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Pl 17 is a novel gene independent of known downy mildew resistance genes in the cultivated sunflower (Helianthus annuus L.)

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Pl 17 , a novel downy mildew resistance gene independent of known downy mildew resistance genes in sunflowers, was genetically mapped to linkage group 4 of the sunflower genome.

Abstract

Downy mildew (DM), caused by Plasmopara halstedii (Farl.). Berl. et de Toni, is one of the serious sunflower diseases in the world due to its high virulence and the variability of the pathogen. DM resistance in the USDA inbred line, HA 458, has been shown to be effective against all virulent races of P. halstedii currently identified in the USA. To determine the chromosomal location of this resistance, 186 F 2:3 families derived from a cross of HA 458 with HA 234 were phenotyped for their resistance to race 734 of P. halstedii. The segregation ratio of the population supported that the resistance was controlled by a single dominant gene, Pl 17 . Simple sequence repeat (SSR) and single nucleotide polymorphism (SNP) primers were used to identify molecular markers linked to Pl 17 . Bulked segregant analysis using 849 SSR markers located Pl 17 to linkage group (LG) 4, which is the first DM gene discovered in this linkage group. An F2 population of 186 individuals was screened with polymorphic SSR and SNP primers from LG4. Two flanking markers, SNP SFW04052 and SSR ORS963, delineated Pl 17 in an interval of 3.0 cM. The markers linked to Pl 17 were validated in a BC3 population. A search for the physical location of flanking markers in sunflower genome sequences revealed that the Pl 17 region had a recombination frequency of 0.59 Mb/cM, which was a fourfold higher recombination rate relative to the genomic average. This region can be considered amenable to molecular manipulation for further map-based cloning of Pl 17 .

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References

  • Baack EJ, Whitney KD, Rieseberg LH (2005) Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species. New Phytol 167:623–630

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bachlava E, Radwan OE, Abratti G, Tang S, Gao W, Heesacker AF, Bazzalo ME, Zambelli A, Leon AJ, Knapp SJ (2011) Downy mildew (Pl 8 and Pl 14 ) and rust (R Adv ) resistance genes reside in close proximity to tandemly duplicated clusters of non-TIR-like NBS-LRR-encoding genes on sunflower chromosomes 1 and 13. Theor Appl Genet 122:1211–1221

    Article  PubMed  Google Scholar 

  • Bert PF, Tourvielle 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 103:992–997

    Article  CAS  Google Scholar 

  • Bouzidi MF, Badaoui S, Cambon F, Vear F, De Labrouhe DT, 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 104:592–600

    Article  CAS  PubMed  Google Scholar 

  • Bowers JE, Bachlava E, Brunick RL, Rieseberg LH, Knapp SJ et al (2012) Development of a 10,000 locus genetic map of the sunflower genome based on multiple crosses. Genes Genomes Genet 2:721–729

    CAS  Google Scholar 

  • Brahm L, Röcher T, Friedt W (2000) PCR-based markers facilitating marker assisted selection in sunflower for resistance to downy mildew. Crop Sci 40:676–682

    Article  CAS  Google Scholar 

  • de Romano AB, Romano C, Bulos M, Altieri E, Sala C (2010) A new gene for resistance to downy mildew in sunflower. In: Proceedings of International Symposium “Sunflower breeding on resistance to diseases”, Krasnodar, Russia, June 23–24, 2010

  • Dußle CM, Hahn V, Knapp SJ, Bauer E (2004) Pl Arg from Helianthus argophyllus is unlinked to other known downy mildew resistance genes in sunflower. Theor Appl Genet 109:1083–1086

    Article  PubMed  Google Scholar 

  • Faris JD, Haen KM, Gill BS (2000) Saturation map** of a gene-rich recombination hot spot region in wheat. Genetics 154:823–835

    PubMed Central  CAS  PubMed  Google Scholar 

  • Flor HH (1955) Host-parasite interaction in flax rust-its genetics and other implication. Phytopathology 45:680–685

    Google Scholar 

  • Franchel J, Bouzidi MF, Bronner G, Vear F, Nicolas P, Mouzeyar S (2013) Positional cloning of a candidate gene for resistance to the sunflower downy mildew, Plasmopara halstedii race 300. Theor Appl Genet 126:359–367

    Article  PubMed  Google Scholar 

  • Gedil MA, Slabaugh MB, Berry S, Segers B, Peleman J, Michelmore R, Miller JF, Gulya T, Knapp SJ (2001) Candidate disease resistance genes in sunflower cloned using conserved nucleotide binding site motifs: genetic map** and linkage to downy mildew resistance gene Pl 1 . Genome 44:205–212

    Article  CAS  PubMed  Google Scholar 

  • Gentzbittel L, Vear F, Zhang YX, Berville A (1995) Development of a consensus linkage RFLP map of cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 90:1079–1086

    Article  CAS  PubMed  Google Scholar 

  • Gill KS, Gill BS, Endo TR, Boyko EV (1996) Identification and high-density map** of gene-rich regions in chromosome group 5 of wheat. Genetics 143:1001–1012

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gong L, Gulya TJ, Markell SG, Hulke BS, Qi LL (2013) Genetic map** of rust resistance genes in confection sunflower line HA-R6 and oilseed line RHA 397. Theor Appl Genet 126:2039–2049

    Article  CAS  PubMed  Google Scholar 

  • Gulya TJ (2007) Distribution of Plasmopara halstedii races from sunflower around the world. In: Lebeda A, Spencer-Phillips PTN (eds) Proceedings of 2nd International Downy Mildew Symposium, Palacký University, Olomouc and JOLA, Czech Republic, 2–6 July 2007. Advances in Downy Mildew Research, vol 3, pp 121–134

  • Gulya TJ, Miller JF, Viranyi F, Sackston WE (1991) Proposed internationally standardized methods for race identification of Plasmopara halstedii. Helia 14(15):11–20

    Google Scholar 

  • Gulya TJ, Markell S, McMullen M, Harveson B, Osborne L (2011) New virulent races of downy mildew: distribution, status of DM resistant hybrids, and USDA sources of resistance. In: Proceedings of 33th Sunflower Research Forum, Fargo, 12–13 Jan 2011 http://www.sunflowernsa.com/uploads/resources/575/gulya_virulentracesdownymildew.pdf

  • Horn R, Kusterer B, Lazarescu E, Prufe M, Friedt W (2003) Molecular map** of the Rf1 gene restoring pollen fertility in PET1-based F 1 hybrids in sunflower (Helianthus annuus L.). Theor Appl Genet 106:599–606

    CAS  PubMed  Google Scholar 

  • Huang L, Brooks SA, Fellers JP, Gill BS (2003) Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploidy genome of bread wheat. Genetics 164:655–664

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Ann Rev Phytopathol 39:285–312

    Article  CAS  Google Scholar 

  • Hulke BS, Miller JF, Gulya TJ, Vick BA (2010) Registration of the oilseed sunflower genetic stocks HA 458, HA 459, and HA 460 possessing genes for resistance to downy mildew. J Plant Reg 4:93–97

    Article  Google Scholar 

  • Islam MR, Shepherd KW (1991) Present status of genetics of rust resistance in flax. Euphytica 55:255–267

    Article  Google Scholar 

  • Jones DA, Dickinson MJ, Balint-Kurti PJ, Dixon MS, Jones JDG (1993) Two complex resistance loci revealed in tomato by classical and RFLP map** of the Cf-2, Cf-4, Cf-5, and Cf9 genes for resistance to Cladosporium fulvum. Mol Plant Microbe Interact 6:348–357

    Article  CAS  Google Scholar 

  • Künzel G, Korzun L, Meister A (2000) Cytologically integrated physical RFLP maps for the barley genome based on translocation breakpoints. Genetics 154:397–412

    PubMed Central  PubMed  Google Scholar 

  • Lawson RR, Goulter KC, Henry RJ, Kong GA, Kochman JK (1998) Marker-assisted selection for two rust resistance genes in sunflower. Mol Breed 4:227–234

    Article  CAS  Google Scholar 

  • Liu Z, Gulya TJ, Seiler GJ, Vick BA, Jan CC (2012) Molecular map** of the Pl 16 downy mildew resistance gene from HA-R4 to facilitate marker-assisted selection in sunflower. Theor Appl Genet 125:121–131

    Article  CAS  PubMed  Google Scholar 

  • Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO et al (1998) The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817–1832

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130

    CAS  PubMed  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. Proc Natl Acad Sci USA 88:9828–9832

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Miller JF, Gulya TJ (1987) Inheritance of resistance to race 3 downy mildew in sunflower. Crop Sci 27:210–212

    Article  Google Scholar 

  • Miller JF, Gulya TJ (1988) Registration of 6 downy mildew resistant sunflower germplasm lines. Crop Sci 28:1040–1041

    Article  Google Scholar 

  • Miller JF, Gulya TJ (1991) Inheritance of resistance to race 4 of downy mildew derived from interspecific crosses in sunflower. Crop Sci 31:40–43

    Article  Google Scholar 

  • Molinero-Ruiz ML, Dominguez J, Melero-Vara JM (2000) Races of isolates of Plasmopara halstedii from Spain and studies on their virulence. Plant Dis 86:736–740

    Article  Google Scholar 

  • Molinero-Ruiz ML, Melero-Vara JM, Dominguez J (2003) Inheritance of resistance to two races of sunflower downy mildew (Plasmopara halstedii) in two Helianthus annuus L. lines. Euphytica 131:47–51

    Article  CAS  Google Scholar 

  • Mouzeyar S, Roeckel-Drevet P, Gentzbittel L, Philippon J, de Labrouhe DT, Vear F, Nicolas P (1995) RFLP and RAPD map** of the sunflower Pl 1 locus for resistance to Plasmopara halstedii race 1. Theor Appl Genet 91:733–737

    Article  CAS  PubMed  Google Scholar 

  • Mulpuri S, Liu Z, Feng J, Gulya TJ, Jan CC (2009) Inheritance and molecular map** of a downy mildew resistance gene, Pl 13 in cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 119:795–803

    Article  CAS  PubMed  Google Scholar 

  • Pegadaraju V, Nipper R, Hulke BS, Qi LL, Schultz Q (2013) De novo sequencing of the sunflower genome for SNP discovery using the RAD (Restriction site Associated DNA) approach. BMC Genomics 14:556

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Qi LL, Hulke BS, Vick BA, Gulya TJ (2011) Molecular map** of the rust resistance gene R 4 to a large NBS-LRR cluster on linkage group 13 of sunflower. Theor Appl Genet 123:351–358

    Article  CAS  PubMed  Google Scholar 

  • Qi LL, Seiler GJ, Hulke BS, Vick BA, Gulya TJ (2012) Genetics and map** of the R 11 gene conferring resistance to recently emerged rust races, tightly linked to male fertility restoration, in sunflower (Helianthus annuus L.). Theor Appl Genet 125:921–932

    Article  CAS  PubMed  Google Scholar 

  • Qi LL, Ma GJ, Long YM, Hulke BS, Markell SG (2015) Relocation of a rust resistance gene R 2 and its marker-assisted gene pyramiding in confection sunflower (Helianthus annuus L.). Theor Appl Genet. doi:10.1007/s00122-014-2446-0

  • Radwan O, Bouzidi MF, Vear F, Philippon J, Tourvieille de Labrouhe D, Nicolas P, Mouzeyar S (2003) Identification of non-TIR-NBS-LRR markers linked to the P l5 /P l8 locus for resistance to downy mildew in sunflower. Theor Appl Genet 106:1438–1446

    CAS  PubMed  Google Scholar 

  • Radwan O, Bouzidi MF, Nicolas P, Mouzeyar S (2004) Development of PCR markers for the Pl 5 /Pl 8 locus for resistance to Plasmopara halstedii in sunflower, Helianthus annuus L. from complete CC-NBS-LRR sequences. Theor Appl Genet 109:176–185

    Article  CAS  PubMed  Google Scholar 

  • 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 280:111–125

    Article  CAS  PubMed  Google Scholar 

  • Rahim M, Jan CC, Gulya TJ (2002) Inheritance of resistance to sunflower downy mildew races 1, 2 and 3 in cultivated sunflower. Plant Breed 121:57–60

    Article  Google Scholar 

  • Rashid KY, Desjardins ML, Kaminski DA (2006) Diseases of sunflower in Manitoba and Saskatchewan in 2005. Can Plant Dis Surv 2006, 86:114–115. Available at http://phytopath.ca/download/cpds-archive/vol86/CPDS_vol_86_No_1_%281-130%292006.pdf

  • Richter TE, Ronald PC (2000) The evolution of disease resistance genes. Plant Mol Biol 42:195–204

    Article  CAS  PubMed  Google Scholar 

  • Roeckel-Drevet P, Gagne G, Mouzeyar S, Gentzbittel L, Philippon J, Nicolas P, de Labrouhe DT, Vear F (1996) Colocation of downy mildew (Plasmopara halstedii) resistance genes in sunflower (Helianthus annuus L.). Euphytica 91:225–228

    CAS  Google Scholar 

  • Roeckel-Drevet P, Coehlo V, Tourvieille J, Nicolas P, Tourvieille de Labrouhe D (1997) Lack of genetic variability in French identified races of Plasmopara halstedii, the cause of downy mildew in sunflower Helianthus annuus. Can J Microbiol 43:260–263

    Article  CAS  Google Scholar 

  • Roeckel-Drevet P, Tourvieille J, Gulya TJ, Charmet G, Nicolas P, Tourvieille de Labrouhe D (2003) Molecular variability of sunflower downy mildew, Plasmopara halstedii, from different continents. Can J Microbiol 49:492–502

    Article  CAS  PubMed  Google Scholar 

  • Schmidt R, West J, Love K, Lenehan Z, Lister C et al (1995) Physical map and organization of Arabidopsis thaliana chromosome 4. Science 270:480–483

    Article  CAS  PubMed  Google Scholar 

  • Slabaugh MB, Yu JK, Tang SX, Heesacker A, Hu X, Lu GH, Bidney D, Han F, Knapp SJ (2003) Haploty** and map** a large cluster of downy mildew resistance gene candidates in sunflower using multilocus intron fragment length polymorphisms. Plant Biotechnol J 1:167–185

    Article  CAS  PubMed  Google Scholar 

  • Song WY, Pi LY, Wang GL, Gardner J, Holsten T et al (1997) Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9:1279–1287

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Talukder ZI, Gong L, Hulke BS, Pegadaraju V, Song QJ, Schultz Q, Qi LL (2014) A high-density SNP map of sunflower derived from RAD-sequencing facilitating fine-map** of the rust resistance gene R 12 . PLoS One 9(7):e98628. doi:10.1371/journal.pone.0098628

    Article  PubMed Central  PubMed  Google Scholar 

  • Tan AS, Jan CC, Gulya TJ (1992) Inheritance of resistance to race 4 of sunflower downy mildew in wild sunflower accessions. Crop Sci 32:949–952

    Article  Google Scholar 

  • Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW et al (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tosi L, Beccari G (2007) A new race, 704, of Plasmopara halstedii pathogen of sunflower downy mildew in Italy. Plant Dis 91:463

    Article  Google Scholar 

  • Tosi L, Zazzerini A (2004) First report of downy mildew caused by Plasmopara halstedii races 700 and 703 of sunflower (Helianthus annuus) in Italy. Plant Dis 88:1284

    Article  Google Scholar 

  • Tourvieille de Labrouhe D, Mouzeyar S, Lafon S, Regnaylt Y (1991) Evolution des races de mildiou (Plasmopara halstedii) sur touresol en France. In: Proceedings of 3rd International Conference on Plant Disease, Bordeaux, ANPP, Paris, France, pp 777–784

  • Tourvieille de Labrouhe D, Lafon S, Walse P, Raulic I (2000) A new race of Plasmopara halstedii, pathogen of sunflower downy mildew. Oleagineux 7:404–405

    Google Scholar 

  • Tourvieille de Labrouhe D, Mestries E, Walse P (2005) Quelles perspectives pour la lute genetique vis-à-vis du mildiou du tournesol? Oleagineux 12:85–93

    Google Scholar 

  • Van Ooijen JW (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations, Kyazma BV, Wageningen, Netherlands

  • Vear F, Gentzbittel L, Philippon J, Mouzeyar S, Mestries E, Roeckel-Drevet P, de Labroube DT, Nicolas P (1997) The genetics of resistance to five races of downy mildew (Plasmopara halstedii) in sunflower (Helianthus annuus L.). Theor Appl Genet 95:584–589

    Article  Google Scholar 

  • Vear F, Seriveys H, Petit A, Serre F, Boudon JP, Roche S, Walser P, Tourieille D de Labrouhe (2008) Origins of major genes for downy mildew resistance in sunflower. In: Proceedings of 17th International Sunflower Conference Cordoba, Spain, 2008. Consejería de Agricultura y Pesca, pp 125–130

  • Vincourt P, As-sadi F, Bordat A, Langlade NB, Gouzy J, Pouilly N, Lippi Y, Serre F, Godiard L, Tourvieille de Labrouhe D, Vear F (2012) Consensus map** of major resistance genes and independent QTL for quantitative resistance to sunflower downy mildew. Theor Appl Genet 125:909–920

    Article  PubMed  Google Scholar 

  • Viranyi F (2008) Research progress in sunflower diseases and their management. In: Proceedings of 17th International Sunflower Conference, Fargo, 2008, pp 15–28

  • Wei F, Wing RA, Wise RP (2002) Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell 14:1903–1917

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wieckhorst S, Bachlava E, Dußle CM, Tang S, Gao W, Saski C, Knapp SJ, Schön CC, Hahn V, Bauer E (2010) Fine map** of the sunflower resistance locus Pl ARG introduced from the wild species Helianthus argophyllus. Theor Appl Genet 121:1633–1644

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu JK, Tang S, Slabaugh MB, Heesacker A, Cole G et al (2003) Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Sci 43:367–387

    Article  CAS  Google Scholar 

  • Yue B, Vick BA, Cai X, Hu J (2010) Genetic map** for the Rf1 (fertility restoration) gene in sunflower (Helianthus annuus L.) by SSR and TRAP markers. Plant Breed 129:24–28

    Article  CAS  Google Scholar 

  • Zimmer DE (1974) Physiological specialization between races of Plasmopara halstedii in America and Europe. Phytopathol 64:1465–1467

    Article  Google Scholar 

  • Zimmer DE, Kinman ML (1972) Downy mildew resistance in cultivated sunflower and its inheritance. Crop Sci 12:749–751

    Article  Google Scholar 

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Acknowledgments

The authors would like to thank Dr. Loren Rieseberg for providing access to the Sunflower Genome Data Repository. We also thank Drs. Brent Hulke and Zengcui Zhang for critical review of the manuscript, and Angelia Hogness for technical assistance. This project was supported by the National Sunflower Association Agreement 12-D02 and the USDA-ARS CRIS Project No. 5442-21000-039-00D. Mention of trade names or commercial products in this report is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. The USDA is an equal opportunity provider and employer.

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The authors declare that they have no conflict of interest.

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Correspondence to L. L. Qi.

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Communicated by V. Hahn.

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Qi, L.L., Long, Y.M., Jan, C.C. et al. Pl 17 is a novel gene independent of known downy mildew resistance genes in the cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 128, 757–767 (2015). https://doi.org/10.1007/s00122-015-2470-8

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