title: Strategies for RUN1 Deployment Using RUN2 and REN2 to Manage Grapevine Powdery Mildew Informed by Studies of Race Specificity.
abstract: The Toll/interleukin-1 receptor nucleotide-binding site leucine-rich repeat gene, "resistance to Uncinula necator 1" (RUN1), from Vitis rotundifolia was recently identified and confirmed to confer resistance to the grapevine powdery mildew fungus Erysiphe necator (syn. U. necator) in transgenic V. vinifera cultivars. However, sporulating powdery mildew colonies and cleistothecia of the heterothallic pathogen have been found on introgression lines containing the RUN1 locus growing in New York (NY). Two E. necator isolates collected from RUN1 vines were designated NY1-131 and NY1-137 and were used in this study to inform a strategy for durable RUN1 deployment. In order to achieve this, fitness parameters of NY1-131 and NY1-137 were quantified relative to powdery mildew isolates collected from V. rotundifolia and V. vinifera on vines containing alleles of the powdery mildew resistance genes RUN1, RUN2, or REN2. The results clearly demonstrate the race specificity of RUN1, RUN2, and REN2 resistance alleles, all of which exhibit programmed cell death (PCD)-mediated resistance. The NY1 isolates investigated were found to have an intermediate virulence on RUN1 vines, although this may be allele specific, while the Musc4 isolate collected from V. rotundifolia was virulent on all RUN1 vines. Another powdery mildew resistance locus, RUN2, was previously mapped in different V. rotundifolia genotypes, and two alleles (RUN2.1 and RUN2.2) were identified. The RUN2.1 allele was found to provide PCD-mediated resistance to both an NY1 isolate and Musc4. Importantly, REN2 vines were resistant to the NY1 isolates and RUN1REN2 vines combining both genes displayed additional resistance. Based on these results, RUN1-mediated resistance in grapevine may be enhanced by pyramiding with RUN2.1 or REN2; however, naturally occurring isolates in North America display some virulence on vines with these resistance genes. The characterization of additional resistance sources is needed to identify resistance gene combinations that will further enhance durability. For the resistance gene combinations currently available, we recommend using complementary management strategies, including fungicide application, to reduce populations of virulent isolates.
authors.affiliation: First and seventh authors: CSIRO Agriculture Flagship, Urrbrae, South Australia 5064, Australia; second author: Department of Plant Biology, University of Pécs, Pécs 7624, Hungary; third and sixth authors: Department of Viticulture and Enology, University of California, Davis 95616; fourth author: Institute of Plant and Environment Protection, Beijing Academy of Agriculture & Forestry Sciences, Beijing 100097; fifth author: Plant Pathology and Plant-Microbe Biology Section, Cornell University, New York State Agricultural Experiment Station, Geneva 14456; eighth author: Horticulture Section, Cornell University, New York State Agricultural Experiment Station, Geneva; and ninth author: United States Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY 14456.
authors.forename: Angela
authors.initials: A
authors.lastname: Feechan
authors.affiliation: First and seventh authors: CSIRO Agriculture Flagship, Urrbrae, South Australia 5064, Australia; second author: Department of Plant Biology, University of Pécs, Pécs 7624, Hungary; third and sixth authors: Department of Viticulture and Enology, University of California, Davis 95616; fourth author: Institute of Plant and Environment Protection, Beijing Academy of Agriculture & Forestry Sciences, Beijing 100097; fifth author: Plant Pathology and Plant-Microbe Biology Section, Cornell University, New York State Agricultural Experiment Station, Geneva 14456; eighth author: Horticulture Section, Cornell University, New York State Agricultural Experiment Station, Geneva; and ninth author: United States Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY 14456.
authors.forename: Marianna
authors.initials: M
authors.lastname: Kocsis
authors.affiliation: First and seventh authors: CSIRO Agriculture Flagship, Urrbrae, South Australia 5064, Australia; second author: Department of Plant Biology, University of Pécs, Pécs 7624, Hungary; third and sixth authors: Department of Viticulture and Enology, University of California, Davis 95616; fourth author: Institute of Plant and Environment Protection, Beijing Academy of Agriculture & Forestry Sciences, Beijing 100097; fifth author: Plant Pathology and Plant-Microbe Biology Section, Cornell University, New York State Agricultural Experiment Station, Geneva 14456; eighth author: Horticulture Section, Cornell University, New York State Agricultural Experiment Station, Geneva; and ninth author: United States Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY 14456.
authors.forename: Summaira
authors.initials: S
authors.lastname: Riaz
authors.affiliation: First and seventh authors: CSIRO Agriculture Flagship, Urrbrae, South Australia 5064, Australia; second author: Department of Plant Biology, University of Pécs, Pécs 7624, Hungary; third and sixth authors: Department of Viticulture and Enology, University of California, Davis 95616; fourth author: Institute of Plant and Environment Protection, Beijing Academy of Agriculture & Forestry Sciences, Beijing 100097; fifth author: Plant Pathology and Plant-Microbe Biology Section, Cornell University, New York State Agricultural Experiment Station, Geneva 14456; eighth author: Horticulture Section, Cornell University, New York State Agricultural Experiment Station, Geneva; and ninth author: United States Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY 14456.
authors.forename: Wei
authors.initials: W
authors.lastname: Zhang
authors.affiliation: First and seventh authors: CSIRO Agriculture Flagship, Urrbrae, South Australia 5064, Australia; second author: Department of Plant Biology, University of Pécs, Pécs 7624, Hungary; third and sixth authors: Department of Viticulture and Enology, University of California, Davis 95616; fourth author: Institute of Plant and Environment Protection, Beijing Academy of Agriculture & Forestry Sciences, Beijing 100097; fifth author: Plant Pathology and Plant-Microbe Biology Section, Cornell University, New York State Agricultural Experiment Station, Geneva 14456; eighth author: Horticulture Section, Cornell University, New York State Agricultural Experiment Station, Geneva; and ninth author: United States Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY 14456.
authors.forename: David M
authors.initials: DM
authors.lastname: Gadoury
authors.affiliation: First and seventh authors: CSIRO Agriculture Flagship, Urrbrae, South Australia 5064, Australia; second author: Department of Plant Biology, University of Pécs, Pécs 7624, Hungary; third and sixth authors: Department of Viticulture and Enology, University of California, Davis 95616; fourth author: Institute of Plant and Environment Protection, Beijing Academy of Agriculture & Forestry Sciences, Beijing 100097; fifth author: Plant Pathology and Plant-Microbe Biology Section, Cornell University, New York State Agricultural Experiment Station, Geneva 14456; eighth author: Horticulture Section, Cornell University, New York State Agricultural Experiment Station, Geneva; and ninth author: United States Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY 14456.
authors.forename: M Andrew
authors.initials: MA
authors.lastname: Walker
authors.affiliation: First and seventh authors: CSIRO Agriculture Flagship, Urrbrae, South Australia 5064, Australia; second author: Department of Plant Biology, University of Pécs, Pécs 7624, Hungary; third and sixth authors: Department of Viticulture and Enology, University of California, Davis 95616; fourth author: Institute of Plant and Environment Protection, Beijing Academy of Agriculture & Forestry Sciences, Beijing 100097; fifth author: Plant Pathology and Plant-Microbe Biology Section, Cornell University, New York State Agricultural Experiment Station, Geneva 14456; eighth author: Horticulture Section, Cornell University, New York State Agricultural Experiment Station, Geneva; and ninth author: United States Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY 14456.
authors.forename: Ian B
authors.initials: IB
authors.lastname: Dry
authors.affiliation: First and seventh authors: CSIRO Agriculture Flagship, Urrbrae, South Australia 5064, Australia; second author: Department of Plant Biology, University of Pécs, Pécs 7624, Hungary; third and sixth authors: Department of Viticulture and Enology, University of California, Davis 95616; fourth author: Institute of Plant and Environment Protection, Beijing Academy of Agriculture & Forestry Sciences, Beijing 100097; fifth author: Plant Pathology and Plant-Microbe Biology Section, Cornell University, New York State Agricultural Experiment Station, Geneva 14456; eighth author: Horticulture Section, Cornell University, New York State Agricultural Experiment Station, Geneva; and ninth author: United States Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY 14456.
authors.forename: Bruce
authors.initials: B
authors.lastname: Reisch
authors.affiliation: First and seventh authors: CSIRO Agriculture Flagship, Urrbrae, South Australia 5064, Australia; second author: Department of Plant Biology, University of Pécs, Pécs 7624, Hungary; third and sixth authors: Department of Viticulture and Enology, University of California, Davis 95616; fourth author: Institute of Plant and Environment Protection, Beijing Academy of Agriculture & Forestry Sciences, Beijing 100097; fifth author: Plant Pathology and Plant-Microbe Biology Section, Cornell University, New York State Agricultural Experiment Station, Geneva 14456; eighth author: Horticulture Section, Cornell University, New York State Agricultural Experiment Station, Geneva; and ninth author: United States Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY 14456.
authors.forename: Lance
authors.initials: L
authors.lastname: Cadle-Davidson
mesh_terms: D000483:Alleles; D001203:Ascomycota / Q000502:physiology*; D015415:Biomarkers; D001947:Breeding; D060467:Disease Resistance / Q000235:genetics*; D005838:Genotype; D010935:Plant Diseases / Q000276:immunology / Q000382:microbiology / Q000517:prevention & control*; D018515:Plant Leaves / Q000276:immunology / Q000382:microbiology; D010940:Plant Proteins / Q000235:genetics*; D040641:Quantitative Trait Loci / Q000235:genetics; D013045:Species Specificity; D027843:Vitis / Q000235:genetics* / Q000276:immunology / Q000382:microbiology
chemical_list: D015415:Biomarkers; D010940:Plant Proteins