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Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape.

Gambetta GA, Matthews MA, Shaghasi TH, McElrone AJ, Castellarin SD - Planta (2010)

Bottom Line: However, many fruits such as grape are nonclimacteric, where the onset of ripening results from the integration of multiple hormone signals including sugars and abscisic acid (ABA).Finally, exogenous sucrose and ABA regulated key orthologs in culture, similar to their regulation in the field.This study identifies novel candidates in the control of nonclimacteric fruit ripening and demonstrates that grape orthologs of key sugar and ABA-signaling components are regulated by sugar and ABA in fleshy fruit.

View Article: PubMed Central - PubMed

Affiliation: Department of Viticulture and Enology, University of California, Davis, CA 95616, USA. gagambetta@ucdavis.edu

ABSTRACT
The onset of ripening involves changes in sugar metabolism, softening, and color development. Most understanding of this process arises from work in climacteric fruits where the control of ripening is predominately by ethylene. However, many fruits such as grape are nonclimacteric, where the onset of ripening results from the integration of multiple hormone signals including sugars and abscisic acid (ABA). In this study, we identified ten orthologous gene families in Vitis vinifera containing components of sugar and ABA-signaling pathways elucidated in model systems, including PP2C protein phosphatases, and WRKY and homeobox transcription factors. Gene expression was characterized in control- and deficit-irrigated, field-grown Cabernet Sauvignon. Sixty-seven orthologous genes were identified, and 38 of these were expressed in berries. Of the genes expressed in berries, 68% were differentially expressed across development and/or in response to water deficit. Orthologs of several families were induced at the onset of ripening, and induced earlier and to higher levels in response to water deficit; patterns of expression that correlate with sugar and ABA accumulation during ripening. Similar to field-grown berries, ripening phenomena were induced in immature berries when cultured with sucrose and ABA, as evidenced by changes in color, softening, and gene expression. Finally, exogenous sucrose and ABA regulated key orthologs in culture, similar to their regulation in the field. This study identifies novel candidates in the control of nonclimacteric fruit ripening and demonstrates that grape orthologs of key sugar and ABA-signaling components are regulated by sugar and ABA in fleshy fruit.

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Summary of the gene families involved in sugar signaling examined in this work. Components are presented in their proposed positions in the signaling network. Gene families are 1 the putative SUT2 sucrose sensor, 2, 3 core G-protein signaling components GPA1 and RGS1, 4 hexokinases (Hxk), 6. Snf1-related kinases (SnRK1s), 7 WRKY transcription factors. The expression patterns of each gene in both control (C) and water deficit (ED) are summarized across three developmental stages I prior to the onset of ripening, II at the onset of ripening, and III late in ripening (See Supplemental File 1 for more detailed data). Asterisks denote significant changes in expression with time (P < 0.05, ANOVA), and boxes denote significant differences between treatments (P < 0.05, Tukey’s HSD). Mean level of expression in log2 copies/ng RNA are expressed categorically as false color according to the legend above (n = 3). Signaling network figure adapted from Rolland et al. (2006)
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Fig4: Summary of the gene families involved in sugar signaling examined in this work. Components are presented in their proposed positions in the signaling network. Gene families are 1 the putative SUT2 sucrose sensor, 2, 3 core G-protein signaling components GPA1 and RGS1, 4 hexokinases (Hxk), 6. Snf1-related kinases (SnRK1s), 7 WRKY transcription factors. The expression patterns of each gene in both control (C) and water deficit (ED) are summarized across three developmental stages I prior to the onset of ripening, II at the onset of ripening, and III late in ripening (See Supplemental File 1 for more detailed data). Asterisks denote significant changes in expression with time (P < 0.05, ANOVA), and boxes denote significant differences between treatments (P < 0.05, Tukey’s HSD). Mean level of expression in log2 copies/ng RNA are expressed categorically as false color according to the legend above (n = 3). Signaling network figure adapted from Rolland et al. (2006)

Mentions: Expression profiling was carried out in berry skins of field-grown Cabernet Sauvignon in order to identify those orthologs expressed during ripening. In addition, expression profiles under both control- and deficit-irrigated (denoted ED, Early water Deficit) conditions were compared in order to identify orthologs whose expression pattern reflected the advancement of ripening under ED. Water deficits were applied continuously from fruit set until to the onset of ripening, resulting in an average difference in midday leaf water potential of 0.36 MPa before the onset of ripening and no difference during ripening (Table 1). Of the 67 orthologous genes identified, 38 (57%) were expressed in grape berries. A summary of the expression profiles of all the genes examined in this study can be found in Figs. 4 and 5 while more detailed expression data is contained in Suppl. File 1. The majority of these genes were differentially regulated during berry development, with 26 (68%) exhibiting statistically significant changes with time in control and/or ED (Figs. 4, 5). There were few statistically significant differences in the magnitude of expression between control and ED (Figs. 4, 5, Suppl. File 1). Six genes exhibited statistically significant differences between control and ED. Four of these instances, VvHB8, VvSnRK5, VvPP2C-3, and VvPP2C-7, all exhibit elevated levels of expression in ED at or just prior to the onset of ripening (See Suppl. File 1 for exact expression values).Table 1


Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape.

Gambetta GA, Matthews MA, Shaghasi TH, McElrone AJ, Castellarin SD - Planta (2010)

Summary of the gene families involved in sugar signaling examined in this work. Components are presented in their proposed positions in the signaling network. Gene families are 1 the putative SUT2 sucrose sensor, 2, 3 core G-protein signaling components GPA1 and RGS1, 4 hexokinases (Hxk), 6. Snf1-related kinases (SnRK1s), 7 WRKY transcription factors. The expression patterns of each gene in both control (C) and water deficit (ED) are summarized across three developmental stages I prior to the onset of ripening, II at the onset of ripening, and III late in ripening (See Supplemental File 1 for more detailed data). Asterisks denote significant changes in expression with time (P < 0.05, ANOVA), and boxes denote significant differences between treatments (P < 0.05, Tukey’s HSD). Mean level of expression in log2 copies/ng RNA are expressed categorically as false color according to the legend above (n = 3). Signaling network figure adapted from Rolland et al. (2006)
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Related In: Results  -  Collection

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Fig4: Summary of the gene families involved in sugar signaling examined in this work. Components are presented in their proposed positions in the signaling network. Gene families are 1 the putative SUT2 sucrose sensor, 2, 3 core G-protein signaling components GPA1 and RGS1, 4 hexokinases (Hxk), 6. Snf1-related kinases (SnRK1s), 7 WRKY transcription factors. The expression patterns of each gene in both control (C) and water deficit (ED) are summarized across three developmental stages I prior to the onset of ripening, II at the onset of ripening, and III late in ripening (See Supplemental File 1 for more detailed data). Asterisks denote significant changes in expression with time (P < 0.05, ANOVA), and boxes denote significant differences between treatments (P < 0.05, Tukey’s HSD). Mean level of expression in log2 copies/ng RNA are expressed categorically as false color according to the legend above (n = 3). Signaling network figure adapted from Rolland et al. (2006)
Mentions: Expression profiling was carried out in berry skins of field-grown Cabernet Sauvignon in order to identify those orthologs expressed during ripening. In addition, expression profiles under both control- and deficit-irrigated (denoted ED, Early water Deficit) conditions were compared in order to identify orthologs whose expression pattern reflected the advancement of ripening under ED. Water deficits were applied continuously from fruit set until to the onset of ripening, resulting in an average difference in midday leaf water potential of 0.36 MPa before the onset of ripening and no difference during ripening (Table 1). Of the 67 orthologous genes identified, 38 (57%) were expressed in grape berries. A summary of the expression profiles of all the genes examined in this study can be found in Figs. 4 and 5 while more detailed expression data is contained in Suppl. File 1. The majority of these genes were differentially regulated during berry development, with 26 (68%) exhibiting statistically significant changes with time in control and/or ED (Figs. 4, 5). There were few statistically significant differences in the magnitude of expression between control and ED (Figs. 4, 5, Suppl. File 1). Six genes exhibited statistically significant differences between control and ED. Four of these instances, VvHB8, VvSnRK5, VvPP2C-3, and VvPP2C-7, all exhibit elevated levels of expression in ED at or just prior to the onset of ripening (See Suppl. File 1 for exact expression values).Table 1

Bottom Line: However, many fruits such as grape are nonclimacteric, where the onset of ripening results from the integration of multiple hormone signals including sugars and abscisic acid (ABA).Finally, exogenous sucrose and ABA regulated key orthologs in culture, similar to their regulation in the field.This study identifies novel candidates in the control of nonclimacteric fruit ripening and demonstrates that grape orthologs of key sugar and ABA-signaling components are regulated by sugar and ABA in fleshy fruit.

View Article: PubMed Central - PubMed

Affiliation: Department of Viticulture and Enology, University of California, Davis, CA 95616, USA. gagambetta@ucdavis.edu

ABSTRACT
The onset of ripening involves changes in sugar metabolism, softening, and color development. Most understanding of this process arises from work in climacteric fruits where the control of ripening is predominately by ethylene. However, many fruits such as grape are nonclimacteric, where the onset of ripening results from the integration of multiple hormone signals including sugars and abscisic acid (ABA). In this study, we identified ten orthologous gene families in Vitis vinifera containing components of sugar and ABA-signaling pathways elucidated in model systems, including PP2C protein phosphatases, and WRKY and homeobox transcription factors. Gene expression was characterized in control- and deficit-irrigated, field-grown Cabernet Sauvignon. Sixty-seven orthologous genes were identified, and 38 of these were expressed in berries. Of the genes expressed in berries, 68% were differentially expressed across development and/or in response to water deficit. Orthologs of several families were induced at the onset of ripening, and induced earlier and to higher levels in response to water deficit; patterns of expression that correlate with sugar and ABA accumulation during ripening. Similar to field-grown berries, ripening phenomena were induced in immature berries when cultured with sucrose and ABA, as evidenced by changes in color, softening, and gene expression. Finally, exogenous sucrose and ABA regulated key orthologs in culture, similar to their regulation in the field. This study identifies novel candidates in the control of nonclimacteric fruit ripening and demonstrates that grape orthologs of key sugar and ABA-signaling components are regulated by sugar and ABA in fleshy fruit.

Show MeSH
Related in: MedlinePlus