Scientia Agricultura Sinica ›› 2013, Vol. 46 ›› Issue (14): 2979-2989.doi: 10.3864/j.issn.0578-1752.2013.14.014

• HORTICULTURE • Previous Articles     Next Articles

Spatial and Temporal Accumulation of Flavanols, Activity and Tissue Localization of Leucoanthocyanidin Reductase Induced by Soil Drought in Developing Grape Berries

 WEN  Peng-Fei, NIU  Xing-Yan, XING  Yan-Fu, GAO  Mei-Ying, NIU  Tie-Quan   

  1. College of Horticulture, Shanxi Agricultural University, Taigu 030801, Shanxi
  • Received:2012-12-14 Online:2013-07-15 Published:2013-05-21

Abstract: 【Objective】The effects of soil drought on the spatial and temporal accumulation of flavanols, enzyme activity and tissue localization of its biosynthetic key enzyme, leucoanthocyanidin reductase (LAR), during the grape berry development were studied.【Method】The 5-year old grapevine (Vitis vinifera L. cv. Cabernet Sauvignon) was used as materials, and the grapevine was subjected to soil drought stress simulated by controlling irrigation through the rain-preventing shelter and root-cutting groove during grape berry development. The spatial and temporal accumulation of flavanols and the enzyme activity of LAR in different parts of the grape berry were analyzed by spectrophotometer method, and the tissue localization of LAR was detected by the immunohistochemical localization. 【Result】 Results indicated that the growth of grape berry was significantly inhibited by soil drought during its development, and an obvious accumulation of total phenol in berry was induced by soil drought, especially in the young berry period. The accumulation pattern of flavanols and total flavan-3-ols in skin and flesh during grape berry development were not changed by soil drought, whereas an obvious accumulation of flavanols and total flavan-3-ols induced by soil drought was observed, and this effect was organ- and development-dependent. The LAR enzyme activity in skin and flesh was induced by soil drought, especially in the young berry period. There were no obvious changes of tissue localization of LAR1 and LAR2 in the skin and flesh under soil drought, but an increasing signal was detected, especially in the vascular bundle.【Conclusion】All the results of this study suggested that soil drought could induce the accumulation of LAR1 and LAR2 proteins in different parts of berry at different development stages, resulted in the increase of LAR enzyme activity in corresponding part and developing stage, and induced the accumulation of flavanols and total flavan-3-ols during grape berry development.

Key words: grape berry , soil drought , flavanols , LAR , tissue localization

[1]Dixon R A, Xie D -Y, Sharma S B. Proanthocyanidins-a final frontier in flavonoid research? New Phytologist, 2005, 165:9-28.

[2]Eftekhari M, Alizadeh M, Ebrahimi P. Evaluation of the total phenolics and quercetin content of foliage in mycorrhizal grape (Vitis vinifera L.) varieties and effect of postharvest drying on quercetion yield. Industrial Crops and Products, 2012, 38:160-165.

[3]Skerget M, Kotnik P, Hadolin M, Hras A R, Simionic M, Knez Z. Phenols, proanthocyanidins, flavones and flavonols in some plant materials and their antioxidant activities. Food Chemistry, 2005, 89:191-198.

[4]Leifert W R, Abeywardena M Y. Cardioprotective actions of grape polyphenols. Nutrition Research, 2008, 28:729-737.

[5]Prasain J K, Carlson S H, Wyss J M. Flavonids and age-related disease: Risk, benefits and critical windows. Maturitas, 2010, 66:163-171.

[6]Rodrigo R, Miranda A, Vergara L. Modulation of endogenous antioxidant system by wine polyphenols in human disease. Clinica Chimica Acta, 2011, 412:410-424.

[7]Sano T, Oda E, Yamashita T, Naemura A, Ijiri Y, Yamakoshi J, Yamamoto J. Anti-thrombotic effect of proanthocyanidins, a purified ingredient of grape seed. Thrombosis Research, 2005, 115:115-121.

[8]Araùjo J R, Goncalves P, Martel F. Chemopreventive effect of dietary polyphenols in colorectal cancer cell lines. Nutrition Research, 2011, 31:77-87.

[9]Ollé D, Guiraud J L, Souquet J M, Terrier N, Ageorges A, Cheynier V, Verries C. Effect of pre- and postveraison water deficit on proanthocyanidins and anthocyanin accumulation during Shiraz berry development. Australian Journal of Grape and Wine Research, 2011, 17:90-100.

[10]温鹏飞, 邢延富, 牛铁泉, 高美英, 牛兴艳. UV-C对葡萄果实发育过程中黄烷醇类多酚积累及隐色花色素还原酶表达的影响. 中国农业科学, 2012, 45: 4428-4436.

Wen P F, Xing Y F, Niu T Q, Gao M Y, Niu X Y. Accumulation of flavanols, expression of leucoanthocyanidin reductase induced by UV-C irradiation during grape berry development. Scientia Agricultura Sinica, 2012, 45:4428-4436. (in Chinese)

[11]Girona J, Marsal J, Mata M, Campo J D, Basile B. Phenological sensitivity of berry growth and composition of Tempranillo grapevines (Vitis vinifera L.) to water stress. Australian Journal of Grape and Wine Research, 2009, 15: 268-277.

[12]Schroeter H, Heiss C, Spencer J P E, Keen C L, Lupton J R, Schmitz H H. Recommending flavanols and procyanidins for cardiovascular health: Current knowledge and future needs. Molecular Aspects of Medicine, 2010, 31:546-557.

[13]Serafini M, Bugianesi R, Maiani G, Valtuena S, De Santis S, Crozier A. Plasma antioxidants from cholcolate. Nature, 2003, 424:1013.

[14]Quiroga A M, Deis L, Cavagnaro J B, Bottini R, Silva M F. Water stress and abscisic acid exogenous supply produce differential enhancements in the concentration of selected phenolic compounds in Cabernet Sauvignon. Journal of Berry Research, 2012, 2:33-44.

[15]Wen P F, Chen J Y, Wan S B, Kong W F, Zhang P, Wang W, Zhan J C, Pan Q H, Huang W D. Salicylic acid activates phenylalanine ammonia-lyase in grape berry in response to high temperature stress. Plant Growth Regulation, 2008, 55:1-10.

[16]Wang W, Tang K, Yang H R, Wen P F, Zhang P, Wang H L, Huang W D. Distribution of resveratrol and stilbene synthase in young grape plants (Vitis vinifera L. cv. Cabernet Sauvignon) and the effect of UV-C on its accumulation. Plant Physiology and Biochemistry, 2010, 48:142-152.

[17]Wang Y S, Gao L P, Shan Y, Liu Y J, Tian Y W, Xia T. Influence of shade on flavonoid biosynthesis in tea (Camellia sinensis (L.) O. Kuntze). Scientia Horticulturae, 2012, 141:7-16.

[18]Castellarin S D, Matthews M A, Di Gaspero G, Gambetta G A. Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta, 2007, 227:101-112.

[19]Acevedo-Opazo C, Ortega-Farias S, Fuentes S. Effects of grapevine (Vitis vinifera L.) water status on water consumption, vegetative growth and grape quality: An irrigation scheduling application to achieve regulated deficit irrigation. Agricultural Water Management, 2010, 97:956–964.

[20]Bonghi C, Rizzini F M, Gambuti A, Moio L, Chkaiban L, Tonutti P. Phenol compound metabolism and gene expression in the skin of wine grape (Vitis vinifera L.) berries subjected to partial postharvest dehydration. Postharvest Biology and Technology, 2012, 67:102-109.

[21]Sánchez-Rodríguez E, Moreno D A, Ferreres F, Rubio-Wilhelmi M M, Ruiz J M. Differential responses of five cherry tomato varieties to water stress: Changes on phenolic metabolites and related enzymes. Phytochemistry, 2011, 72:723-729.

[22]Ojeda H, Andary C, Kraeva E, Carbonneau A, Deloire A. Influence of pre- and postveraison water deficit on synthesis and concentration of skin phenolic compounds during berry growth of Vitis vinifera cv. Shiraz. American Journal of Enology Viticulture, 2002, 53:261-267.

[23]Koundouras S, Marinos V, Gkoulioti A, Kotseridis Y, Van Leeuwen C. Influence of vineyard location and vine water status on fruit maturation of non-irrigated cv. Agiorgitiko (Vitis vinifera L.). Effects on wine phenolic and aroma components. Journal of Agricultural and Food Chemistry, 2006, 54:5077-5086.

[24]Maugé C, Granier T, d’Estaintot BL, Gargouri M, Manigand C, Schmitter JM, Chaudière J, Gallois B. Crystal structure and catalytic mechanism of leucoanthocyanidin reductase from Vitis vinifera. Journal of Molecular and Biology, 2010, 397:1079-1091.

[25]Bogs J, Downey M O, Harvey J S, Ashto A R, Tanner G J, Robinson S P. Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves. Plant Physiology, 2005, 139:652-663.

[26]马春雷, 乔小燕, 陈亮. 茶树无色花色素还原酶基因克隆及表达分析. 茶叶科学, 2010, 30:27-36.

Ma C L, Qiao X Y, Chen L. Cloning and expression analysis of leucoanthocyanidin reductase gene of tea plant (Camellia sinensis). Journal of Tea Science, 2010, 30:27-36. (in Chinese)

[27]Wang H L, Wang W, Zhang P, Pan Q H, Zhan J C, Huang W D. Gene transcript accumulation, tissue and subcellular localization of anthocyanidin synthase (ANS) in developing grape berries. Plant Science, 2010, 179:103-113.

[28]温鹏飞, 杨运良, 高美英, 牛铁泉, 邢延富, 牛兴艳. 干旱胁迫对葡萄果实发育过程中黄烷醇类多酚积累及LAR表达的影响. 园艺学报, 2012, 39:2341-2351.

Wen P F, Yang Y L, Gao M Y, Niu T Q, Xing Y F, Niu X Y. The effects of soil drought on flavanols accumulation and LAR expression during the development of grape berry. Acta Horticulturae Sinica, 2012, 39:2341-2351. (in Chinese)

[29]温鹏飞, 郑宏佳, 牛铁泉, 高美英, 仓国营, 杨运良. 延迟采收对葡萄果实多酚类物质含量的影响. 山西农业大学学报: 自然科学版, 2011, 31:446-450.

Wen P F, Zheng H J, Niu T Q, Gao M Y, Cang G Y, Yang Y L. Effects of late harvest on the polyphenols concentration in grape berry. Journal of Shanxi Agricultural University (Natural Science Edition), 2011, 31:446-450. (in Chinese)

[30]Waterhouse A L, Ignelzi S, Shirley J R. A comparison of methods for quantifying oligomeric proanthocyanidins from grape seed extracts. American Journal of Enology and Viticulture, 2000, 51:383-389.

[31]Ivanova V, Stefova M, Vojnoski B, Dornyei A, Márk L, Dimovska V, Stafilov T, Kilár F. Identification of polyphenolic compounds in red and white grape varieties grown in R. Macedonia and changes of their content during ripening. Food Research International, 2011, 44:2851-2860.

[32]Hou Z X, Huang W D. Immunohistochemical localization of IAA and ABP1 in strawberry shoot apexes during floral induction. Planta, 2005, 222:678-687.

[33]Cadot Y, Castelló M T M, Chevalier M. Flavan-3-ol compositional changes in grape berries (Vitis vinifera L. cv. Cabernet Franc) before veraison, using two complementary analytical approaches, HPLC reversed phase and histochemistry. Analytica Chimica Acta, 2006, 563:65-75.

[34]Jeong S T, Goto-Yamamoto N, Kobayashi S, Esaka M. Effects of plant hormones and shading on the accumulation of anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins. Plant Science, 2004, 167:247-252.

[35]Hou F Y, Wang Q M, Dong S X, Li A X, Zhang H Y, Xie B T, Zhang  L M. Accumulation and gene expression of anthocyanin in storage roots of purple-fleshed sweet potato(Ipomoea batatas (L.) Lam) under weak light conditions. Agricultural Sciences in China, 2010, 9:1588-1593.

[36]Koyama K, Ikeda H, Poudel P R, Goto-Yamamoto N. Light quality affects flavonoid biosynthesis in young berries of Cabernet Sauvignon grape. Phytochemistry, 2012, 78:54-64.

[37]Caralho I S, Cavaco T, Carvalho L M, Duque P. Effect of photoperoid on flavonoid pathway activity in sweet potato (Ipomoea batatas (L.) Lam.) leaves. Food Chemistry, 2010, 118:384-390.

[38]Jaleel C A, Manivannan P, Sankar B, Kishorekumar A, Gopi R, Somasundaram R, Panneerselvam R. Induction of drought stress tolerance by ketoconazole in Catharanthus roseus is mediated by enhanced antioxidant potentials and secondary metabolite accumulation. Colloids and Surfaces B: Biointerfaces, 2007, 60: 201-206.

[39]Yiu J C, Tseng M J, Liu C W, Kuo C T. Modulaiton of NaCl stress in Caspsicum annuum L. seedlings by catechin. Scientia Horticulturae, 2012, 134:200-209.

[40]Oh M M, Carey E E, Rajashekar C B. Enviromental stresses induce health-promoting phytochemicals in lettuce. Plant Physiology and Biochemistry, 2009, 47:578-583.

[41]Niki E. Assessment of antioxidant capacity in vitro and in vivo. Free Radical Biology & Medicine, 2010, 49:503-515.

[42]Peterlunger E, Sivilotti P, Colussi V. Water stress increased polyphenolic quality in ‘Merlot’ grapes. ISHS Acta Horticulture, 2005, 689:293-300.

[43]Gagné S, Lacampagne S, Claisse O, Gény L. Leucoanthocyanidin reductase and anthocyanidin reductase gene expression and activity in flowers, young berries and skins of Vitis vinifera L. cv. Cabernet-Sauvignon during development. Plant Physiology and Biochemistry, 2009, 47:282-290.

[44]刘 松. 极端干旱环境下植物体内多酚类物质含量及其对逆境的响应研究[D]. 北京: 北京林业大学, 2007.

Liu S. Study on plant phenolic compound content and their response to hyperarid extreme environment [D]. Beijing: Beijing Forestry University, 2007. (in Chinese)

[45]Saslowsky D, Winkel-Shirley B. Localization of flavonoid enzymes in Arabidopsis roots. Plant Journal, 2001, 27:37-48.

[46]张平. 葡萄果实二氢黄酮醇还原酶抗体制备、定位以及低温、水杨酸的影响[D]. 北京: 中国农业大学, 2010.

Zhang P. Antibody preparation, localization of DFR and the effect of both low temperature and SA in grape berry [D]. Beijing: China Agricultural University, 2010. (in Chinese)

[47]Pan Q H, Wang L, Li J M. Amounts and subcellular localization of stilbene synthase in response of grape berries to UV irradiation. Plant Science, 2009, 176:360-366.
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