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Chromosomal location of the crown rust resistance gene Pc98 in cultivated oat (Avena sativa L.)

Abstract

Key message

SNP loci linked to the crown rust resistance gene Pc98 were identified by linkage analysis and KASP assays were developed for marker-assisted selection in breeding programs.

Abstract

Crown rust is among the most damaging diseases of oat and is caused by Puccinia coronata var. avenae f. sp. avenae (Urban and Marková) (Pca). Host resistance is the preferred method to prevent crown rust epidemics. Pc98 is a race-specific, seedling crown rust resistance gene obtained from the wild oat Avena sterilis accession CAV 1979 that is effective at all growth stages of oat. Virulence to Pc98 has been very low in the Pca populations that have been tested. The objectives of this study were to develop SNP markers linked to Pc98 for use in marker-assisted selection and to locate Pc98 on the oat consensus map. The Pc98 gene was mapped using F2:3 populations developed from the crosses Pc98/Bingo and Pc98/Kasztan, where Pc98 is a single-gene line carrying Pc98. Both populations were evaluated in seedling inoculation experiments. Pc98 was mapped relative to Kompetitive Allele-Specific PCR SNP markers in both populations, placing Pc98 on the Mrg20 linkage group of the consensus map. Pc98 was bracketed by two SNP markers GMI_ES22_c3052_382_kom399 and GMI_ES14_lrc18344_662_kom398 in the Pc98/Bingo mapping population with genetic distances of 0.9 cM and 0.3 cM, respectively. Pc98 co-segregated with four SNP markers in the Pc98/Kasztan population, and the closest flanking markers were GMI_DS_LB_6017_kom367 and avgbs2_153634.1.59_kom410 with genetic distances of 0.7 cM and 0.3 cM, respectively. Two SNP loci defined a haplotype that accurately predicted Pc98 status in a diverse group of oat germplasm, which will be valuable for marker-assisted selection of Pc98 in breeding of new oat cultivars.

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Fig. 1

Availability of data and materials

Data supporting the current study can be obtained by contacting the corresponding author (curt.mccartney@canada.ca).

Abbreviations

CORE:

Collaborative Oat Research Enterprise

GBS:

Genotyping-by-sequencing

IT:

Infection type

KASP:

Kompetitive Allele-Specific PCR

LOD:

Logarithm of odds

MAS:

Marker-assisted selection

Pca :

Puccinia coronata var. avenae f. sp. avenae

RFLP:

Restriction fragment length polymorphism

SNP:

Single nucleotide polymorphism

References

  1. Admassu-Yimer B, Bonman JM, Esvelt Klos K (2018) Mapping of crown rust resistance gene Pc53 in oat (Avena sativa). PLoS ONE 13:e0209105. https://doi.org/10.1371/journal.pone.0209105

  2. Aung T, Chong J, Leggett M (1996) The transfer of crown rust resistance gene Pc94 from a wild diploid to cultivated hexaploid oat. In: Proceedings of the 9th European and Mediterranean cereal rusts and powdery mildews conference, pp 2–6

  3. Bekele WA, Wight CP, Chao S, Howarth CJ, Tinker NA (2018) Haplotype-based genotyping-by-sequencing in oat genome research. Plant Biotechnol J 16:1452–1463. https://doi.org/10.1111/pbi.12888

  4. Cabral AL, Gnanesh BN, Fetch JM, McCartney C, Fetch T, Park RF, Menzies JG, McCallum B, Nanaiah GK, Goyal A (2014) Oat fungal diseases and the application of molecular marker technology for their control. In: Future challenges in crop protection against fungal pathogens. Springer, pp 343–358. https://doi.org/10.1007/978-1-4939-1188-2_12

  5. Carson ML (2008) Virulence frequencies in oat crown rust in the United States from 2001 through 2005. Plant Dis 92:379–384. https://doi.org/10.1094/PDIS-92-3-0379

  6. Carson ML (2011) Virulence in oat crown rust (Puccinia coronata f. sp. avenae) in the United States from 2006 through 2009. Plant Dis 95:1528–1534. https://doi.org/10.1094/PDIS-09-10-0639

  7. Chaffin AS, Huang Y-F, Smith S, Bekele WA, Babiker E, Gnanesh BN, Foresman BJ, Blanchard SG, Jay JJ, Reid RW (2016) A consensus map in cultivated hexaploid oat reveals conserved grass synteny with substantial subgenome rearrangement. Plant Genome-US. https://doi.org/10.3835/plantgenome2015.10.0102

  8. Chen G, Chong J, Prashar S, Procunier J (2007) Discovery and genotyping of high-throughput SNP markers for crown rust resistance gene Pc94 in cultivated oat. Plant Breed 126:379–384. https://doi.org/10.1111/j.1439-0523.2007.01364.x

  9. Chong J, Chen G (2006) In search of effective crown rust resistance sources in Avena sterilis. In: American Oat Workers Conference, Fargo, USA, 23–26 July 2006. https://wheat.pw.usda.gov/Oat_Newsletters/AOWC/

  10. Chong J, Leonard K, Salmeron J (2000) A North American system of nomenclature for Puccinia coronata f. sp. avenae. Plant Dis 84:580–585. https://doi.org/10.1094/PDIS.2000.84.5.580

  11. Chong J, Gruenke J, Dueck R, Mayert W, Fetch JM, McCartney C (2011) Virulence of Puccinia coronata f. sp. avenae in the Eastern Prairie Region of Canada during 2007–2009. Can J Plant Pathol 33:77–87. https://doi.org/10.1080/07060661.2010.546957

  12. Doehlert DC, McMullen MS, Hammond JJ (2001) Genotypic and environmental effects on grain yield and quality of oat grown in North Dakota. Crop Sci 41:1066–1072. https://doi.org/10.2135/cropsci2001.4141066x

  13. Endo R, Boewe G (1958) Losses caused by crown rust of oats in 1956 and 1957. Plant Dis Rep 42:1126–1128

  14. Esvelt Klos K, Yimer BA, Babiker EM, Beattie AD, Bonman JM, Carson ML, Chong J, Harrison SA, Ibrahim AM, Kolb FL (2017) Genome-wide association mapping of crown rust resistance in oat elite germplasm. Plant Genome-US. https://doi.org/10.3835/plantgenome2016.10.0107

  15. FAOSTAT database (2019) Food and Agriculture Organization of the United Nations. http://www.fao.org/faostat/en/#data/QC. Accessed 15 Aug 2019

  16. Fleischmann G, McKenzie R (1968) Inheritance of crown rust resistance in Avena sterilis. Crop Sci 8:710–713. https://doi.org/10.2135/cropsci1968.0011183X000800060020x

  17. Fleischmann G, McKenzie RIH, Shipton WA (1971) Inheritance of crown rust resistance genes in Avena sterilis collections from Israel, Portugal, and Tunisia. Can J Genet Cytol 13:251–255. https://doi.org/10.1139/g71-042

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

  19. Forsberg RA, Shands HL (1989) Oat breeding. Plant Breed Rev 6:167–207. https://doi.org/10.1002/9781118061039.ch5

  20. Frey KJ, Browning JA (1971) Breeding crop plants for disease resistance. In: Mutation breeding for disease resistance

  21. Gnanesh BN, Fetch JM, Menzies JG, Beattie AD, Eckstein PE, McCartney CA (2013) Chromosome location and allele-specific PCR markers for marker-assisted selection of the oat crown rust resistance gene Pc91. Mol Breed 32:679–686. https://doi.org/10.1007/s11032-013-9900-6

  22. Gnanesh BN, Fetch JM, Zegeye T, McCartney CA, Fetch T (2014) Oat. In: Alien gene transfer in crop plants, vol 2. Springer, pp 51–73. https://doi.org/10.1007/978-1-4614-9572-7_3

  23. Gnanesh BN, McCartney CA, Eckstein PE, Fetch JWM, Menzies JG, Beattie AD (2015) Genetic analysis and molecular mapping of a seedling crown rust resistance gene in oat. Theor Appl Genet 128:247–258. https://doi.org/10.1007/s00122-014-2425-5

  24. Hoffman DL, Chong J, Jackson EW, Obert DE (2006) Characterization and mapping of a crown rust resistance gene complex (Pc58) in TAM O-301. Crop Sci 46:2630–2635. https://doi.org/10.2135/cropsci2006.01.0014

  25. Holland JB, Munkvold GP (2001) Genetic relationships of crown rust resistance, grain yield, test weight, and seed weight in oat. Crop Sci 41:1041–1050. https://doi.org/10.2135/cropsci2001.4141041x

  26. Huang Y-F, Poland JA, Wight CP, Jackson EW, Tinker NA (2014) Using genotyping-by-sequencing (GBS) for genomic discovery in cultivated oat. PLoS ONE 9:e102448. https://doi.org/10.1371/journal.pone.0102448

  27. Humphreys DG, Mather DE (1996) Heritability of β-glucan, groat percentage, and crown rust resistance in two oat crosses. Euphytica 91:359–364. https://doi.org/10.1007/BF00033098

  28. Kebede AZ, Friesen-Enns JR, Gnanesh BN, Menzies JG, Fetch JWM, Chong J, Beattie AD, Paczos-Grzęda E, McCartnedsy CA (2018) Mapping oat crown rust resistance gene Pc45 confirms association with PcKM. G3-Genes Genom Genet 9:505–511. https://doi.org/10.1534/g3.118.200757

  29. Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugenic 12:172–175. https://doi.org/10.1111/j.1469-1809.1943.tb02321.x

  30. Lin Y, Gnanesh BN, Chong J, Chen G, Beattie AD, Fetch JWM, Kutcher HR, Eckstein PE, Menzies JG, Jackson EW (2014) A major quantitative trait locus conferring adult plant partial resistance to crown rust in oat. BMC Plant Biol 14:250. https://doi.org/10.1186/s12870-014-0250-2

  31. Lorieux M (2012) MapDisto: fast and efficient computation of genetic linkage maps. Mol Breed 30:1231–1235. https://doi.org/10.1007/s11032-012-9706-y

  32. Manisterski J, Wahl I (1995) Studies on oat crown rust in Israel. Petria 5:50–54

  33. Martens JW, Dyck PL (1989) Genetics of resistance to rust in cereals from a Canadian perspective. Can J Plant Pathol 11:78–85. https://doi.org/10.1080/07060668909501152

  34. Martínez-Villaluenga C, Peñas E (2017) Health benefits of oat: current evidence and molecular mechanisms. Curr Opin Food Sci 14:26–31. https://doi.org/10.1016/j.cofs.2017.01.004

  35. McCallum BD, Fetch T, Chong J (2007) Cereal rust control in Canada. Aust J Agr Res 58:639–647. https://doi.org/10.1071/ar06145

  36. Menzies JG, Xue A, Gruenke J, Dueck R, Deceuninck S, Chen Y (2019) Virulence of Puccinia coronata var avenae f. sp. avenae (oat crown rust) in Canada during 2010 to 2015. Can J Plant Pathol 41:379–391. https://doi.org/10.1080/07060661.2019.1577300

  37. Murphy HC (1935) Physiologic specialization in Puccinia coronata avenae. USDA Tech Bull 433:1–48

  38. Nazareno ES, Li F, Smith M, Park RF, Kianian SF, Figueroa M (2018) Puccinia coronata f. sp. avenae: a threat to global oat production. Mol Plant Pathol 19:1047–1060. https://doi.org/10.1111/mpp.12608

  39. Paczos-Grzeda E (2004) Pedigree, RAPD and simplified AFLP-based assessment of genetic relationships among Avena sativa L. cultivars. Euphytica 138:13–22. https://doi.org/10.1023/B:EUPH.0000047055.99322.7a

  40. Paczos-Grzeda E, Sowa S (2019) Virulence structure and diversity of Puccinia coronata f. sp. avenae P. Syd. & Syd. in Poland during 2013 to 2015. Plant Dis. https://doi.org/10.1094/pdis-10-18-1820-re

  41. Paczos-Grzęda EM, Bednarek PT, Koroluk A (2014) Zastosowanie markerów silicoDArT do oceny polimorfizmu międzyodmianowego Avena sativa L. Folia Pomeranae Universitatis Technologiae Stetinensis 310:75–84

  42. Rooney WL, Rines HW, Phillips RL (1994) Identification of RFLP markers linked to crown rust resistance genes Pc 91 and Pc 92 in oat. Crop Sci 34:940–944. https://doi.org/10.2135/cropsci1994.0011183X003400040019x

  43. Rothman PG (1984) Registration of four stem rust and crown rust resistant oat germplasm lines. Crop Sci 24:1217–1218. https://doi.org/10.2135/cropsci1984.0011183X002400060064x

  44. Simons MD, Martens JW, McKenzie RIH, Nishiyama I, Sadanaga K, Sebesta J, Thomas H (1978) Oats: a standardized system of nomenclature for genes and chromosomes and catalog of genes governing characters vol 509, 509 edn. United States Department of Agriculture

  45. Smulders MJM, van de Wiel CCM, van den Broeck HC, van der Meer IM, Israel-Hoevelaken TPM, Timmer RD, van Dinter BJ, Braun S, Gilissen LJWJ (2018) Oats in healthy gluten-free and regular diets: a perspective. Food Res Int 110:3–10. https://doi.org/10.1016/j.foodres.2017.11.031

  46. Tinker NA, Chao S, Lazo GR, Oliver RE, Huang Y-F, Poland JA, Jellen EN, Maughan PJ, Kilian A, Jackson EW (2014) A SNP genotyping array for hexaploid oat. Plant Genome-US. https://doi.org/10.3835/plantgenome2014.03.0010

  47. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. https://doi.org/10.1093/jhered/93.1.77

  48. Welch RW (2012) The oat crop: production and utilization. Springer, Berlin. https://doi.org/10.1007/978-94-011-0015-1

  49. Wight CP, O’Donoughue LS, Chong J, Tinker NA, Molnar SJ (2005) Discovery, localization, and sequence characterization of molecular markers for the crown rust resistance genes Pc38, Pc39, and Pc48 in cultivated oat (Avena sativa L.). Mol Breed 14:349–361. https://doi.org/10.1007/s11032-005-0148-7

  50. Winkler LR, Bonman JM, Chao S, Admassu Yimer B, Bockelman H, Esvelt Klos K (2016) Population structure and genotype-phenotype associations in a collection of oat landraces and historic cultivars. Front Plant Sci 7:1077. https://doi.org/10.3389/fpls.2016.01077

  51. Wong LSL, McKenzie RIH, Harder DE, Martens JW (1983) The inheritance of resistance to Puccinia coronata and of floret characters in Avena sterilis. Can J Genet Cytol 25:329–335. https://doi.org/10.1139/g83-052

  52. Zhao J, Wang M, Chen X, Kang Z (2016) Role of alternate hosts in epidemiology and pathogen variation of cereal rusts. Annu Rev Phytopathol 54:207–228. https://doi.org/10.1146/annurev-phyto-080615-095851

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Acknowledgements

The authors thank Leslie Bezte, Suzanne Enns, Alain Ngantcha, and Sharon Deceuninck for technical support. The study was funded by the Prairie Oat Growers Association - Prairie Oat Breeding Consortium Agricultural Innovation Project with matching funding from Agriculture and Agri-Food Canada (AAFC) Growing Forward II.

Author information

JZ, AZK, JGM, EPG, JC, JWMF, ADB, YYP, and CAM planned and organized the study. JZ, AZK, and CAM designed DNA markers and collected marker data. JZ and JGM collected crown rust data. EPG developed mapping populations. JZ and CAM conducted linkage analyses. All authors contributed to and approved the final manuscript.

Correspondence to Curt A. McCartney.

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Zhao, J., Kebede, A.Z., Menzies, J.G. et al. Chromosomal location of the crown rust resistance gene Pc98 in cultivated oat (Avena sativa L.). Theor Appl Genet (2020) doi:10.1007/s00122-020-03535-x

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