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Selective sweep at the Rpv3 locus during grapevine breeding for downy mildew resistance

Abstract

The Rpv3 locus is a major determinant of downy mildew resistance in grapevine (Vitis spp.). A selective sweep at this locus was revealed by the DNA genotyping of 580 grapevines, which include a highly diverse set of 265 European varieties that predated the spread of North American mildews, 82 accessions of wild species, and 233 registered breeding lines with North American ancestry produced in the past 150 years. Artificial hybridisation and subsequent phenotypic selection favoured a few Rpv3 haplotypes that were introgressed from wild vines and retained in released varieties. Seven conserved haplotypes in five descent groups of resistant varieties were traced back to their founders: (1) ‘Munson’, a cross between two of Hermann Jaeger’s selections of V. rupestris and V. lincecumii made in the early 1880s in Missouri, (2) V. rupestris ‘Ganzin’, first utilised for breeding in 1879 by Victor Ganzin in France, (3) ‘Noah’, selected in 1869 from intermingled accessions of V. riparia and V. labrusca by Otto Wasserzieher in Illinois, (4) ‘Bayard’, a V. rupestris × V. labrusca offspring generated in 1882 by George Couderc in France, and (5) a wild form closely related to V. rupestris accessions in the Midwestern United States and introgressed into ‘Seibel 4614’ in the 1880s by Albert Seibel in France. Persistence of these Rpv3 haplotypes across many of the varieties generated by human intervention indicates that a handful of vines with prominent resistance have laid the foundation for modern grape breeding. A rampant hot spot of NB-LRR genes at the Rpv3 locus has provided a distinctive advantage for the adaptation of native North American grapevines to withstand downy mildew. The coexistence of multiple resistance alleles or paralogues in the same chromosomal region but in different haplotypes counteracts efforts to pyramidise them in a diploid individual via conventional breeding.

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Acknowledgments

This research was supported by funds from the Italian Ministry of Agriculture, VIGNA project; from the Regional Government of Friuli Venezia Giulia, Grape Breeding Project. We thank the following germplasm repositories for providing grapevine accessions: National Clonal Germplasm Repository, United States Department of Agriculture-Agricultural Research Service, University of California (Davis, CA); United States Department of Agriculture-Plant Genetic Resources Unit, Cornell University (Geneva, NY); Domaine de Vassal INRA Experimental Unit, Centre of Grapevine Genetic Resources, Marseillan plage, France; Höhere Bundeslehranstalt und Bundesamt für Wein- und Obstbau HBLAuBA, Klosterneuburg, Austria; Forschungsanstalt Geisenheim, Germany; Regional Agency for Agricultural Development, Friuli Venezia Giulia, Italy. We also thank Werner Morandell for providing grapevine accessions held at the vineyard ‘Lieselehof - Museum of Viticulture’, Kaltern, Italy, and Peter Cousins (USDA-PGRU, Geneva, NY) for useful information about the V. rupestris in situ preservation sites in Missouri.

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Correspondence to Gabriele Di Gaspero.

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Communicated by C. Schön.

Electronic supplementary material

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Supplementary Material S1 Collection sites of native V. rupestris accessions in Southern Missouri. (PDF 13 kb)

122_2011_1703_MOESM2_ESM.pdf

Supplementary Material S2 List of parent vines most frequently used for grapevine breeding, number of registered seedlings they have generated, and number of registered offspring produced per year through conventional breeding (Vitis International Variety Catalogue, http://www.vivc.de/index.php, as of May 2010). (PDF 37 kb)

Supplementary Material S3 Primer sequences used to detect microsatellite markers in this study. (PDF 11 kb)

122_2011_1703_MOESM4_ESM.xls

Supplementary Material S4 Allele size at the microsatellite loci UDV305 and UDV737 in 580 grapevine accessions. Conserved haplotypes are highlighted by coloured background. Breeding lines supposed to belong to same gene pool but not containing the conserved haplotypes are in black background. First generation hybrids of wild species and V. vinifera lacking the conserved haplotypes are in grey background. (XLS 121 kb)

122_2011_1703_MOESM5_ESM.pdf

Supplementary Material S5 Haplotypic structure at six microsatellite loci spanning 1.2 Mbp from 24.8 Mbp to 26.0 Mbp on chromosome 18 in representative individuals of different descent groups among DM resistant breeding lines. (PDF 47 kb)

122_2011_1703_MOESM6_ESM.ppt

Supplementary Material S6 Kinship of mildew resistant breeding lines and genealogy of non-vinifera Rpv3 haplotypes. B stands for Burdin, BS for Bertille Seyve, C for Couderc, FR for Freiburg, GM for Geisenheim, JS for Joannès Seyve, KL for Klosterneuburg, L for Landot, MM is a series of selections from the Centre of Grape Breeding, Kishinau, Moldova, S stands for Seibel, SV for Seyve-Villard. Coloured background indicates the presence of North American Rpv3 haplotypes: Rpv3 299−279 is yellow, Rpv3 null−297 is purple, Rpv3 321−312 is red, Rpv3 null−271 is ochre, Rpv3 null−287 is brown, Rpv3 361−297 is grey, and Rpv3 299−314 is green. White background stands for V. vinifera haplotypes, unless asterisked. Asterisks indicate resistant varieties for which the genotype could not be determined in this study. Dotted boxes indicate the accessions used as the second parent in the cross that generated the offspring reported underneath. Question mark indicates dubious parentage, pound signs (#) indicate erroneously recorded parents based on the genotype of its descendants. The symbol † indicates extinct individuals, the symbol × indicates individuals that did not generate progeny. (PPT 784 kb)

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Di Gaspero, G., Copetti, D., Coleman, C. et al. Selective sweep at the Rpv3 locus during grapevine breeding for downy mildew resistance. Theor Appl Genet 124, 277–286 (2012). https://doi.org/10.1007/s00122-011-1703-8

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  • DOI: https://doi.org/10.1007/s00122-011-1703-8

Keywords

  • Powdery Mildew
  • Downy Mildew
  • Downy Mildew Resistance
  • Descent Group
  • Methyl Anthranilate