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Developmental and Metabolic Plasticity of White-Skinned Grape Berries in Response to Botrytis cinerea during Noble Rot.
Plant Physiol. 2015 Dec; 169(4):2422-43.PP

Abstract

Noble rot results from exceptional infections of ripe grape (Vitis vinifera) berries by Botrytis cinerea. Unlike bunch rot, noble rot promotes favorable changes in grape berries and the accumulation of secondary metabolites that enhance wine grape composition. Noble rot-infected berries of cv Sémillon, a white-skinned variety, were collected over 3 years from a commercial vineyard at the same time that fruit were harvested for botrytized wine production. Using an integrated transcriptomics and metabolomics approach, we demonstrate that noble rot alters the metabolism of cv Sémillon berries by inducing biotic and abiotic stress responses as well as ripening processes. During noble rot, B. cinerea induced the expression of key regulators of ripening-associated pathways, some of which are distinctive to the normal ripening of red-skinned cultivars. Enhancement of phenylpropanoid metabolism, characterized by a restricted flux in white-skinned berries, was a common outcome of noble rot and red-skinned berry ripening. Transcript and metabolite analyses together with enzymatic assays determined that the biosynthesis of anthocyanins is a consistent hallmark of noble rot in cv Sémillon berries. The biosynthesis of terpenes and fatty acid aroma precursors also increased during noble rot. We finally characterized the impact of noble rot in botrytized wines. Altogether, the results of this work demonstrated that noble rot causes a major reprogramming of berry development and metabolism. This desirable interaction between a fruit and a fungus stimulates pathways otherwise inactive in white-skinned berries, leading to a greater accumulation of compounds involved in the unique flavor and aroma of botrytized wines.

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Authors+Show Affiliations

Blanco-Ulate B
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.).
Amrine KC
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.).
Collins TS
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.).
Rivero RM
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.).
Vicente AR
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.).
Morales-Cruz A
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.).
Doyle CL
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.).
Ye Z
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.).
Allen G
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.).
Heymann H
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.).
Ebeler SE
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.).
Cantu D
Department of Viticulture and Enology, University of California, Davis, California 95616 (B.B.-U., K.C.H.A., T.S.C., A.M.-C., C.L.D., Z.Y., H.H., S.E.E., D.C.);Viticulture and Enology Program, Washington State University, Tri-Cities, Richland, Washington 99354 (T.S.C.);Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain (R.M.R.);Consejo Nacional de Investigaciones Científicas y Técnicas, 1900 La Plata, Argentina (A.R.V.);Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, 1900 La Plata, Argentina (A.R.V.); andDolce Winery, Oakville, California 94562 (G.A.) dacantu@ucdavis.edu.

MeSH

AnthocyaninsBotrytisFruitGene Expression ProfilingGene Expression Regulation, DevelopmentalGene Expression Regulation, PlantHost-Pathogen InteractionsMetabolomicsPlant DiseasesVitisWine

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

26450706

Citation

Blanco-Ulate, Barbara, et al. "Developmental and Metabolic Plasticity of White-Skinned Grape Berries in Response to Botrytis Cinerea During Noble Rot." Plant Physiology, vol. 169, no. 4, 2015, pp. 2422-43.
Blanco-Ulate B, Amrine KC, Collins TS, et al. Developmental and Metabolic Plasticity of White-Skinned Grape Berries in Response to Botrytis cinerea during Noble Rot. Plant Physiol. 2015;169(4):2422-43.
Blanco-Ulate, B., Amrine, K. C., Collins, T. S., Rivero, R. M., Vicente, A. R., Morales-Cruz, A., Doyle, C. L., Ye, Z., Allen, G., Heymann, H., Ebeler, S. E., & Cantu, D. (2015). Developmental and Metabolic Plasticity of White-Skinned Grape Berries in Response to Botrytis cinerea during Noble Rot. Plant Physiology, 169(4), 2422-43. https://doi.org/10.1104/pp.15.00852
Blanco-Ulate B, et al. Developmental and Metabolic Plasticity of White-Skinned Grape Berries in Response to Botrytis Cinerea During Noble Rot. Plant Physiol. 2015;169(4):2422-43. PubMed PMID: 26450706.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Developmental and Metabolic Plasticity of White-Skinned Grape Berries in Response to Botrytis cinerea during Noble Rot. AU - Blanco-Ulate,Barbara, AU - Amrine,Katherine C H, AU - Collins,Thomas S, AU - Rivero,Rosa M, AU - Vicente,Ariel R, AU - Morales-Cruz,Abraham, AU - Doyle,Carolyn L, AU - Ye,Zirou, AU - Allen,Greg, AU - Heymann,Hildegarde, AU - Ebeler,Susan E, AU - Cantu,Dario, Y1 - 2015/10/08/ PY - 2015/08/13/received PY - 2015/10/06/accepted PY - 2015/10/10/entrez PY - 2015/10/10/pubmed PY - 2016/9/22/medline SP - 2422 EP - 43 JF - Plant physiology JO - Plant Physiol VL - 169 IS - 4 N2 - Noble rot results from exceptional infections of ripe grape (Vitis vinifera) berries by Botrytis cinerea. Unlike bunch rot, noble rot promotes favorable changes in grape berries and the accumulation of secondary metabolites that enhance wine grape composition. Noble rot-infected berries of cv Sémillon, a white-skinned variety, were collected over 3 years from a commercial vineyard at the same time that fruit were harvested for botrytized wine production. Using an integrated transcriptomics and metabolomics approach, we demonstrate that noble rot alters the metabolism of cv Sémillon berries by inducing biotic and abiotic stress responses as well as ripening processes. During noble rot, B. cinerea induced the expression of key regulators of ripening-associated pathways, some of which are distinctive to the normal ripening of red-skinned cultivars. Enhancement of phenylpropanoid metabolism, characterized by a restricted flux in white-skinned berries, was a common outcome of noble rot and red-skinned berry ripening. Transcript and metabolite analyses together with enzymatic assays determined that the biosynthesis of anthocyanins is a consistent hallmark of noble rot in cv Sémillon berries. The biosynthesis of terpenes and fatty acid aroma precursors also increased during noble rot. We finally characterized the impact of noble rot in botrytized wines. Altogether, the results of this work demonstrated that noble rot causes a major reprogramming of berry development and metabolism. This desirable interaction between a fruit and a fungus stimulates pathways otherwise inactive in white-skinned berries, leading to a greater accumulation of compounds involved in the unique flavor and aroma of botrytized wines. SN - 1532-2548 UR - https://www.unboundmedicine.com/medline/citation/26450706/Developmental_and_Metabolic_Plasticity_of_White_Skinned_Grape_Berries_in_Response_to_Botrytis_cinerea_during_Noble_Rot_ DB - PRIME DP - Unbound Medicine ER -
Grapherence [↓41 ↑99]

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