leaf
was sampled three times (indicated as 1, 2 and 3), except for the last one (only sampled twice).
5
4
3
2
1
0
2
5
8
Truss number
11
0.4
0.2
6
2
Starch content (mg cm2)
Carbohydrates content (mg g–1 f.wt)
30
0.6
0
F. 3. The concentrations of total sugars (*) and starch (+) in the
roots of tomato plants. Samples were taken concomitantly with the first
samplings of the leaves as indicated in Fig. 2.
40
A
10
14
18
6
10
14
Hours
18
6
B
1.5
1
0.5
20
0
10
0
6
F. 5. Diurnal changes in total sugars (A) and starch (B) contents in
tomato leaves next to trusses no. 2 (U), 4 (D), 6 (*), 8 (E) and 10 (+).
2
5
8
Truss number
11
F. 4. The concentrations of total sugars (*) and starch (+) in
tomato stem sections sampled next to the indicated leaves at the
termination of the experiment.
stem showed a constant increase in both (Table 1). The leaf
next to truss number 11 contained four times as much total
sugar and 13 times as much starch as the leaf next to the
536
Pressman et al.—Carbon Content and Tomato Root DeŠelopment
T     1. Calculated total soluble sugar and starch contents on the first sampling of tomato leaŠes next to successiŠe trusses
Sugars
Starch
Truss
number
Leaf f.wt
(g)
(mg g−" f.wt)
(mg per leaf)
(mg g−" f.wt)
(mg per leaf)
2
5
8
11
52±9³5±3
107±4³5±8
85±5³4±2
91±1³6±8
6±2
8±4
9±6
15±2
328±0
902±1
820±8
1385±7
5±1
10±2
27±4
38±0
270±0
1095±5
2342±7
3465±6
T     2. Calculated minimum contents of total soluble sugars and starch in Šarious ŠegetatiŠe organs of tomato plants at the
stage of fiŠe or six trusses plus two or three inflorescences
Sugars (g)
per leaf or
g tissue
Number or
weight
Leaves
Leaves
Leaves
Leaves
Roots
Stem*
Total
up to first truss
next to trusses 1–3
next to trusses 4–6
up to sixth truss (total)
9
9
9
27
1700 g
670 g
0±175
0±24
0±90
0±006
0±024
Total
1±57
2±15
8±10
11±82
10±2
16±0
38±02
Starch (g)
per leaf or
g tissue
0±328
0±376
1±10
0±0058
0±012
Total
2±16
3±38
9±90
15±44
9±8
8±0
33±34
* For the calculation, 50 % of the final weight of the stem (1338 g) was estimated at this stage.
T     3. Total sugars and starch content (mg g−" f.wt) in leaŠes next to truss number 11 (at the stage of fruit set and
deŠeloping fruitlets), at Šarious dates following the remoŠal of eŠery two out of three leaŠes along the entire stem (®), and in
control plants (­), in two tomato cultiŠars
Total sugars
522
522
144
144
®
­
®
­
5
10
15
5
10
15
8±2³0±6
9±0³0±9
9±8³0±3
9±9³0±6
6±0³0±4
8±6³0±7
7±0³0±3
8±9³0±5
5±8³0±6
9±7³0±9
7±6³0±7
10±2³0±9
45±7³5±7
67±5³3±5
30±7³3±0
69±9³5±7
30±9³5±9
63±1³7±0
17±8³1±7
58±7³3±8
29±3³4±7
84±2³7±2
22±6³2±6
50±3³4±0
second truss. Even the leaves next to truss number five
contained about three and four times as much sugar and
starch, respectively, as those next to truss number two. It
was also calculated that at the end of the experiment the
stem contained about 30 g sugar and 16 g starch. The total
contents of total sugars and starch in the roots, at that stage,
were 11±5 and 11 g, respectively (data not shown).
At the stage where the roots ceased growing (five–six
trusses per plant), all the leaves were present on the plant
and, according to our calculations, they contained at least
11±8 g sugar and 15±4 g starch (Table 2). The roots and the
stem contained an additional 26 g sugar and 19 g starch.
Therefore, the minimum total carbon reserves in the
vegetative organs, at that stage of development consisted of
38 g soluble sugars and 35 g starch.
Removing two thirds of the leaves, leaving a single leaf
per truss, caused a marked decrease in the total sugar and
starch content in the leaf next to truss number 11 in the two
cultivars examined (Table 3). The decrease in starch content
Carbohydrates content (mg g–1 f.wt)
Leaves
Starch
24
Total sugars
20
16
Starch
12
8
4
0
522
144
522
144
Cultivar
F. 6. Total sugars and starch concentrations (mg g−" f.wt) in the
stems of side shoots of two tomato cultivars, 15 d after the removal of
two thirds of the leaves of the main stem or side shoot of the whole
plant (+). *, Control plants.
Pressman et al.—Carbon Content and Tomato Root DeŠelopment
could be detected as early as 5 d after treatments, earlier
than that of the sugars. The stems of the side shoots of the
treated plants, of both cultivars, contained 50 % of the total
sugars and starch, compared with the side shoots of the
control plants (Fig. 6).
DISCUSSION
Our results show that after a period of rapid growth, the
root systems of tomato plants with five or six fruit trusses
and two or three inflorescences cease growing (Fig. 1). This
is in agreement with previous observations (Leonard and
Head, 1958 ; Hurd et al., 1979). However, the data presented
in the present paper do not agree with previous interpretations that the reduction in growth rate and the die back of
part of the root system is solely a result of its relative
weakness in competition with the developing fruits.
Data in Fig. 2 show gradual increases, with increasing
truss number, in sugars and starch concentration in the
leaves. They also show that the upper, younger part of the
stem, although associated with the most active trusses,
contained more total sugars than the lower parts, and that
there was no parallel reduction in the concentrations of
starch along the stem (Fig. 4). Moreover, the concentration
of carbohydrates in the roots (Fig. 3) did not change
throughout the 197 d of the experiment. These results
indicate that even in the presence of increasing numbers of
flowers, fruitlets and developing fruits on the plant, there
was no depletion of the carbohydrate pool. On the contrary,
the sugars and starch contents in the leaves increased with
increasing truss number, up to number 11 (Table 1), owing
to the fact that concentration of carbohydrates increased,
while the leaf size remained constant. The calculated reserves
of carbohydrates in the vegetative organs at the stage of
root-growth decline (Table 2) did not include the leaves
above the sixth fruit truss ; these leaves support two or three
additional inflorescences. Therefore, these calculated reserves can be considered as minimal. Since young tomato
leaves become carbon sources early in their development
(Hocking and Steer, 1994), the contribution of an additional
six to nine leaves, with high carbohydrate content (Fig. 2,
Table 1), to the total carbohydrate storage pool, should be
taken into account. In addition, the content of only 50 % of
the final stem weight was calculated and showed net
amounts of 38 g of sugars and 33 g of starch. Moreover, it
has been suggested (Hocking and Steer, 1994) that much of
the carbon in the storage pool in the tomato stem may never
be remobilized and used by the plant. The results of the
present study, with side shoots (Fig. 6), suggest that the
stem may act as a source in case of carbohydrate deficiency.
The fact that the stored sugars and starch in the leaves can
undergo diurnal fluctuations (Fig. 5), indicates that these
compounds are free to be released and translocated to the
various sinks according to demand. Data in Table 3,
showing the removal of two thirds of the leaves markedly
decreased the carbohydrate content in the remaining leaves,
support this indication. These results strongly argue against
the possibility that the high carbohydrate content in the
upper leaves is a reflection of leaf structure rather than low
537
sink demand. Wolf and Rudich (1988) found that fruits of
determinate, field grown processing tomatoes accumulate
96–113 mg d. wt d−". Carbon import rates in fruits of
indeterminate, glasshouse tomatoes were measured by
Walker and Ho (1977), who observed an import of
5±87–3±11 mg h−" per fruit, with higher import rates to the
smaller fruits. On a per day basis, a smaller fruit was
calculated to import 70±4 mg and a large one only 37±3 mg
of carbon. Out of five to six trusses per plant only four are
at different stages of development. Assuming eight fruits per
truss and an average import of 53±9 mg d−" per fruit, results
in a total import of 1±7 g d−" carbon into the entire trusses of
developing fruits. Even with the additional import into the
inflorescences, one may consider there to be a very large
surplus of carbohydrates in the source pools (Tables 1 and
2). These calculations support the statement of Tanaka and
Fujita (1974) that in tomato plants the source exceeds the
sink, and they conform with the conclusion of Hocking and
Steer (1994) that tomato is sink- rather than source-limited
with respect to carbon assimilates. On the basis of the above
results and calculations, we would like to suggest that the
decrease in root growth rate or the cessation of root growth
is not due to assimilate deficiency. Tripp et al. (1991 a, b)
found that the presence of very high concentrations of
starch in the leaves, due to CO enrichment, did not prevent
#
the reduction in root mass ; this supports our suggestion.
Flowers, and especially fruits, may dramatically affect the
development of the entire plant. In monocarpic species they
cause senescence and death. One of the main hypothetical
factors involved in these processes is hormonal (Sklensky
and Davis, 1993). We would like to suggest that such a
factor, originating in the developing fruits, may be involved
in suppressing the root growth of the tomato plant.
Furthermore, Huber (1983) found that young plants of
various species with relatively low root weights accumulated
starch in their leaves. In a separate experiment we found
that the leaves of mature plants (bearing up to 11 trusses,
with a restricted root system) accumulated starch (data not
shown). These findings may indicate that sugars and starch
accumulate in the leaves because of a low demand for
carbohydrates in the other organs. We therefore suggest
that the carbohydrate accumulation in the leaves (Fig. 2) is
at least partially a result of the reduction in sink strength of
the root system during the reproductive phase of the plant.
ACKNOWLEDGEMENT
This work was supported by CALAR II (Cooperative Arid
Lands Agricultural Research Program) of US AID.
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