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

Journal of Experimental Botany, Jan 2010

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 13C 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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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

Yong-Gen Yin 1 Yoshie Kobayashi 1 Atsuko Sanuki 1 Satoru Kondo 0 Naoya Fukuda 1 Hiroshi Ezura 1 Sumiko Sugaya 1 Chiaki Matsukura 1 0 Graduate School of Horticulture, Chiba University , Matsudo 648, Matsudo, Chiba, 271-8510, Japan 1 Graduate School of Life and Environmental Sciences, University of Tsukuba , 1-1-1 Tennoudai, Tsukuba, Ibaraki 305-8572, Japan 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 13C 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. - Salinity stress improves the fruit quality of tomato (Solanum lycopersicum) by increasing the level of total soluble solids, including sugars, organic acids, and amino acids in fruits (Tal et al., 1979; Ho et al., 1987; Adams, 1991; Balibrea et al., 1996, 1999; Gao et al., 1998; Krauss et al., 2006; Saito et al., 2008). An increase in soluble solids enhances not only the market value of fresh fruit but also its processing efficiency, because it increases flavour and lowers water content (Stark et al., 1996). Sugar content is most important in terms of fruit taste. Many studies have used model plants in an attempt to understand the mechanism of the effect of salinity stress in enhancing the accumulation of metabolites in plant tissues. However, in the tomato plant, most investigations into salinity stress have been agronomic and have tended to explain the phenomenon as a concentration effect due to a reduction in the size of the fruit (Ehret and Ho, 1986; Ho et al., 1987; Sakamoto et al., 1999). Invertase and sucrose synthase have been the enzymes most studied in order to elucidate the control mechanisms of sink strength and sugar level in fruit (Balibrea et al., 1996, 1999; reviewed in Nguyen-Quoc and Foyer, 2001). During the last decade, cell-wall invertase has attracted attention as a key player to determine fruit sugar level (Fridman et al., 2000, 2004; Baxter et al., 2005). In addition, there is positive correlation between cytoplasmic invertase and hexose contents in salinity-stressed fruit (Balibrea et al., 2006). On the other hand, early studies have related the level of soluble solids in ripe tomato fruit to the starch level in the immature and mature green fruit stages (Davies and Cocking, 1965; Dinar and Stevens, 1981; Schaffer and Petreikov, 1997). However, there is much less information regarding the regulation of starch biosynthesis and accumulation by invertase (Ntchobo et al., 1999; Li et al., 2002). ADP-glucose pyrophosphorylase (AGPase, EC 2.7.7.27) has been proposed to regulate starch biosynthesis during the early stages of the developing fruit (Schaffer and Petreikov, 1997; Schaffer et al., 2000). AGPase catalyses the synthesis of ADP-glucose from glucose-1-phosphate and ATP (Preiss, 1988). Evidence from starch-deficient mutants, transgenic plants, and kinetic analyses has confirmed that this reaction is the first regulatory step in starch synthesis in plants (Tsai and Nelson, 1966; Lin et al., 1988; Mu llerRo ber et al., 1992; Stark et al., 1992). Plant AGPase is a hetero-tetrameric enzyme composed of two small and two large subunits, and all subunits are required for normal enzyme function. In tomato AGPase, there are two isoforms of the small subunit and three isoforms of the large subunit (Chen and Janes, 1997). One gene encoding the small subunit (AgpS1) and three genes encoding the large subunit (AgpL1, L2, and L3) have so far been isolated as cDNAs (Chen et al., 1998; (...truncated)


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Yong-Gen Yin, Yoshie Kobayashi, Atsuko Sanuki, Satoru Kondo, Naoya Fukuda, Hiroshi Ezura, Sumiko Sugaya, Chiaki Matsukura. 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, Journal of Experimental Botany, 2010, pp. 563-574, 61/2, DOI: 10.1093/jxb/erp333