Advertisement

Theoretical and Applied Genetics

, Volume 125, Issue 8, pp 1663–1675 | Cite as

A reference genetic map of Muscadinia rotundifolia and identification of Ren5, a new major locus for resistance to grapevine powdery mildew

  • Sophie Blanc
  • Sabine Wiedemann-Merdinoglu
  • Vincent Dumas
  • Pere Mestre
  • Didier MerdinogluEmail author
Original Paper

Abstract

Muscadinia rotundifolia, a species closely related to cultivated grapevine Vitis vinifera, is a major source of resistance to grapevine downy and powdery mildew, two major threats to cultivated traditional cultivars of V. vinifera respectively caused by the oomycete Plasmopara viticola and the ascomycete Erisyphe necator. The aim of the present work was to develop a reference genetic linkage map based on simple sequence repeat (SSR) markers for M. rotundifolia. This map was created using S1 M. rotundifolia cv. Regale progeny, and covers 948 cM on 20 linkage groups, which corresponds to the expected chromosome number for muscadine. The comparison of the genetic maps of V. vinifera and M. rotundifolia revealed a high macrosynteny between the genomes of both species. The S1 progeny was used to assess the general level of resistance of M. rotundifolia to P. viticola and E. necator, by scoring different parameters of pathogen development. A quantitative trait locus (QTL) analysis allowed us to highlight a major QTL on linkage group 14 controlling resistance to powdery mildew, which explained up to 58 % of the total phenotypic variance. This QTL was named ‘Resistance to Erysiphe Necator 5’ (Ren5). A microscopic evaluation E. necator mycelium development on resistant and susceptible genotypes of the S1 progeny showed that Ren5 exerts its action after the formation of the first appressorium, and acts by delaying, and then stopping, mycelium development.

Keywords

Quantitative Trait Locus Powdery Mildew Simple Sequence Repeat Marker Quantitative Trait Locus Analysis Downy Mildew 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Work funded by the French “Agence Nationale de Recherche” (ANR-08-GENM-007). We are grateful to E. Duchêne for useful discussions on statistical methods. We thank P. Coste and M.-A. Dorne for excellent technical assistance in plant growing and inoculum maintenance, V. Tharreau, N. Choisne and P. Blasi for providing primer sequences and M. Erhardt for assistance with scanning electron microscopy.

Supplementary material

122_2012_1942_MOESM1_ESM.docx (50 kb)
Supplementary material 1 (DOCX 49 kb)
122_2012_1942_MOESM2_ESM.docx (44 kb)
Supplementary material 2 (DOCX 44 kb)

References

  1. Adam-Blondon A-F, 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 109:1017–1027PubMedCrossRefGoogle Scholar
  2. Anonymous (2009) Descriptor list for grapevine varieties and Vitis species, 2nd edn. Office International de la Vigne et du Vin (OIV), ParisGoogle Scholar
  3. Barker CL, Donald T, Pauquet J, Ratnaparkhe MB, Bouquet A, Adam-Blondon A-F, Thomas MR, Dry I (2005) Genetic and physical mapping of the grapevine powdery mildew resistancegene, Run1, using a bacterial artificial chromosome library. Theor Appl Genet 111:370–377PubMedCrossRefGoogle Scholar
  4. Baudoin A, Olaya G, Delmotte F, Colcol JF, Sierotzki H (2008) QoI Resistance of Plasmopara viticola and Erysiphe necator in the Mid-Atlantic United States. Plant Manag Netw Plant Health Prog. doi: 10.1094/PHP-2008-0211-02-RS Google Scholar
  5. Bellin D, Peressotti E, Merdinoglu D, Wiedemann-Merdinoglu S, Adam-Blondon A-F, Cipriani G et al (2009) Resistance to Plasmopara viticola in grapevine ‘Bianca’ is controlled by a major dominant gene causing localised necrosis at the infection site. Theor Appl Genet 120:163–176PubMedCrossRefGoogle Scholar
  6. Blasi P, Blanc S, Prado E, Rühl EH, Mestre P, Merdinoglu D (2011) Construction of a reference linkage map of Vitis amurensis and genetic mapping of Rpv8, a locus conferring resistance to grapevine downy mildew. Theor Appl Genet 123:43–53PubMedCrossRefGoogle Scholar
  7. Boubals D (1959) Amélioration de la résistance de la vigne au mildiou (Plasmopara viticola (Berk et Curt.) Berlese et de Toni). Recherche de géniteurs de résistance. Annales de l’amélioration des plantes 6:481–525Google Scholar
  8. Bouquet A (1980) Vitis × Muscadinia hybridization: a new way in grape breeding for disease resistance in France. Proc 3rd Intl Symp On Grape Breeding, pp 177–197Google Scholar
  9. Bouquet A (1983) Contribution à l’étude de l’espèce Muscadinia rotundifolia (Michx) Small et de ses hybrides avec Vitis vinifera L.—applications en sélection. Dissertation, University of Bordeaux IIGoogle Scholar
  10. Bowers JE, Dangl GS, Vignani R, Meredith CP (1996) Isolation and characterization of new polymorphic simple sequence repeat loci in grape (Vitis vinifera L.). Genome 39:628–633PubMedCrossRefGoogle Scholar
  11. Bowers JE, Dangl GS, Meredith CP (1999) Development and characterization of additional microsatellite DNA markers for grape. Am J Enol Vitic 50:243–246Google Scholar
  12. Calonnec A, Cartolaro P, Poupot C, Dubourdieu D, Darriet P (2004) Effects of Uncinula necator on the yield and quality of grapes (Vitis vinifera) and wine. Plant Pathol 53:434–445CrossRefGoogle Scholar
  13. Chen WJ, Delmotte F, Richard-Cervera S, Douence L, Greif C, Corio-Costet MF (2007) At least two origins of fungicide resistance in grapevine downy mildew populations. Appl Environ Microbiol 73(16):5162–5172PubMedCrossRefGoogle Scholar
  14. Chin DB, Arroyo-Garcia R, Ochoa OE, Kesseli RV, Lavelle DO et al (2001) Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa). Genetics 157:831–849PubMedGoogle Scholar
  15. Cipriani G, Di Gaspero G, Canaguier A, Jusseaume J, Tassin J, Lemainque A, Vincent Thareau V, Adam-Blondon A-F, Testolin R (2011) Molecular linkage maps: strategies, resources and achievements. In: A-F Adam-Blondon, JM Martinez-Zapater, Chittaranjan Kole (eds) Genetics, genomics and breeding of grapes. Science Publishers and CRC Press, Florida, pp 111–136Google Scholar
  16. Dalbó MA, Ye GN, Weeden NF, Steinkellner H, Sefc KM, Reisch BI (2000) A gene controlling sex in grapevines placed on a molecular marker-based genetic map. Genome 43:333–340PubMedCrossRefGoogle Scholar
  17. Di Gaspero G, Cipriani G, Marrazzo MT, Andreetta D, Castro MJ, Peterlunger E et al (2005) Isolation of (AC)n-microsatellites in Vitis vinifera L. and analysis of genetic background in grapevines under marker assisted selection. Mol Breed 15:11–20CrossRefGoogle Scholar
  18. 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 for R-gene candidates. Theor Appl Genet 114:1249–1263PubMedCrossRefGoogle Scholar
  19. Dick MW (2002) Binomials in the Peronosporales, Sclerosporales and Pythiales. In: Spencer PTN, Gisi U, Lebeda A (eds) Advances in Downy Mildew Research. Kluwer Academic Publishers, Dordrecht, pp 225–266Google Scholar
  20. Doligez A, Bouquet A, Danglot Y, Lahogue L, Riaz S, Meredith P et al (2002) Genetic mapping of grapevine (Vitis vinifera L.) applied to the detection of QTLs for seedlessness and berry weight. Theor Appl Genet 105:780–795PubMedCrossRefGoogle Scholar
  21. Doligez A, Adam-Blondon AF, Cipriani G, Di Gaspero G, Laucou V, Merdinoglu D et al (2006) An integrated SSR map of grapevine based on five mapping populations. Theor Appl Genet 113:369–382PubMedCrossRefGoogle Scholar
  22. Doucleff M, Jin Y, Gao F, Riaz S, Krivanek AF, Walker MA (2004) A genetic linkage map of grape, utilizing Vitis rupestris and Vitis arizonica. Theor Appl Genet 109:1178–1187PubMedCrossRefGoogle Scholar
  23. Dubos B (2002) Maladies cryptogamiques de la vigne, Féret edn. Bordeaux, FranceGoogle Scholar
  24. Fischer BM, Salakhutdinov I, Akkurt M, Eibach R, Edwards KJ, Töpfer R et al (2004) Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor Appl Genet 108:501–515PubMedCrossRefGoogle Scholar
  25. Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci USA 98:373–378PubMedCrossRefGoogle Scholar
  26. Furuya S, Mochizuki M, Saito S, Kobayashi H, Takayanagi T, Suzuki S (2010) Monitoring of QoI fungicide resistance in Plasmopara viticola populations in Japan. Pest Manag Sci 66:1268–1272PubMedCrossRefGoogle Scholar
  27. Gadoury DM, Seem RC, Ficke A, Wilcox WF (2001) The epidemiology of powdery mildew on Concord grapes. Phytopathology 91:948–955PubMedCrossRefGoogle Scholar
  28. Galet P (1977) Les maladies et les parasites de la vigne, Imp. Paysan du Midi: Montpellier, France, vol. IGoogle Scholar
  29. Gallais A (1990) Quantitative genetics of doubled haploid populations and application to the theory of line development. Genetics 124:199–206PubMedGoogle Scholar
  30. Geffroy V, Macadre C, David P, Pedrosa-Harand A, Dauga C, Sevignac M, Langin T (2009) Molecular analysis of a large subtelomeric nucleotidebinding-site-leucine-rich-repeat family in two representative génotypes of the major gene pools of Phaseolus vulgaris. Genetics 181:405–419PubMedCrossRefGoogle Scholar
  31. Gisi U (2002) Chemical control of downy mildews. In: Spencer-Phillips PTN, Gisi U, Lebeda A (eds) Advances in Downy Mildew Research. Kluwer Academic Publishers, Dordrecht, pp 119–159Google Scholar
  32. Gisi U, Sierotzki H (2008) Fungicide modes of action and resistance in downy mildews. Eur J Plant Pathol 122(1):157–167CrossRefGoogle Scholar
  33. Gisi U, Waldner M, Kraus N, Dubuis PH, Sierotzki H (2007) Inheritance of resistance to carboxylic acid amide (CAA) fungicides in Plasmopara viticola. Plant Pathol 56:199–208CrossRefGoogle Scholar
  34. Grando MS, Bellin D, Edwards KJ, Pozzi C, Stefanini M, Velasco R (2003) Molecular linkage maps of Vitis vinifera L. and Vitis riparia Mchx. Theor Appl Genet 106:1213–1224PubMedGoogle Scholar
  35. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467PubMedCrossRefGoogle Scholar
  36. Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175Google Scholar
  37. Lafon R, Clerjeau M (1988) Downy mildew. In: Pearson RC, Goheen AC (eds) Compendium of grape diseases. Am Phytopathol Soc, St. Paul, pp 11–13Google Scholar
  38. Lowe KM, Walker MA (2006) Genetic linkage map of the interspecific grape rootstock cross Ramsey (Vitis champinii) × Riparia Gloire (Vitis riparia). Theor Appl Genet 112:1582–1592PubMedCrossRefGoogle Scholar
  39. Marguerit E, Boury C, Manicki A, Donnart M, Butterlin G, Némorin A et al (2009) Genetic dissection of sex determinism, inflorescence morphology and downy mildew resistance in grapevine. Theor Appl Genet 118:1261–1278PubMedCrossRefGoogle Scholar
  40. Merdinoglu D, Wiedemann-Merdinoglu S, Coste P, Dumas V, Haetty S, Butterlin G et al (2003) Genetic analysis of downy mildew resistance derived from Muscadinia rotundifolia. Acta Hortic 603:451–456Google Scholar
  41. Merdinoglu D, Butterlin G, Bevilacqua L, Chiquet V, Adam-Blondon AF, Decroocq S (2005) Development and characterization of a large set of microsatellite markers in grapevine (Vitis vinifera L.) suitable for multiplex PCR. Mol Breed 15:349–366CrossRefGoogle Scholar
  42. Miclot AS, Wiedemann-Merdinoglu S, Duchêne E, Merdinoglu D, Mestre P (2012) A standardised method for the quantitative analysis of resistance to grapevine powdery mildew. Eur J Plant Pathol. doi: 10.1007/s10658-011-9922-z Google Scholar
  43. Moreira FM, Madini A, Marino R, Zulini L, Stefanini M, Velasco R, Kozma P, Grando MS (2010) Genetic linkage maps of two interspecific grape crosses (Vitis spp.) used to localize quantitative trait loci for downy mildew resistance. Tree Gen Genomes 7:153–167CrossRefGoogle Scholar
  44. Moroldo M, Paillard S, Marconi R, Fabrice L, Canaguier A, Cruaud C et al (2008) A physical map of the heterozygous grapevine ‘Cabernet Sauvignon’ allows mapping candidate genes for disease resistance. BMC Plant Biol 8:66PubMedCrossRefGoogle Scholar
  45. Mullins MG, Bouquet A, Williams LE (1992) Biology of the grapevine. Cambridge Univ. Press, New YorkGoogle Scholar
  46. Olien WC (1990) The muscadine grape: Botany, viticulture, history and current industry. Hort Sci 25:732–739Google Scholar
  47. Olmo HP (1986) The potential role of (vinifera × rotundifolia) hybrids in grape variety improvement. Experientia 42:921–926CrossRefGoogle Scholar
  48. Patel GI, Olmo HP (1955) Cytogenetics of Vitis: I. The hybrid of V. vinifera × V. rotundifolia. Am J Bot 42:141–159CrossRefGoogle Scholar
  49. Pauquet J, Bouquet A, This P, Adam-Blondon AF (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 103:1201–1210CrossRefGoogle Scholar
  50. Pool RM, Pearson RC, Welser MJ, Lakso AN, Seem RC (1984) Influence of powdery mildew on yield and growth of Rosette grapevines. Plant Dis 68:590–593Google Scholar
  51. Regner F, Hack R, Santiago JL (2006) Highly variable Vitis microsatellite loci for the identification of Pinot Noir clones. Vitis 45:85–91Google Scholar
  52. Riaz S, Dangl GS, Edward KJ, Meredith CP (2004) A microsatellite marker based framework linkage map of Vitis vinifera L. Theor Appl Genet 108:864–872PubMedCrossRefGoogle Scholar
  53. Riaz S, Tenscher A, Smith B, Ng D, Walker M (2008) Use of SSR markers to assess identity, pedigree, and diversity of cultivated Muscadinia rotundifolia. J Am Soc Hort Sci 133:559–568Google Scholar
  54. Riaz S, Tenscher AC, Ramming DW, Walker MA (2011) Using a limited mapping strategy to identify major QTLs for resistance to grapevine powdery mildew (Erysiphe necator) and their use in marker-assisted breeding. Theor Appl Genet 122:1059–1073PubMedCrossRefGoogle Scholar
  55. Richter TE, Pryor TJ, Bennetzen JL, Hulbert SH (1995) New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics 141:373–381PubMedGoogle Scholar
  56. Rumbolz J, Kassemeyer HH, Steinmetz V, Deising HB, Mendgen K, Mathys D, Wirtz S (2000) Differentiation of infection structures of the powdery mildew fungus Uncinula necator and adhesion to the host cuticle. Can J Bot 78(3):409–421Google Scholar
  57. Salmaso M, Malacarne G, Troggio M, Faes G, Stefanini M, Grando MS et al (2008) A grapevine (Vitis vinifera L.) genetic map integrating the position of 139 expressed genes. Theor Appl Genet 116:1129–1143PubMedCrossRefGoogle Scholar
  58. Sefc KM, Regner F, Turetschek E, Glössl J, Steinkellner H (1999) Identification of microsatellite sequences in Vitis riparia and their applicability for genotyping of different Vitis species. Genome 42:367–373PubMedGoogle Scholar
  59. Small JK (1913) Flora of the southeastern United States, 2nd edn. New York, p 1394Google Scholar
  60. Sudupak MA, Bennetzen JL, Hulbert SH (1993) Unequal exchange and meiotic instability of disease-resistance genes in the Rpl region of maize. Genetics 133:119–125PubMedGoogle Scholar
  61. Thomas MR, Scott NS (1993) Microsatellite repeats in grapevine reveal DNA polymorphism when analysed as sequence-tagged sites (STSs). Theor Appl Genet 86:985–990Google Scholar
  62. Troggio M, Malacarne G, Coppola G, Segala C, Cartwright DA, Pindo M et al (2007) A dense single-nucleotide polymorphism-based genetic linkage map of grapevine (Vitis vinifera L.) anchoring Pinot Noir bacterial artificial chromosome contigs. Genetics 176:2637–2650PubMedCrossRefGoogle Scholar
  63. Van Ooijen JW (2009) MapQTL6.0, Software for the mapping of quantitative trait loci in experimental populations of diploid species. Wageningen, Kyazma B.V., the NetherlandsGoogle Scholar
  64. Van Ooijen JW, Voorrips RE (2001) Joinmap3.0, Software for the calculation of genetic linkage maps. Plant Research Int., Wageningen, Kyazma B.V., the NetherlandsGoogle Scholar
  65. Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2(12):e1326PubMedCrossRefGoogle Scholar
  66. Weaver RJ (1976) Grape growing. Wiley, New York, p 371Google Scholar
  67. Welter LJ, Göktürk-Baydar N, Akkurt M, Maul E, Eibach R, Töpfer R et al (2007) Genetic mapping and localization of quantitative trait loci affecting fungal disease resistance and leaf morphology in grapevine (Vitis vinifera L). Mol Breed 20:359–374CrossRefGoogle Scholar
  68. Wiedemann-Merdinoglu S, Prado E, Coste P, Dumas V, Butterlin G, and Merdinoglu D (2006) Genetic analysis of resistance to downy mildew derived from Muscadinia rotundifolia. Ninth International Conference on Grape Genetics and Breeding. Udine. Italy, July 2–6Google Scholar
  69. Wilcox WF, Burr JA, Riegel DG, Wong FP (2003) Practical resistance to QoI fungicides in New York populations of Uncinula necator associated with quantitative shifts in pathogen sensitivities. (Abstr.). Phytopathology 93:S90Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Sophie Blanc
    • 1
    • 2
  • Sabine Wiedemann-Merdinoglu
    • 1
    • 2
  • Vincent Dumas
    • 1
    • 2
  • Pere Mestre
    • 1
    • 2
  • Didier Merdinoglu
    • 1
    • 2
    Email author
  1. 1.Santé de la Vigne et Qualité du VinINRA-UDSColmar CedexFrance
  2. 2.Santé de la Vigne et Qualité du VinUniversité de StrasbourgColmarFrance

Personalised recommendations