Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Grapevine fanleaf virus affects grape (Vitis vinifera) berry anthocyanin content via the transcriptional regulation of anthocyanin biosynthetic genes

Maja Rupnik-Cigoj A B C F , Anastazija Jež-Krebelj A B C , Simone D. Castellarin D , Kajetan Trošt A , Paolo Sivilotti A E and Maruša Pompe-Novak A B
+ Author Affiliations
- Author Affiliations

A School for Viticulture and Enology, University of Nova Gorica (UNG), Glavni trg 8, 5271 Vipava, Slovenia.

B Department of Biotechnology and Systems Biology, National Institute of Biology (NIB), Večna Pot 111, 1000 Ljubljana, Slovenia.

C Regional Development Agency of Northern Primorska Ltd, Nova Gorica (RRA SP), Trg Edvarda Kardelja 3, 5000 Nova Gorica.

D Wine Research Centre, The University of British Columbia, 2205 East Mall, Vancouver, BC, Canada.

E University of Udine, Department of Agricultural, Food, Environmental and Animal Sciences, via delle Scienze 206, Udine, Italy.

F Corresponding author. Email: maja.cigoj1@gmail.com

Functional Plant Biology 45(7) 771-782 https://doi.org/10.1071/FP18014
Submitted: 14 April 2017  Accepted: 24 January 2018   Published: 13 March 2018

Abstract

Grapevine fanleaf virus (GFLV) causes grapevine fanleaf degeneration, one of the oldest known viral diseases of grapevines. The virus has been found in all winegrowing regions around the world. In the seasons 2011–12 a comparison between field grown GFLV-infected and healthy grapevines was conducted for the cultivars Schioppettino in North-Eastern Italy and Refošk in South-Western Slovenia. Our research showed that GFLV infection caused a drop of the yield due to reduction of both cluster weight and berry weight. Besides the yield, the berry composition was also affected; in detail, anthocyanin concentration increased in both varieties but significantly only in the case of Schioppettino. Upregulation of the F3ʹ5ʹH gene and downregulation of F3ʹH gene in the berries of GFLV infected vines compared with the ones of healthy control vines resulted in modified proportions between di- and tri- hydroxylated or methylated derivatives of anthocyanins. The F3H1 gene was identified to be the most strongly regulated gene of the flavonoid biosynthetic pathway by GFLV infection, indicating its important role in increasing anthocyanin concentration in grapes of GFLV infected vines as compared with healthy controls.

Additional keywords: anthocyanins, gene expression, grape quality, yield.


References

Andret-Link P, Laporte C, Ritzenthaler C, Demangeat G, Vigne E, Laval V (2004) Grapevine fanleaf virus: still a major threat to the grapevine industry. Journal of Plant Pathology 86, 183–195.

Baebler Š, Stare K, Kovač M, Blejec A, Prezelj N, Stare T, Kogovšek P, Pompe-Novak M, Rosahl S, Ravnikar M, Gruden K (2011) Dynamics of responses in compatible potato-potato virus Y interaction are modulated by salicylic acid. PLoS One 6, e29009
Dynamics of responses in compatible potato-potato virus Y interaction are modulated by salicylic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFemsA%3D%3D&md5=0a440138951bc2a576b440fd0a519adeCAS |

Barbagallo MG, Guidoni S, Hunter JJ (2011) Berry size and qualitative characteristics of Vitis vinifera L. cv. Syrah. South African Journal of Enology and Viticulture 32, 129–136.

Bogs J, Ebadi A, Mcdavid D, Robinson SP (2006) Identification of the flavonoid hydroxylases from grapevine and their regulation during fruit development. Plant Physiology 140, 279–291.
Identification of the flavonoid hydroxylases from grapevine and their regulation during fruit development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCgtro%3D&md5=e21ff8826bf3d43f6ddf9128ab25e3b6CAS |

Boss PK, Davies C, Robinson SP (1996) Analysis of the expression of anthocyanin pathway genes in developing Vitis vinifera L. cv. Shiraz grape berries and the implications for pathway regulation. Plant Physiology 111, 1059–1066.
Analysis of the expression of anthocyanin pathway genes in developing Vitis vinifera L. cv. Shiraz grape berries and the implications for pathway regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltVGgt78%3D&md5=d75a8ff1011bf2c6c22f167dd0fa9065CAS |

Bubola M, Sivilotti P, Janjanin D, Poni S (2017) Early leaf removal has a larger effect than cluster thinning on grape phenolic composition in cv. Teran. American Journal of Enology and Viticulture 68, 234–242.
Early leaf removal has a larger effect than cluster thinning on grape phenolic composition in cv. Teran.Crossref | GoogleScholarGoogle Scholar |

Cabaleiro C, Segura A, Garcia-Berrios JJ (1999) Effects of grapevine leafroll-associated virus 3 on the physiology and must of Vitis vinifera L. cv. Albariño following contamination in the field. American Journal of Enology and Viticulture 50, 40–44.

Castellarin SD, Di Gaspero G, Marconi R, Nonis A, Peterlunger E, Paillard S, Adam-Blondon AF, Testolin R (2006) Colour variation in red grapevines (Vitis vinifera L.): genomic organisation, expression of flavonoid 3ʹ-hydroxylase, flavonoid 3ʹ,5ʹ-hydroxylase genes and related metabolite profiling of red cyanidin/blue delphinidin-based anthocyanins in berry skin. BMC Genomics 7, 12
Colour variation in red grapevines (Vitis vinifera L.): genomic organisation, expression of flavonoid 3ʹ-hydroxylase, flavonoid 3ʹ,5ʹ-hydroxylase genes and related metabolite profiling of red cyanidin/blue delphinidin-based anthocyanins in berry skin.Crossref | GoogleScholarGoogle Scholar |

Castellarin SD, Pfeiffer A, Sivilotti P, Degan M, Peterlunger E, Di Gaspero G (2007) Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant, Cell & Environment 30, 1381–1399.
Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1yhsrnO&md5=45c76ac7b9b2a546ba8a4421015be53fCAS |

Čepin U, Gutiérrez-Aguirre I, Balažic L, Pompe-Novak M, Gruden K, Ravnikar M (2010) A one-step reverse transcription real-time PCR assay for the detection and quantitation of grapevine fanleaf virus. Journal of Virological Methods 170, 47–56.
A one-step reverse transcription real-time PCR assay for the detection and quantitation of grapevine fanleaf virus.Crossref | GoogleScholarGoogle Scholar |

Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B, Chermak D, Antony G, White FF, Somerville SC, Mudgett MB, Frommer WB (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527–532.
Sugar transporters for intercellular exchange and nutrition of pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVOrsbbM&md5=0ea5357aeb6c72f01f306163b2bdac0cCAS |

Chiumenti M, Mohorianu I, Roseti V, Saldarelli P, Dalmay T, Minafra A (2016) High-throughput-sequencing-based identification of a grapevine fanleaf virus satellite RNA in Vitis vinifera. Archives of Virology 161, 1401–1403.
High-throughput-sequencing-based identification of a grapevine fanleaf virus satellite RNA in Vitis vinifera.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XisFOnsb8%3D&md5=8b0748c260906d00ba007430a8265a0bCAS |

Choné X, Van Leeuwen C, Dubourdieu D, Gaudilleres JP (2001) Stem water potential is a sensitive indicator of grapevine water status. Annals of Botany 87, 477–483.
Stem water potential is a sensitive indicator of grapevine water status.Crossref | GoogleScholarGoogle Scholar |

Cretazzo E, Padilla C, Carambula C, Hita I, Salmer E, Cifre J (2010) Comparison of the effects of different virus infections on performance of three Majorcan grapevine cultivars in field conditions. Annals of Applied Biology 156, 1–12.
Comparison of the effects of different virus infections on performance of three Majorcan grapevine cultivars in field conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFOntbY%3D&md5=714d606557b6d96ca359edccd1fbea0cCAS |

Deluc LG, Quilici DR, Decendit A, Grimplet J, Wheatley MD, Schlauch KA, Mérillon J-M, 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 Genomics 10, 212
Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay.Crossref | GoogleScholarGoogle Scholar |

Engel EA, Escobar PF, Rojas LA, Rivera PA, Fiore N, Valenzuela PDT (2010) A diagnostic oligonucleotide microarray for simultaneous detection of grapevine viruses. Journal of Virological Methods 163, 445–451.
A diagnostic oligonucleotide microarray for simultaneous detection of grapevine viruses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtlekug%3D%3D&md5=65771a5fcf93c6a11667abfc6d40073cCAS |

Espinoza C, Vega A, Medina C, Schlauch K, Cramer G, Arce-Johnson P (2007) Gene expression associated with compatible viral diseases in grapevine cultivars. Functional & Integrative Genomics 7, 95–110.
Gene expression associated with compatible viral diseases in grapevine cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitVGqur4%3D&md5=6546b45b3dffe3820cbfaaa1d73d3ca7CAS |

Falginella L, Di Gaspero G, Castellarin SD (2012) Expression of flavonoid genes in the red grape berry of ‘Alicante Bouschet’ varies with the histological distribution of anthocyanins and their chemical composition. Planta 236, 1037–1051.
Expression of flavonoid genes in the red grape berry of ‘Alicante Bouschet’ varies with the histological distribution of anthocyanins and their chemical composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVWnsLrF&md5=55af17b682074e60c440c962004cc423CAS |

Ferrara G, Mazzeo A, Matarrese AMS, Pacucci C, Punzi R, Faccia M, Trani A, Gambacorta G (2015) Application of abscisic acid (S-ABA) and sucrose to improve colour, anthocyanin content and antioxidant activity of cv. crimson seedless grape berries. Australian Journal of Grape and Wine Research 21, 18–29.
Application of abscisic acid (S-ABA) and sucrose to improve colour, anthocyanin content and antioxidant activity of cv. crimson seedless grape berries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvV2hs74%3D&md5=1dac4cb6e3bb2654c35d5d75c98d652dCAS |

Fuchs M, Schmitt-Keichinger C, Sanfaçon H (2017) Chapter Two – A renaissance in nepovirus research provides new insights into their molecular interface with hosts and vectors. Advances in Virus Research 97, 61–105.
Chapter Two – A renaissance in nepovirus research provides new insights into their molecular interface with hosts and vectors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1c7islaluw%3D%3D&md5=db96b44c2d9e68e3f6bb86b87e91a1deCAS |

Goto-Yamamoto N, Wan GH, Masaki K, Kobayashi S (2002) Structure and transcription of three chalcone synthase genes of grapevine (Vitis vinifera). Plant Science 162, 867–872.
Structure and transcription of three chalcone synthase genes of grapevine (Vitis vinifera).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksVSns7s%3D&md5=a95dde2dc1ba705de62ef3ae94134c65CAS |

Gould KS, Lister C (2006) Flavonoid function in plants. In ‘Flavonoids: chemistry, biochemistry and applications’. (Eds OM Andersen, KR Markham) pp. 397–441. (CRC Press Taylor & Francis: Boca Raton, FL, USA)

Guan L, Dai Z, Wu BH, Wu J, Merlin I, Hilbert G, Renaud C, Gomès E, Edwards E, Li SH, Delrot S (2016) Anthocyanin biosynthesis is differentially regulated by light in the skin and flesh of white-fleshed and teinturier grape berries. Planta 243, 23–41.
Anthocyanin biosynthesis is differentially regulated by light in the skin and flesh of white-fleshed and teinturier grape berries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVGlsrnE&md5=3b86147bc1ebbc1648a917cdde7320beCAS |

Guidoni S, Hunter JJ (2012) Anthocyanin profile in berry skins and fermenting must/wine, as affected by grape ripeness level of Vitis vinifera cv. Shiraz/R99. European Food Research and Technology 235, 397–408.
Anthocyanin profile in berry skins and fermenting must/wine, as affected by grape ripeness level of Vitis vinifera cv. Shiraz/R99.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtF2rsrfN&md5=f342c26e0fdd91298ff60ad00f338afeCAS |

Guidoni S, Mannini F, Ferrandino A, Argamante N, Di Stefano R (1997) The effect of grapevine leafroll and rugose wood sanitation on agronomic performance and berry and leaf phenolic content of a ‘Nebbiolo’ clone (Vitis vinifera L.). American Journal of Enology and Viticulture 48, 438–442.

Gupta AK, Kaur N (2005) Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. Journal of Biosciences 30, 761–776.
Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnt1yhug%3D%3D&md5=89531e0388a1ffd8fc0cf7f9ebd4b62aCAS |

Hausmann L, Koglmeier W, During H, Salakhutdinov I, Zyprian E, Korn B, Velasco R, Topfer R (2003) High-density DNA arrays for grapevine research. Acta Horticulturae 135–138.
High-density DNA arrays for grapevine research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtVWqsLk%3D&md5=9c92388eaf8e7293c3e6220b50a45f7eCAS |

He T, Cramer GR (1996) Abscisic acid concentrations are correlated with leaf area reductions in two salt-stressed rapid-cycling Brassica species. Plant and Soil 179, 25–33.
Abscisic acid concentrations are correlated with leaf area reductions in two salt-stressed rapid-cycling Brassica species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XisFelsLY%3D&md5=489da0add8b6812ecf3ada51f2915fd1CAS |

Herrera JC, Bucchetti B, Sabbatini P, Comuzzo P, Zulini L, Vecchione A, Peterlunger E, Castellarin SD (2015) Effect of water deficit and severe shoot trimming on the composition of Vitis vinifera L. Merlot grapes and wines. Australian Journal of Grape and Wine Research 21, 254–265.
Effect of water deficit and severe shoot trimming on the composition of Vitis vinifera L. Merlot grapes and wines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXpt1Kktrw%3D&md5=e407fc6e718a83cdabce24f99ef7bbf6CAS |

Hewitt WB, Goheen AC, Raski DJ, Gooding GVJ (1962) Studies on virus diseases of the grapevine in California. Vitis 3, 57–83.

Hunter JJ, Pisciotta A, Voschenk CG, Archer E, Novello V, Deloire A, Nadal M (2004) Role of harvesting time/optimal ripeness in zone/terroir expression. In ‘Proceedings for the Joint Conference on Viticultural Zoning’, November 2004, Cape Town, South Africa. pp. 466–478.

Hren M, Nikolić P, Rotter A, Blejec A, Terrier N, Ravnikar M, Dermastia M, Gruden K (2009) ‘Bois noir’ phytoplasma induces significant reprogramming of the leaf transcriptome in the field grown grapevine. BMC Genomics 10, 460
‘Bois noir’ phytoplasma induces significant reprogramming of the leaf transcriptome in the field grown grapevine.Crossref | GoogleScholarGoogle Scholar |

Jeong ST, Goto-Yamamoto N, Hashizume K, Esaka M (2006) Expression of the flavonoid 3ʹ-hydroxylase and flavonoid 3ʹ,5ʹ-hydroxylase genes and flavonoid composition in grape (Vitis vinifera). Plant Science 170, 61–69.
Expression of the flavonoid 3ʹ-hydroxylase and flavonoid 3ʹ,5ʹ-hydroxylase genes and flavonoid composition in grape (Vitis vinifera).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFektbrF&md5=403cf0a150d0d950afe8ca95563d37beCAS |

Kliewer MW, Dokoozlian NK (2005) Leaf area/crop weight ratios of grapevines: influence on fruit composition and wine quality. American Journal of Enology and Viticulture 56, 170–181.

Komar V, Vigne E, Demangeat G, Lemaire O (2008) Cross-protection as control strategy against grapevine fanleaf virus in naturally infected vineyards. Plant Disease 92, 1689–1694.
Cross-protection as control strategy against grapevine fanleaf virus in naturally infected vineyards.Crossref | GoogleScholarGoogle Scholar |

Lecourieux F, Kappel C, Lecourieux D, Serrano A, Torres E, Arce-Johnson P, Delrot S (2014) An update on sugar transport and signalling in grapevine. Journal of Experimental Botany 65, 821–832.
An update on sugar transport and signalling in grapevine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisFOjtr0%3D&md5=346a5053c96dc0ae8f828ea044cb9d5eCAS |

Liebenberg A, Freeborough MJ, Visser CJ, Bellstedt DU, Burger JT (2009) Genetic variability within the coat protein gene of grapevine fanleaf virus isolates from South Africa and the evaluation of RT-PCR, DAS-ELISA and immunostrips as virus diagnostic assays. Virus Research 142, 28–35.
Genetic variability within the coat protein gene of grapevine fanleaf virus isolates from South Africa and the evaluation of RT-PCR, DAS-ELISA and immunostrips as virus diagnostic assays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltlKqtbk%3D&md5=a961b79a6ae3d26069d4477ecb105e14CAS |

Lovisolo C, Perrone I, Carra A, Ferrandino A, Flexas J, Medrano H, Schubert A (2010) Drought-induced changes in development and function of grapevine (Vitis spp.) organs and in their hydraulic and non-hydraulic interactions at the whole-plant level: a physiological and molecular update. Functional Plant Biology 37, 98–116.
Drought-induced changes in development and function of grapevine (Vitis spp.) organs and in their hydraulic and non-hydraulic interactions at the whole-plant level: a physiological and molecular update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlyhsrs%3D&md5=ba3c2fdeb550e8182fcbf9c8cb894a64CAS |

Maliogka VI, Martelli GP, Fuchs M, Katis NI (2015) Chapter Six – Control of viruses infecting grapevine. Advances in Virus Research 91, 175–227.
Chapter Six – Control of viruses infecting grapevine.Crossref | GoogleScholarGoogle Scholar |

Mannini F (2003) Virus elimination in grapevine and crop performance. In ‘Proceedings of the Congress of the 14th International Council for the Study of Virus and Virus-like Diseases of the Grapevine’, September 2003, Locorotondo (BA), Italy. pp. 234–239.

Martelli GP (2014) Grapevine-infecting viruses. Journal of Plant Pathology 96, 7–8.

Martelli GP, Savino V (1990) Fanleaf degeneration. In ‘Compendium of grape diseases’. (Eds RC Pearson, A Goheen) pp. 48–49. (APS Press: St Paul, MN, USA)

Mattivi F, Guzzon R, Vrhovšek U, Stefanini M, Velasco R (2006) Metabolite profiling of grape: Flavonols and anthocyanins. Journal of Agricultural and Food Chemistry 54, 7692–7702.
Metabolite profiling of grape: Flavonols and anthocyanins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptlWitLw%3D&md5=4c9a13d47f0f884dc5cc18be7f6a3bb9CAS |

McDowell JM, Dangl JL (2000) Signal transduction in the plant immune response. Trends in Biochemical Sciences 25, 79–82.
Signal transduction in the plant immune response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXht1KrsrY%3D&md5=04cae871ae9e56526474785b17c708aaCAS |

Munns R, Cramer GR (1996) Is coordination of leaf and root growth mediated by abscisic acid? Opinion. Plant and Soil 185, 33–49.
Is coordination of leaf and root growth mediated by abscisic acid? Opinion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntlyjug%3D%3D&md5=c353780b951069e5871d53d73524f996CAS |

Nadal M, Hunter JJ (2007) Different wine styles as related to ripeness level of Syrah/R 99 grapes. In ‘Proceedings for the International Intervitis Interfructa Congress’, April 2007, Stuttgart, Germany. pp. 139–148.

Nadal M, Volschenk CG, Hunter JJ (2004) Phenolic extraction during fermentation as affected by ripeness level of Syrah/R99 grapes. In ‘Proceedings for the joint conference on viticultural zoning, November 2004, Cape Town, South Africa’. pp. 479–487.

Orak HH (2007) Total antioxidant activities, phenolics, anthocyanins, polyphenoloxidase activities of selected red grape cultivars and their correlations. Scientia Horticulturae 111, 235–241.
Total antioxidant activities, phenolics, anthocyanins, polyphenoloxidase activities of selected red grape cultivars and their correlations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltVWlsA%3D%3D&md5=f69b8816774b16e6f1b0b0d41c874f98CAS |

Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45
A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=15aa2bf3061ac5fcd9c20e8f4dae7ce5CAS |

Pinto C, Pinho D, Sousa S, Pinheiro M, Egas C, Gomes AC (2014) Unravelling the diversity of grapevine microbiome. PLoS One 9, e85622
Unravelling the diversity of grapevine microbiome.Crossref | GoogleScholarGoogle Scholar |

Prezelj N, Covington E, Roitsch T, Gruden K, Fragner L, Weckwerth W, Chersicola M, Vodopivec M, Dermastia M (2016) Metabolic consequences of infection of grapevine (Vitis vinifera L.) cv. ‘Modra frankinja’ with Flavescence Dorée phytoplasma. Frontiers in Plant Science 7, 711
Metabolic consequences of infection of grapevine (Vitis vinifera L.) cv. ‘Modra frankinja’ with Flavescence Dorée phytoplasma.Crossref | GoogleScholarGoogle Scholar |

Raski DJ, Goheen AC, Lider LA, Meredith CP (1983) Strategies against grapevine fanleaf virus and its nematode vector. Plant Disease 67, 335–339.
Strategies against grapevine fanleaf virus and its nematode vector.Crossref | GoogleScholarGoogle Scholar |

Ribaut JM, Pilet PE (1991) Effects of water stress on growth, osmotic potential and abscisic acid content of maize roots. Physiologia Plantarum 81, 156–162.
Effects of water stress on growth, osmotic potential and abscisic acid content of maize roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtl2qtLk%3D&md5=688c66c926f55a701b057d730dd6182aCAS |

Roby G, Matthews MA (2004) Relative proportions of seed, skin and flesh, in ripe berries from Cabernet Sauvignon grapevines grown in a vineyard. Australian Journal of Grape and Wine Research 10, 74–82.
Relative proportions of seed, skin and flesh, in ripe berries from Cabernet Sauvignon grapevines grown in a vineyard.Crossref | GoogleScholarGoogle Scholar |

Rolland F, Sheen J (2005) Sugar sensing and signalling networks in plants. Biochemical Society Transactions 33, 269–271.
Sugar sensing and signalling networks in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovFynsA%3D%3D&md5=330a06b94344bd0aa318e90582ade2a3CAS |

Sade D, Sade N, Shriki O, Lerner S, Gebremedhin A, Karavani A, Brotman Y, Osorio S, Fernie AR, Willmitzer L, Czosnek H, Moshelion M (2014) Water balance, hormone homeostasis, and sugar signaling are all involved in tomato resistance to tomato yellow leaf curl virus. Plant Physiology 165, 1684–1697.
Water balance, hormone homeostasis, and sugar signaling are all involved in tomato resistance to tomato yellow leaf curl virus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlKntbnK&md5=8a219af2f02b9451edfe9290c0ca9d92CAS |

Santini D, Rolle L, Cascio P, Mannini F (2011) Modifications in chemical, physical and mechanical properties of ‘Nebbiolo’ (Vitis vinifera L.) grape berries induced by mixed virus infection. South African Journal of Enology and Viticulture 32, 183–189.

Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA (1965) Sap pressure in vascular plants. Science 148, 339–346.
Sap pressure in vascular plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvlsVKquw%3D%3D&md5=3580858182c09a7f8fd84bf2799d2409CAS |

Sparvoli F, Martin C, Scienza A, Gavazzi G, Tonelli C (1994) Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.). Plant Molecular Biology 24, 743–755.
Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltVSru7o%3D&md5=ad4995d3ab6981bc53272fa3471c7a58CAS |

Šuklje K, Baša-Česnik H, Janeš L, Kmecl V, Vanzo A, Deloire A, Sivilotti P, Lisjak K (2013) The effect of leaf area to yield ratio on secondary metabolites in grapes and wines of Vitis vinifera L. cv. Sauvignon blanc. Journal International des Sciences de la Vigne et du Vin 47, 83–97.

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome 3, research0034

Vega A, Gutiérrez RA, Peña-Neira A, Cramer GR, Arce-Johnson P (2011) Compatible GLRaV-3 viral infections affect berry ripening decreasing sugar accumulation and anthocyanin biosynthesis in Vitis vinifera. Plant Molecular Biology 77, 261–274.
Compatible GLRaV-3 viral infections affect berry ripening decreasing sugar accumulation and anthocyanin biosynthesis in Vitis vinifera.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGlsLrF&md5=4e5d905d4ea53b27adc6e635ee5d7cc8CAS |

Vivier MA, Pretorius IS (2002) Genetically tailored grapevines for the wine industry. Trends in Biotechnology 20, 472–478.
Genetically tailored grapevines for the wine industry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotFyqur8%3D&md5=ead100f6ff99555dc6cc660517fbdf72CAS |

Weller SA, Elphinstone JG, Smith NC, Boonham N, Stead DE (2000) Detection of Ralstonia solanacearum strains with a quantitative, multiplex, real-time, fluorogenic PCR (TaqMan) assay. Applied and Environmental Microbiology 66, 2853–2858.
Detection of Ralstonia solanacearum strains with a quantitative, multiplex, real-time, fluorogenic PCR (TaqMan) assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkslKlsb8%3D&md5=8354a8fc5ff2276282eb7693029eed7bCAS |

Zhang YP, Uyemoto JK, Golino DA, Rowhani A (1998) Nucleotide sequence and RT-PCR detection of a virus associated with grapevine rupestris stem-pitting disease. Phytopathology 88, 1231–1237.
Nucleotide sequence and RT-PCR detection of a virus associated with grapevine rupestris stem-pitting disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntlWlt7g%3D&md5=35d8265f26a85824ac1498e9a8e3392bCAS |