Abstract
The major genes controlling sunflower downy mildew resistance have been designated as Pl genes. Ten of the more than 20 Pl genes reported have been mapped. In this study, we report the molecular mapping of gene Pl 16 in a sunflower downy mildew differential line, HA-R4. It was mapped on the lower end of linkage group (LG) 1 of the sunflower reference map, with 12 markers covering a distance of 78.9 cM. One dominant simple sequence repeat (SSR) marker, ORS1008, co-segregated with Pl 16 , and another co-dominant expressed sequence tag (EST)-SSR marker, HT636, was located 0.3 cM proximal to the Pl 16 gene. The HT636 marker was also closely linked to the Pl 13 gene in another sunflower differential line, HA-R5. Thus the Pl 16 and Pl 13 genes were mapped to a similar position on LG 1 that is different from the previously reported Pl 14 gene. When the co-segregating and tightly linked markers for the Pl 16 gene were applied to other germplasms or hybrids, a unique band pattern for the ORS1008 marker was detected in HA-R4 and HA-R5 and their F1 hybrids. This is the first report to provide two tightly linked markers for both the Pl 16 and Pl 13 genes, which will facilitate marker-assisted selection in sunflower resistance breeding, and provide a basis for the cloning of these genes.
References
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
Bakker E, Borm T, Prins P, van der Vossen E, Uenk G, Arens M, de Boer J, van Eck H, Muskens M, Vossen J, van der Linden G, van Ham R, Klein-Lankhorst R, Visser R, Smant G, Bakker J, Goverse A (2011) A genome-wide genetic map of NB-LRR disease resistance loci in potato. Theor Appl Genet 123:493–508
Bert PF, De Labrouhe DT, 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
Bhattacharyya MK, Narayanan NN, Gao H, Santra DK, Salimath SS, Kasuga T, Liu Y, Espinosa B, Ellison L, Marek L, Shoemaker R, Gijzen M, Buzzell RI (2005) Identification of a large cluster of coiled coil-nucleotide binding site-leucine rich repeat-type genes from the Rps1 region containing Phytophthora resistance genes in soybean. Theor Appl Genet 111:75–86
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
Bouzidi MF, Franchel J, Tao Q, Stormo K, Mraz A, Nicolas P, Mouzeyar S (2006) A sunflower BAC library suitable for PCR screening and physical mapping of targeted genomic regions. Theor Appl Genet 113:81–89
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
Carrillo RJ, Dragan AI, Privalov PL (2010) Stability and DNA-binding ability of the bZIP dimers formed by the ATF-2 and c-Jun transcription factors. J Mol Biol 396:431–440
Danilova TV, Kuklev MYu, Andreeva GN, Shevelukha VS, Karlov GI (2007) Cloning and analysis of the resistance gene fragments from silverleaf sunflower Helianthus agrophyllus. Russ J Genet 43:381–386
de Romano AB, Romano C, Bulos M, Altieri E, Sala C (2010) A new gene for resistance to downy mildew in sunflower. In: Proc Int Symposium “Sunflower breeding on resistance to diseases”, Krasnodar, Russia, June 23–24
Delmotte F, Giresse X, Richard-Cervera S, M’Baya J, Vear F, Tourvieille J, Walser P, de Labrouhe DT (2008) Single nucleotide polymorphism reveal multiple introductions into France of Plasmopara halstedii, the plant pathogen causing sunflower downy mildew. Infect Genet Evol 8:534–540
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
Feng J, Jan CC (2008) Introgression and molecular tagging of Rf 4 , a new male fertility restoration gene from wild sunflower Helianthus maximiliani L. Theor Appl Genet 117:241–249
Feng JH, Vick BA, Lee MK, Zhang HB, Jan CC (2006) Construction of BAC and BIBAC libraries from sunflower and identification of linkage group-specific clones by overgo hybridization. Theor Appl Genet 113:23–32
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 mapping and linkage to downy mildew resistance gene Pl1. Genome 44:205–212
Gentzbittel L, Mouzeyar F, Badaoui S, Mestries E, Vear F, de Labrouhe DT, Nicolas P (1998) Cloning of molecular markers for disease resistance in sunflower, Helianthus annuus L. Theor Appl Genet 96:519–525
Gu L, Guo R (2007) Genome-wide detection and analysis of alternative splicing for nucleotide binding site-leucine-rich repeats sequences in rice. J Genet Genomics 34:247–257
Gulya TJ (1985) Registration of five disease-resistant sunflower germplasms. Crop Sci 25:719–720
Gulya TJ (2007) Distribution of Plasmopara halstedii races from sunflower around the world. In: Proc II Int Downy Mildew Symposium. Palcky University, Olomouc and JOLA, Czech Republic, July 2–6, pp 135–142
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 132:303–311
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: Proc 33th Sunflower Research Forum. Fargo ND, January 12–13 http://www.sunflowernsa.com/uploads/resources/575/gulya_virulentracesdownymildew.pdf
Heesacker A, Kishore VK, Gao W, Tang S, Kolkman JM, Gingle A, Matvienko M, Kozik A, Michelmore RM, Lai Z, Rieseberg LH, Knapp SJ (2008) SSRs and INDELs mined from the sunflower EST database: abundance, polymorphisms, and cross-taxa utility. Theor Appl Genet 117:1021–1029
Hewezi T, Mouzeyar S, Thion L, Rickauer M, Alibert G, Nicolas P, Kallerhoff J (2006) Antisense expression of a NBS-LRR sequence in sunflower (Helianthus annuus L.) and tobacco (Nicotiana tabacum L.): evidence for a dual role in plant development and fungal resistance. Transgenic Res 15:165–180
Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527
Kanazin V, Marek LF, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11746–11750
Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
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 111:1532–1544
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 for experimental and natural populations. Genomics 1:174–181
Liu RH, Meng JL (2003) MapDraw: a Microsoft Excel macro for drawing genetic linkage maps based on given genetic linkage data. Hereditas 25:317–321
Liu Z, Mulpuri S, Feng J, Vick BA, Jan CC (2011) Molecular mapping of the Rf 3 fertility restoration gene to facilitate its utilization in breeding confection sunflower. Mol Breed. doi: 10.1007/s11032-011-9563-0
McHale LK, Truco MJ, Kozik A, Wroblewski T, Ochoa OE, Lahre KA, Knapp SJ, Michelmore RW (2009) The genomic architecture of disease resistance in lettuce. Theor Appl Genet 118:565–580
Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO, Zhang Z, Michelmore RW (1998a) The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817–1832
Meyers BC, Shen KA, Rohani P, Gaut BS, Michelmore RW (1998b) Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 10:1833–1846
Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834
Michelmore RW (2003) The impact zone: genomics and breeding for durable disease resistance. Curr Opin Plant Biol 6:397–404
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
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
Miller JF, Rodriguez RH, Gulya TJ (1988) Evaluation of genetic materials for inheritance of resistance to Race 4 rust in sunflower. In: Proc 12th Int Sunflower Conf, Novi Sad, Yugoslavia, July 25–29. International Sunflower Association, Paris, pp 361–365
Miller JF, Gulya TJ, Seiler GJ (2002) Registration of five fertility restorer sunflower germplasms. Crop Sci 42:989–991
Molestina, CJ (1988) Manejo del cultivo, control de plagas y enfermedades del girasol. Dialogo XXII. IICA/BID/PROCISUR. Montivideo, Uruguay
Molinero-Ruiz ML, Melero-Vara JM, Dominguez J (2002) Inheritance of resistance to race 330 of Plasmopara halstedii in three sunflower lines. Plant Breed 121:61–65
Molinero-Ruiz ML, Melero-Vara JM, Domiınguez J (2003) Inheritance of resistance to two races of sunflower downy mildew (Plasmopara halstedii) in two Helianthus annuus L. lines. Euphytica 131:47–51
Mouzeyar S, Roeckel-Drevet P, Gentzbittel L, Philippon J, de Labrouhe DT, Vear F, Nicolas P (1995) RFLP and RAPD mapping of the sunflower Pl 1 locus for resistance to Plasmopara halstedii race 1. Theor Appl Genet 91:733–737
Mulpuri S, Liu Z, Feng J, Gulya TJ, Jan CC (2009) Inheritance and molecular mapping of a downy mildew resistance gene, Pl 13 in cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 119:795–803
O’Shea EK, Rutkowski R, Kim PS (1989) Evidence that the leucine zipper is a coiled-coil. Science 243:538–542
Özdemir N, Horn R, Friedt W (2004) Construction and characterization of a BAC library for sunflower (Helianthus annuus L.). Euphytica 138:177–183
Panković D, Radovanović N, Jocić S, Satovic Z, Skorić D (2007) Development of co-dominant amplified polymorphic sequence markers for resistance of sunflower to downy mildew race 730. Plant Breed 126:440–444
Plocik A, Layden J, Kesseli R (2004) Comparative analysis of NBS domain sequences of NBS-LRR disease resistance genes from sunflower, lettuce, and chicory. Mol Phylogenet Evol 31:153–163
Qi LL, Hulke BS, Vick BA, Gulya TJ (2011) Molecular mapping 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
Radwan O, Bouzidi MF, Vear F, Philippon J, de Labrouhe DT, Nicolas P, Mouzeyar S (2003) Identification of non-TIR-NBS-LRR markers linked to the Pl 5 /Pl 8 locus for resistance to downy mildew in sunflower. Theor Appl Genet 106:1438–1446
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
Radwan O, Mouzeyar S, Nicolas P, Bouzidi MF (2005) Induction of a sunflower CC-NBS-LRR resistance gene analogue during incompatible interaction with Plasmopara halstedii. J Exp Bot 56:567–575
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
Radwan O, Bouzidi MF, Mouzeyar S (2011) Molecular characterization of two types of resistance in sunflower to Plasmopara halstedii, the causal agent of downy mildew. Phytopathology 101:970–979
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
Ratnaparkhe MB, Wang X, Li J, Compton RO, Rainville LK, Lemke C, Kim C, Tang H, Paterson AH (2011) Comparative analysis of peanut NBS-LRR gene clusters suggests evolutionary innovation among duplicated domains and erosion of gene microsynteny. New Phytol. doi: 10.1111/j.1469-8137.2011.03800.x
Roath WW, Miller JF, Gulya T (1986) Registration of sunflower parental lines HA 821 and HA 822. Crop Sci 26:217
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
Slabaugh MB, Yu JK, Tang S, Heesacker A, Hu X, Lu G, Bidney D, Han F, Knapp SJ (2003) Haplotyping and mapping a large cluster of downy mildew resistance gene candidates in sunflower using multilocus intron fragment length polymorphisms. Plant Biotechnol J 1:167–185
Tang S, Kishore VK, Knapp SJ (2003) PCR-multiplexes for a genome-wide framework of simple sequence repeat marker loci in cultivated sunflower. Theor Appl Genet 107:6–19
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
Wieckhorst S, Bachlava E, Dußle CM, Tang S, Gao W, Saski C, Knapp SJ, Schön CC, Hahn V, Bauer E (2010) Fine mapping of the sunflower resistance locus Pl ARG introduced from the wild species Helianthus argophyllus. Theor Appl Genet 121:1633–1644
Yang S, Feng Z, Zhang X, Jiang K, Jin X, Hang Y, Chen JQ, Tian D (2006) Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol Biol 62:181–193
Yang S, Tang F, Gao M, Krishnan HB, Zhu H (2010) R gene-controlled host specificity in the legume–rhizobia symbiosis. Proc Natl Acad Sci USA 107:18735–18740
Yu JK, Tang S, Slabaugh MB, Heesacker A, Cole G, Herring MJ, Soper J, Han F, Chu WC, Webb DM, Thompson L, Edwards KJ, Berry S, Leon A, Olungu C, Maes N, Knapp SJ (2003) Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Sci 43:367–387
Zhang X, Feng Y, Cheng H, Tian D, Yang S, Chen JQ (2011) Relative evolutionary rates of NBS-encoding genes revealed by soybean segmental duplication. Mol Genet Genomics 285:79–90
Zhou T, Wang Y, Chen JQ, Araki H, Jing ZQ, Jiang K, Shen JD, Tian D (2004) Genome-wide identification of NBS genes in rice reveals significant expansion of divergent non-TIR NBS genes. Mol Genet Gen 406:402–415
Acknowledgments
The authors thank Lisa A. Brown, Marjorie A. Olson, Megan K. Ramsett, and Leonard W. Cook for technical assistance. Dr. Sujatha Mulpuri (Directorate of Oilseeds Research, Rajendranagar, Hyderabad, India) provided the phenotyping data for the F2 population derived from HA-R5 × HA 821 to P. halstedii races 300, 700, 730, and 770. We also thank Larry G. Campbell and Steven S. Xu for critical review of the manuscript.
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122_2012_1820_MOESM1_ESM.ppt
Supplemental Fig. 1 Representative genotyping of the F2 individuals derived from the cross of HA-R4 × HA 821 with both parents (P1–HA-R4, P2–HA 821) and F1s using the ORS1008 marker on a denaturing polyacrylamide gel (a) and the HT636 marker on a nondenaturing polyacrylamide gel (b), respectively. A, H, and B represent the homozygous resistant, heterozygous resistant, and homozygous susceptible F2 individuals to downy mildew, respectively. The arrows indicate the markers. M indicates a 100 bp plus ladder Gelpilot (Qiagen). A ~510 bp band is also noticed among different phenotypes (PPT 376 kb)
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Liu, Z., Gulya, T.J., Seiler, G.J. et al. Molecular mapping of the Pl 16 downy mildew resistance gene from HA-R4 to facilitate marker-assisted selection in sunflower. Theor Appl Genet 125, 121–131 (2012). https://doi.org/10.1007/s00122-012-1820-z
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DOI: https://doi.org/10.1007/s00122-012-1820-z