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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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Relative expression levels of AGPase genes in developing tomato fruit grown under control and saline conditions. (A) AgpL1, (B) AgpL2, (C) AgpL3, (D) AgpS1. Open and shaded columns indicate control (0 mM NaCl) and salinity (160 mM NaCl) treatments, respectively. The horizontal axis indicates fruit developing stages (DAF). Values are means ±SE (n=5). The asterisks indicate statistical significance of means in the same developing stage estimated using Fisher's PLSD test (*P <0.05, **P <0.01).
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fig7: Relative expression levels of AGPase genes in developing tomato fruit grown under control and saline conditions. (A) AgpL1, (B) AgpL2, (C) AgpL3, (D) AgpS1. Open and shaded columns indicate control (0 mM NaCl) and salinity (160 mM NaCl) treatments, respectively. The horizontal axis indicates fruit developing stages (DAF). Values are means ±SE (n=5). The asterisks indicate statistical significance of means in the same developing stage estimated using Fisher's PLSD test (*P <0.05, **P <0.01).

Mentions: Before performing a transcriptional analysis of AGPase, the effect of salinity stress on AGPase activity in ‘Micro-Tom’ fruit was confirmed. As shown in Fig. 6, fruit at the immature green stage (10–14 DAF) had high AGPase activity, but this activity declined at the mature green stage (18–26 DAF). Although it was not significant, salinity stress tended to enhance AGPase activity by almost 1.87 times that of the control at the immature green fruit stage, but activity was not affected in mature green fruit. To clarify how AGPase genes are regulated under the salinity stress at different development stages, the expression patterns of AgpL1, L2, L3, and S1 genes in developing fruit were investigated by qRT-PCR (Fig. 7). Transcriptional levels of the genes are presented relative to that of AgpL1 in control fruit at 10 DAF. In ‘Micro-Tom’ fruit, the major Agp isoforms were AgpS1, L1, and L2. The AgpL3 transcript was also detectable; however, it was only 1.8% of the AgpL1 transcription level in control fruit at 10 DAF (Fig. 7C). Of all the AGPase genes, AgpS1 showed the highest expression throughout fruit development, which corresponded to 7.6–11.1 times that of AgpL1 during the early developing stages (Fig. 7D). Of the large subunit-encoding genes, AgpL1 was the most highly expressed (Fig. 7A). During the early fruit development stages (10–22 DAF), AgpL1 and AgpS1 were strongly expressed and both were clearly up-regulated by salinity stress. The expression of both of these genes peaked at 10 DAF in the control and at 14 DAF in the salinity-stressed fruit. These expression levels declined rapidly after the peak. At 34 DAF, they decreased to 1.5% and 0.8% of each peak level in AgpL1, and 6.9% and 11.8% in AgpS1 in the control and salinity-stressed fruits, respectively. AgpL2 expression was less than half that of AgpL1 at most developmental stages and was relatively lower than the other two genes, changing little throughout fruit development (Fig. 7B).


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)

Relative expression levels of AGPase genes in developing tomato fruit grown under control and saline conditions. (A) AgpL1, (B) AgpL2, (C) AgpL3, (D) AgpS1. Open and shaded columns indicate control (0 mM NaCl) and salinity (160 mM NaCl) treatments, respectively. The horizontal axis indicates fruit developing stages (DAF). Values are means ±SE (n=5). The asterisks indicate statistical significance of means in the same developing stage estimated using Fisher's PLSD test (*P <0.05, **P <0.01).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig7: Relative expression levels of AGPase genes in developing tomato fruit grown under control and saline conditions. (A) AgpL1, (B) AgpL2, (C) AgpL3, (D) AgpS1. Open and shaded columns indicate control (0 mM NaCl) and salinity (160 mM NaCl) treatments, respectively. The horizontal axis indicates fruit developing stages (DAF). Values are means ±SE (n=5). The asterisks indicate statistical significance of means in the same developing stage estimated using Fisher's PLSD test (*P <0.05, **P <0.01).
Mentions: Before performing a transcriptional analysis of AGPase, the effect of salinity stress on AGPase activity in ‘Micro-Tom’ fruit was confirmed. As shown in Fig. 6, fruit at the immature green stage (10–14 DAF) had high AGPase activity, but this activity declined at the mature green stage (18–26 DAF). Although it was not significant, salinity stress tended to enhance AGPase activity by almost 1.87 times that of the control at the immature green fruit stage, but activity was not affected in mature green fruit. To clarify how AGPase genes are regulated under the salinity stress at different development stages, the expression patterns of AgpL1, L2, L3, and S1 genes in developing fruit were investigated by qRT-PCR (Fig. 7). Transcriptional levels of the genes are presented relative to that of AgpL1 in control fruit at 10 DAF. In ‘Micro-Tom’ fruit, the major Agp isoforms were AgpS1, L1, and L2. The AgpL3 transcript was also detectable; however, it was only 1.8% of the AgpL1 transcription level in control fruit at 10 DAF (Fig. 7C). Of all the AGPase genes, AgpS1 showed the highest expression throughout fruit development, which corresponded to 7.6–11.1 times that of AgpL1 during the early developing stages (Fig. 7D). Of the large subunit-encoding genes, AgpL1 was the most highly expressed (Fig. 7A). During the early fruit development stages (10–22 DAF), AgpL1 and AgpS1 were strongly expressed and both were clearly up-regulated by salinity stress. The expression of both of these genes peaked at 10 DAF in the control and at 14 DAF in the salinity-stressed fruit. These expression levels declined rapidly after the peak. At 34 DAF, they decreased to 1.5% and 0.8% of each peak level in AgpL1, and 6.9% and 11.8% in AgpS1 in the control and salinity-stressed fruits, respectively. AgpL2 expression was less than half that of AgpL1 at most developmental stages and was relatively lower than the other two genes, changing little throughout fruit development (Fig. 7B).

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