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Salinity induces carbohydrate accumulation and sugar-regulated starch biosynthetic genes in tomato (Solanum lycopersicum L. cv. 'Micro-Tom') fruits in an ABA- and osmotic stress-independent manner.

Yin YG, Kobayashi Y, Sanuki A, Kondo S, Fukuda N, Ezura H, Sugaya S, Matsukura C - J. Exp. Bot. (2009)

Bottom Line: Tracer analysis with (13)C confirmed that elevated carbohydrate accumulation in fruits exposed to salinity stress was confined to the early development stages and did not occur after ripening.The results indicate that salinity stress enhanced carbohydrate accumulation as starch during the early development stages and it is responsible for the increase in soluble sugars in ripe fruit.These results indicate AgpL1 and AgpS1 are involved in the promotion of starch biosynthesis under the salinity stress in ABA- and osmotic stress-independent manners.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennoudai, Tsukuba, Ibaraki, Japan.

ABSTRACT
Salinity stress enhances sugar accumulation in tomato (Solanum lycopersicum) fruits. To elucidate the mechanisms underlying this phenomenon, the transport of carbohydrates into tomato fruits and the regulation of starch synthesis during fruit development in tomato plants cv. 'Micro-Tom' exposed to high levels of salinity stress were examined. Growth with 160 mM NaCl doubled starch accumulation in tomato fruits compared to control plants during the early stages of development, and soluble sugars increased as the fruit matured. Tracer analysis with (13)C confirmed that elevated carbohydrate accumulation in fruits exposed to salinity stress was confined to the early development stages and did not occur after ripening. Salinity stress also up-regulated sucrose transporter expression in source leaves and increased activity of ADP-glucose pyrophosphorylase (AGPase) in fruits during the early development stages. The results indicate that salinity stress enhanced carbohydrate accumulation as starch during the early development stages and it is responsible for the increase in soluble sugars in ripe fruit. Quantitative RT-PCR analyses of salinity-stressed plants showed that the AGPase-encoding genes, AgpL1 and AgpS1 were up-regulated in developing fruits, and AgpL1 was obviously up-regulated by sugar at the transcriptional level but not by abscisic acid and osmotic stress. These results indicate AgpL1 and AgpS1 are involved in the promotion of starch biosynthesis under the salinity stress in ABA- and osmotic stress-independent manners. These two genes are differentially regulated at the transcriptional level, and AgpL1 is suggested to play a regulatory role in this event.

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Fruit development of cv. ‘Micro-Tom’. (A) Flowering (0) and fruit at 10, 14, 18, 22, 26, 34, and 42 d after flowering (DAF) grown under control conditions. In this work, fruit at 10–14, 18–26, 34, and 42 DAF were defined as immature green, mature green, yellow, and red stages, respectively. (B) Fresh weight (shaded bars) and brix (%) (black circles) of red-ripe fruit grown under control (0 mM NaCl) and various salinity conditions (80–160 mM NaCl). Right and left vertical axes correspond to brix (%) and fresh weight, respectively. Values are means ±SD (n=50). Different letters indicate statistical significance of means estimated using Fisher's PLSD test (P <0.05).
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fig1: Fruit development of cv. ‘Micro-Tom’. (A) Flowering (0) and fruit at 10, 14, 18, 22, 26, 34, and 42 d after flowering (DAF) grown under control conditions. In this work, fruit at 10–14, 18–26, 34, and 42 DAF were defined as immature green, mature green, yellow, and red stages, respectively. (B) Fresh weight (shaded bars) and brix (%) (black circles) of red-ripe fruit grown under control (0 mM NaCl) and various salinity conditions (80–160 mM NaCl). Right and left vertical axes correspond to brix (%) and fresh weight, respectively. Values are means ±SD (n=50). Different letters indicate statistical significance of means estimated using Fisher's PLSD test (P <0.05).

Mentions: Fruits were sampled from plants grown under the two growth conditions at 10, 14, 18, 22, 26, 34, and 42 DAF as shown in Fig. 1A. At the start of this experiment, the effect of salinity intensity on fruit brix (%) and fresh weight of red ripe fruit in cv. ‘Micro-Tom’ was examined (Fig. 1B). Fruit brix (%) increased in response to the elevation of the stress level of the salinity and finally reached 1.6-times that of control fruit in the 160 mM NaCl condition. By contrast, fresh fruit weight decreased to 82–62% of the control in the given salinity conditions exhibiting an inverse correlation to the brix. Although size of the plants was concomitantly decreased under the salinity stress, the ratio of fruits to foliage was kept almost the same in both of the conditions on a fresh and a dry weight basis (see Supplementary Fig. S2 at JXB online). In order to dissect the dynamic alteration of carbohydrate in salinity-stressed fruit, plants treated with 160 mM NaCl were investigated using the following analyses. To avoid an excessive concentration effect due to the salinity stress, similar sized fruits were selectively used between both conditions in each developmental stage through the present work (see Supplementary Fig. S1 at JXB online). Soluble sugar contents (glucose, fructose, and sucrose) of developing fruits were determined in fresh fruit grown under saline and normal conditions (Fig. 2). In the control fruits, sugar levels gradually decreased (glucose, sucrose, and total sugar) or were unchanged (fructose) during fruit development (10–34 DAF) and, apart from sucrose, increased slightly by the end of the maturation stage (42 DAF). Sugar levels of salinity-stressed fruit were unchanged at 34 DAF but had increased substantially by 42 DAF; however, only sucrose had been kept at a similar level during this period even under saline conditions. Salinity stress enhanced the accumulation of glucose by 2.43 times, fructose by 2.05 times, sucrose by 7.87 times, and total sugars by 2.27 times at 42 DAF compared with those of the control. The promotion effect of the salinity stress on the accumulation of soluble sugars in red-ripe fruit was also confirmed on a dry weight basis (see Supplementary Fig. S3 at JXB online). Water contents were 90.7 (10 DAF), 91.8 (18 DAF), 89.9 (26 DAF), and 93.2% (42 DAF) in control fruits and 85.9 (10 DAF), 85.8 (18 DAF), 86.7 (26 DAF), and 90.9% (42 DAF) in the salinity-stressed fruits (data not shown). In contrast to the sugar contents, salinity stress enhanced starch accumulation during the early fruit development stages by 5.04 (10 DAF), 2.13 (18 DAF), and 2.91 (26 DAF) times compared to those of the control, respectively. Accumulation of starch granules in the fruits at 10 DAF was visualized by Periodic acid–Schiff (PAS) staining (see Supplementary Fig. S4 at JXB online). Figure 3 shows that enhanced starch accumulation was observed in the fruit of plants exposed to the salinity stress in developmental fruits. However, in the pericarp, starch only accumulated in the inner pericarp but not in the outer pericarp and exocarp (see Supplementary Fig. S4A, D at JXB online). By 26 DAF, starch had started to disappear from control fruit but was still accumulating in the salinity-stressed fruit. In those fruit, starch disappearance was delayed compared to the control (34 DAF).


Salinity induces carbohydrate accumulation and sugar-regulated starch biosynthetic genes in tomato (Solanum lycopersicum L. cv. 'Micro-Tom') fruits in an ABA- and osmotic stress-independent manner.

Yin YG, Kobayashi Y, Sanuki A, Kondo S, Fukuda N, Ezura H, Sugaya S, Matsukura C - J. Exp. Bot. (2009)

Fruit development of cv. ‘Micro-Tom’. (A) Flowering (0) and fruit at 10, 14, 18, 22, 26, 34, and 42 d after flowering (DAF) grown under control conditions. In this work, fruit at 10–14, 18–26, 34, and 42 DAF were defined as immature green, mature green, yellow, and red stages, respectively. (B) Fresh weight (shaded bars) and brix (%) (black circles) of red-ripe fruit grown under control (0 mM NaCl) and various salinity conditions (80–160 mM NaCl). Right and left vertical axes correspond to brix (%) and fresh weight, respectively. Values are means ±SD (n=50). Different letters indicate statistical significance of means estimated using Fisher's PLSD test (P <0.05).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2803223&req=5

fig1: Fruit development of cv. ‘Micro-Tom’. (A) Flowering (0) and fruit at 10, 14, 18, 22, 26, 34, and 42 d after flowering (DAF) grown under control conditions. In this work, fruit at 10–14, 18–26, 34, and 42 DAF were defined as immature green, mature green, yellow, and red stages, respectively. (B) Fresh weight (shaded bars) and brix (%) (black circles) of red-ripe fruit grown under control (0 mM NaCl) and various salinity conditions (80–160 mM NaCl). Right and left vertical axes correspond to brix (%) and fresh weight, respectively. Values are means ±SD (n=50). Different letters indicate statistical significance of means estimated using Fisher's PLSD test (P <0.05).
Mentions: Fruits were sampled from plants grown under the two growth conditions at 10, 14, 18, 22, 26, 34, and 42 DAF as shown in Fig. 1A. At the start of this experiment, the effect of salinity intensity on fruit brix (%) and fresh weight of red ripe fruit in cv. ‘Micro-Tom’ was examined (Fig. 1B). Fruit brix (%) increased in response to the elevation of the stress level of the salinity and finally reached 1.6-times that of control fruit in the 160 mM NaCl condition. By contrast, fresh fruit weight decreased to 82–62% of the control in the given salinity conditions exhibiting an inverse correlation to the brix. Although size of the plants was concomitantly decreased under the salinity stress, the ratio of fruits to foliage was kept almost the same in both of the conditions on a fresh and a dry weight basis (see Supplementary Fig. S2 at JXB online). In order to dissect the dynamic alteration of carbohydrate in salinity-stressed fruit, plants treated with 160 mM NaCl were investigated using the following analyses. To avoid an excessive concentration effect due to the salinity stress, similar sized fruits were selectively used between both conditions in each developmental stage through the present work (see Supplementary Fig. S1 at JXB online). Soluble sugar contents (glucose, fructose, and sucrose) of developing fruits were determined in fresh fruit grown under saline and normal conditions (Fig. 2). In the control fruits, sugar levels gradually decreased (glucose, sucrose, and total sugar) or were unchanged (fructose) during fruit development (10–34 DAF) and, apart from sucrose, increased slightly by the end of the maturation stage (42 DAF). Sugar levels of salinity-stressed fruit were unchanged at 34 DAF but had increased substantially by 42 DAF; however, only sucrose had been kept at a similar level during this period even under saline conditions. Salinity stress enhanced the accumulation of glucose by 2.43 times, fructose by 2.05 times, sucrose by 7.87 times, and total sugars by 2.27 times at 42 DAF compared with those of the control. The promotion effect of the salinity stress on the accumulation of soluble sugars in red-ripe fruit was also confirmed on a dry weight basis (see Supplementary Fig. S3 at JXB online). Water contents were 90.7 (10 DAF), 91.8 (18 DAF), 89.9 (26 DAF), and 93.2% (42 DAF) in control fruits and 85.9 (10 DAF), 85.8 (18 DAF), 86.7 (26 DAF), and 90.9% (42 DAF) in the salinity-stressed fruits (data not shown). In contrast to the sugar contents, salinity stress enhanced starch accumulation during the early fruit development stages by 5.04 (10 DAF), 2.13 (18 DAF), and 2.91 (26 DAF) times compared to those of the control, respectively. Accumulation of starch granules in the fruits at 10 DAF was visualized by Periodic acid–Schiff (PAS) staining (see Supplementary Fig. S4 at JXB online). Figure 3 shows that enhanced starch accumulation was observed in the fruit of plants exposed to the salinity stress in developmental fruits. However, in the pericarp, starch only accumulated in the inner pericarp but not in the outer pericarp and exocarp (see Supplementary Fig. S4A, D at JXB online). By 26 DAF, starch had started to disappear from control fruit but was still accumulating in the salinity-stressed fruit. In those fruit, starch disappearance was delayed compared to the control (34 DAF).

Bottom Line: Tracer analysis with (13)C confirmed that elevated carbohydrate accumulation in fruits exposed to salinity stress was confined to the early development stages and did not occur after ripening.The results indicate that salinity stress enhanced carbohydrate accumulation as starch during the early development stages and it is responsible for the increase in soluble sugars in ripe fruit.These results indicate AgpL1 and AgpS1 are involved in the promotion of starch biosynthesis under the salinity stress in ABA- and osmotic stress-independent manners.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennoudai, Tsukuba, Ibaraki, Japan.

ABSTRACT
Salinity stress enhances sugar accumulation in tomato (Solanum lycopersicum) fruits. To elucidate the mechanisms underlying this phenomenon, the transport of carbohydrates into tomato fruits and the regulation of starch synthesis during fruit development in tomato plants cv. 'Micro-Tom' exposed to high levels of salinity stress were examined. Growth with 160 mM NaCl doubled starch accumulation in tomato fruits compared to control plants during the early stages of development, and soluble sugars increased as the fruit matured. Tracer analysis with (13)C confirmed that elevated carbohydrate accumulation in fruits exposed to salinity stress was confined to the early development stages and did not occur after ripening. Salinity stress also up-regulated sucrose transporter expression in source leaves and increased activity of ADP-glucose pyrophosphorylase (AGPase) in fruits during the early development stages. The results indicate that salinity stress enhanced carbohydrate accumulation as starch during the early development stages and it is responsible for the increase in soluble sugars in ripe fruit. Quantitative RT-PCR analyses of salinity-stressed plants showed that the AGPase-encoding genes, AgpL1 and AgpS1 were up-regulated in developing fruits, and AgpL1 was obviously up-regulated by sugar at the transcriptional level but not by abscisic acid and osmotic stress. These results indicate AgpL1 and AgpS1 are involved in the promotion of starch biosynthesis under the salinity stress in ABA- and osmotic stress-independent manners. These two genes are differentially regulated at the transcriptional level, and AgpL1 is suggested to play a regulatory role in this event.

Show MeSH