Red blotch disease alters grape berry development and metabolism by interfering with the transcriptional and hormonal regulation of ripening.
Grapevine red blotch-associated virus (GRBaV) is a major threat to the wine industry in the USA. GRBaV infections (aka red blotch disease) compromise crop yield and berry chemical composition, affecting the flavor and aroma properties of must and wine. In this study, we combined genome-wide transcriptional profiling with targeted metabolite analyses and biochemical assays to characterize the impact of the disease on red-skinned berry ripening and metabolism. Using naturally infected berries collected from two vineyards, we were able to identify consistent berry responses to GRBaV across different environmental and cultural conditions. Specific alterations of both primary and secondary metabolism occurred in GRBaV-infected berries during ripening. Notably, GRBaV infections of post-véraison berries resulted in the induction of primary metabolic pathways normally associated with early berry development (e.g. thylakoid electron transfer and the Calvin cycle), while inhibiting ripening-associated pathways, such as a reduced metabolic flux in the central and peripheral phenylpropanoid pathways. We show that this metabolic reprogramming correlates with perturbations at multiple regulatory levels of berry development. Red blotch caused the abnormal expression of transcription factors (e.g. NACs, MYBs, and AP2-ERFs) and elements of the post-transcriptional machinery that function during red-skinned berry ripening. Abscisic acid, ethylene, and auxin pathways, which control both the initiation of ripening and stress responses, were also compromised. We conclude that GRBaV infections disrupt normal berry development and stress responses by altering transcription factors and hormone networks, which result in the inhibition of ripening pathways involved in the generation of color, flavor, and aroma compounds.
Department of Viticulture and Enology, University of California Davis, Davis, CA 95616, USA.|Department of Plant Sciences, University of California Davis, Davis, CA 95616, USA.
Barbara
B
Blanco-Ulate
Department of Viticulture and Enology, University of California Davis, Davis, CA 95616, USA.|Department of Food Science, The Pennsylvania State University, University Park, PA 16802, USA.
Helene
H
Hopfer
Department of Viticulture and Enology, University of California Davis, Davis, CA 95616, USA.
Rosa
R
Figueroa-Balderas
Department of Viticulture and Enology, University of California Davis, Davis, CA 95616, USA.
Zirou
Z
Ye
CEBAS-CSIC, Campus de Espinardo, 30100, Murcia, Spain.
Rosa M
RM
Rivero
CEBAS-CSIC, Campus de Espinardo, 30100, Murcia, Spain.
Alfonso
A
Albacete
CEBAS-CSIC, Campus de Espinardo, 30100, Murcia, Spain.
Francisco
F
Pérez-Alfocea
Department of Viticulture and Enology, University of California Davis, Davis, CA 95616, USA.|Department of Agronomy, Londrina State University, Celso Garcia Cid Road, Londrina, PR, 86057-970, Brazil.
Renata
R
Koyama
Department of Viticulture and Enology, University of California Davis, Davis, CA 95616, USA.
Michael M
MM
Anderson
University of California Cooperative Extension, Sonoma County, Santa Rosa, CA 95403, USA.
Rhonda J
RJ
Smith
Department of Viticulture and Enology, University of California Davis, Davis, CA 95616, USA.
Susan E
SE
Ebeler
Department of Viticulture and Enology, University of California Davis, Davis, CA 95616, USA.
Dario
D
Cantu
D005638:Fruit / Q000254:growth & development / Q000378:metabolism / Q000821:virology; D017791:Geminiviridae / Q000502:physiology*; D020869:Gene Expression Profiling; D020411:Oligonucleotide Array Sequence Analysis; D010935:Plant Diseases / Q000821:virology; D027843:Vitis / Q000254:growth & development / Q000378:metabolism / Q000821:virology*
Developmental regulation; metabolic flux; perennial woody crop; plant–virus interaction; secondary metabolism; viral disease; véraison