Season-Dependent Fruit Loading: Effect on Dry Mass, Water, and ...
Journal of Plant Nutrition, 29: 347–359, 2006 Copyright © Taylor & Francis Group, LLC ISSN: 0190-4167 print / 1532-4087 online DOI: 10.1080/01904160500476962
Season-Dependent Fruit Loading: Effect on Dry Mass, Water, and Nitrogen Allocation in Tomato Plants M. K. Darawsheh1 and D. L. Bouranis2 1
National Agricultural Research Foundation, Agricultural Research Station of Palama-Karditsa, Palama-Karditsa, Greece 2 Plant Physiology Laboratory, Department of Plant Biology, Faculty of Agricultural Biotechnology, Agricultural University of Athens, Athens, Greece
ABSTRACT Tomato plants were grown hydroponically in greenhouse under common commercial cultivation practice during two seasons: winter, with lower temperatures (LT) and summer, with higher temperatures of (HT), and results were compared. The effect of season on fruit load was drastic and the hypothesis was advanced that nitrogen (N) homeostasis at the whole plant level might be significantly affected, as measured by the extractable N of the stem. During LT, dry-mass accumulation occurred more or less at the same rate in all plant parts. The high fruit load at HT altered the picture, with dry-mass accumulation present at different rates in the various plant organs. Low temperatures positively affected root weight, which was significantly higher; influenced root morphology; and negatively affected fruit load. There were significant differences between the two seasons at the time of flowering, fruit setting, and fruit maturation in terms of the number of leaves and inflorescences on the main stem and in the rate of their appearance. In summer, water content of leaves and roots was lower, but not that of stem. Also, water content of roots increased considerably increase in the last five weeks, which coincided with the temperature and fruit-load decrease at the end of the season. Nitrogen concentration of leaves was higher than that of roots throughout HT, while extractable N concentration increased significantly at the middle part of the stem, where it bore the main fruit load. This effect was more profound when more fruits were ripening. Low temperature conditions were characterized by a significant decrease of root water content, while extractable N allocation was not significantly affected and root total N was higher. Received 7 May 2004; accepted 7 July 2005. Address correspondence to M. K. Darawsheh, National Agricultural Research Foundation, Agricultural Research Station of Palama-Karditsa, 1 St. Goulianou, 43200 Palama-Karditsa, Greece. E-mail: [email protected] 347
348
M. K. Darawsheh and D. L. Bouranis
Keywords: tomato plant, nitrogen, dry mass, water content, fruit loading
INTRODUCTION Temperature is an important growth factor that influences root growth, as well as the absorption of water and essential element ions (Jones, 1997; Nielsen, 1974; Barber and Boulding, 1984). Low temperature directly reduces nutrient uptake by plants, as expected for any physiological process that is dependent on respiratory energy. Plants compensate for this temperature inhibition of uptake through acclimation. Acclimation is the adjustment by individual plants to compensate for the decline in performance following exposure to stress. This homeostatic adjustment occurs through changes in the activity or synthesis of new biochemical constituents. These biochemical changes then cause a cascade of effects that are observed at other levels, such as changes in rate or environmental sensitivity of a specific process and growth rate of whole plants. Acclimation to stress always occurs within the lifetime of an individual, usually within days to weeks (Lampers et al., 1998). Temperature has a considerable effect on the time of fruit maturation. Time of ripening is dependent on the temperature of the fruit, while temperature of other organs has little effect. With respect to the time of ripening, the sensitivity of fruits to temperature increases in mature green fruits (Verkerk, 1966; Hurd and Graves, 1985; Adams et al., 2001); in particular, respiration increases as a function of temperature. This temperature effect on respiration is characteristic of most heterothermic organisms and is a consequence of the temperature sensitivity of the enzymatically catalyzed reactions involved in respiration and of the increased ATP requirements; as metabolic rates increase, the temperature stimulation of respiration reflects the increased demand for energy to support the increased rates of biosynthesis, transport, and protein turnover that occur at high temperatures. Temperature acclimation results in homeostasis of respiration (Lampers et al., 1998). Many subtropical plants grow poorly or become damaged at low temperatures (chilling injury). Part of such an injury is associated with the photosynthetic apparatus. The following aspects play a role: decrease in membrane fluidity, changes in the activity of membrane-associated enzymes and processes such as the photosynthetic electron transport, and loss of activity of cold-sensitive enzymes (Lampers et al., 1998). Variation in growth rate with temperature is associated with changes in plant carbon balance. A positive carbon balance can be maintained at adverse temperatures by changes in the pattern of resource allocation to leaves and non-photosynthetic plant parts. The effect of temperature on biomass allocation in the vegetative stage is that the relative investment of biomass in roots is lowest at a certain optimum temperature and increases at both higher and lower temperatures. This process is found both when the temperature of the entire plant is varied and when only root temperature is changed (constant shoot temperature) (Bowen, 1991). Although nutrient uptake does
Season-Dependent Fruit Loading
349
depend on root temperature in short-term experiments, it is likely that longterm temperature effects on biomass partitioning are due to their influence on nutrient uptake. There is evidence that at a low temperature, growth controls the rate of nutrient uptake rather than being controlled by it (Clarkson et al., 1998). Plants exposed to a fluctuating temperature regime often suffer no overall loss of yield when compared with those grown under a constant regime under the same temperature (Hurd and Graves, 1985; Khayat et al., 1985; De Koning, 1988, 1990). Furthermore, dry-matter partitioning is not greatly affected by temperature (Heuvelink, 1995). However, fluctuations in temperature may affect the pattern of crop yield, as the rate of developmental events such as fruit maturation is determined largely by temperature, which also affects the rate of fruit growth. Tomato plants have, within certain limits, the ability to integrate temperature. In this paper, we quantify the effect of temperature homeostasis on tomato fruit loading and, in turn, on both total and extractable nitrogen (N) homeostasis, in plants cultivated during the period of lower temperatures of winter versus the period of higher temperatures of summer.
MATERIALS AND METHODS Tomato plants (cv. ‘Dombito’) were cultivated hydroponically in a greenhouse according to commercial practice; quartz sand (0.2–0.5 mm in diameter) was used as substrate. Two experiments were conducted, the first one during the period of low temperatures of winter (LT) and the second one during the period of high temperatures of the summer (HT) (Table 1). Seeds were sown on a mixture of peat and quartz sand at a ratio of 1:1 on September 14 for the winter and April 1 for the summer. The first transplantation took place October 1 (winter) and April 20 (summer), when plants presented their second leaf (17 and 19 d after sowing, respectively). Seedlings were placed in pots containing quartz sand, where they grew up to the appearance of the sixth leaf, and were irrigated with Hoagland nutrient solution diluted to one-quarter. At this stage (38 and 50 d after sowing for winter and summer, respectively) 54 plants were selected for uniformity and transplanted into new pots (30 cm in height and diameter) containing 12 kg of quartz sand each and placed in a commercial greenhouse in three rows (18 plants per row) at distances 70 cm between rows and 50 cm within rows. Afterward, a Hoagland nutrient solution was used for irrigation and a drip-irrigation system was adopted for 8 h. In order to avoid accumulation of inorganics in the substrate, deionized water was added to the substrate every third day. The rest of the handling conformed to commercial practice. Sampling took place regularly on a weekly basis and was performed randomly from three plants. In order to avoid the loss of roots during sampling, after cutting of the aerial plant part, the rhizosphere was placed in a plastic tank containing deionized water and the grains of the substrate were removed
350
M. K. Darawsheh and D. L. Bouranis Table 1 Week average temperature and solar radiation during the examined periods
Weeks after 2nd transplanting
4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
Week average temperature T◦ C
Week average solar radiation SR mJ m−2
LT 1st LT group (T 15–19◦ C and SR 6–8 MJ m−2 ) 15.7 18.0 16.3 19.0 2nd LT group (T 9–13◦ C and SR 4–8 MJ m−2 ) 12.7 12.3 11.3 11.5 12.0 9.5 10.9 3rd LT group (T 14–18◦ C and SR 12–18 MJ m−2 ) 13.7 15.6 15.5 17.8 18.1 HT 1st HT group (T 26–30◦ C and SR 26–28 MJ m−2 ) 29.2 26.1 29.5 2nd HT group (T 33–35◦ C and SR 29–32 MJ m−2 ) 34.8 33.2 33.1 34.8 33.8 3rd HT group (T 26–31◦ C and SR 22–28 MJ m−2 ) 31.1 30.2 30.1 29.1 29.7 26.7 27.2
8.8 8.1 6.2 6.8 4.2 3.8 4.8 5.5 5.2 8.4 7.0 12.4 15.4 15.5 14.2 18.1
26.1 27.5 28.2 31.9 29.7 29.8 30.8 29.1 28.3 28.1 27.3 26.1 25.4 24.2 22.3
Season-Dependent Fruit Loading
351
carefully by hand. Then the roots were washed again with deionized water and blotted on paper. The aerial upper part was separated into leaves, stems, and fruit to get fresh weight for each part. Each sample was oven-dried at 65◦ C until constant weight. Total N was determined by the micro-Kjeldahl method, followed by distillation (Mills and Jones, 1996). Prior to stem extraction and determination of total N in the extract, stems were cut in three parts (upper, middle, and basal) and weighed; then each part was cut into small pieces, placed into a conical flask, and extracted with 50 mL of sodium acetate-acetic acid buffer solution (pH 4.8) for 20 min under constant stirring (Drosolpoulos, et al., 1996). N was determined following digestion as described for powdered tissues. Graphs fit and statistical analysis was performed by means of the Statistica software package.
RESULTS AND DISCUSSION Effects on Developmental Events and Fruit Load Effect of season was observed at the time of flowering, fruit setting, and fruit maturation, and the rate of the appearance of leaves and inflorescences on the stem. In particular, fruit setting took place in the eleventh and fifth week after second transplantation for LT and HT, respectively. Such a difference between winter and summer in the timing of fruit setting and fruit loading (in winter it was reduced) (Figure 1) resulted in a differential allocation of dry mass, water, and N within plant organs during the season. The appearance rate of leaves and inflorescences was at about 6 d and 19 d during winter and about 3 d and 9 d during summer, respectively. The final number of leaves and inflorescences for plants at the same age (170 d after sowing) was 30 and 8 in winter and 45 and 13 in summer, respectively. The initiation of flowering, fruit setting, and fruit maturation took place in the winter at 25, 53, and 107 days, respectively, and in summer at 12, 25, and 54 days after the emergence of the sixth leaf. The appearance of the first inflorescence occurred at the time of the emergence of the eighth or ninth leaf in both seasons, and the appearance of new inflorescence occurred after the emergence of every third leaf thereafter. Fruit setting coincided with the emergence of the twelth leaf and the appearance of the second inflorescence in both seasons. Fruit maturation took place with the emergence of the twenty-forth leaf and the sixth inflorescence in both seasons. Thus, season did not affect these developmental events. Tomato plants present the following developmental phases: a short period of initial growth of vegetative organs with the same rate, a long period of intense growth of all plant organs, a period of decreased root growth rate, a period of fruit maturation and first harvesting (during which a small increase in root weight occurs), and a final period of slight increase (Mills and Jones, 1996). Seasonal temperatures affected plant growth, and the effect was more intense in
352
M. K. Darawsheh and D. L. Bouranis
Figure 1. Effect of HT vs. LT on fruit loading tomato plants—(a) total fruit, (b) ripe fruit, and (c) green fruit load. Vertical bars represent max. and min. values error and horizontal lines denote LS.
the growth of the aerial parts compared with that of the roots (Figure 2). Season affected fruit loading more than it did the growth of vegetative organs. The final root weight compared with that of the other organs was higher in winter, with fewer branches carrying thicker and shorter secondary roots. Effect on Dry-Mass Allocation Dry-mass ratio of aerial organs to roots was twice as high in the summer as in the winter (Figure 3) and is correlated with the favorable influence of high temperature on the growth of the aerial parts. Temperatures less than 15◦ C favor root development, causing retardation in the growth of the aerial parts (Gosselin and Trudel, 1983a, 1983b; Bubgee and White, 1984). This effect is based on the effect of temperature on the allocation of photosynthates in the various organs (Bubgee and White, 1984; Gosselin and Trudel, 1982). Fruit loading remarkably affected dry-mass allocation between vegetative organs and root (Figure 3). This ratio increased with the increase of fruit loading in both seasons, and was most prominent in the summer. With the approach of fruit maturation, the ratio was stabilized. This balance between vegetative organs and root is developmental, affected by the shift from the vegetative to reproductive phase and fruit loading
Season-Dependent Fruit Loading
353
Figure 2. Effect of HT vs. LT on fresh-mass allocation in leaves (a), stem (b), and root (c) of tomato plants and (d) the aerial vegetative parts/roots ratio (fresh wt. basis). Vertical bars represent max. and min. values error and horizontal lines denote LS.
as an important sink for carbohydrates and nutrients; thus, it causes redistribution of growth and N (Richards et al., 1979). Fruit growth increases demand on the shoot and root system for both N and photosynthates. This demand continues to increase and becomes increasingly competitive with vegetative growth (Fisher, 1977), then decreases with the increasing size of the fruits; the rate of demand for photosynthates by these sinks depends on their intensity and capacity (Walker and Ho, 1977; Walker and Thornley, 1977). Tomato fruits present high intensity as sinks at the initial stages, and sink capacity increases with the increase in fruit size, remaining thereafter as sinks with a large capacity for photosynthates (Tanaka et al., 1974). During fruit loading, remobilization and redistribution of carbohydrates to fruits is observed from leaves and the stem (Hewitt and Marrush, 1986). Production rate of photosynthates is reflected in the produced dry biomass (Ho, 1976). Dry-mass partitioning is dynamic, depending on the current relationship between sinks and sources prevailing at low vs. high temperatures, and is regulated by the level of saccharose (Ho and Show, 1977; Walker and Ho, 1977). Aspects of this relationship in tomato have been described previously (Cooper and Thornely, 1976). The effect of fruit loading was higher in terms of root increase and lower in shoots and leaves. During winter with the absence of fruit loading (from the
354
M. K. Darawsheh and D. L. Bouranis
Figure 3. Effect of HT vs. LT on dry-mass allocation in leaves (a), stem (b), and root (c) of tomato plants and (d) the aerial vegetative parts/roots ratio (dry wt. basis). Vertical bars represent max. and min. values error and horizontal lines denote LS.
initial stages up to the 14th week), roots presented a higher rate of increase compared with leaves and stems. After the increase in the fruits, the rate of increase of dry mass continued at the same or a higher rate in leaves and stems, while in roots it decreased. The effect of fruit loading on the increase of the roots it is revealed in the changes in the dry mass during summer. Fruit increase caused a cessation of root rate of increase, while after fruit maturation a significant increase in root and stem dry mass took place.
Effect on Water Content Water content of the roots was higher than that of leaves and stems (Figure 4), this was clearer during winter, indicating that water translocation from the roots to the aerial parts was affected more than was water absorption. In addition, there was a tendency in leaves and stems to decrease their water content smoothly with age. In contrast, the changes in root water content during winter were intense and positively correlated with changes in temperature. It is remarkable that during summer, root water content was almost stable, presenting a considerable increase in the last five weeks.
Season-Dependent Fruit Loading
355
Figure 4. Effect of HT vs. LT on water content (g water g−1 dw) of (a) leaves, (b) stem, and (c) roots of tomato plants. Vertical bars represent max. and min. values error and horizontal lines denote LS.
Increase in root temperature increased water-use efficiency, and this result may be due to a reduced resistance in water translocation in the aerial organs, reduced cytoplasmic fluidity, and increased membrane permeability of water (Abdelhafez et al., 1971). Accumulation of unsaturated fatty acids in roots under low temperatures may reduce cell permeability of water and its absorption (Cornillon, 1974). Effect on Nitrogen Nitrogen concentration was higher in winter than in summer, especially in the roots (Figure 5c and 5d). The opposite was observed in the concentration of the extractable nitrogenous compounds of the stems (Figure 5a and 5b). Higher extractable N concentration (except during the period in which the green fruit presented the higher increase) was observed during summer. This result is indicative of N-transport during the period of higher temperatures during summer, while N accumulated in the roots during the period of lower temperatures. This phenomenon has been reported (Clarkson and Warner, 1979; Nordin, 1977; Gosselin and Trudel, 1982) and the negative effect of low temperature in the translocation of N was more profound when nitrate-N was the N source in the
356
M. K. Darawsheh and D. L. Bouranis
Figure 5. Effect of HT vs. LT on nitrogen distribution within tomato plants during development—allocation of extractable total nitrogen from the upper, middle, and lower part of the stem during HT (a) and LT (b), and of total nitrogen of leaves vs. roots during HT (c) and LT (d). Vertical bars represent max. and min. values error and horizontal lines denote LS.
nutrient solution (Gosselin and Trudel, 1982; Ganmore-Newman and Kafkafi, 1980), which was the case in our experiment. Fruit loading is a strong sink for N, which accumulates mainly in the fruit during fruit development (Halbrooks and Wilcox, 1980). During the period of high green fruit increase in summer, extractable N concentration decreased drastically, particularly at the middle part of the stem, where the fruit load is. During the same period (high green fruit increase) N concentration was also decreased at the leaves and roots; also, extractable N concentration was greatly increased when more fruits were ripening. These data quantify the notable effect of fruit load on the N status and allocation within the plant as it relates to allocation of dry matter. An increase in temperature causes a higher demand in fruits for N, and alters its distribution (Papadopoulos and Tiessen, 1987; Gosselin and Trudel, 1982). Short-term changes of leaf N presented a strong positive correlation with leaf water content at LT (r = 0.89) compared with HT (r = 0.46). Furthermore, short-term changes of root N levels did not seem to correlate with root water content (r = −0.36 in winter and r = 0.13 in summer); however, seasonal changes or long-term
Season-Dependent Fruit Loading
357
alterations suggest that the higher water content during LT might correlate with the higher total root N. CONCLUSIONS Comparing plants of the same age in each season, we found that in summer the appearance rate of leaves and inflorescences occurred at about 3 d and 9 d, respectively, and their final numbers were 45 and 13, respectively. The initiation of flowering, fruit setting, and fruit maturation was at 1.5, 5, and 7.5 weeks after the second transplantation, respectively. Dry-mass ratio of aerial organs to roots was two times higher in summer; fruit loading was remarkably higher and significantly affected dry-mass allocation between vegetative organs and roots. Water content of leaves and roots was lower in summer, but not that of stems, and water content of roots presented a considerable increase in the last five weeks, which coincided with the temperature and fruit load decrease at the end of the season. Nitrogen concentration of leaves was higher than that of roots throughout the season. Extractable N concentration presented a significant increase at the middle part of the stem, where the main fruit load was, and this increase was more profound when more fruits were ripening. In winter, the appearance rate of leaves and inflorescences was at 6 d and 19 d, respectively, and their final numbers were 30 and 8, respectively. The initiation of flowering, fruit setting, and fruit maturation occurred at 3.5, 8, and 15 weeks after the second transplantation, respectively. Fruit loading was erratic, and most fruits were green. Root dry mass was remarkably higher after the twelth week, and this period was also characterized by a significant decrease in root water content. Extractable N allocation was not affected significantly, and root total N was higher. ACKNOWLEDGMENTS The work is dedicated to the memory of our teacher, Prof. C. A. Niavis. REFERENCES Abdelhafez, A.T., H. Harssema, G. Veri, and K. Verkerk. 1971. Effect of soil and air temperature on growth, development and water use of tomato. Neth. J. Agr. Sci. 19: 67–75. Adams, S. R., K. E. Cockshul, and C. R. J. Cave. 2001. Effect of temperature on the growth and development of tomato fruits. Annals of Botany 88: 869–877. Barber, S. A., and D. R. Boulding (eds.). 1984. Roots, nutrient and water influx, and plant growth, ASA Special Publication 136. Madison, WI: American Society of Agronomy.
358
M. K. Darawsheh and D. L. Bouranis
Bowen, G. D. 1991. Soil temperature, root growth and plant function. In Plant roots: The hidden half, eds. Y. Waisel, A. Eshel, and U. Kafkafi, 309–330. New York: Marcel Dekker. Bubgee, B., and J. White. 1984. Tomato growth as effected by root-zone temperature and addition of Gibberellic acid and kinetin to nutrient solution. Journal of American Society for Horticultural Science 109 (1): 121–125. Clarkson, D. T., M. J. Earnshaw, P. J. White, and H. D. Cooper. 1998. Temperature dependent factors influencing nutrient uptake: An analysis of responses at different levels of organization. In Plants and temperature, eds. S. P. Long and F. I. Woodward, 281–309. Cambridge, U.K.: Company of Biologists. Clarkson, D. T., and A. Warner. 1979. Relationships between root temperature and transport of ammonium and nitrate ions by Italian ryegrass. Plant Physiology 64: 557–561. Cooper, A. J., and J. H. Thornely. 1976. Response of dry matter partitioning, growth and carbon and nutrient level in root temperature experimental and theory. Annals of Botany 40: 1139–1152. Cornillon, P. 1974. Comportement de la tomate en fonction de la temp´erature du substrat [Effects of root temperature on the absorption of mineral elements by tomatoes]. Annals of Agronomy 25: 753–777. De Koning, A. N. M. 1988. The effect of different day/night temperature regimes on growth, development and yield of glasshouse tomatoes. Journal of Horticultural Science 63: 465–471. De Koning, A. N. M. 1990. Long-term temperature integration of tomato: Growth and development under alternating temperature regimes. Scientia Horticulturae 45: 117–127. Drosolpoulos, J. B., G. G. Kouchaji, and D. L. Bouranis. 1996. Seasonal dynamic of mineral and carbohydrate by walnut tree leaves. Journal of Plant Nutrition 19 (3&4): 493–516. Fisher, K. J. 1977. Competition effects between fruit trusses of the tomato plant. Scientica Horticulturae 7: 37–42. Ganmore-Newman, R., and V. Kafkafi. 1980. Nutrient composition of tomato plants. Agronomy Journal 72: 762–765. Gosselin, A., and M. J. Trudel. 1982. Influence of root-zone temperature on growth, development and mineral content of tomato plant Vendor. Canadian Journal of Plant Science 62: 751–757. Gosselin, A., and M. J. Trudel. 1983a. Interaction between air and root temperature on greenhouse tomato: Growth and development and yield. Journal of American Society for Horticultural Science 108: 901–905. Gosselin, A., and M. J. Trudel. 1983b. Interaction between air and root temperature on greenhouse tomato: Mineral composition of plants. Journal of American Society for Horticultural Science 108: 905–909. Halbrooks, M. C., and G. E. Wilcox. 1980. Tomato plant development and elemental accumulation. Journal of American Society for Horticultural Science 105: 826–828.
Season-Dependent Fruit Loading
359
Heuvelink, E. 1995. Effect of temperature on biomass allocation in tomato (Lycopersicon esculentum). Physiologia Plantarum 94: 447–452. Hewitt, J. D., and M. Marrush. 1986. Remobilization of non-structural carbohydrate from vegetative tissue to tomato fruit in tomato. Journal of American Society for Horticultural Science 11(1): 142–145. Ho, L. C. 1976. The effect of current photosynthesis on the origin of translocation in old tomato leaves. Annals of Botany 40: 1153–1163. Ho, L. C., and A. F. Show. 1977. Carbon economy and translocation of C14 in leaflets of seven leaf tomato during leaf expansion. Annals of Botany 15: 125–137. Hurd, R. G., and C. J. Graves. 1985. Some effects of air and root temperature on yield and quality of glasshouse tomatoes. Journal of Horticultural Science 60(3): 359–371. Jones, J. B., Jr. 1997. Hydroponics: A practical guide for the soilless grower. Boca Raton, FL: St. Lucie Press. Khayat, E., D. Ravad, and N. Zieslin. 1985. The effects of various nighttemperature regimes on the vegetative growth and fruit production of tomato plants. Scientia Horticulture 27: 9–13. Lampers, H., F. S. Chapin, and T. L. Ponms. 1998. Plant physiological ecology, 5, 59, 117, 251. New York: Springer-Verlag. Mills, H. A., and J. B. Jones, Jr. 1996. Plant analysis handbook II. Athens, Georgia: MicroMacro Publishing, Inc. Nielsen, K. F. 1974. Roots and root temperatures. In The plant root and its environment, ed. E. W. Carson, 293–333. Charlottesville, VA: University Press of Virginia. Nordin, A. 1977. Effect of low temperature on ion uptake and ion translocation in wheat. Physiologia Plantarum 39: 305–310. Papadopoulos, A. P., and H. Tiessen. 1987. Root and air temperature effect on the elemental composition of tomato. Journal of American Society for Horticultural Science 112(6): 988–993. Richards, D., F. H. Goubran, and K. E. Collins. 1979. Root-shoot equilibria in fruiting tomato plant. Annals of Botany 43: 401–404. Tanaka, A., K. Fujita, and K. Kikuchi. 1979. Nutrient-physiological studies on tomato plant: Translocation of photosynthates. Soil Science and Plant Nutrition 20(2): 163–171. Verkerk, K. 1966. Temperature response in early tomato production. Acta Horticulturae 4: 26–31. Walker, A. J., and L. C. Ho. 1977. Carbon translocation in the tomato: Carbon import and fruit growth. Annals of Botany 41: 813–823. Walker, A. J., and J. H. Thornley. 1977. The tomato fruit: Import, growth, respiration and carbon metabolism at different fruit sizes and temperature. Annals of Botany 41: 977–985.
Season-Dependent Fruit Loading: Effect on Dry Mass, Water, and Nitrogen Allocation in Tomato Plants M. K. Darawsheh1 and D. L. Bouranis2 1
National Agricultural Research Foundation, Agricultural Research Station of Palama-Karditsa, Palama-Karditsa, Greece 2 Plant Physiology Laboratory, Department of Plant Biology, Faculty of Agricultural Biotechnology, Agricultural University of Athens, Athens, Greece
ABSTRACT Tomato plants were grown hydroponically in greenhouse under common commercial cultivation practice during two seasons: winter, with lower temperatures (LT) and summer, with higher temperatures of (HT), and results were compared. The effect of season on fruit load was drastic and the hypothesis was advanced that nitrogen (N) homeostasis at the whole plant level might be significantly affected, as measured by the extractable N of the stem. During LT, dry-mass accumulation occurred more or less at the same rate in all plant parts. The high fruit load at HT altered the picture, with dry-mass accumulation present at different rates in the various plant organs. Low temperatures positively affected root weight, which was significantly higher; influenced root morphology; and negatively affected fruit load. There were significant differences between the two seasons at the time of flowering, fruit setting, and fruit maturation in terms of the number of leaves and inflorescences on the main stem and in the rate of their appearance. In summer, water content of leaves and roots was lower, but not that of stem. Also, water content of roots increased considerably increase in the last five weeks, which coincided with the temperature and fruit-load decrease at the end of the season. Nitrogen concentration of leaves was higher than that of roots throughout HT, while extractable N concentration increased significantly at the middle part of the stem, where it bore the main fruit load. This effect was more profound when more fruits were ripening. Low temperature conditions were characterized by a significant decrease of root water content, while extractable N allocation was not significantly affected and root total N was higher. Received 7 May 2004; accepted 7 July 2005. Address correspondence to M. K. Darawsheh, National Agricultural Research Foundation, Agricultural Research Station of Palama-Karditsa, 1 St. Goulianou, 43200 Palama-Karditsa, Greece. E-mail: [email protected] 347
348
M. K. Darawsheh and D. L. Bouranis
Keywords: tomato plant, nitrogen, dry mass, water content, fruit loading
INTRODUCTION Temperature is an important growth factor that influences root growth, as well as the absorption of water and essential element ions (Jones, 1997; Nielsen, 1974; Barber and Boulding, 1984). Low temperature directly reduces nutrient uptake by plants, as expected for any physiological process that is dependent on respiratory energy. Plants compensate for this temperature inhibition of uptake through acclimation. Acclimation is the adjustment by individual plants to compensate for the decline in performance following exposure to stress. This homeostatic adjustment occurs through changes in the activity or synthesis of new biochemical constituents. These biochemical changes then cause a cascade of effects that are observed at other levels, such as changes in rate or environmental sensitivity of a specific process and growth rate of whole plants. Acclimation to stress always occurs within the lifetime of an individual, usually within days to weeks (Lampers et al., 1998). Temperature has a considerable effect on the time of fruit maturation. Time of ripening is dependent on the temperature of the fruit, while temperature of other organs has little effect. With respect to the time of ripening, the sensitivity of fruits to temperature increases in mature green fruits (Verkerk, 1966; Hurd and Graves, 1985; Adams et al., 2001); in particular, respiration increases as a function of temperature. This temperature effect on respiration is characteristic of most heterothermic organisms and is a consequence of the temperature sensitivity of the enzymatically catalyzed reactions involved in respiration and of the increased ATP requirements; as metabolic rates increase, the temperature stimulation of respiration reflects the increased demand for energy to support the increased rates of biosynthesis, transport, and protein turnover that occur at high temperatures. Temperature acclimation results in homeostasis of respiration (Lampers et al., 1998). Many subtropical plants grow poorly or become damaged at low temperatures (chilling injury). Part of such an injury is associated with the photosynthetic apparatus. The following aspects play a role: decrease in membrane fluidity, changes in the activity of membrane-associated enzymes and processes such as the photosynthetic electron transport, and loss of activity of cold-sensitive enzymes (Lampers et al., 1998). Variation in growth rate with temperature is associated with changes in plant carbon balance. A positive carbon balance can be maintained at adverse temperatures by changes in the pattern of resource allocation to leaves and non-photosynthetic plant parts. The effect of temperature on biomass allocation in the vegetative stage is that the relative investment of biomass in roots is lowest at a certain optimum temperature and increases at both higher and lower temperatures. This process is found both when the temperature of the entire plant is varied and when only root temperature is changed (constant shoot temperature) (Bowen, 1991). Although nutrient uptake does
Season-Dependent Fruit Loading
349
depend on root temperature in short-term experiments, it is likely that longterm temperature effects on biomass partitioning are due to their influence on nutrient uptake. There is evidence that at a low temperature, growth controls the rate of nutrient uptake rather than being controlled by it (Clarkson et al., 1998). Plants exposed to a fluctuating temperature regime often suffer no overall loss of yield when compared with those grown under a constant regime under the same temperature (Hurd and Graves, 1985; Khayat et al., 1985; De Koning, 1988, 1990). Furthermore, dry-matter partitioning is not greatly affected by temperature (Heuvelink, 1995). However, fluctuations in temperature may affect the pattern of crop yield, as the rate of developmental events such as fruit maturation is determined largely by temperature, which also affects the rate of fruit growth. Tomato plants have, within certain limits, the ability to integrate temperature. In this paper, we quantify the effect of temperature homeostasis on tomato fruit loading and, in turn, on both total and extractable nitrogen (N) homeostasis, in plants cultivated during the period of lower temperatures of winter versus the period of higher temperatures of summer.
MATERIALS AND METHODS Tomato plants (cv. ‘Dombito’) were cultivated hydroponically in a greenhouse according to commercial practice; quartz sand (0.2–0.5 mm in diameter) was used as substrate. Two experiments were conducted, the first one during the period of low temperatures of winter (LT) and the second one during the period of high temperatures of the summer (HT) (Table 1). Seeds were sown on a mixture of peat and quartz sand at a ratio of 1:1 on September 14 for the winter and April 1 for the summer. The first transplantation took place October 1 (winter) and April 20 (summer), when plants presented their second leaf (17 and 19 d after sowing, respectively). Seedlings were placed in pots containing quartz sand, where they grew up to the appearance of the sixth leaf, and were irrigated with Hoagland nutrient solution diluted to one-quarter. At this stage (38 and 50 d after sowing for winter and summer, respectively) 54 plants were selected for uniformity and transplanted into new pots (30 cm in height and diameter) containing 12 kg of quartz sand each and placed in a commercial greenhouse in three rows (18 plants per row) at distances 70 cm between rows and 50 cm within rows. Afterward, a Hoagland nutrient solution was used for irrigation and a drip-irrigation system was adopted for 8 h. In order to avoid accumulation of inorganics in the substrate, deionized water was added to the substrate every third day. The rest of the handling conformed to commercial practice. Sampling took place regularly on a weekly basis and was performed randomly from three plants. In order to avoid the loss of roots during sampling, after cutting of the aerial plant part, the rhizosphere was placed in a plastic tank containing deionized water and the grains of the substrate were removed
350
M. K. Darawsheh and D. L. Bouranis Table 1 Week average temperature and solar radiation during the examined periods
Weeks after 2nd transplanting
4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
Week average temperature T◦ C
Week average solar radiation SR mJ m−2
LT 1st LT group (T 15–19◦ C and SR 6–8 MJ m−2 ) 15.7 18.0 16.3 19.0 2nd LT group (T 9–13◦ C and SR 4–8 MJ m−2 ) 12.7 12.3 11.3 11.5 12.0 9.5 10.9 3rd LT group (T 14–18◦ C and SR 12–18 MJ m−2 ) 13.7 15.6 15.5 17.8 18.1 HT 1st HT group (T 26–30◦ C and SR 26–28 MJ m−2 ) 29.2 26.1 29.5 2nd HT group (T 33–35◦ C and SR 29–32 MJ m−2 ) 34.8 33.2 33.1 34.8 33.8 3rd HT group (T 26–31◦ C and SR 22–28 MJ m−2 ) 31.1 30.2 30.1 29.1 29.7 26.7 27.2
8.8 8.1 6.2 6.8 4.2 3.8 4.8 5.5 5.2 8.4 7.0 12.4 15.4 15.5 14.2 18.1
26.1 27.5 28.2 31.9 29.7 29.8 30.8 29.1 28.3 28.1 27.3 26.1 25.4 24.2 22.3
Season-Dependent Fruit Loading
351
carefully by hand. Then the roots were washed again with deionized water and blotted on paper. The aerial upper part was separated into leaves, stems, and fruit to get fresh weight for each part. Each sample was oven-dried at 65◦ C until constant weight. Total N was determined by the micro-Kjeldahl method, followed by distillation (Mills and Jones, 1996). Prior to stem extraction and determination of total N in the extract, stems were cut in three parts (upper, middle, and basal) and weighed; then each part was cut into small pieces, placed into a conical flask, and extracted with 50 mL of sodium acetate-acetic acid buffer solution (pH 4.8) for 20 min under constant stirring (Drosolpoulos, et al., 1996). N was determined following digestion as described for powdered tissues. Graphs fit and statistical analysis was performed by means of the Statistica software package.
RESULTS AND DISCUSSION Effects on Developmental Events and Fruit Load Effect of season was observed at the time of flowering, fruit setting, and fruit maturation, and the rate of the appearance of leaves and inflorescences on the stem. In particular, fruit setting took place in the eleventh and fifth week after second transplantation for LT and HT, respectively. Such a difference between winter and summer in the timing of fruit setting and fruit loading (in winter it was reduced) (Figure 1) resulted in a differential allocation of dry mass, water, and N within plant organs during the season. The appearance rate of leaves and inflorescences was at about 6 d and 19 d during winter and about 3 d and 9 d during summer, respectively. The final number of leaves and inflorescences for plants at the same age (170 d after sowing) was 30 and 8 in winter and 45 and 13 in summer, respectively. The initiation of flowering, fruit setting, and fruit maturation took place in the winter at 25, 53, and 107 days, respectively, and in summer at 12, 25, and 54 days after the emergence of the sixth leaf. The appearance of the first inflorescence occurred at the time of the emergence of the eighth or ninth leaf in both seasons, and the appearance of new inflorescence occurred after the emergence of every third leaf thereafter. Fruit setting coincided with the emergence of the twelth leaf and the appearance of the second inflorescence in both seasons. Fruit maturation took place with the emergence of the twenty-forth leaf and the sixth inflorescence in both seasons. Thus, season did not affect these developmental events. Tomato plants present the following developmental phases: a short period of initial growth of vegetative organs with the same rate, a long period of intense growth of all plant organs, a period of decreased root growth rate, a period of fruit maturation and first harvesting (during which a small increase in root weight occurs), and a final period of slight increase (Mills and Jones, 1996). Seasonal temperatures affected plant growth, and the effect was more intense in
352
M. K. Darawsheh and D. L. Bouranis
Figure 1. Effect of HT vs. LT on fruit loading tomato plants—(a) total fruit, (b) ripe fruit, and (c) green fruit load. Vertical bars represent max. and min. values error and horizontal lines denote LS.
the growth of the aerial parts compared with that of the roots (Figure 2). Season affected fruit loading more than it did the growth of vegetative organs. The final root weight compared with that of the other organs was higher in winter, with fewer branches carrying thicker and shorter secondary roots. Effect on Dry-Mass Allocation Dry-mass ratio of aerial organs to roots was twice as high in the summer as in the winter (Figure 3) and is correlated with the favorable influence of high temperature on the growth of the aerial parts. Temperatures less than 15◦ C favor root development, causing retardation in the growth of the aerial parts (Gosselin and Trudel, 1983a, 1983b; Bubgee and White, 1984). This effect is based on the effect of temperature on the allocation of photosynthates in the various organs (Bubgee and White, 1984; Gosselin and Trudel, 1982). Fruit loading remarkably affected dry-mass allocation between vegetative organs and root (Figure 3). This ratio increased with the increase of fruit loading in both seasons, and was most prominent in the summer. With the approach of fruit maturation, the ratio was stabilized. This balance between vegetative organs and root is developmental, affected by the shift from the vegetative to reproductive phase and fruit loading
Season-Dependent Fruit Loading
353
Figure 2. Effect of HT vs. LT on fresh-mass allocation in leaves (a), stem (b), and root (c) of tomato plants and (d) the aerial vegetative parts/roots ratio (fresh wt. basis). Vertical bars represent max. and min. values error and horizontal lines denote LS.
as an important sink for carbohydrates and nutrients; thus, it causes redistribution of growth and N (Richards et al., 1979). Fruit growth increases demand on the shoot and root system for both N and photosynthates. This demand continues to increase and becomes increasingly competitive with vegetative growth (Fisher, 1977), then decreases with the increasing size of the fruits; the rate of demand for photosynthates by these sinks depends on their intensity and capacity (Walker and Ho, 1977; Walker and Thornley, 1977). Tomato fruits present high intensity as sinks at the initial stages, and sink capacity increases with the increase in fruit size, remaining thereafter as sinks with a large capacity for photosynthates (Tanaka et al., 1974). During fruit loading, remobilization and redistribution of carbohydrates to fruits is observed from leaves and the stem (Hewitt and Marrush, 1986). Production rate of photosynthates is reflected in the produced dry biomass (Ho, 1976). Dry-mass partitioning is dynamic, depending on the current relationship between sinks and sources prevailing at low vs. high temperatures, and is regulated by the level of saccharose (Ho and Show, 1977; Walker and Ho, 1977). Aspects of this relationship in tomato have been described previously (Cooper and Thornely, 1976). The effect of fruit loading was higher in terms of root increase and lower in shoots and leaves. During winter with the absence of fruit loading (from the
354
M. K. Darawsheh and D. L. Bouranis
Figure 3. Effect of HT vs. LT on dry-mass allocation in leaves (a), stem (b), and root (c) of tomato plants and (d) the aerial vegetative parts/roots ratio (dry wt. basis). Vertical bars represent max. and min. values error and horizontal lines denote LS.
initial stages up to the 14th week), roots presented a higher rate of increase compared with leaves and stems. After the increase in the fruits, the rate of increase of dry mass continued at the same or a higher rate in leaves and stems, while in roots it decreased. The effect of fruit loading on the increase of the roots it is revealed in the changes in the dry mass during summer. Fruit increase caused a cessation of root rate of increase, while after fruit maturation a significant increase in root and stem dry mass took place.
Effect on Water Content Water content of the roots was higher than that of leaves and stems (Figure 4), this was clearer during winter, indicating that water translocation from the roots to the aerial parts was affected more than was water absorption. In addition, there was a tendency in leaves and stems to decrease their water content smoothly with age. In contrast, the changes in root water content during winter were intense and positively correlated with changes in temperature. It is remarkable that during summer, root water content was almost stable, presenting a considerable increase in the last five weeks.
Season-Dependent Fruit Loading
355
Figure 4. Effect of HT vs. LT on water content (g water g−1 dw) of (a) leaves, (b) stem, and (c) roots of tomato plants. Vertical bars represent max. and min. values error and horizontal lines denote LS.
Increase in root temperature increased water-use efficiency, and this result may be due to a reduced resistance in water translocation in the aerial organs, reduced cytoplasmic fluidity, and increased membrane permeability of water (Abdelhafez et al., 1971). Accumulation of unsaturated fatty acids in roots under low temperatures may reduce cell permeability of water and its absorption (Cornillon, 1974). Effect on Nitrogen Nitrogen concentration was higher in winter than in summer, especially in the roots (Figure 5c and 5d). The opposite was observed in the concentration of the extractable nitrogenous compounds of the stems (Figure 5a and 5b). Higher extractable N concentration (except during the period in which the green fruit presented the higher increase) was observed during summer. This result is indicative of N-transport during the period of higher temperatures during summer, while N accumulated in the roots during the period of lower temperatures. This phenomenon has been reported (Clarkson and Warner, 1979; Nordin, 1977; Gosselin and Trudel, 1982) and the negative effect of low temperature in the translocation of N was more profound when nitrate-N was the N source in the
356
M. K. Darawsheh and D. L. Bouranis
Figure 5. Effect of HT vs. LT on nitrogen distribution within tomato plants during development—allocation of extractable total nitrogen from the upper, middle, and lower part of the stem during HT (a) and LT (b), and of total nitrogen of leaves vs. roots during HT (c) and LT (d). Vertical bars represent max. and min. values error and horizontal lines denote LS.
nutrient solution (Gosselin and Trudel, 1982; Ganmore-Newman and Kafkafi, 1980), which was the case in our experiment. Fruit loading is a strong sink for N, which accumulates mainly in the fruit during fruit development (Halbrooks and Wilcox, 1980). During the period of high green fruit increase in summer, extractable N concentration decreased drastically, particularly at the middle part of the stem, where the fruit load is. During the same period (high green fruit increase) N concentration was also decreased at the leaves and roots; also, extractable N concentration was greatly increased when more fruits were ripening. These data quantify the notable effect of fruit load on the N status and allocation within the plant as it relates to allocation of dry matter. An increase in temperature causes a higher demand in fruits for N, and alters its distribution (Papadopoulos and Tiessen, 1987; Gosselin and Trudel, 1982). Short-term changes of leaf N presented a strong positive correlation with leaf water content at LT (r = 0.89) compared with HT (r = 0.46). Furthermore, short-term changes of root N levels did not seem to correlate with root water content (r = −0.36 in winter and r = 0.13 in summer); however, seasonal changes or long-term
Season-Dependent Fruit Loading
357
alterations suggest that the higher water content during LT might correlate with the higher total root N. CONCLUSIONS Comparing plants of the same age in each season, we found that in summer the appearance rate of leaves and inflorescences occurred at about 3 d and 9 d, respectively, and their final numbers were 45 and 13, respectively. The initiation of flowering, fruit setting, and fruit maturation was at 1.5, 5, and 7.5 weeks after the second transplantation, respectively. Dry-mass ratio of aerial organs to roots was two times higher in summer; fruit loading was remarkably higher and significantly affected dry-mass allocation between vegetative organs and roots. Water content of leaves and roots was lower in summer, but not that of stems, and water content of roots presented a considerable increase in the last five weeks, which coincided with the temperature and fruit load decrease at the end of the season. Nitrogen concentration of leaves was higher than that of roots throughout the season. Extractable N concentration presented a significant increase at the middle part of the stem, where the main fruit load was, and this increase was more profound when more fruits were ripening. In winter, the appearance rate of leaves and inflorescences was at 6 d and 19 d, respectively, and their final numbers were 30 and 8, respectively. The initiation of flowering, fruit setting, and fruit maturation occurred at 3.5, 8, and 15 weeks after the second transplantation, respectively. Fruit loading was erratic, and most fruits were green. Root dry mass was remarkably higher after the twelth week, and this period was also characterized by a significant decrease in root water content. Extractable N allocation was not affected significantly, and root total N was higher. ACKNOWLEDGMENTS The work is dedicated to the memory of our teacher, Prof. C. A. Niavis. REFERENCES Abdelhafez, A.T., H. Harssema, G. Veri, and K. Verkerk. 1971. Effect of soil and air temperature on growth, development and water use of tomato. Neth. J. Agr. Sci. 19: 67–75. Adams, S. R., K. E. Cockshul, and C. R. J. Cave. 2001. Effect of temperature on the growth and development of tomato fruits. Annals of Botany 88: 869–877. Barber, S. A., and D. R. Boulding (eds.). 1984. Roots, nutrient and water influx, and plant growth, ASA Special Publication 136. Madison, WI: American Society of Agronomy.
358
M. K. Darawsheh and D. L. Bouranis
Bowen, G. D. 1991. Soil temperature, root growth and plant function. In Plant roots: The hidden half, eds. Y. Waisel, A. Eshel, and U. Kafkafi, 309–330. New York: Marcel Dekker. Bubgee, B., and J. White. 1984. Tomato growth as effected by root-zone temperature and addition of Gibberellic acid and kinetin to nutrient solution. Journal of American Society for Horticultural Science 109 (1): 121–125. Clarkson, D. T., M. J. Earnshaw, P. J. White, and H. D. Cooper. 1998. Temperature dependent factors influencing nutrient uptake: An analysis of responses at different levels of organization. In Plants and temperature, eds. S. P. Long and F. I. Woodward, 281–309. Cambridge, U.K.: Company of Biologists. Clarkson, D. T., and A. Warner. 1979. Relationships between root temperature and transport of ammonium and nitrate ions by Italian ryegrass. Plant Physiology 64: 557–561. Cooper, A. J., and J. H. Thornely. 1976. Response of dry matter partitioning, growth and carbon and nutrient level in root temperature experimental and theory. Annals of Botany 40: 1139–1152. Cornillon, P. 1974. Comportement de la tomate en fonction de la temp´erature du substrat [Effects of root temperature on the absorption of mineral elements by tomatoes]. Annals of Agronomy 25: 753–777. De Koning, A. N. M. 1988. The effect of different day/night temperature regimes on growth, development and yield of glasshouse tomatoes. Journal of Horticultural Science 63: 465–471. De Koning, A. N. M. 1990. Long-term temperature integration of tomato: Growth and development under alternating temperature regimes. Scientia Horticulturae 45: 117–127. Drosolpoulos, J. B., G. G. Kouchaji, and D. L. Bouranis. 1996. Seasonal dynamic of mineral and carbohydrate by walnut tree leaves. Journal of Plant Nutrition 19 (3&4): 493–516. Fisher, K. J. 1977. Competition effects between fruit trusses of the tomato plant. Scientica Horticulturae 7: 37–42. Ganmore-Newman, R., and V. Kafkafi. 1980. Nutrient composition of tomato plants. Agronomy Journal 72: 762–765. Gosselin, A., and M. J. Trudel. 1982. Influence of root-zone temperature on growth, development and mineral content of tomato plant Vendor. Canadian Journal of Plant Science 62: 751–757. Gosselin, A., and M. J. Trudel. 1983a. Interaction between air and root temperature on greenhouse tomato: Growth and development and yield. Journal of American Society for Horticultural Science 108: 901–905. Gosselin, A., and M. J. Trudel. 1983b. Interaction between air and root temperature on greenhouse tomato: Mineral composition of plants. Journal of American Society for Horticultural Science 108: 905–909. Halbrooks, M. C., and G. E. Wilcox. 1980. Tomato plant development and elemental accumulation. Journal of American Society for Horticultural Science 105: 826–828.
Season-Dependent Fruit Loading
359
Heuvelink, E. 1995. Effect of temperature on biomass allocation in tomato (Lycopersicon esculentum). Physiologia Plantarum 94: 447–452. Hewitt, J. D., and M. Marrush. 1986. Remobilization of non-structural carbohydrate from vegetative tissue to tomato fruit in tomato. Journal of American Society for Horticultural Science 11(1): 142–145. Ho, L. C. 1976. The effect of current photosynthesis on the origin of translocation in old tomato leaves. Annals of Botany 40: 1153–1163. Ho, L. C., and A. F. Show. 1977. Carbon economy and translocation of C14 in leaflets of seven leaf tomato during leaf expansion. Annals of Botany 15: 125–137. Hurd, R. G., and C. J. Graves. 1985. Some effects of air and root temperature on yield and quality of glasshouse tomatoes. Journal of Horticultural Science 60(3): 359–371. Jones, J. B., Jr. 1997. Hydroponics: A practical guide for the soilless grower. Boca Raton, FL: St. Lucie Press. Khayat, E., D. Ravad, and N. Zieslin. 1985. The effects of various nighttemperature regimes on the vegetative growth and fruit production of tomato plants. Scientia Horticulture 27: 9–13. Lampers, H., F. S. Chapin, and T. L. Ponms. 1998. Plant physiological ecology, 5, 59, 117, 251. New York: Springer-Verlag. Mills, H. A., and J. B. Jones, Jr. 1996. Plant analysis handbook II. Athens, Georgia: MicroMacro Publishing, Inc. Nielsen, K. F. 1974. Roots and root temperatures. In The plant root and its environment, ed. E. W. Carson, 293–333. Charlottesville, VA: University Press of Virginia. Nordin, A. 1977. Effect of low temperature on ion uptake and ion translocation in wheat. Physiologia Plantarum 39: 305–310. Papadopoulos, A. P., and H. Tiessen. 1987. Root and air temperature effect on the elemental composition of tomato. Journal of American Society for Horticultural Science 112(6): 988–993. Richards, D., F. H. Goubran, and K. E. Collins. 1979. Root-shoot equilibria in fruiting tomato plant. Annals of Botany 43: 401–404. Tanaka, A., K. Fujita, and K. Kikuchi. 1979. Nutrient-physiological studies on tomato plant: Translocation of photosynthates. Soil Science and Plant Nutrition 20(2): 163–171. Verkerk, K. 1966. Temperature response in early tomato production. Acta Horticulturae 4: 26–31. Walker, A. J., and L. C. Ho. 1977. Carbon translocation in the tomato: Carbon import and fruit growth. Annals of Botany 41: 813–823. Walker, A. J., and J. H. Thornley. 1977. The tomato fruit: Import, growth, respiration and carbon metabolism at different fruit sizes and temperature. Annals of Botany 41: 977–985.
