Skip to main content
SpringerLink
Log in

Functional Analysis of VvBG1 During Fruit Development and Ripening of Grape

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

β-glucosidase (BG) was believed to take part in abscisic acid (ABA) synthesis via hydrolysis of ABA glucose ester to release active ABA during plant growth and development. However, there is no genetic evidence available to indicate the role of genes during fruit ripening. Here, the expression patterns of three genes (VvBG1, VvBG2, and VvBG3) encoding β-glucosidase were analyzed during grape fruit development, and it was found that β-glucosidase activity increased in grape fruit in response to various stresses. Furthermore, to verify the function of β-glucosidase during fruit ripening, heterogeneous expression of the VvBG1 gene in strawberry fruit was validated, and the results showed that the VvBG1 over-expression increased β-glucosidase and promoted the fruit ripening process in strawberry. In addition, we found that ABA contents increased in the VvBG1 over-expression of strawberry fruit, which induced fruit anthocyanin, soluble solid accumulation, and fruit softening. Moreover, genes related to coloring (CHS, CHI, F3H, and UFGT), softening (PG1, PL1, and EXP1), and aroma (SAAT, and QR) were up-regulated. This work will elucidate the specific roles of VvBGs in the synthesis of ABA and provide some new insights into the ABA-controlled grape ripening mechanism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055

    Article  CAS  PubMed  Google Scholar 

  • Audran C, Borel C, Frey A, Sotta B, Meyer C, Simonneau T, Marion-Poll A (1998) Expression studies of the zeaxanthin epoxidase gene in Nicotiana plumbaginifolia. Plant Physiol 118:1021–1028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ban T, Ishimaru M, Kobayashi S, Goto-Yamamoto SN, Horiuchi S (2003) Abscisic acid and 2,4-dichlorophenoxyacetic acid affect the expression of anthocyanin biosynthetic pathway genes in ‘Kyoho’ grape berries. J Hortic Sci Biotech 78:586–589

    Article  CAS  Google Scholar 

  • Bogs J, Jaffe FW, Takos AM, Walker AR, Robinson SP (2007) The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol 143(3):1347–1361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castellarin SD, Gambetta GA, Wada H, Krasnow MN, Cramer GR, Peterlunger E, Shackel KA, Matthews MA (2015) Characterization of major ripening events during softening in grape: turgor, sugar accumulation, abscisic acid metabolism, colour development, and their relationship with growth. J Exp Bot 67:erv483

    Google Scholar 

  • Chai YM, Jia HF, Li CL, Dong QH, Shen YY (2011) FaPYR1 is involved in strawberry fruit ripening. J Exp Bot 62:5079–5089

    Article  CAS  PubMed  Google Scholar 

  • Chernys JT, Zeevaart JAD (2007) Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol 124:343–353

    Article  Google Scholar 

  • Coombe BG (1976) The development of fleshy fruits. Ann Rev Plant Physiol 27:507–528

    Article  Google Scholar 

  • Deluc LG, Quilici DR, Decendit A, Grimplet J, Wheatley MD, Schlauch KA, Merillon JM, Cushman JC, Cramer GR (2009) Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay. BMC Genom 10:212

    Article  CAS  Google Scholar 

  • Esen A (1993) β-Glucosidases. In: Esen A (ed) β-Glucosidases: biochemistry and molecular biology. ACS symposium series. American Chemical Society, Washington, pp 1–14

    Chapter  Google Scholar 

  • Finkelstein RR, Gampala S, Rock C (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl. 1):S15–S45

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galpaz N, Wang Q, Menda N, Zair D, Hirschberg J (2008) Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J 53(5):717–730

    Article  CAS  PubMed  Google Scholar 

  • Gambetta GA, Matthews MA, Shaghasi TH, McElrone AJ, Castellarin SD (2010) Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape. Planta 232:219–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giovannoni JJ (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol 52:725–749

    Article  CAS  PubMed  Google Scholar 

  • Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16:170–180

    Article  Google Scholar 

  • Giribaldi M, Gény L, Delrot S, Schubert A (2010) Proteomic analysis of the effects of ABA treatments on ripening Vitis vinifera berries. J Exp Bot 61:2447–2458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang CL, Zhang DP, Jia WS (2001) A study of the sources of abscisic acid in grape berry during its late developmental phases. Acta Hortic Sin 28:385–391

    Google Scholar 

  • Hoth S, Morgante M, Sanchez JP, Hanafey MK, Tingey SV, Chua NH (2002) Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J Cell Sci 115:4891–4900

    Article  CAS  PubMed  Google Scholar 

  • Kleczkowski K, Schell J (1995) Phytohormone conjugates: nature and function. Crit Rev Plant Sci 14:283–298

    Article  CAS  Google Scholar 

  • Kobashi K, Gemma H, Iwahori S (2000) Abscisic acid content and sugar metabolism of peaches grown under water stress. J Am Soc Hortic Sci 125(4):425–428

    CAS  Google Scholar 

  • Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Shinozaki KY, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia HF, Wang YH, Sun MZ et al (2013) Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytol 198(2):453–465

    Article  CAS  PubMed  Google Scholar 

  • Kleczkowski K, Schell J, Bandur DR (1995) Phytohormone conjugates: nature and function. Plant Sci 14:283–298

    Article  CAS  Google Scholar 

  • Koyama K, Sadamatsu K, Goto-Yamamoto N (2010) Abscisic acid stimulated ripening and gene expression in berry skins of the Cabernet Sauvignon grape. Funct Integr Genomics 10:367–381

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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. Func Integr Genomics 10:135–146

    Article  CAS  Google Scholar 

  • 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. J Plant Physiol 169(1):78–85

    Article  CAS  PubMed  Google Scholar 

  • Morant AV, Jørgensen K, Jørgensen C, Paquette SM, Sάnchez-Pèrez R, Møller BL, Bak S (2008) β–Glucosidases as detonators of plant chemical defense. Phytochemistry 69:1795–1813

    Article  CAS  PubMed  Google Scholar 

  • Nambara E, Marion-poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  CAS  PubMed  Google Scholar 

  • Owen SJ, Lafond MD, Bowen P, Bogdanoff C, Usher K, Abrams SR (2009) Profiles of abscisic acid and its catabolites in developing merlot grape (Vitis vinifera) berries. Am J Enol Vitic 60:277–284

    CAS  Google Scholar 

  • Ren J, Sun L, Wu JF, Zhao SL, Wang CL, Wang YP, Ji K, Leng P (2010) Cloning and expression analysis of cDNAs for ABA 8′-hydroxylase during sweet cherry fruit maturation and under stress conditions. J Plant Physiol 167:1486–1493

    Article  CAS  PubMed  Google Scholar 

  • Rodrigo MJ, Marcos JF, Alferez F, Mallent MD, Zacarias L (2003) Characterization of pinalate, a novel Citrus sinensis mutant with a fruit-specific alteration that results in yellow pigmentation and decreased ABA content. J Exp Bot 54(383):727–738

    Article  CAS  PubMed  Google Scholar 

  • Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302

    Article  CAS  PubMed  Google Scholar 

  • Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48

    Article  CAS  PubMed  Google Scholar 

  • Soto A, Ruiz KB, Ravaglia D, Costa G, Torrigiani P (2013) ABA may promote or delay peach fruit ripening through modulation of ripening- and hormone-related gene expression depending on the developmental stage. Plant Physiol Biochem 64:11–24

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Zhang M, Ren J, Qi JX, Zhang GJ, Leng P (2010) Reciprocity between abscisic acid and ethylene at the onset of berry ripening and after harvest. BMC Plant Biol 10:257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun L, Wang YP, Chen P, Ren J, Ji K, Li Q, Li P, Dai SJ, Leng P (2011) Transcriptional regulation of SlPYL, SlPP2C and SlSnRK2 gene families encoding ABA signal core components during tomato fruit development and drought stress. J Exp Bot 62:5659–5669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun L, Yuan B, Zhang M, Wang L, Cui MM, Wang Q, Leng P (2012a) Fruit-specific RNAi-mediated suppression of SlNCED1 increases both lycopene and b–carotene contents in tomato fruit. J Exp Bot 63:3097–3108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun L, Sun YF, Zhang M et al (2012b) Suppression of 9–cis-epoxycarotenoid dioxygenase (NCED), which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomatoes. Plant Physiol 158:283–298

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun YF, Chen P, Duan CR et al (2013) Transcriptional regulation of genes encoding key enzymes of abscisic acid metabolism during melon (Cucumis melo L.) fruit development and ripening. J Plant Growth Regul 32:233–244

    Article  CAS  Google Scholar 

  • Taylor IB, Burbidge A, Thompson AJ (2000) Control of abscisic acid synthesis. J Exp Bot 51:1563–1574

    Article  CAS  PubMed  Google Scholar 

  • Wang YP, Wang Y, Ji K et al (2013) The role of abscisic acid in regulating cucumber fruit development and ripening and its transcriptional regulation. Plant Physiol Biol 64:70–79

    Article  CAS  Google Scholar 

  • Wegrzyn TF, MacRae EA (1992) Pectinesterase, polygalacturonase, and β-galactosidase during softening of ethylene-treated kiwifruit. HortScience 27:900–902

    CAS  Google Scholar 

  • Wheeler S, Loveys B, Ford C, Davies C (2009) The relationship between the expression od abscisic acid biosynthesis genes, accumulation of abscisic acid and the promotion of Vitis vinifera L. berry ripening by abscisic acid. Aust J Grape Wine Res 15:195–204

    Article  CAS  Google Scholar 

  • Zaharah SS, Singh Z, Symons GM, Rei JB (2013) Mode of action of abscisic acid in triggering ethylene biosynthesis and softening during ripening in mango fruit. Postharvest Biol Technol 75:37–44

    Article  CAS  Google Scholar 

  • Zhang JJ, Wang X, Yu O, Tang JJ, Gu XG, Wan XC, Fang CB (2011) Metabolic profiling of strawberry (Fragaria × ananassa Duch.) during fruit development and maturation. J Exp Bot 62:1103–1118

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to express our gratitude to Jiangsu Academy of Agricultural Sciences for providing the grape material. This work was supported by the China National Natural Science Fund (31401847, 31401846), the Natural Science Foundation of China (31361140358), Jiangsu Natural Science Fund (BK20140707), China Postdoctoral Science Fund (2014M561663), and the Central university basic research and operating expenses of special funding (KJQN201541).

Author information

Authors and Affiliations

  1. Key Laboratory of Genetics and Fruit Development, Horticultural College, Nanjing Agricultural University, NO. 1 Weigang, Xuanwu, Nanjing, 210095, Jiangsu, People’s Republic of China

    Haifeng Jia, Chen Wang, Cheng Zhang, Muhammad Salman Haider, Pengcheng Zhao, Zhongjie Liu, Lingfei Shangguan, Tariq Pervaiz & Jinggui Fang

Authors
  1. Haifeng Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Muhammad Salman Haider
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pengcheng Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhongjie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lingfei Shangguan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tariq Pervaiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jinggui Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Haifeng Jia or Jinggui Fang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jia, H., Wang, C., Zhang, C. et al. Functional Analysis of VvBG1 During Fruit Development and Ripening of Grape. J Plant Growth Regul 35, 987–999 (2016). https://doi.org/10.1007/s00344-016-9597-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-016-9597-y

Keywords

Search

Navigation