Abstract
Downy mildew is a fungal disease of sunflower that can lead to severe yield losses. The damage caused by the pathogen can be controlled by growing resistant sunflower varieties. Gene Pl arg was introgressed into cultivated sunflower from the wild species Helianthus argophyllus and provides resistance against all known downy mildew races. In this study, we used a mapping population from the cross-RHA 419/RHA-N-49. We identified a new co-segregating simple sequence repeat marker ORS675 and confirmed the co-segregation of markers ORS716 and ORS662 with Pl arg gene. The markers were validated on two registered resistant inbred lines RHA 443 and RHA 464, as well as on twenty inbred lines RH 1–20 obtained through methods of classical breeding. Molecular marker ORS716 was assessed for usefulness in selecting resistant progeny in 12 BC populations. Markers were found to be valuable for molecular breeding in diverse genetic backgrounds and enabled transfer of the resistance gene in different sunflower genotypes.
Similar content being viewed by others
References
Albourie JM, Tourvieille J, Tourvieille de Labrouhe D (1998) Resistance to metalaxyl in isolates of the sunflower pathogen Plasmopara halstedii. Eur J Plant Pathol 104:235–242
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
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
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
Bowers JE, Bachlava E, Brunick RL, Rieseberg LH, Knapp SJ, Burke JM (2012) Development of a 10, 000 locus genetic map of the sunflower genome based on multiple crosses. G3 2:721–729
Conaway-Bormans CA, Marchetti MA, Johnson CW, McClung AM, Park WD (2003) Molecular markers linked to the blast resistance gene Pi-z in rice for use in marker-assisted selection. Theor Appl Genet 107:1014–1020
de Romano A, Romano C, Bulos M, Altieri E, Sala C (2010) A new gene for resistance to downy mildew in sunflower. Proceedings of 8th European sunflower biotechnology conference, Antalya, Turkey, pp 141–146
Dimitrijevic A, Imerovski I, Miladinovic D, Tancic S, Dusanic N, Jocic S, Miklic V (2010) Use of SSR markers in identification of sunflower isogenic lines in late generations of backcrossing. Helia 33:191–198
Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321
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
Fesenko IA, Kuklev MY, Karlov GI (2012) Development of a breeder-friendly functional codominant DNA marker for the I 2 locus covering resistance to Fusarium oxysporum f. sp. lycopersici. Mol Breeding 31:495–499
Frisch M, Melchinger AE (2001) Marker-assisted backcrossing for introgression of a recessive gene. Crop Sci 41:1485–1494
Gentzbittel L, Mouzeyar S, Badaoui S, Mestries E, Vear F, Tourvieille De Labrouhe D, Nicolas P (1998) Cloning of molecular markers for disease resistance in sunflower Helianthus annuus L. Theor Appl Genet 96:519–525
Grewal TS, Rossnagel BG, Scoles GJ (2008) Validation of molecular markers for covered smut resistance and marker-assisted introgression of loose and covered smut resistance into hulless barley. Mol Breeding 21:37–48
Gulya TJ (2007) Distribution of Plasmopara halstedii races from sunflower around the world: advances in downy mildew research. Palacky University and JOLA Publishers 3:121–134
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. Proceedings of 33th sunflower research Forum Fargo ND, January 12–13
Gupta SK, Charpe A, Prabhu KV, Haque QMR (2006) Identification and validation of molecular markers linked to the leaf rust resistance gene Lr19 in wheat. Theor Appl Genet 113:1027–1036
Hassan E, Hoeft E, Zenglu L, Tulsieram L (2011) Genetic markers for Orobanche resistance in sunflower. US Patent No. 7,872,170
Heesacker A, Kishore VK, Gao W et al (2008) SSRs and INDELs mined from the sunflower EST database: abundance, polymorphisms, and cross-taxa utility. Theor Appl Genet 117:1021–1029
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
Jocic S, Miladinovic D, Imerovski I, Dimitrijevic A, Cvejic S, Nagl N, Kondic-Spika A (2012) Towards sustainable downy mildew resistance in sunflower. Helia 35:61–72
Kaya Y, Jocic S, Miladinovic D (2012) Molecular breeding. In: Gupta SK (ed) Technological innovations in major world oil crops: breeding, vol 1, 1st edn. Springer, Dordrecht, pp 85–129
Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12:172–175
Liu Z, Gulya TJ, Seiler GJ, Vick BA, Jan C-C (2012) 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
McMullen MD, Kresovich S, Villeda HS et al (2009) Genetic properties of the maize nested association mapping population. Science 325:737–740
Miklas PN (2002) Marker assisted selection for disease resistance in common bean. Annu Rep Bean Improv Coop 45:1–3
Miklic V, Dusanic N, Jocic S (2011) Sunflower seed production. In: Milosevic M, Kobiljski B (eds) Seed production, vol 2. Institute of Field and Vegetable Crops, Novi Sad, pp 196–264 (in Serbian)
Miller JF, Gulya TJ, Seiler GJ (2002) Registration of five fertility restorer sunflower germplasms. Crop Sci 42:989–991
Miller JF, Gulya TJ, Vick BA (2006) Registration of imidazolinone herbicide-resistant maintainer (HA 442) and fertility restorer (RHA 443) oilseed sunflower germplasms. Crop Sci 46:483
Mouzeyar S, Roeckel-Drevet P, Gentzbittel L, Philippon J, Tourvieille de Labrouhe D, Vear F (1995) RFLP and RAPD mapping of the sunflower Pl 1 locus for resistance to Plasmopara halstedii race 1. Theor Appl Genet 91:733–737
Mudge J (1999) Marker-assisted selection for soybean cyst nematode and accompanying agronomic traits. Ph. D. thesis, University of Minnesota
Muller MH, Latreille M, Tollon C (2011) The origin and evolution of a recent agricultural weed: population genetic diversity of weedy populations of sunflower (Helianthus annuus L.) in Spain and France. Evol Appl 4:499–514
Mulpuri S, Liu Z, Feng J, Gulya TJ, Jan C-C (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
Namayanja A, Buruchara R, Mahuku G, Rubaihayo P, Kimani P, Mayanja S, Eyedu H (2006) Inheritance of resistance to angular leaf spot in common bean and validation of the utility of resistance linked markers for marker assisted selection outside the mapping population. Euphytica 151:361–369
Ortiz-Barrientos D, Reiland J, Hey J, Noor MAF (2002) Recombination and the divergence of hybridizing species. Genetica 116:167–178
Pashley CH, Ellis JR, McCauley DE, Burke JM (2006) EST databases as a source for molecular markers: lessons from Helianthus. J Hered 97:381–388
Perez-Vich B, Berry ST (2010) Molecular breeding. In: Hu J, Seiler G, Kole C (eds) Genetics. Science Publishers, Enfield, Genomics and Breeding of Sunflower, pp 221–251
Permingeat HR, Romagnoli MV, Vallejos RH (1998) A simple method for isolating high yield and quality DNA from cotton (Gossypium hirsutum L.) leaves. Plant Mol Biol Rep 16:1–6
Radwan O, Bouzidi MF, Nicolas P, Mouzeyar S (2004) Development of PCR markers for Pl 5 /Pl 8 locus for resistance to Plasmopara halstedii in sunflower, Helianthus annuus L. from complete CC–NBS–LRR sequence. Theor Appl Genet 109:176–185
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 NBSLRR disease resistance proteins in sunflower. Mol Genet Genomics 280:111–125
Rahim M, Jan C-C, Gulya TJ (2002) Inheritance of resistance to sunflower downy mildew races 1, 2 and 3 in cultivated sunflower. Plant Breeding 121:57–60
Rani A, Kumar V, Mourya V, Singh RK, Husain SM (2011) Validation of SSR markers linked to null kunitz trypsin inhibitor allele in Indian soybean [Glycine max (L.) Merr.] population. J Plant Biochem Biot 20:258–261
Rieseberg LH, Baird SJE, Gardner KA (2000) Hybridization, introgression, and linkage evolution. Plant Mol Biol 42:205–224
Roeckel-Drevet P, Gagne G, Mouzeyar S, Gentzbittel L, Philippon J, Nicolas P, Tourvieille de Labrouhe D, Vear F (1996) Colocation of downy mildew (Plasmopara halstedii) resistance genes in sunflower (Helianthus annuus L.). Euphytica 91:225–228
Sakr N (2010) Studies on pathogenicity in Plasmopara halstedii (sunflower downy mildew). Int J Life Sci 4:48–59
Sharp PJ, Johnston S, Brown G, McIntosh RA, Pallotta M, Carter M, Bariana HS, Khatkar S, Laugdah ES, Singh RP, Khairallah M, Potter R, Jones MGK (2001) Validation of molecular markers for wheat breeding. Aust J Agric Res 52:1357–1366
Sheeba NK, Viraktamath BC, Sivaramakrishnan S, Gangashetti MG, Khera P, Sundaram RM (2009) Validation of molecular markers linked to fertility restorer gene (s) for WA-CMS lines of rice. Euphytica 167:217–227
Slabaugh MB, Yu J-K, 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, Yu J-K, Slabaugh B, Shintani K, Knapp J (2002) Simple sequence repeat map of the sunflower genome. Theor Appl Genet 105:1124–1136
Van Ooijen JW (2006) JoinMap_ 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen
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 95:584–589
Vear F, Serre F, Roche S, Walser P, Tourvieille de Labrouhe D (2007) Recent research on downy mildew resistance useful for breeding industrial-use sunflowers. Helia 30:45–54
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
Yu J-K, Tang S, Slabaugh MB, Heesacker A, Cole G, Herring M, Soper J, Han F, Chu W, Webb DM, Thompson L, Edwards KJ, Berry S, Leon AJ, Grondona M, Olungu C, Maes N, Knapp SJ (2003) Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Sci 43:367–387
Acknowledgments
The authors are grateful to Mr. Zvonimir Sakac for technical assistance in preparation of the manuscript. This work was supported by the Ministry of Education, Science and Technological Development, Republic of Serbia, project TR 31025.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Imerovski, I., Dimitrijevic, A., Miladinovic, D. et al. Identification and validation of breeder-friendly DNA markers for Pl arg gene in sunflower. Mol Breeding 34, 779–788 (2014). https://doi.org/10.1007/s11032-014-0074-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11032-014-0074-7