Abstract
The aim of this study was to examine the effect of abscisic acid (ABA), sucrose, and auxin on grape fruit development and to assess the mechanism of these three factors on the grape fruit ripening process. Different concentrations of ABA, sucrose, and auxin were used to treat the grape fruit, and the ripening-related indices, such as physiological and molecular level parameters, were analyzed. The activity of BG protein activity was analyzed during the fruit development. Sucrose, ABA, and auxin influenced the grape fruit sugar accumulation in different ways, as well as the volatile compounds, anthocyanin content, and fruit firmness. ABA and sucrose induced, but auxin blocked, the ripening-related gene expression levels, such as softening genes PE, PG, PL, and CELL, anthocyanin genes DFR, CHI, F3H, GST, CHS, and UFGT, and aroma genes Ecar, QR, and EGS. ABA, sucrose, and glucose induced the fruit dry weight accumulation, and auxin mainly enhanced fruit dry weight through seed weight accumulation. In the early development of grape, starch was the main energy storage; in the later, it was glucose and fructose. Sucrose metabolism pathway-related gene expression levels were significant for glucose and fructose accumulation. BG protein activity was important in the regulation of grape ABA content levels. ABA plays a core role in the grape fruit development; sucrose functions in fruit development through two pathways: one was ABA dependent, the other ABA independent. Auxin blocked ABA accumulation to regulate the fruit development process.
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Abbreviations
- ABA:
-
Abscisic acid
- IAA:
-
Indole-3-acetic acid
- NDGA:
-
Nordihydroguaiaretic acid
- NPA:
-
1-N-Naphthylphthalamic acid
Reference
Ai TN, Naing AH, Arun M, Lim SH, Kim CK (2016) Sucrose-induced anthocyanin accumulation in vegetative tissue of Petunia plants requires anthocyanin regulatory transcription factors. Plant Sci 252:144–150
Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055
Anderson JV, Doğramacı M, Horvath DP, Foley ME, Chao WS, Suttle JC, Thimmapuram J, Hernandez AG, Ali S, Mikel MA (2012) Auxin and ABA act as central regulators of developmental networks associated with paradormancy in Canada thistle (Cirsium arvense). Functional Integrative Genomics 12(3):515–531
Andrews PK, Li S (1995) Cell wall hydrolytic enzyme activity during development of nonclimacteric sweet cherry (Pruns avium L.) fruit. J. Hortic Sci 70:561–567
Baker RF, Leach KA, Boyer NR, Swyers MJ, Benitez-Alfonso Y, Skopelitis T, Luo A, Sylvester A, Jackson D, Braun DM (2016) Sucrose transporter ZmSut1 expression and localization uncover new insights into sucrose phloem loading. Plant Physiology pp.00884.
Basson CE, Groenewald JH, Kossmann J et al (2010) Sugar and acid-related quality attributes and enzyme activities in strawberry fruits: invertase is the main sucrose hydrolysing enzyme. Food Chem 121(4):1156–1162
Cakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R (2003) A grape ASR protein involved in sugar and abscisic acid signaling. Plant Cell 15:2165–2180
Coombe BG (1992) Research on development and ripening of the grape berry. Am J Enol Vitic 43:101–110
Corso M, Vannozzi A, Ziliotto F, Zouine M, Maza E, Nicolato T, Vitulo N, Meggio F, Valle G, Bouzayen M, Müller M, Munné-Bosch S, Lucchin M, Bonghi C (2016) Grapevine rootstocks differentially affect the rate of ripening and modulate auxin-related genes in cabernet sauvignon berries. Front Plant Sci 7(382)
Dong J, Zhang YT, Tang XW, Jin WM, Han ZH (2013) Differences in volatile ester composition between Fragaria×ananassa and F. vesca and implications for strawberry aroma patterns. Sci Horti (Amsterdam) 150:47–53
Engelen FAV, Molthoff JW, Conner AJ, Nap JP, Pereira A, Stiekema WJ (1995) pBINPLUS: an improved plant transformation vector based on pBIN19. Transgen Res 4:288–290
Fernie AR, Roessner U, Geigenberger P (2001) The sucrose analog palatinose leads to a stimulation of sucrose degradation and starch synthesis when supplied to discs of growing potato tubers. Plant Physiol 125:1967–1977
Fu FQ, Mao WH, Shi K, Zhou YH, Asami T et al (2008) A role of brassinosteroids in early fruit development in cucumber. J Exp Bot 59:2299–2308
Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102
Giovannoni JJ (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol 52:725–749
Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16:170–180
Han Y, Dang RH, Li JX, Jiang J, Zhang N, Jia MR, Wei LZ, Li ZQ, Li BB, Jia WS (2015) SUCROSE NONFERMENTING1-RELATED PROTEIN KINASE2.6, an ortholog of OPEN STOMATA1, is a negative regulator of strawberry fruit development and ripening. Plant Physiol 167(3):915–930
Hardie WJ, O'brien TP, Jaudzems VG (1996) Morphology, anatomy and development of the pericarp after anthesis in grape, Vitis vinifera L. Aust J Grape Wine Res 2(2):97–142
Hardy J (1967) Sucrose breakdown and synthesis in the ripening grape berry. Aust J Biol Sci 20:465–470
Huang H, Xie S, Xiao Q, Wei B, Zheng L, Wang Y, Cao Y, Zhang X, Long T, Li Y, Hu Y, Yu G, Liu H, Liu Y, Huang Z, Zhang J, Huang Y (2016) Sucrose and ABA regulate starch biosynthesis in maize through a novel transcription factor, ZmEREB156. Sci Rep 6:27590
Jia HF, Chai YM, Li CL, Lu D, Luo JJ, Qin L, Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157:188–199
Jia HF, Zhang C, Pervaiz T, Zhao PC, Liu ZJ, Wang BJ, Wang C, Zhang L, Fang JG, Qian JP (2015) Jasmonic acid involves in grape fruit ripening and resistant against botrytis cinerea. Functional Integrative Genomics 16(1):1–16
Kaplan F, Guy CL (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44(5):730–743
Koyama K, Sadamatsu K, Goto-Yamamoto N (2010) Abscisic acid stimulated ripening and gene expression in berry skins of the Cabernet Sauvignon grape. Functional Integrative Genomics 10(3):367–381
Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109–1120
Lee S, Chung EJ, Joung YH, Choi D (2010) Non-climacteric fruit ripening in pepper: increased transcription of EIL-like genes normally regulated by ethylene. Functional Integrative Genomics 10:135–146
Li Q, Li P, Sun L, Wang Y, Ji K, Sun Y, Dai S, Chen P, Duan C, Leng P (2012) Expression analysis of β-glucosidase genes that regulate abscisic acid homeostasis during watermelon(Citrullus lanatus) development and under stress conditions. Journal Plant Physiology 169(1):78–85
Nambara E, Marion-poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185
Nardozza S, Boldingh HL, Osorio S et al (2013) Metabolic analysis of kiwifruit (Actinidia deliciosa) berries from extreme genotypes reveals hallmarks for fruit starch metabolism. J Exp Bot 64(16):5049–5063
Neta-Sharir I, Shoseyov O, Weiss D (2000) Sugars enhance the expression of gibberellin-induced genes in developing petunia flowers. Physiol Plant 109(2):196–202
Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150
Qin G, Zhu Z, Wang W, Cai J, Chen Y, Li L, Tian S (2016) A tomato vacuolar invertase inhibitor mediates sucrose metabolism and influences fruit ripening. Plant Physiology pp.01269.
Robinson NL, Hewitt JD, Bennett AB (1988) Sink metabolism in tomato fruit I. Developmental changes in carbohydrate metabolizing enzymes Plant Physiology 87(3):727–730
Seymour GB, Østergaard L, Chapman NH, Knapp S, Martin C (2013) Fruit development and ripening. Annu Rev Plant Biol 64:219–241
Solfanclli C, Poggi A, Loreti E (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140:637–646
Su L, Diretto G, Purgatto E, Danoun S, Zouine M, Li Z, Roustan JP, Bouzayen M, Giuliano G, Chervin C (2015) Carotenoid accumulation during tomato fruit ripening is modulated by the auxin-ethylene balance. BMC Plant Biol 15:114
Sun C, Palmqvist S, Olsson H (2003) A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter. Plant Cell 15:2076–2092
Symons G, Davies C, Shavrukov Y, Dry I, Reid J et al (2006) Grapes on steroids. Brassinosteroids are involved in grape berry ripening Plant Physiol 140:150–158
Tadiello A, Ziosi V, Negri AS, Noferini M, Fiori G, Busatto N, Espen L, Costa G12, Trainotti L (2016) On the role of ethylene, auxin and a GOLVEN-like peptide hormone in the regulation of peach ripening. BMC Plant Biol 16:44
Trainotti L, Tadiello A, Casadoro G (2007) The involvement of auxin in the ripening of climacteric fruits comes of age: the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. J Exp Bot 58:3299–3308
Villalobos-González L, Peña-Neira A, Ibáñez F, Pastenes C (2016) Long-term effects of abscisic acid (ABA) on the grape berry phenylpropanoid pathway: gene expression andmetabolite content. Plant Physiol Biochem 105:213–223
Wang N, Duhita N, Ariizumi T, Ezura H (2016) Involvement of vacuolar processing enzyme slvpe5 in post-transcriptional process of invertase in sucrose accumulation in tomato. Plant Physiology Biochemistry 108:71–78
Wegrzyn TF, MacRae EA (1992) Pectinesterase, polygalacturonase, and β-galactosidase during softening of ethylene-treated kiwifruit. Hortscience 27:900–902
Xing L, Zhao Y, Gao J, Xiang C, Zhu JK (2016) The ABA receptor PYL9 together with PYL8 plays an important role in regulating lateral root growth. Sci Rep 6:27177
Yuan RC, Carbaugh DH (2007) Effects of NAA, AVG, and 1-MCP on ethylene biosynthesis, preharvest fruit drop, fruit maturity, and quality of ‘Golden supreme’ and ‘Golden delicious’ apples. Hortscience 42:101–105
Zhang M, Leng P, Zhang GL, Li XX (2009) Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. J Plant Physiol 166:1241–1252
Acknowledgements
We would like to express our gratitude to Jiangsu Academy of Agricultural Sciences for providing the grape material. This work was supported by the Jiangsu Natural Science Fund (BK20140707), Key Laboratory of the Ministry of Agriculture (ZW2014009), China National Natural Science Fund (31401847), China National Natural State Key Laboratory of the Ministry of Agriculture (NYB-201508-1) Science Fund (31361140358), and State Key Laboratory of the Ministry of Agriculture (NYB-201508-1).
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Jia, H., Xie, Z., Wang, C. et al. Abscisic acid, sucrose, and auxin coordinately regulate berry ripening process of the Fujiminori grape. Funct Integr Genomics 17, 441–457 (2017). https://doi.org/10.1007/s10142-017-0546-z
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DOI: https://doi.org/10.1007/s10142-017-0546-z