2017 Volume 86 Issue 3 Pages 311-316
With the continuing trend of global warming, the adverse impact of high temperature and the inevitably accompanying drought stress on the growth of Japanese apricot trees (Prunus mume Siebold et Zucc.) are of concern. Therefore, the effects of these factors on photosynthesis and carbohydrate translocation were analyzed. An investigation was conducted at average daytime temperatures of 24°C, 30°C, and 34°C under both irrigated and drought conditions. The 34°C temperature was higher than the open air temperature by 5°C. Stable isotope 13C was administered to trees to determine carbohydrate positioning. Under the drought stress condition, the photosynthetic rate declined accompanied by temperature elevation, and at the highest temperature of 34°C, 13C concentrations in the twigs and roots were lower than those in the irrigated trees at 24°C. Two-way analysis of variance revealed a trend of 13C translocation to the young organs above ground, and old organs, while roots were affected by water status, temperature, and their combination, respectively. In the irrigated trees, the photosynthetic rate reduction was not detected, even at higher temperatures. However, translocation incompetence reflecting a decline in 13C concentration in the roots was observed at 34°C. These results indicate that the permissible diurnal average temperature during summer for the growth of Japanese apricot trees is approximately up to 30°C, and in the temperature range around this irrigation is helpful to facilitate regular functioning of carbohydrate translocation under drought stress conditions.
Global warming resulting from an increasing atmospheric concentration of carbon dioxide and other greenhouse gases could jeopardize agriculture, forestry, and other industries that use the natural environment (IPCC, 2001). The increase in global mean surface temperature for the years 2081–2100 relative to 1986–2005 is likely to be in the range of 2.6°C–4.8°C derived from model simulations, unless countermeasures are taken to reduce the emission of greenhouse gases (IPCC, 2013). In the production area of Japanese apricot trees in Wakayama Prefecture, Japan, damage to growth has occurred during the last three decades due to exposure to high temperatures and a lack of precipitation. Under the current situation of advancing global warming, broad scale retardation of Japanese apricot trees in the production area has become a concern.
In apricot trees, the harmful results of excluding irrigation have chiefly been shown by the comparatively small increase in the cross-section areas of the trunks, death of some branches, and failure in many cases to produce fruit buds the following year (Hendrickson and Veihmeyer, 1950). Tsuchida et al. (2011) also demonstrated that drought stress inhibits growth and carbohydrate accumulation in Japanese apricot trees. These results prove that the sugar translocation rate limits the growth rate (Hewitt and Curtis, 1948). However, very little information has been obtained regarding the effect of a combination of drought stress and high temperature, which strictly control tree growth, on carbohydrate metabolism in Japanese apricot trees. To conduct a detailed analysis of carbohydrate metabolism, tracing carbohydrate translocation from the source to the sink in the trees is crucial.
In the present investigation, we administered stable isotope 13C to Japanese apricot trees to determine the influence of high temperature and drought stress on carbohydrate translocation in individual organs in order to understand the impact of the predicted future increases in temperature.
Six-year-old Japanese apricot (Prunus mume Siebold et Zucc.) ‘Nanko’ trees planted in 100-L pots in greenhouses at the Japanese Apricot Laboratory, Minabe, Hidaka, Wakayama Prefecture, Japan (latitude 33°82'N, longitude 135°35'E) were investigated just after harvest and when twig elongation stopped (excluding vigorous shoots). Average diurnal temperature ± SE (n = 693, measured per hour) in the three greenhouses from 7:00 AM to 6:00 PM was maintained at 24 ± 0.13°C, 30 ± 0.12°C, and 34 ± 0.19°C, respectively, during July 11 to September 6, 2005. Temperatures of 24°C and 30°C were controlled using a cooling installation. During this period, the diurnal average temperature ± SE of the open air was 29.0 ± 0.09°C. During the night (from 6:00 PM to 7:00 AM), greenhouses were opened and cooling installations were turned off and the average temperature ± SE (n = 679, measured per hour) was maintained at 24 ± 0.05°C, which was the same as the open air temperature. Concurrently with starting temperature control, three trees were subjected to drought stress, and the other three trees were appropriately irrigated in each greenhouse until September 6, 2005. Throughout the experiment, the drought-stressed trees were provided with 2 L of water at an interval of 3 days, whereas the irrigated trees were provided with 10 L of water in order to outflow from the pot bottom at an interval of 2 or 3 days; consequently, the soils were kept wet throughout the experiment. The irrigated trees in the greenhouse maintained at 24°C during the daytime were designated as the control.
The predawn leaf water potential at 5:00 AM under clear conditions was measured using a commercial pressure chamber (model DIK-7002; Daiki Rika Co., Ltd., Japan) at an interval of 5–12 days from just before starting the investigation to August 30.
Apparent photosynthetic and transpiration rates at 10:00 AM under clear conditions were also measured at an interval of 9–16 days until August 24 using a portable photosynthesis system (model LI-6400; Li-Cor Inc., USA). Measurement of these three items was conducted regardless of the irrigation timing.
13C applicationOn August 29, 2005, 10 L of water were applied to irrigate trees, whereas drought-stressed trees were not irrigated. On August 30, whole trees were completely enclosed in a clear vinyl bag (0.15-mm thick) to prevent gas leaks. Three Erlenmeyer flasks containing 4.0 g of Ba13CO3 (98%, Kyokuko-Tsusho Co., Ltd., Japan) were placed inside the bag. 13CO2 was released by adding 30 mL of 50% lactic acid to Ba13CO3 at 10:30 AM, 11:30 AM, and 01:00 PM. A fan was also placed inside the bag to ensure that the air was well mixed during labeling with 13CO2. The vinyl bag was removed at 3:00 PM to terminate 13CO2 application.
One week after 13C application (September 6), the trees were divided into leaves, current twigs, 2-year-old twigs, twigs older than 3 years, trunk (under the grafted site), fine roots (<2 mm in diameter), middle roots (2–20 mm in diameter), and large roots (>20 mm in diameter). All components were dried using forced air at 80°C, and dry weight was measured. Dried matter was ground to a fine powder.
Measurement of 13CApproximately 1 mg of the powdered samples was used to determine the total carbon and isotopic ratio between 12C and 13C. The 13C atom percentage in each organ was analyzed using a mass-spectral stable isotope analyzer (model EX-130S; Nihon Bunko Co., Ltd., Japan). The excess 13C atom percentage was calculated by subtracting the 13C atom percentage in the organs from that in an untreated tree (1.1 atom percentage). The total carbon content was determined from the carbon ratio and total dry weight of each sample. The amount of active 13C absorption by each organ was given by the 13C content in the sample and was calculated as 13C atom excess percentage × total carbon content in the sample. The 13C concentration was obtained by dividing the amount of 13C absorbed in the sample by the dry weight of the sample.
A significance test of leaf water potential, photosynthetic rate, 13C concentration, and dry weight of each organ between the control and other applications for each organ was performed using Dunnett’s multiple range test. In addition, Tukey’s multiple range test was applied for trees under the drought stress condition. Furthermore, the data were subjected to two-way analysis of variance (ANOVA) with water status and temperature as factors.
The distribution ratio of the 13C concentration was determined by dividing the amount of 13C absorbed in the organ by the total amount of excess 13C absorbed in the entire plant.
The leaf water potential (Fig. 1) and photosynthetic (Fig. 2) and transpiration rates (Fig. 3) under the drought stress condition were lower than those of the control tree (irrigated, 24°C) regardless of the temperature. Leaves of the drought-stressed trees wilted just before irrigation regardless of the temperature.
Effects of temperature and water status on the leaf water potential of Japanese apricot ‘Nanko’ trees. Trees were maintained at diurnal temperatures of 24°C, 30°C, and 34°C, and the groups were subjected to irrigation or drought stress during July 11 to September 6, 2005. Vertical bars indicate standard errors of the mean (n = 3). * and ** represent values significantly lower than those of the control tree (24°C, irrigated) at the 5 and 1% level, respectively by Dunnett’s multiple range test (n = 3). Different letters indicate significant differences among drought-stressed trees at the 5% level by Tukey’s multiple range test (n = 3).
Effects of temperature and water status on the photosynthetic rate of Japanese apricot ‘Nanko’ trees. Trees were maintained at diurnal temperatures of 24°C, 30°C, and 34°C, and the groups were subjected to irrigation or drought stress during July 11 to September 6, 2005. Vertical bars indicate standard errors of the mean (n = 3). * and ** represent values significantly lower than those of the control tree (24°C, irrigated) at the 5 and 1% level, respectively by Dunnett’s multiple range test (n = 3). Different letters indicate significant differences among drought-stressed trees at the 5% level by Tukey’s multiple range test (n = 3).
Effects of temperature and water status on the transpiration rate of Japanese apricot ‘Nanko’ trees. Trees were maintained at diurnal temperatures of 24°C, 30°C, and 34°C, and the groups were subjected to irrigation or drought stress during July 11 to September 6, 2005. Vertical bars indicate standard errors of the mean (n = 3). †† represents values significantly higher than those of the control tree (24°C, irrigated) at the 1% level by Dunnett’s multiple range test (n = 3). * and ** represent values significantly lower than those of the control tree (24°C, irrigated) at the 5 and 1% level, respectively by Dunnett’s multiple range test (n = 3). Different letters indicate significant differences among drought-stressed trees at the 5% level by Tukey’s multiple range test (n = 3).
These three values of the irrigated trees were not different among the different temperatures, whereas under the drought stress condition, these three values just before 13C application (August 24 or 30) declined with rising temperature, i.e., the leaf water potentials at 30°C and 34°C were lower than that at 24°C and the photosynthetic and transpiration rates of trees at 34°C were lower than those at 24°C.
An interactional effect of water status and temperature was detected for the leaf water potential (Table 1). The photosynthetic and transpiration rates were affected by water status.
P value subjected to two-way ANOVA for significance of treatmentz effects on leaf water potential, photosynthetic rate, and transpiration rate of Japanese apricot trees ‘Nanko’.
In the current twigs, fine roots, and middle roots, the 13C concentration in the drought-stressed tree at 34°C were lower than those in the control trees (Fig. 4). Moreover, in the large roots, the 13C concentration in both the irrigated and drought-stressed trees at 34°C was lower than that in the control trees. There was no significant difference in the 13C concentration of any organ among the different temperatures under the drought stress condition.
The 13C absorption concentration in the individual organs of Japanese apricot ‘Nanko’ trees. Vertical bars indicate standard errors of the mean (n = 3). Trees were maintained at diurnal temperatures of 24°C, 30°C, and 34°C, and the groups were subjected to irrigation or drought stress during July 11 to September 6, 2005. 13C was applied on August 30, 2005 and samples for the determination of 13C concentration were obtained on September 6, 2005. * represent values significantly lower than those of the control tree (24°C, irrigated) at the 5% level by Dunnett’s multiple range test (n = 3).
The 13C concentrations in the current twigs, middle roots, and large roots were effected by water status, those in the trunk were significantly affected by temperature, and those in the fine roots were affected by both the water status and temperature (Table 2). P values obtained through two-way ANOVA revealed a trend in the 13C concentration in the young organs above ground being affected by water status, that in the old organs being affected by temperature, and that in the roots being affected by both water status and temperature.
P value subjected to two-way ANOVA at significance of treatmentz effects on 13C concentration in each organ of Japanese apricot trees ‘Nanko’.
The 13C distribution ratio was calculated from the 13C concentration in the organs (Fig. 4) and the dry weight of the organs (Fig. 5). There was no significant difference in the dry weight of any organ among the different conditions; nonetheless, extension of vigorous shoots was inhibited under drought conditions (data not shown). The 13C distribution ratios in the current twigs and roots (sum of the rates in the fine roots, middle roots, and large roots) of all drought-stressed trees were lower than those of the irrigated trees at each temperature (Fig. 6). The 13C distribution ratio in the leaves was the highest at 34°C in three temperature applications, irrespective of the plants being irrigated or drought stressed, whereas that in the trunk and roots was at a low level. In addition, that in over 3-year-old twigs in irrigated trees was also at a low level.
Dry weight of the individual organs of Japanese apricot ‘Nanko’ trees. Trees were maintained at diurnal temperatures of 24°C, 30°C, and 34°C, and the groups were subjected to irrigation or drought stress during July 11 to September 6, 2005. Samples for the determination of dry weight were obtained on September 6, 2005. Vertical bars indicate standard errors of the mean (n = 3). Significant differences were not detected between the control tree and other trees by Dunnett’s multiple range test and Tukey’s multiple range test among drought-stressed trees (n = 3).
The 13C distribution rate in each organ of Japanese apricot ‘Nanko’ trees. Trees were maintained at diurnal temperatures of 24°C, 30°C, and 34°C, and the groups were subjected to irrigation or drought stress during July 11 to September 6, 2005. 13C was applied on August 30, 2005 and samples for the determination of 13C concentration and dry weight were obtained on September 6, 2005. The distribution ratio of 13C in each organ was determined by dividing the amount of 13C absorbed in individual organs by the total amount of excess 13C absorbed in whole trees. The 13C absorbed per unit of dry weight for each organ was obtained by dividing the amount of 13C absorbed in the organ by the dry weight of the organ.
Under the drought stress condition, leaf water potential (Fig. 1), the photosynthetic rate (Fig. 2), and transpiration rate (Fig. 3) declined with the increase in temperature. If a plant does not obtain a sufficient water supply, resulting in water stress, stomatal closure, and a reduction in transpiration occurs, with a consequent increase in the leaf temperature (Martinez, 1994). Moreover, ambient temperature increases, as well as an increase in the vapor pressure deficit, normally results in water stress and stomatal closure (Berry and Bjӧrkman, 1980). Therefore, high temperature under drought stress conditions likely accelerates the reduction in the leaf water potential and photosynthetic and transpiration rates of Japanese apricot trees.
Previous reports clarified that water stress reduces the 13C translocation rate in the shoots of pear trees (Teng et al., 1999) and the satsuma mandarin (Yakushiji and Morinaga, 1998), and that drought stress inhibits the accumulation of carbohydrates in the branches and roots of the Japanese apricot tree (Tsuchida et al., 2011). In the present experiment, the 13C concentration in the twigs, fine roots, middle roots, and large roots of the drought-stressed trees at 34°C was low (Fig. 4), and the P value, as calculated by two-way ANOVA, indicating that the 13C translocation to the twigs is effected by water stress, while that to the fine roots is influenced by not only water stress, but also high temperature (Table 2). Therefore, a drought stress condition seriously diminishes carbohydrate translocation to the twigs and that to the fine roots is more sensitive to environmental alteration than twigs.
Nevertheless, there was no significant difference in the dry weight of trees among the different conditions (Fig. 5). This result can be attributed to the short period (2 months) of stress application. Tsuchida et al. (2011) demonstrated that the dry weight of Japanese apricot trees declined over approximately a 3-month period of drought stress; therefore, a period of drought stress longer than 2 months is likely to cause visible tree growth inhibition. However, in this investigation, root re-extension of the trees exposed to drought and high temperature conditions during the autumn may have been suppressed because of the lack of carbohydrates.
Irrigated Japanese apricot trees maintained a high leaf water potential (Fig. 1), photosynthetic rate (Fig. 2), and transpiration rate (Fig. 3), regardless of high temperatures. It has previously been shown that sweet cherry trees under high temperature and dry soil conditions resulted in decreased accumulation of carbohydrates; however, if they are irrigated sufficiently, the photosynthetic rate is relatively high and the nonstructural carbohydrate concentration is maintained at almost the same level as that at low temperatures (Beppu et al., 2003), while well-watered plants placed in high atmospheric humidity maintained open stomata as the temperature increased over a wide range (Berry and Bjӧrkman, 1980). These results indicate that the functions of transpiration and photosynthesis within Japanese apricot trees can adapt to high temperatures if the trees are sufficiently irrigated. However, at 34°C, even if trees are irrigated, the 13C concentration in the large roots (Fig. 4) and 13C distribution rates in the 3-year-old twigs, trunk, and roots were low (Fig. 6). Moreover, P values obtained using a two-way ANOVA suggested that 13C translocation to the old organs and roots is inhibited by high temperatures (Table 2). Carbohydrate is first partitioned to maintain respiration, following which partition to the leaves, stems, branches, and finally, the trunk occurs (Grossman and DeJong, 1994b). Maintenance respiration is sensitive to temperature, approximately doubling when the temperature increases from 20°C to 30°C (Amthor, 1989; Grossman and DeJong, 1994a). In addition, root activity is supported by residual carbohydrates after above-ground growth (Grossman and DeJong, 1994b). These reports suggest inhibition in carbohydrate supply to old stems and roots under a high temperature condition is caused by excess respiration, resulting in a shortage of residual carbohydrates for these organs.
The 13C distribution rate in the leaves at 34°C was the highest of all organs, irrespective of the plants being irrigated or drought stressed (Fig. 6). This result suggests that carbohydrates synthesized in the leaves are interrupted for translocation to other organs at high temperatures. There are very few other data on the effects of high temperatures on carbohydrate translocation from source to sink in woody plants. Therefore, further studies are required to explain this phenomenon.
Considering the facts described above, the permissible diurnal average temperature for the growth of Japanese apricot trees during summer is up to approximately 30°C. In this temperature range, irrigation is helpful to maintain regular functioning of photosynthesis and carbohydrate translocation even under drought stress conditions.
An increase in global mean surface temperature for the years 2081–2100 relative to 1986–2005 is likely to be in the range of 2.6°C–4.8 °C, unless countermeasure are taken (IPCC, 2013). The possible realization of the highest temperature in this investigation of 34°C, 5.0°C higher than the normal temperature, is uncertain as this is the worst case scenario; however, Japanese apricot trees may suffer from frequent drought stress in the future. Therefore, irrigation will become more important in several cultivation techniques.
We gratefully acknowledge Minehiro Nishino for field maintenance and assistance with this investigation.
