Skip to main content
Log in

Resistance to Erysiphe necator in the grapevine ‘Kishmish vatkana’ is controlled by a single locus through restriction of hyphal growth

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Vitis vinifera ‘Kishmish vatkana’, a cultivated grapevine from Central Asia, does not produce visible symptoms in response to natural or artificial inoculation with the fungus Erysiphe necator Schwein., the casual agent of powdery mildew. ‘Kishmish vatkana’ allowed pathogen entry into epidermal cells at a rate comparable to that in the susceptible control Vitis vinifera ‘Nimrang’, but was able to limit subsequent hyphal proliferation. Density of conidiophores was significantly lower in ‘Kishmish vatkana’ (33.6 ± 8.7 conidiophores mm−2) than in ‘Nimrang’ (310.5 ± 24.0 conidiophores mm−2) by 120 h after inoculation. A progeny of 310 plants from a ‘Nimrang’ × ‘Kishmish vatkana’ cross were scored for the presence or absence of visible conidiophores throughout two successive seasons. Phenotypic segregation revealed the presence of a single dominant allele termed Resistance to Erysiphe necator 1 (REN1), which was heterozygous in ‘Kishmish vatkana’. A bulked segregant analysis was carried out using 195 microsatellite markers uniformly distributed across the entire genome. For each marker, association with the resistance trait was inferred by measuring in the bulks the ratio of peak intensities of the two alleles inherited from ‘Kishmish vatkana’. The phenotypic locus was assigned to linkage group 13, a genomic region in which no disease resistance had been reported previously. The REN1 position was restricted to a 7.4 cM interval by analyzing the 310 offspring for the segregation of markers that surrounded the target region. The closest markers, VMC9H4-2, VMCNG4E10-1 and UDV-020, were located 0.9 cM away from the REN1 locus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adam-Blondon AF, Roux C, Claux D, Butterlin G, Merdinoglu D, This P (2004) Mapping 245 SSR markers on the Vitis vinifera genome: a tool for grape genetics. Theor Appl Genet 109:1017–1027

    Article  PubMed  CAS  Google Scholar 

  • Akkurt M, Welter L, Maul E, Töpfer R, Zyprian E (2006) Development of SCAR markers linked to powdery mildew (Uncinula necator) resistance in grapevine (Vitis vinifera L. and Vitis sp.). Mol Breed 19:103–111

    Article  Google Scholar 

  • Barker CL, Donald T, Pauquet J, Ratnaparkhe MB, Bouquet A, Adam-Blondon AF, Thomas MR, Dry I (2005) Genetic and physical mapping of the grapevine powdery mildew resistance gene, Run1, using a bacterial artificial chromosome library. Theor Appl Genet 111:370–377

    Article  PubMed  CAS  Google Scholar 

  • Bouquet A (1986) Introduction dans l’espèce Vitis vinifera L. d’un caractère de résistance à l’oidium (Uncinula necator Schw. Burr.) issu de l’espèce Muscadinia rotundifolia (Michx.) Small. Vignevini 12(suppl):141–146

    Google Scholar 

  • Boyd LA, Smith PH, Foster EM, Brown JKM (1995) The effect of allelic variation at the Mla resistance locus in barley on the early development of Erysiphe graminis f.sp. hordei and host responses. Plant J 7:959–968

    Article  CAS  Google Scholar 

  • Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Töpsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705

    Article  PubMed  Google Scholar 

  • Castellarin SD, Di Gaspero G, Marconi R, Nonis A, Peterlunger E, Paillard S, Adam-Blondon A-F, Testolin R (2006) Colour variation in red grapevines (Vitis vinifera L.): genomic organisation, expression of flavonoid 3′-hydroxylase, flavonoid 3′,5′-hydroxylase genes and related metabolite profiling of red cyanidin-/blue delphinidin-based anthocyanins in berry skin. BMC Genomics 7:12

    Article  PubMed  Google Scholar 

  • Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu J-L, Hückelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977

    Article  PubMed  CAS  Google Scholar 

  • Consonni C, Humphry ME, Hartmann HA, Livaja M, Durner J, Westphal L, Vogel J, Lipka V, Kemmerling B, Schulze-Lefert P, Somerville SC, Panstruga R (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat Genet 38:716–720

    Article  PubMed  CAS  Google Scholar 

  • Dalbó MA, Ye GN, Weeden NF, Wilcox WF, Reisch BI (2001) Marker-assisted selection for powdery mildew resistance in grapes. J Am Soc Hort Sci 26:83–89

    Google Scholar 

  • de Givry S, Bouchez M, Chabrier P, Milan D, Schiex T (2005) CarthaGene: multipopulation integrated genetic and radiation hybrid mapping. Bioinformatics 21:1703–1704

    Article  PubMed  Google Scholar 

  • Di Gaspero G, Cipriani G, Adam-Blondon AF, Testolin R (2007) Linkage maps of grapevine displaying the chromosomal locations of 420 microsatellite markers and 82 markers from R-gene candidates. Theor Appl Genet 114:1249–1263

    Article  PubMed  CAS  Google Scholar 

  • Doligez A, Adam-Blondon AF, Cipriani G, Di Gaspero G, Laucou V, Merdinoglu D, Meredith CP, Riaz S, Roux C, This P (2006) An integrated SSR map of grapevine based on five mapping populations. Theor Appl Genet 113:369–382

    Article  PubMed  CAS  Google Scholar 

  • Donald TM, Pellerone F, Adam-Blondon AF, Bouquet A, Thomas MR, Dry IB (2002) Identification of resistance gene analogs linked to a powdery mildew resistance locus in grapevine. Theor Appl Genet 104:610–618

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Eibach R, Zyprian E, Welter L, Töpfer R (2007) The use of molecular markers for pyramiding resistance genes in grapevine breeding. Vitis 46:120–124

    CAS  Google Scholar 

  • Epstein L, Bassien S (2003) Patterns of pesticide use in California and the implications for strategies for reduction of pesticides. Annu Rev Phytopathol 41:351–375

    Article  PubMed  CAS  Google Scholar 

  • Fernandez L, Doligez A, Lopez G, Thomas MR, Bouquet A, Torregrosa L (2006) Somatic chimerism, genetic inheritance, and mapping of the fleshless berry (flb) mutation in grapevine (Vitis vinifera L.). Genome 49:721–728

    Article  PubMed  CAS  Google Scholar 

  • Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N, Neu C, Cabral A, Parker JE (2005) Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILTY1 complex in plant innate immunity. Plant Cell 17:2601–2613

    Article  PubMed  CAS  Google Scholar 

  • Filippenko IM, Stin LT (1977) Szort evropejskogo vida Vitis vinifera L. Dzhandzhal kara usztojcsiv k oidiumu. (Vitis vinifera L. ‘Dzhandzhal kara’ is resistant to powdery mildew). Bull Nauchn Inform CGL im IV Michurina 25:57–58. Michurinsk, Russia

    Google Scholar 

  • Fischer BM, Salakhutdinov I, Akkurt M, Eibach R, Edwards KJ, Töpfer R, Zyprian EM (2004) Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor Appl Genet 108:501–515

    Article  PubMed  CAS  Google Scholar 

  • Fung RW, Gonzalo M, Fekete C, Kovacs LG, He Y, Marsh E, McIntyre LM, Schachtman DP, Qiu W (2007) Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol. doi:10.1104/pp.107.108712

    PubMed  Google Scholar 

  • Goto-Yamamoto N, Wan GH, Masaki K, Kobayashi S (2002) Structure and transcription of three chalcone synthase genes of grapevine (Vitis vinifera). Plant Sci 162:867–872

    Article  CAS  Google Scholar 

  • IPGRI, UPOV, OIV (1997) Descripteurs de la Vigne (Vitis spp.). Union internationale pour la protection des obtentions végétales, Genève, Suisse; Office International de la Vigne et du Vin, Paris, France; Institut international des ressources phytogénétiques, Rome, Italy

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180–1183

    Article  PubMed  CAS  Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. PNAS 88:9828–9832

    Article  PubMed  CAS  Google Scholar 

  • Miller TC, WD Gubler (2004) Sensitivity of California isolates of Uncinula necator to trifloxystrobin and spiroxamine, and update on triadimefon sensitivity. Plant Dis 88:1205–1212

    Article  CAS  Google Scholar 

  • Negrul AM (1936) The genetic basis of grape breeding. Bulletin of applied botany, genetics and plant breeding. The Lenin Academy of Agricultural Sciences. Moscow

    Google Scholar 

  • Negrul AM (1968) The origin of the cultivated vine. Dokl Sel’skohoz Acad Timirjazev 139:329–338

    Google Scholar 

  • Pauquet J, Bouquet A, This P, Adam-Blondon A-F (2001) Establishment of a local map of AFLP markers around the powdery mildew resistance gene Run1 in grapevine and assessment of their usefulness for marker assisted selection. Theor Appl Genet 103:1201–1210

    Article  CAS  Google Scholar 

  • Pearson RC (1988) Powdery mildew. In: Pearson RC, Goheen AC (eds) Compendium of grape diseases. APS, St Paul

    Google Scholar 

  • Rumbolz J, Kassenmayer HH, Steinmetz V, Deising HB, Mendgen K, Mathys D, Wirtz S, Guggenheim R (2000) Differentiation of infection structures of the powdery mildew fungus Uncinula necator and adhesion to the host cuticle. Can J Bot 78:409–421

    Article  Google Scholar 

  • Saccardo PA (1882) Sylloge Fungorum. 1: 22 Padua, Italy

  • Stein M, Dittgen J, Sanchez-Rodriquez C, Hou B-H, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–746

    Article  PubMed  CAS  Google Scholar 

  • This P, Lacombe T, Thomas M (2006) Historical origin and genetic diversity of wine grapes. Trends Genet 22:511–519

    Article  PubMed  CAS  Google Scholar 

  • Vojtovic KA (1987) Vospriimchivost sortov vinograda k oidiumu. In: Novüje kompleksno - ustojchevüje stolovüje sorta vinograda i metodü ih polichenija. (Powdery mildew susceptibility of grapevine cultivars. In: New complex resistant table grape cultivars and methods for breeding.) Kisinev Kartja Moldovenjaske, Kishinev, Moldova, pp 42–46

  • Wan Y, Schwaniniger H, He P, Wang Y (2007) Comparison of resistance to powdery mildew and downy mildew in Chinese wild grapes. Vitis 46:132–136

    Google Scholar 

  • Welter LJ, Göktürk-Baydar N, Akkurt M, Maul E, Eibach R, Töpfer R, Zyprian EM (2007) Genetic mapping and localization of quantitative trait loci affecting fungal disease resistance and leaf morphology in grapevine (Vitis vinifera L). Mol Breed 20:359–374

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Uzbek Research Institute of Horticulture, Viticulture and Enology, Tashkent, Uzbekistan for kindly providing the original plant of ‘Kishmish vatkana’. We also thank A. Pfeiffer for SSR genotyping, A. Szabo for plant growing, and T. Dula for phenotypic tests, W. Qiu for facilitating the transfer of ‘Kishmish vatkana’ to Missouri State University, and J. Howard and C. Coleman for proofreading the manuscript. This research was supported by the Hungarian Scientific Research Fund OTKA K62535, USDA-CSREES Federal Appropriation Grant 2004-38901-02138, and by the Regional Administration of Friuli Venezia Giulia (Italy).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gabriele Di Gaspero.

Additional information

Communicated by H. Nybom.

Electronic supplementary material

Below is the link to the electronic supplementary material.

122_2007_680_MOESM1_ESM.tif

Figure S1. Microsatellite markers used for bulked segregant analysis. A set of 291 microsatellite markers scattered over the genome was selected in order to evenly cover all linkage groups. Microsatellites belonged to the markers series scu, UDV, VMC, VrZag, VVI, and VVS (Di Gaspero et al., 2007). Marker orders and distances are based on the consensus map of Doligez et al. (2006). Gaps were filled in with additional markers present in the consensus map of Di Gaspero et al. (2007). Each additional marker was projected onto the map of Doligez et al. (2006) in the interval between the surrounding two markers shared by the two maps in a position at the centre center of the interval. No map distance is given for these markers in this map. Bold markers were heterozygous in ‘Kishmish vatkana’ and hence informative for BSA (TIF 6.34 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hoffmann, S., Di Gaspero, G., Kovács, L. et al. Resistance to Erysiphe necator in the grapevine ‘Kishmish vatkana’ is controlled by a single locus through restriction of hyphal growth . Theor Appl Genet 116, 427–438 (2008). https://doi.org/10.1007/s00122-007-0680-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-007-0680-4

Keywords

Navigation