Advertisement

Theoretical and Applied Genetics

, Volume 125, Issue 5, pp 909–920 | Cite as

Consensus mapping of major resistance genes and independent QTL for quantitative resistance to sunflower downy mildew

  • Patrick VincourtEmail author
  • Falah As-sadi
  • Amandine Bordat
  • Nicolas B. Langlade
  • Jerome Gouzy
  • Nicolas Pouilly
  • Yannick Lippi
  • Frédéric Serre
  • Laurence Godiard
  • Denis Tourvieille de Labrouhe
  • Felicity VearEmail author
Original Paper

Abstract

Major gene resistance to sunflower downy mildew (Plasmopara halstedii) races 304 and 314 was found to segregate independently from the resistance to races 334, 307 and 304 determined by the gene Pl2, already positioned on Linkage Group (LG) 8 of sunflower molecular maps. Using a consensus SSR–SNP map constructed from the INEDI RIL population and a new RIL population FU × PAZ2, the positions of Pl2 and Pl5 were confirmed and the new gene, denoted Pl21, was mapped on LG13, at 8 cM from Pl5. The two RIL populations were observed for their quantitative resistance to downy mildew in the field and both indicated the existence of a QTL on LG8 at 20–40 cM from the major resistance gene cluster. In addition, for the INEDI population, a strong QTL on LG10, reported previously, was confirmed and a third QTL was mapped on LG7. A growth chamber test methodology, significantly correlated with field results, also revealed the major QTL on LG10, explaining 65 % of variability. This QTL mapped in the same area as a gene involved in stomatal opening and root growth, which may be suggested as a possible candidate to explain the control of this character. These results indicate that it should be possible to combine major genes and other resistance mechanisms, a strategy that could help to improve durability of sunflower resistance to downy mildew.

Keywords

Downy Mildew Helianthus Annuus Quantitative Resistance Downy Mildew Resistance Major Resistance Gene 
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

We would like to thank S. Roche, M-C. Boniface, N. Blanchet, D. Jolivot, P. Walser and the INRA farm, greenhouse and growth chamber teams at Clermont-Ferrand and Toulouse for their expert technical help. PROMOSOL provided financial support for this research. SNP genotyping data were obtained in collaboration with the companies BIOGEMMA, SYNGENTA SEEDS, SOLTIS and RAGT, during the “SUNYFUEL” project, financially supported by the French National Research Agency, and the OLEOSOL project, with the financial support from the Midi Pyrénées Region, the European Fund for Regional Development (EFRD), and the French Fund for Competitiveness Clusters (FUI).

Supplementary material

122_2012_1882_MOESM1_ESM.xlsx (95 kb)
Supplementary file 1: Helianthus annuus candidate gene sequences chosen for SNP identification and mapping (CG_code, HU_cluster (http://www.heliagene.org) or HP_cluster (http://www.heliagene.org/HP), Arabidopsis thaliana_homologue, FWD_primer_name, FWD_primer_sequence, REV_primer_name, REV_primer_sequence) (XLSX 94 kb)
122_2012_1882_MOESM2_ESM.xlsx (14 kb)
Supplementary file 2: List of 48 sunflower lines used to detect SNP polymorphism on candidate genes (XLSX 14 kb)
122_2012_1882_MOESM3_ESM.xlsx (1.5 mb)
Supplementary file 3: Consensus map built on INEDI and FU × PAZ2 RIL populations (XLSX 1573 kb)
122_2012_1882_MOESM4_ESM.txt (2 kb)
Supplementary file 4: Partial sequence of CG0103 (fasta format) (TXT 1 kb)
122_2012_1882_MOESM5_ESM.txt (1 kb)
Supplementary file 5: Partial sequence of CG0449 (fasta format) (TXT 0 kb)

References

  1. Allard C (1978) Invasion et colonisation systémique de la plantule de Tournesol (Helianthus annuus L.) par le Plasmopara halstedii (Farl.) Berl. Et de Toni. Ann. Phytopathol. 10(2):197–217Google Scholar
  2. Allègre M, Daire X, Héloir MC, Trouvelot S, Mercier L, Adrian M, Pugin A (2007) Stomatal deregulation in Plasmopara viticola-infected grapevine leaves. New Phytol 173:832–840PubMedCrossRefGoogle Scholar
  3. An SH, Sohn KH, Choi HW, Hwang IS, Lee SC, Hwang BK (2008) Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 228:61–78PubMedCrossRefGoogle Scholar
  4. Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, Charcosset A, Joets J (2004) BioMercator: integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics 20(14):2321–2326CrossRefGoogle Scholar
  5. As-Sadi F, Carrere S, Gascuel Q, Hourlier T, Rengel D, Le Paslier MC, Bordat A, Boniface MC, Brunel D, Gouzy J, Godiard L, Vincourt P (2011) Transcriptomic analysis of the interaction between Helianthus annuus and its obligate parasite Plasmopara halstedii shows single nucleotide polymorphisms in CRN sequences. BMC Genomics 12:498PubMedCrossRefGoogle Scholar
  6. Barker G, Batley J, O’ Sullivan H, Edwards KJ, Edwards D (2003) Redundancy based detection of sequence polymorphisms in expressed sequence tag data using autoSNP. Bioinformatics 19:421–422PubMedCrossRefGoogle Scholar
  7. Bert P-F, Tourvieille de Labrouhe D, Philippon J, Mouzeyar S, Jouan I, Nicolas P, Vear F (2001) Identification of a second linkage group carrying genes controlling resistance to downy mildew (Plasmopara halstedii) in sunflower (Helianthus annuus L.). Theor Appl Genet 103:992–997CrossRefGoogle Scholar
  8. Bert P-F, Deschamp-Guillaume G, Serre F, Jouan I, Tourvieille de Labrouhe D, Nicolas P, Vear F (2004) Comparative genetic analysis of quantitative traits in sunflower (Helianthus annuus L.) 3. Characterisation of QTL involved in resistance to Sclerotinia sclerotiorum and Phoma macdonaldii. Theor Appl Genet 109:865–874PubMedCrossRefGoogle Scholar
  9. Bertero de Romano A, Romano C, Bulos M, Alteri E, Sala C (2010) A new gene for resistance to downy mildew in sunflower. In: Proceedings of ISA Symposium “Progress in breeding sunflower for resistance to disease”, Krasnodar, Russia, 21–24 June 2010, pp 142–147Google Scholar
  10. Bouzidi MF, Badaoui S, Cambon F, Vear F, Tourvielle de Labrouhe D, Nicolas P, Mouzeyar S (2002) Molecular analysis of a major locus for resistance to downy mildew in sunflower with specific PCR-based markers. Theor Appl Genet 104:592–600PubMedCrossRefGoogle Scholar
  11. Bret-Mestries E (1996) Recherche de QTL (quantitative trait loci) impliquées dans la résistance du tournesol (Helianthus annuus L.) à la pourriture blanche, causée par Sclerotinia sclerotiorum (Lib.) de Bary. Doctoral Thesis, Univ. Clermont-Ferrand II, INRA Clermont-Ferrand, France, p 152Google Scholar
  12. Doyle LJ, Doyle JJ (1990) Isolation of plant DNA from fresh tissue. Focus 12(1):13–15Google Scholar
  13. Dussle CM, Hahn V, Knapp SJ, Bauer E (2004) Pl arg from Helianthus annuus is unlinked to other known downy mildew resistance genes in sunflower. Theor Appl Genet 109:1083–1086PubMedCrossRefGoogle Scholar
  14. de Givry S, Bouchez M, Chabrier P, Milan D, Schiex T (2005) CARTHAGENE: multipopulation integrated genetic and radiated hybrid mapping. Bioinformatics 21:1703–1704PubMedCrossRefGoogle Scholar
  15. Goossen PG, Sackston WE (1967) Transmission and biology of sunflower downy mildew. Can J Bot 546:5–10Google Scholar
  16. Gulya TJ (2007) Distribution of Plasmopara halstedii races from sunflower around the world. pp 135–142. In: “Advances in Downy Mildew Research” Proceedings of the 2nd International, Downy Mildew Symposium. Palcky, University in Olomouc and JOLA, v.o.s., 2–6 July 2007, vol 3. Kostelec na Hane, Czech RepublicGoogle Scholar
  17. Gulya TJ, Sackston WE, Viranyi F, Masirevic S, Rashid KY (1991) New races of the sunflower downy mildew pathogen (Plasmopara halstedii) in Europe and North and South America. J Phytopathol 132:303–311CrossRefGoogle Scholar
  18. Gulya TJ, Tourvieille de Labrouhe D, Maširevic S, Penaud A, Rashid K, Viranyi F (1998) Proposal for standardized nomenclature and identification of races of Plasmopara halstedii (sunflower downy mildew). In: Proceedings of the ISA Symposium “Sunflower Downy Mildew”, Fargo, USA, 13–14 January 1998, pp 130–136Google Scholar
  19. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877PubMedCrossRefGoogle Scholar
  20. Hyten DL, Song Q, Choi IY, Yoon MS, Specht JE, Matukumalli LK, Nelson RL, Shoemaker RC, Young ND, Cregan PB (2008) High-throughput genotyping with the GoldenGate assay in the complex genome of soybean. Theo Appl Gen 116:945–952CrossRefGoogle Scholar
  21. Jourjon MF, Jasson S, Marcel J, Ngom B, Mangin B (2005) MCQTL: multi-allelic QTL mapping in multi-cross design. Bioinformatics 21:128–130PubMedCrossRefGoogle Scholar
  22. Lai Z, Livingstone K, Zou Y, Church SA, Knapp SJ, Andrews J, Rieseberg LH (2005) Identification and mapping of SNPs from ESTs in sunflower. Theor Appl Genet 111(8):1532–1544PubMedCrossRefGoogle Scholar
  23. Leppik EE (1962) Distribution of downy mildew and some other seed-borne pathogens of sunflower. FAO Plant Prot Bull 10:126–129Google Scholar
  24. Lin CH, Yeakley JM, McDaniel TK, Shen R (2009) Medium- to High-throughput SNP genotyping using veracode microbeads. Methods Mol Med 496:129–142Google Scholar
  25. Louvet J, Kermoal JP (1966) Le mildiou menace-t-il la culture du tournesol en France? C.R.AAcad. Agri 12:896–902Google Scholar
  26. Molinero-Ruiz ML, Molinero-Vera JM, Dominguez J (2002) Inheritance of resistance to race 330 of Plasmopara halstedii in three sunflower lines. Plant Breeding 121:61–65CrossRefGoogle Scholar
  27. Molinero-Ruiz ML, Molinero-Vera JM, Dominguez J (2003) Inheritance of resistance to two races of sunflower downy mildew (Plasmopara halstedii) in two Helianthus annuus L. lines. Euphytica 131:47–51CrossRefGoogle Scholar
  28. Mouzeyar S, Tourvieille de Labrouhe D, Vear F (1993) Histopathological studies of résistance of sunflower (Helianthus annuus L.) to downy mildew (Plasmopara halstedii Farl. Berlese et de Toni). J Phytopathology 139:289–297CrossRefGoogle Scholar
  29. Mouzeyar S, Tourvieille de Labrouhe D, Vear F (1994) Effect of host-race combination on resistance of sunflower, Helianthus annuus L., to Downy Mildew Plasmopara halstedii. J Phytopathol 141(3): 249–258Google Scholar
  30. Mouzeyar S, Roeckel-Drevet P, Phillipon J, Gentzbittel L, Vear F, Tourvieille de Labrouhe D, Nicolas P (1995) RFLP and RAPD mapping of the sunflower Pl1 gene for résistance to Plasmopara halstedii race 1. Theor Appl Genet 91:733–737CrossRefGoogle Scholar
  31. Mulpuri S, Liu Z, Feng F, Gulya TJ, Jan CC (2009) Inheritance and molecular mapping of a downy mildew resistance gene, Pl13 in cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 119: 795–803Google Scholar
  32. Novotelnova NS (1960) Biological characteristics of Plasmopara halstedii (Farl.) Berl. Et de Toni on sunflower. Botan Zhur 45:1283–1300 (In Russian)Google Scholar
  33. Pandey S, Assmann SM (2004) The Arabidopsis putative G protein-coupled receptor GCR1 interacts with the Gprotein alpha subunit GPA1 and regulates abscisic acid signaling. Plant Cell 16:1616–1632PubMedCrossRefGoogle Scholar
  34. Pandey S, Monshausen GB, Ding L, Assmann S (2008) Regulation of root-wave response by extra large and conventional G proteins in Arabidopsis thaliana. Plant J 55(2):311–322PubMedCrossRefGoogle Scholar
  35. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2008) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14(1):21–29PubMedCrossRefGoogle Scholar
  36. Porebski S, Grant Bailey L, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Reporter 15(1):8–15CrossRefGoogle Scholar
  37. Radwan O, Bouzidi MF, Vear F, Phillipon J, Tourvieille de Labrouhe D, Nicolas P, Mouzeyar S (2002) Identification of non-TIR-NBS-LRR markers linked to the Pl5/Pl8 locus for resistance to downy mildew in sunflower. Theor Appl Genet 106:1438–1446Google Scholar
  38. Radwan O, Gandhi S, Heesacker A, Whitaker B, Taylor C, Plocik A, Kesseli R, Kozik A, Michelmore RW, Knapp SJ (2008) Genetic diversity and genomic distribution of homologs encoding NBS-LRR disease resistance proteins in sunflower. Mol Genet Genomics 280:111–125PubMedCrossRefGoogle Scholar
  39. Radwan O, Bouzidi M, Mouzeyar S (2011) Molecular characterization of two types of resistance in sunflower to plasmopara halstedii, the causal agent of downy mildew. Phytopathology 101(8):970–979PubMedCrossRefGoogle Scholar
  40. Roeckel-Drevet P, Gagne G, Mouzeyar S, Gentzbittel L, Phillipon J, Nicolas P, Tourvieille de Labrouhe D, Vear F (1996) Colocation of downy mildew (Plasmopara halstedii) résistance genes in sunflower (Helianthus annuus L.). Euphytica 91:225–228Google Scholar
  41. Ralser M, Querfurth R, Warnatz HJ, Lehrach H, Yaspo ML, Krobitsch S (2006) An efficient and economic enhancer mix for PCR. Biophys Res Commun 347:747–751CrossRefGoogle Scholar
  42. Sackston WE (1949) Sunflower diseases in Manitoba in 1948. Can Plant Disease Surv 28:31–33Google Scholar
  43. Sakr N, Ducher M, Tourvieille J, Walser P, Vear F, Tourvieille de Labrouhe D (2009) A Method to Measure Aggressiveness of Plasmopara halstedii (Sunflower Downy Mildew). J Phytopathology 157:133–136CrossRefGoogle Scholar
  44. Shen R, Fan JB, Campbell D, Chang W, Chen J, Doucet D, Yeakley J, Bibikova M, Wickham Garcia E, McBride C, Steemers F, Garcia F, Kermani BG, Gunderson K, Oliphant A (2005) High-throughput SNP genotyping on universal bead arrays. Res/Fundam Mol Mech Mutagenesis 573:70–82CrossRefGoogle Scholar
  45. Stewart HE, Bradshaw JE, Pande B (2003) The effect of the presence of R-genes for resistance to late blight (Phytophthora infestans) of potato (Solanum tuberosum) on the underlying level of field resistance. Plant Pathol 52:193–198CrossRefGoogle Scholar
  46. Tourvieille de Labrouhe D (2003). El mildiu del girasol : manejo de estrategias de control para una eficacia durable, 2° Congreso Argentino de Girasol, Buenos Aires (Argentina), 12 y 13 de Agosto. http://www.asagir.org. ar/2_congreso/P06.- TOURVIEILLE.pps
  47. Tourvieillle de Labrouhe D, Gulya TJ, Masirevic SPenaus A, Rashid KY, Viranyi F (2000). New nomenclature of races of Plasmopara halstedii (sunflower downy mildew). In: Proceedings of the 15th International Sunflower Conference Toulouse France 12-15 June 2000. Int. Sunfl. Assoc.Paris, France, pp I61–66Google Scholar
  48. Tourvieille de Labrouhe D, Serre F, Walser P, Roche S, Vear F (2008) Quantitative resistance to downy mildew (Plasmopara halstedii) in sunflower (Helianthus annuus). Euphytica 164:433–444CrossRefGoogle Scholar
  49. Tourvieille de Labrouhe D, Walser P, Joliovot D, Roche S, Serre F, Delmotte F, Bordat A, Godiard L, Vincourt P, Vear F (2012) Proposal for improvement of sunflower downy mildew race nomenclature. In: Proceedings of the 18th Int. Sunfl. Conf. Mar del Plata, Argentina 26/2–1 March 2012, Int. Sunfl. Assoc.Paris, France, pp 322–327Google Scholar
  50. Vear F (1978) Réaction de certains génotypes de tournesol résistants au mildiou (Plasmopara helianthi) au test de résistance sur plante. Ann Amélior Plantes 28:327–332Google Scholar
  51. Vear F, Gentzbittel L, Philippon J, Mouzeyar S, Mestries E, Roeckel-Drevet P, Tourvieille de Labrouhe D, Nicolas P (1997) The genetics of resistance to five races of downy mildew (Plasmopara halstedii) in sunflower (Helianthus annuus L.). Theor Appl Genet 95:584–589CrossRefGoogle Scholar
  52. Vear F, Serre F, Jouan-Dufournel I, Bert PF, Roche S, Walser P, Tourvieille de Labrouhe D, Vincourt P (2008) Inheritance of quantitative resistance to downy mildew (Plasmopara halstedii) in sunflower (Helianthus annuus L.). Euphytica 164:561–570CrossRefGoogle Scholar
  53. Vear F, Tourvieille de Labrouhe D, Roche S, Boniface MC, Bordat A, Vincourt P (2012) Genetic analysis of the sunflower downy mildew resistance gene Pl2.In: Proceedings of the 18th Int. Sunfl. Conf. Mar del Plata, Argentina, 26/2–1 March 2012. Int. Sunfl. Assoc. Paris, France, pp 328–333Google Scholar
  54. Zhang W, He Sheng Yang, Assmann SM (2008) The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation. Plant J 56:984–996PubMedCrossRefGoogle Scholar
  55. Zimmer DE (1974) Physiological specialization between races of Plasmopara halstedii in America and Europe. Phytopahtology 64:1465–1467CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Patrick Vincourt
    • 1
    • 2
    Email author
  • Falah As-sadi
    • 1
    • 2
  • Amandine Bordat
    • 1
    • 2
  • Nicolas B. Langlade
    • 1
    • 2
  • Jerome Gouzy
    • 1
    • 2
  • Nicolas Pouilly
    • 1
    • 2
  • Yannick Lippi
    • 1
    • 2
  • Frédéric Serre
    • 3
  • Laurence Godiard
    • 1
    • 2
  • Denis Tourvieille de Labrouhe
    • 3
  • Felicity Vear
    • 3
    Email author
  1. 1.Laboratoire des Interactions Plantes-Microorganismes (LIPM), INRA, UMR441Castanet-TolosanFrance
  2. 2.Laboratoire des Interactions Plantes-Microorganismes (LIPM), CNRS, UMR2594Castanet-TolosanFrance
  3. 3.INRA, UMR 1095, Domaine de CrouelleClermont-FerrandFrance

Personalised recommendations