The grapevine VviPrx31 peroxidase as a candidate gene involved in anthocyanin degradation in ripening berries under high temperature

Nooshin Movahed1, Chiara Pastore1, Antonio Cellini1, Gianluca Allegro1, Gabriele Valentini1, Sara Zenoni2, Erika Cavallini2, Erica D’Incà2, Giovanni Battista Tornielli2, Ilaria Filippetti1
1Department of Agricultural Sciences, University of Bologna, Viale Fanin, 46, 40126, Bologna, Italy
2Department of Biotechnology, University of Verona, Strada le Grazie 15, 37134, Verona, Italy

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Archer E, Strauss HE (1989) Effect of shading on the performance of Vitis vinifera L. cv Cabernet Sauvignon. S Afr J Enol Vitic 10:74–77

Barbagallo MG, Lino T, Santalucia G, Scafidi P (2007) Effetti di modificazioni del microclima dai grappoli mediante sfogliatura e copertura con rete ombreggiante sulla qualità dell’uva della cv Pinot nero in Sicilia. Italus Hortus 14:181–185

Barceló AR, Pomar F, Lopez-Serano M, Pedreno MA (2003) Peroxidase: a multifunctional enzyme in grapevines. Funct Plant Biol 30:557–591

Beld M, Martin C, Huits H, Stuitje AR, Gerats AGM (1989) Partial characterization of dihydroflavonol-4-reductase genes. Plant Mol Bio 13:491–502

Bergqvist J, Dokoozlian N, Ebisuda N (2001) Sunlight exposure and temperature effects on berry growth and composition of Cabernet Sauvignon and Grenache in the Central San Joaquin Valley of California. Am J Enol Vitic 52:1–6

Calderón AA, García-Florenciano E, Muñoz R, Ros Barceló A (1992) Gamay grapevine peroxidase: its role in vacuolar anthocyanin(di)n degradation. Vitis 31:139–147

Carbonell-Bejerano P, Santa Maria E, Torrés Perez R, Royo C, Lijavetzky D, Bravo G, Aguirreolea J, Sánchez-Díaz M, Carmen Antolín M, Martinez-Zapater JM (2013) Thermotolerance responses in ripening berries of Vitis vinifera L cv Muscat Hamburg. Plant Cell Physiol 54:1200–1216

Cohen SD, Tarara JM, Gambetta GA, Matthews MA, Kennedy JA (2012) Impact of diurnal temperature variation on grape berry development, proanthocyanidin accumulation, and the expression of flavonoid pathway genes. J Exp Bot 63:2655–2665

Cutanda-Perez MC, Ageorges A, Gomez C, Vialet S, Terrier N, Romieu C, Torregosa L (2009) Ectopic expression of VlmybA1 in grapevine activates a narrow set of genes involved in anthocyanin synthesis and transport. Plant Mol Biol 69:633–648

Dal Santo S, Tornielli GB, Zenoni S, Fasoli M, Farina L, Anesi A, Guzzo F, Delledonne M, Pezzotti M (2013) The plasticity of the grapevine berry transcriptome. Genome Biol 14:R54

Del Pozo-Insfran D, Del Follo-Martinez A, Talcott ST, Brenes CH (2007) Stability of copigmented anthocyanins and ascorbic acid in Muscadine grape juice processed by high hydrostatic pressure. J Food Sci 72:247–253

Deluc L, Grimplet J, Wheatley MD, Tillet RL, Quilici DR, Osborne C, Schooley DA, Schlauch KA, Cushman JC, Cramer GR (2007) Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genom 8(1):429

Downey MO, Dokoozlian NK, Krstic MP (2006) Cultural practice and environmental impacts on the flavonoid composition of grapes and wine: a review of recent research. Am J Enol Vitic 57:257–268

Falginella L, Castellarin SD, Testolin R, Gambetta GA, Morgante M, Di Gaspero G (2010) Expansion and subfunctionalisation of flavonoid 3′,5′-hydroxylases in the grapevine lineage. BMC Genom 11:562. doi: 10.1186/1471-2164-11-562

Fasoli M, Dal Santo S, Zenoni S, Tornielli GB, Farina L, Zamboni A (2012) The grapevine expression atlas reveals a deep transcriptome shift driving the entire plant into a maturation program. Plant Cell 24:3489–3505

Filippetti I, Ramazzotti S, Centinari M, Bucchetti B, Intrieri C (2007) Esperienze triennali sugli effetti del diradamento dei grappoli sulla qualità delle uve della cultivar Sangiovese. Italus Hortus 14:412–416

Goto-Yamamoto N, Wan GH, Masaki K, Kobayashi S (2002) Structure and transcription of three chalcone synthase genes of grapevine (Vitis vinifera). Plant Sci 162:867–872

Grimplet J, Van Hemert J, Crbonell-Bejerano P, Diiaz-Riquelme J, Dickenson J, Fennell A, Pezzotti M, Martinez-Zapater JM (2012) Comparative analysis of grapevine whole-genome gene predictions, functional annotation, categorization and integration of the predicted gene sequences. BMC Res Notes 5:213

Grover A, Mittal D, Negi M, Lavania D (2013) Generating high temperature tolerant transgenic plants: achievements and challenges. Plant Sci 205:38–47

Guidoni S, Ferrandino A, Novello V (2008) Effects of seasonal and agronomical practices on skin anthocyanin profile of nebbiolo grapes. Am J Enol Vitic 59:22–29

Jackman RL, Smith JL (1996) Anthocyanins and Betalains. Natural food colorants. Springer, US, pp 244–309

Jeong ST, Goto-Yamamoto N, Kobayashi S, Esaka M (2004) Effects of plant hormones and shading on the accumulation of anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins. Plant Sci 167:247–252

Keller M, Mills LJ, Wample RL, Spayd SE (2005) Cluster thinning effects on three deficit-irrigated Vitis vinifera L. Am J Enol Vitic 56:91–103

Kliewer WM, Schultz HB (1964) Influence of environment on metabolism of organic acids and carbohydrates in Vitis vinifera. II. Light. Am J Enol Vitic 15:119–129

Kliewer WM, Torres RE (1972) Effect of controlled day and night temperatures on grape coloration. Am J Enol Vitic 23:71–77

Kochhar S, Kochhar VK, Khanduja SD (1979) Changes in the pattern of isoperoxidases during maturation of grape berries cv Gulabi as affected by ethephon (2-chloroethyl) phosphonic acid. Am J Enol Vitic 30:275–277

Lakso AN, Kliewer WM (1978) The influence of temperature on malic acid metabolism in grape berries. II. Temperature responses of net dark CO2 fixation and malic acid pools. Am J Enol Vitic 29:145–149

Lin-Wang K, Micheletti D, Palmer J, Volz R, Lozano L, Espley R, Allan AC (2011) High temperature reduces apple fruit colour via modulation of the anthocyanin regulatory complex. Plant Cell Environ 34:1176–1190

Lorenz DH, Eichhorn KW, Bleiholder H, Klose R, Meier U, Weber E (1995) Growth stages of the grapevine: phenological growth stages of the grapevine (Vitis vinifera L. ssp.vinifera). Codes and descriptions according to the extended BBCH scale. Aust J Grape Wine Res 1(2):100–103

Mattivi F, Guzzon R, Vrhovsek U, Stefanini M, Velasco R (2006) Metabolite profiling of grape: flavonols and anthocyanins. J Agric Food Chem 54:7692–7702

McIntyre GN, Kliewer WM, Lider LA (1987) Some limitations of the degree day system as used in viticulture in California. Am J Enol Vitic 38:128–132

Mori K, Sugaya S, Gemma H (2005) Decreased anthocyanin biosynthesis in grape berries grown under elevated night temperature condition. Sci Hortic 105:319–330

Mori K, Goto-Yamamoto N, Kitayama M, Hashizume K (2007) Loss of anthocyanins in red-wine grape under high temperature. J Exp Bot 58:1935–1945

Muñoz C, Gomez-Talquenca S, Chialva C, Ibáñez J, Martinez-Zapater JM, Peña-Neira A, Lijavetzky D (2014) Relationships among gene expression and anthocyanin composition of Malbec grapevine clones. J Agric Food Chem 62:6716–6725

Oren-Shamir M (2009) Does anthocyanin degradation play a significant role in determining pigment concentration in plants. Plant Sci 177:310–316

Oren-Shamir M, Nissim-Levi A (1999) Temperature and gibberellin effect on growth and anthocyanin pigmentation in Photinia leaves. J Hortic Sci Biotec 74:355–360

Passardi F, Theiler G, Zamocky M, Cosio C, Rouhier N, Teixera F, Dunand C (2007) PeroxiBase: the peroxidase database. Phytochem 68:1605–1611

Pastore C, Zenoni S, Tornielli GB, Allegro G, Dal Santo S, Valentini G, Intrieri C, Pezzotti M, Filippetti I (2011) Increasing the source/sink ratio in Vitis vinifera (cv Sangiovese) induces extensive transcriptome reprogramming and modifies berry ripening. BMC Genom 12:631

Pastore C, Zenoni S, Fasoli M, Pezzotti M, Tornielli GB, Filippetti I (2013) Selective defoliation affects plant growth, fruit transcriptional ripening program and flavonoid metabolism in grapevine. BMC Plant Biol 13:30

Pérez FJ, Villegas D, Meja N (2002) Ascorbic acid and flavonoid-peroxidase reaction as a detoxifying system of H2O2 in grapevine leaves. Phytochem 60:573–580

Pfaffl MW, Hageleit M (2001) Validities of mRNA quantification using recombinant RNA and recombinant DNA external calibration curves in real-time RT-PCR. Biotec Letters 23:275–282

Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36

Pilati S, Perazzolli M, Malossini A, Cestaro A, Demattè L, Fontana P, Dal Ri A, Viola R, Velasco R, Moser C (2007) Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at veraison. BMC Genom 8:428

Pirie A, Mullins MG (1980) Concentration of phenolics in the skin of grape berries during fruit development and ripening. Am J Enol Vitic 31:34–36

Pourcel L, Routaboul JM, Cheynier V, Lepiniec L, Debeaoujon I (2006) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 12:29–36

Ramakers JM, Ruijter RHL, Deprez AFM, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66

Rienth M, Torregrosa L, Luchaire N, Chatbanyong R, Lecourieux D, Kelly MT, Romieu C (2014) Day and night heat stress trigger different transcriptomic responses in green and ripening grapevine (Vitis vinifera) fruit. BMC Plant Biol 14:108

Robinson BS, Bretherick MR, Donnelly JK (1989) The heat stability and isoenzyme composition of peroxidases in Ohane grapes. Intern J Food Sci Tech 24:613–618

Sadras VO, Moran MA (2012) Elevated temperature decouples anthocyanins and sugars in berries of Shiraz and Cabernet Franc. Aust J Grape Wine Res 18:115–122

Sadras VO, Petrie PR, Moran MA (2013) Effects of elevated temperature in grapevine. II juice pH, titratable acidity and wine sensory attributes. Aust J Grape Wine Res 18:107–115

Spayd SE, Tarara JM, Mee DL, Ferguson JL (2002) Separation of sunlight and temperature effects on the composition of Vitis vinifera cv Merlot Berries. Am J Enol Vitic 53:171–182

Tarara JM, Lee J, Spayd SE, Scagel CF (2008) Berry temperature and solar radiation alter acylation, proportion, and concentration of anthocyanin in merlot grapes. Am J Enol Vitic 59:235–247

Tognolli M, Penel C, Greppin H, Simon P (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288:129–138

Tomana T, Utsonomya N, Kataoka I (1979) The effect of environmental temperatures on fruit ripening on the tree. I. The effect of temperature around whole vines and clusters on coloration of Kyoho grapes. J Japanese Soc Hort Sci 48:261–266

Ushimaru T, Maki Y, Sano S, Koshiba T, Asada K, Tsuji H (1997) Induction of enzymes involved in the ascorbate-dependent antioxidative system, namely, ascorbate peroxidase, monodehydroascorbate reductase and dehydroascorbate reductase, after exposure to air of rice (Oriza sativa) seedling germinate und water. Plant Cell Physiol 38:541–549

Vaknin H, Bar-Akiva A, Ovadia R, Nissim-Levi A, Forer I, Weiss D, Oren-Shamir M (2005) Active anthocyanin degradation in Brunfelsia calycina (yesterday-today-tomorrow) flowers. Planta 222:19–26

Vámos-Vigyázó L, Haard NF (1981) Polyphenol oxidases and peroxidases in fruits and vegetables. Crit Rev Food Sci Nutr 15:49–127

Van der Meer IM (1999) Agrobacterium mediated transformation of petunia leaf disks plant cell culture protocols. In: Robert D Hall (ed) Methods in molecular biology. Humana Press, USA, pp 327–334

Walker AR, Lee E, Bogs J, McDavid DAJ, Thomas MR, Robinson SP (2007) White grapes arose through mutation of two similar and adjacent regulatory genes. Plant Journal 49:772–785

Waterhouse AL (2002) Wine Phenolics. Ann NY Acad Sci 957:21–36

Wicks AS, Kliewer WM (1983) Further investigations into the relationship between anthocyanins, phenolics and soluble carbohydrates in grape berry skins. Am J Enol Vitic 34:114–116

Winkler A, Cook JA, Kliewer WM, Lider LA (1974) General viticulture. University of California Press, pp 158–165

Xie XB, Li S, Zhang RF, Zhao J, Chen YC, Zhao Q, Yao YX, Zhang XS, Hao YJ (2012) The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant Cell Environ 35:1884–1897

Yamane T, Jeong SK, Goto-Yamamoto N, Koshita Y, Kobayashi S (2006) Effects of temperature on anthocyanin biosynthesis in grape berry skins. Am J Enol Vitic 57:54–59

Zamboni A, Di Carli M, Guzzo F, Stocchero M, Zenoni S, Ferrarini A, Tononi P, Toffali K, Desiderio A, Lilley KS, Pè ME, Benvenuto E, Delledonne M, Pezzotti M (2010) Identification of putative stage-specific grapevine berry biomarkers and omics data integration into networks. Plant Physiol 154:439–1459

Zhang Z, Pang X, Xuewu D, Ji Z, Jiang Y (2005) Role of peroxidase in anthocyanin degradation in litchi fruit pericarp. Food Chem 90:47–52

Zipor G, Duarte P, Carqueijeiro I, Shahar L, Ovadia R, Teper-Bamnolker P, Eshel D, Levin Y, Doron-Faigenboim A, Sottomayor M, Oren-Shamir M (2014) In planta anthocyanin degradation by a vacuolar class III peroxidase in Brunfelsia calycina flowers. New Phytol 205:653–665