Grafting with rootstocks promotes phenolic compound accumulation in grape berry skin during development based on integrative multi-omics analysis

Abstract In viticulture, grafting has been practiced widely and influences grape development as well as berry and wine quality. However, there is limited understanding of the effects of rootstocks on grape phenolic compounds, which are located primarily in the berry skin and contribute to certain sensory attributes of wine. In this study, scion–rootstock interactions were investigated at the green-berry stage and the veraison stage when grapevines were hetero-grafted with three commonly used rootstock genotypes (5BB, 101-14MG, and SO4). Physiological investigations showed that hetero-grafts, especially CS/5BB, contained higher concentrations of total proanthocyanidins (PAs) and various PA components in berry skins compared with the auto-grafted grapevines. Further metabolomics analysis identified 105 differentially accumulated flavonoid compounds, the majority of which, including anthocyanins, PAs, and flavonols, were significantly increased in the berry skins of hetero-grafted grapevines compared with auto-grafted controls. In addition, transcriptomic analysis of the same samples identified several thousand differentially expressed genes between hetero-grafted and auto-grafted vines. The three rootstocks not only increased the transcript levels of stilbene, anthocyanin, PA, and flavonol synthesis genes but also affected the expression of numerous transcription factor genes. Taken together, our results suggest that hetero-grafting can promote phenolic compound accumulation in grape berry skin during development. These findings provide new insights for improving the application value of grafting by enhancing the accumulation of nutritious phenolic components in grape.

[1]  Transcriptomic and biochemical investigations support the role of rootstock-scion interaction in grapevine berry quality , 2020, BMC Genomics.

[2]  Q. Pan,et al.  Comparative physiological, metabolomic, and transcriptomic analyses reveal developmental stage-dependent effects of cluster bagging on phenolic metabolism in Cabernet Sauvignon grape berries , 2019, BMC Plant Biology.

[3]  S. Kallithraka,et al.  Proanthocyanidin content as an astringency estimation tool and maturation index in red and white winemaking technology. , 2019, Food chemistry.

[4]  E. Oprea,et al.  Dietary Anthocyanins and Stroke: A Review of Pharmacokinetic and Pharmacodynamic Studies , 2019, Nutrients.

[5]  A. Bautista‐Ortín,et al.  Rootstock effects on grape anthocyanins, skin and seed proanthocyanidins and wine color and phenolic compounds from Vitis vinifera L. Merlot grapevines. , 2019, Journal of the science of food and agriculture.

[6]  D. Delmas,et al.  Polyphenol Extracts from Red Wine and Grapevine: Potential Effects on Cancers , 2018, Diseases.

[7]  R. Kizek,et al.  Contribution of Red Wine Consumption to Human Health Protection , 2018, Molecules.

[8]  D. Wong,et al.  Combinatorial Regulation of Stilbene Synthase Genes by WRKY and MYB Transcription Factors in Grapevine (Vitis vinifera L.) , 2018, Plant & cell physiology.

[9]  S. Vršič,et al.  Influence of Various Rootstocks on the Yield and Grape Composition of Sauvignon Blanc , 2018 .

[10]  L. Moio,et al.  Metabolic and RNA profiling elucidates proanthocyanidins accumulation in Aglianico grape. , 2017, Food chemistry.

[11]  J. T. Matus,et al.  A group of grapevine MYBA transcription factors located in chromosome 14 control anthocyanin synthesis in vegetative organs with different specificities compared with the berry color locus , 2017, The Plant journal : for cell and molecular biology.

[12]  M. Delledonne,et al.  Grapevine Grafting: Scion Transcript Profiling and Defense-Related Metabolites Induced by Rootstocks , 2017, Front. Plant Sci..

[13]  Jeffrey T Leek,et al.  Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown , 2016, Nature Protocols.

[14]  J. T. Matus Transcriptomic and Metabolomic Networks in the Grape Berry Illustrate That it Takes More Than Flavonoids to Fight Against Ultraviolet Radiation , 2016, Front. Plant Sci..

[15]  S. Kallithraka,et al.  Effect of irrigation regime on perceived astringency and proanthocyanidin composition of skins and seeds of Vitis vinifera L. cv. Syrah grapes under semiarid conditions. , 2016, Food chemistry.

[16]  Tianyu Sun,et al.  Modifications of 'Gold Finger' Grape Berry Quality as Affected by the Different Rootstocks. , 2016, Journal of agricultural and food chemistry.

[17]  Allison J. Miller,et al.  Rootstocks: Diversity, Domestication, and Impacts on Shoot Phenotypes. , 2016, Trends in plant science.

[18]  L. Willmitzer,et al.  GC–MS metabolic profiling of Cabernet Sauvignon and Merlot cultivars during grapevine berry development and network analysis reveals a stage- and cultivar-dependent connectivity of primary metabolites , 2016, Metabolomics.

[19]  C. Ford,et al.  A Grapevine Anthocyanin Acyltransferase, Transcriptionally Regulated by VvMYBA, Can Produce Most Acylated Anthocyanins Present in Grape Skins1 , 2015, Plant Physiology.

[20]  G. Valle,et al.  Comprehensive transcript profiling of two grapevine rootstock genotypes contrasting in drought susceptibility links the phenylpropanoid pathway to enhanced tolerance , 2015, Journal of experimental botany.

[21]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[22]  V. Chalifa-Caspi,et al.  Metabolite and transcript profiling of berry skin during fruit development elucidates differential regulation between Cabernet Sauvignon and Shiraz cultivars at branching points in the polyphenol pathway , 2014, BMC Plant Biology.

[23]  Mario Pezzotti,et al.  Genome and transcriptome analysis of the grapevine (Vitis vinifera L.) WRKY gene family , 2014, Horticulture Research.

[24]  H. Gerós,et al.  Berry Phenolics of Grapevine under Challenging Environments , 2013, International journal of molecular sciences.

[25]  S. Delrot,et al.  Graft union formation in grapevine induces transcriptional changes related to cell wall modification, wounding, hormone signalling, and secondary metabolism , 2013, Journal of experimental botany.

[26]  N. Goto-Yamamoto,et al.  Light quality affects flavonoid biosynthesis in young berries of Cabernet Sauvignon grape. , 2012, Phytochemistry.

[27]  J. Bogs,et al.  R2R3 MYB transcription factors: key regulators of the flavonoid biosynthetic pathway in grapevine , 2012, Protoplasma.

[28]  H. Vila,et al.  Influence of different rootstocks on the vegetative and reproductive performance of Vitis vinifera L. Malbec under irrigated conditions , 2011 .

[29]  W. Qiu,et al.  Berry skin development in Norton grape: Distinct patterns of transcriptional regulation and flavonoid biosynthesis , 2011, BMC Plant Biology.

[30]  Fei He,et al.  Biosynthesis of Anthocyanins and Their Regulation in Colored Grapes , 2010, Molecules.

[31]  A. McElrone,et al.  Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape , 2010, Planta.

[32]  A. Forneck,et al.  (A)sexual reproduction – a review of life cycles of grape phylloxera, Daktulosphaira vitifoliae , 2009 .

[33]  J. T. Matus,et al.  Post-veraison sunlight exposure induces MYB-mediated transcriptional regulation of anthocyanin and flavonol synthesis in berry skins of Vitis vinifera , 2009, Journal of experimental botany.

[34]  P. Fontana,et al.  Ripening and genotype control stilbene accumulation in healthy grapes. , 2008, Journal of agricultural and food chemistry.

[35]  A. Vianello,et al.  Transport and accumulation of flavonoids in grapevine (Vitis vinifera L.) , 2008, Plant signaling & behavior.

[36]  M. Robles,et al.  University of Birmingham High throughput functional annotation and data mining with the Blast2GO suite , 2022 .

[37]  J. Cushman,et al.  Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development , 2007, BMC Genomics.

[38]  Mark Krstic,et al.  Cultural Practice and Environmental Impacts on the Flavonoid Composition of Grapes and Wine: A Review of Recent Research , 2006, American Journal of Enology and Viticulture.

[39]  James A. Kennedy,et al.  Grape and Wine Phenolics: History and Perspective , 2006, American Journal of Enology and Viticulture.

[40]  V. Cheynier,et al.  Structure and Properties of Wine Pigments and Tannins , 2006, American Journal of Enology and Viticulture.

[41]  V. Lauvergeat,et al.  Characterization of a Grapevine R2R3-MYB Transcription Factor That Regulates the Phenylpropanoid Pathway1[W] , 2005, Plant Physiology.

[42]  Véronique Cheynier,et al.  Taste and mouth-feel properties of different types of tannin-like polyphenolic compounds and anthocyanins in wine , 2004 .

[43]  S. Rhee,et al.  MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. , 2004, The Plant journal : for cell and molecular biology.

[44]  Markus Riederer,et al.  UV screening by phenolics in berries of grapevine (Vitis vinifera). , 2003, Functional plant biology : FPB.

[45]  Melané A Vivier,et al.  Genetically tailored grapevines for the wine industry. , 2002, Trends in biotechnology.

[46]  S. A. Anwar,et al.  A Search for More Durable Grape Rootstock Resistance to Root-knot Nematode , 2002, American Journal of Enology and Viticulture.