Abstract
The challenge posed by rapidly changing wheat rust pathogens, both in virulence and in environmental adaptation, calls for the development and application of new techniques to accelerate the process of breeding for durable resistance. To expand the resistance gene pool available for germplasm improvement, a panel of 159 landraces plus old cultivars was evaluated for seedling and adult plant resistance (APR) to over 35 Australian pathotypes of Puccinia triticina, Puccinia graminis f. sp. tritici, and Puccinia striiformis f. sp. tritici. Known seedling resistance (SR) genes for leaf rust (Lr2a, Lr3a, Lr13, Lr23, Lr16, and Lr20), stem rust (Sr12, Sr13, Sr23, Sr30, and Sr36), and stripe rust (Yr3, Yr4, Yr5, Yr9, Yr10, Yr17, and Yr27) were postulated. The APR genes identified via field assessments and marker analyses included the pleiotropic genes (Lr34/Yr18/Sr57, Lr46/Yr29/Sr58, Lr67/Yr46/Sr55, and Sr2/Lr27/Yr30), Lr68, Lr74, and uncharacterized APR. A genome-wide association analysis using linear mixed models detected 79 single nucleotide polymorphism (SNP) markers significantly associated with rust resistance, which were mapped on chromosomes 1A, 1B, 1D, 2A, 2B, 3A, 3B, 3D, 4A, 5A, 5B, 6A, 6B, 6D, 7A, 7B and 7D. SNPs associated with multiple rust resistances probably indicate the presence of new pleiotropic or closely linked genes. SNPs were mapped on chromosome positions (1AL, 1DS, 2AL, 4AS, 5BS, 6DL, and 7AL) that have not been known to carry APR genes. This study revealed the presence of a range of possibly unidentified effective seedling and APRs among the landraces, which might represent new sources of rust resistance for the ongoing effort to develop improved wheat cultivars.
Similar content being viewed by others
References
Babiker E, Gordon T, Chao S, Newcomb M, Rouse M, Jin Y, Wanyera R, Acevedo M, Brown-Guedira G, Williamson S (2015) Mapping resistance to the Ug99 race group of the stem rust pathogen in a spring wheat landrace. Theor Appl Genet 128(4):605–612
Babiker E, Gordon T, Bonman J, Chao S, Rouse M, Brown-Guedira G, Williamson S, Pretorius Z (2016a) Rapid identification of resistance loci effective against Puccinia graminis f. sp. tritici race TTKSK in 33 spring wheat landraces. Plant Dis 100(2):331–336
Babiker EM, Gordon T, Chao S, Rouse MN, Acevedo M, Brown-Guedira G, Wanyera R, Bonman JM (2016b) Molecular mapping of stem rust resistance loci effective against the Ug99 race group of the stem rust pathogen and validation of a SNP marker linked to stem rust resistance gene Sr28. Phytopathology 107(2):208–215
Bajgain P, Rouse M, Bulli P, Bhavani S, Gordon T, Wanyera R, Njau P, Legesse W, Anderson J, Pumphrey M (2015) Association mapping of North American spring wheat breeding germplasm reveals loci conferring resistance to Ug99 and other African stem rust races. BMC Plant Biol 15(1):249
Bansal U, Bossolini E, Miah H, Keller B, Park R, Bariana H (2008) Genetic mapping of seedling and adult plant stem rust resistance in two European winter wheat cultivars. Euphytica 164(3):821–828
Bansal UK, Arief V, Miah H, DeLacy IH & Bariana HS (2010) Association mapping of rust resistance in pre-green revolution wheat accessions. In Borlaug Global Rust Initiative 2010 Technical Workshops, 45
Bansal UK, Arief VN, DeLacy IH, Bariana HS (2013) Exploring wheat landraces for rust resistance using a single marker scan. Euphytica 194(2):219–233
Bansal M, Kaur S, Dhaliwal H, Bains N, Bariana H, Chhuneja P, Bansal U (2016) Mapping of Aegilops umbellulata derived leaf rust and stripe loci in wheat. Plant Pathol 66(1):38–44
Bariana H, Forrest K, Qureshi N, Miah H, Hayden M, Bansal U (2016) Adult plant stripe rust resistance gene Yr71. Mol Breed 36(7):1–10
Basnet BR, Singh S, Lopez-Vera EE, Huerta-Espino J, Bhavani S, Jin Y, Rouse MN, Singh RP (2015) Molecular mapping and validation of SrND643: a new wheat gene for resistance to the stem rust pathogen Ug99 race group. Phytopathology 105(4):470–476
Bonman JM, Babiker EM, Cuesta-Marcos A, Esvelt-Klos K, Brown-Guedira G, Chao S, See D, Chen J, Akhunov E, Zhang J (2015) Genetic diversity among wheat accessions from the USDA National Small Grains Collection. Crop Sci 55(3):1243–1253
Butler D, Cullis B, Gilmour A, Gogel B (2007) ASReml-R estimates variance components under a general linear mixed model by residual maximum likelihood (REML). Analysis of mixed models for S language environments. DPI and F Publications, Queensland, p 131
Calvo-Salazar V, Singh RP, Huerta-Espino J, Cruz-Izquierdo S, Lobato-Ortiz R, Sandoval-Islas S, Vargas-Hernandez M, Germán SE, Silva P, Basnet BR (2015) Genetic analysis of resistance to leaf rust and yellow rust in spring wheat cultivar Kenya Kongoni. Plant Dis 99(8):1153–1160
Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci 110(20):8057–8062
Crossa J, Burgueno J, Dreisigacker S, Vargas M, Herrera-Foessel SA, Lillemo M, Singh RP, Trethowan R, Warburton M, Franco J (2007) Association analysis of historical bread wheat germplasm using additive genetic covariance of relatives and population structure. Genetics 177(3):1889–1913
Daetwyler HD, Bansal UK, Bariana HS, Hayden MJ, Hayes BJ (2014) Genomic prediction for rust resistance in diverse wheat landraces. Theor Appl Genet 127(8):1795–1803
Dracatos PM, Zhang P, Park RF, McIntosh RA, Wellings CR (2016) Complementary resistance genes in wheat selection ‘Avocet R’confer resistance to stripe rust. Theor Appl Genet 129(1):65–76
Forrest K, Pujol V, Bulli P, Pumphrey M, Wellings C, Herrera-Foessel S, Huerta-Espino J, Singh R, Lagudah E, Hayden M (2014) Development of a SNP marker assay for the Lr67 gene of wheat using a genotyping by sequencing approach. Mol Breed 34(4):2109–2118
Gao L, Turner MK, Chao S, Kolmer J, Anderson JA (2016) Genome wide association study of seedling and adult plant leaf rust resistance in elite spring wheat breeding lines. PLoS One 11(2):e0148671
Haile JK, Hammer K, Badebo A, Singh RP, Röder MS (2013) Haplotype analysis of molecular markers linked to stem rust resistance genes in Ethiopian improved durum wheat varieties and tetraploid wheat landraces. Genet Resour Crop Evol 60(3):853–864
Herrera-Foessel SA, Singh RP, Huerta-Espino J, Rosewarne GM, Periyannan SK, Viccars L, Calvo-Salazar V, Lan C, Lagudah ES (2012) Lr68: a new gene conferring slow rusting resistance to leaf rust in wheat. Theor Appl Genet 124(8):1475–1486
Hiebert CW, Kolmer JA, McCartney CA, Briggs J, Fetch T, Bariana H, Choulet F, Rouse MN, Spielmeyer W (2016) Major gene for field stem rust resistance co-locates with resistance gene Sr12 in ‘Thatcher’ wheat. PLoS One 11(6):e0157029
Kaur J, Urmil KB, Khanna R, Saini RG, Bariana H (2009) Molecular mapping of stem rust resistance in HD2009/WL711 recombinant inbred line population. Int J Plant Breed 3:28–33
Kertho A, Mamidi S, Bonman JM, McClean PE, Acevedo M (2015) Genome-wide association mapping for resistance to leaf and stripe rust in winter-habit hexaploid wheat landraces. PLoS One 10(6):e0129580
Klarquist EF, Chen XM, Carter AH (2016) Novel QTL for stripe rust resistance on chromosomes 4A and 6B in soft white winter wheat cultivars. Agronomy 6(1):4
Kolmer J, Garvin D, Jin Y (2011) Expression of a Thatcher wheat adult plant stem rust resistance QTL on chromosome arm 2BL is enhanced by Lr34. Crop Sci 51(2):526–533
Lagudah E, McFadden H, Singh R, Huerta-Espino J, Bariana H, Spielmeyer W (2006) Molecular genetic characterization of the Lr34/Yr18 slow rusting resistance gene region in wheat. Theor Appl Genet 114(1):21–30
Li Z, Lan C, He Z, Singh RP, Rosewarne GM, Chen X, Xia X (2014) Overview and application of QTL for adult plant resistance to leaf rust and powdery mildew in wheat. Crop Sci 54(5):1907–1925
Ma D, Zhou X, Hou L, Bai Y, Li Q, Wang H, Tang M, Jing J (2013) Genetic analysis and molecular mapping of a stripe rust resistance gene derived from Psathynrostachys huashanica Keng in wheat line H9014-121-5-5-9. Mol Breed 32(2):365–372
Ma D, Peng F, Fang Z, Chao K, Jing J, Zhang C (2015) Genetic and molecular mapping of stripe rust resistance genes in wheat cultivar Zhongliang 12. J Phytopathol 163(2):98–104
Mago R, Tabe L, McIntosh R, Pretorius Z, Kota R, Paux E, Wicker T, Breen J, Lagudah E, Ellis J (2011) A multiple resistance locus on chromosome arm 3BS in wheat confers resistance to stem rust (Sr2), leaf rust (Lr27) and powdery mildew. Theor Appl Genet 123(4):615–623
McIntosh R (1975) Cytogenetical studies in wheat VIII. Telocentric mapping and linkage studies involving Sr22 and other genes in chromosome 7AL. Aust J Biol Sci 28(6):531–538
McIntosh RA, Wellings CR, Park RF (1995) Wheat rusts: an atlas of resistance genes. CSIRO Publishing, Melbourne
McVey D, Roelfs A (1975) Postulation of genes for stem rust resistance in the entries of the Fourth International Winter Wheat Performance Nursery. Crop Sci 15(3):335–337
Milus E, Line R (1986) Gene action for inheritance of durable, high-temperature, adult-plant resistance to stripe rust in wheat. Phytopathology 76(4):435–411
Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21(8):2194–2202
Newcomb M, Acevedo M, Bockelman HE, Brown-Guedira G, Goates BJ, Jackson EW, Jin Y, Njau P, Rouse MN, Singh D, Wanyera R, Bonman JM (2013) Field resistance to the Ug99 race group of the stem rust pathogen in spring wheat landraces. Plant Dis 97:882–890
Nirmala J, Chao S, Olivera P, Babiker EM, Abeyo B, Tadesse Z, Imtiaz M, Talbert L, Blake NK, Akhunov E (2016) Markers linked to wheat stem rust resistance gene Sr11 effective to Puccinia graminis f. sp. tritici race TKTTF. Phytopathology 106(11):1352–1358
Njau P, Bhavani S, Huerta-Espino J, Keller B, Singh R (2013) Identification of QTL associated with durable adult plant resistance to stem rust race Ug99 in wheat cultivar ‘Pavon 76’. Euphytica 190(1):33–44
Olivera PD, Kilian A, Wenzl P, Steffenson B (2013) Development of a genetic linkage map for sharon goatgrass (Aegilops sharonensis) and mapping of a leaf rust resistance gene. Genome 56(7):367–376
Olivera P, Newcomb M, Szabo LJ, Rouse M, Johnson J, Gale S, Luster DG, Hodson D, Cox JA, Burgin L (2015) Phenotypic and genotypic characterization of race TKTTF of Puccinia graminis f. sp. tritici that caused a wheat stem rust epidemic in Southern Ethiopia in 2013–14. Phytopathology 105(7):917–928
Park RF (2015) Long term surveys of pathogen populations underpin sustained control of the rust diseases of wheat in Australia. J Proc R Soc NSW 148:15
Park R (2016) Wheat: biotrophic pathogen resistance. In: Wrigley C, Corke H, Seetharaman K, Faubion J (eds) Encyclopedia of food grains, 2nd edn. Academic Press, Oxford, pp 264–272
Park R, McIntosh R (1994) Adult plant resistances to Puccinia recondita f. sp. tritici in wheat. N Z J Crop Hortic Sci 22(2):151–158
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software to teaching—an update. Bioinformatics 28:2537–2539
Pearson TA, Manolio TA (2008) How to interpret a genome-wide association study. JAMA 299(11):1335–1344
Periyannan SK, Qamar ZU, Bansal UK, Bariana HS (2014) Development and validation of molecular markers linked with stem rust resistance gene Sr13 in durum wheat. Crop Pasture Sci 65(1):74–79
Peterson RF, Campbell A, Hannah A (1948) A diagrammatic scale for estimating rust intensity on leaves and stems of cereals. Can J Res 26(5):496–500
Prins R, Dreisigacker S, Pretorius Z, van Schalkwyk H, Wessels E, Smit C, Bender C, Singh D, Boyd LA (2016) Stem rust resistance in a geographically diverse collection of spring wheat lines collected from across Africa. Front Plant Sci:7
Rahmatov M, Rouse MN, Nirmala J, Danilova T, Friebe B, Steffenson BJ, Johansson E (2016) A new 2DS·2RL Robertsonian translocation transfers stem rust resistance gene Sr59 into wheat. Theor Appl Genet 129(7):1383–1392
Ren Y, He Z, Li J, Lillemo M, Wu L, Bai B, Lu Q, Zhu H, Zhou G, Du J (2012) QTL mapping of adult-plant resistance to stripe rust in a population derived from common wheat cultivars Naxos and Shanghai 3/Catbird. Theor Appl Genet 125(6):1211–1221
Rosewarne G, Singh R, Huerta-Espino J, William H, Bouchet S, Cloutier S, McFadden H, Lagudah E (2006) Leaf tip necrosis, molecular markers and β1-proteasome subunits associated with the slow rusting resistance genes Lr46/Yr29. Theor Appl Genet 112(3):500–508
Rouse MN, Nava IC, Chao S, Anderson JA, Jin Y (2012) Identification of markers linked to the race Ug99 effective stem rust resistance gene Sr28 in wheat (Triticum aestivum L.) Theor Appl Genet 125(5):877–885
Rouse MN, Nirmala J, Jin Y, Chao S, Fetch TG Jr, Pretorius ZA, Hiebert CW (2014a) Characterization of Sr9h, a wheat stem rust resistance allele effective to Ug99. Theor Appl Genet 127(8):1681–1688
Rouse MN, Talbert LE, Singh D, Sherman JD (2014b) Complementary epistasis involving Sr12 explains adult plant resistance to stem rust in Thatcher wheat (Triticum aestivum L.) Theor Appl Genet 127(7):1549–1559
Silva P, Calvo-Salazar V, Condón F, Quincke M, Pritsch C, Gutiérrez L, Castro A, Herrera-Foessel S, von Zitzewitz J, Germán S (2015) Effects and interactions of genes Lr34, Lr68 and Sr2 on wheat leaf rust adult plant resistance in Uruguay. Euphytica 204(3):599–608
Singh R, Huerta-Espino J, Bhavani S, Herrera-Foessel S, Singh D, Singh P, Velu G, Mason R, Jin Y, Njau P (2011) Race non-specific resistance to rust diseases in CIMMYT spring wheats. Euphytica 179(1):175–186
Singh RP, Singh PK, Rutkoski J, Hodson DP, He X, Jørgenssen LN, Hovmøller MS, Huerta-Espino J (2016) Disease impact on wheat yield potential and prospects of genetic control. Annu Rev Phytopathol 54:13.1–13.20
Somo M, Pirseyedi SM, Cai X, Sharma Poudel R, Chao S, Marais F (2016) Mapping of Lr56 translocation recombinants in wheat. Plant Breed 135:413–419
Sørensen CK, Hovmøller MS, Leconte M, Dedryver F, de Vallavieille-Pope C (2014) New races of Puccinia striiformis found in Europe reveal race-specificity of long-term effective adult plant resistance in wheat. Phytopathology 104(10):1042–1051
Stakman EC, Stewart D, Loegering WQ (1962) Identification of physiologic races of Puccinia graminis var. tritici. Book 64
Steel RG, Torrie JH, Dickey DA (1997) Principles and procedures of statistics. A biometric approach. McGraw Hill Book Company Inc, New York, p 655
Sthapit J, Newcomb M, Bonman JM, Chen X, See DR (2014) Genetic diversity for stripe rust resistance in wheat landraces and identification of accessions with resistance to stem rust and stripe rust. Crop Sci 54(5):2131–2139
Stubbs R, Prescott J, Dubin H (1986) Cereal disease methodology manual. CIMMYT 46
Temesgen BG (2015) Identification, genetic studies and molecular characterisation of resistance to rust pathogens in wheat. PhD Thesis, The University of Sydney
Thach T, Ali S, de Vallavieille-Pope C, Justesen AF, Hovmøller MS (2016) Worldwide population structure of the wheat rust fungus Puccinia striiformis in the past. Fungal Genet Biol 87:1–8
Turner MK, Kolmer JA, Pumphrey MO, Bulli P, Chao S, Anderson JA (2017) Association mapping of leaf rust resistance loci in a spring wheat core collection. Theor Appl Genet 130(3):1–17
VanRaden P (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91(11):4414–4423
Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L (2014) Characterization of polyploid wheat genomic diversity using a high-density 90 000 single nucleotide polymorphism array. Plant Biotechnol J 12(6):787–796
Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38(2):203–208
Yu LX, Lorenz A, Rutkoski J, Singh RP, Bhavani S, Huerta-Espino J, Sorrells ME (2011) Association mapping and gene–gene interaction for stem rust resistance in CIMMYT spring wheat germplasm. Theor Appl Genet 123(8):1257–1268
Yu LX, Barbier H, Rouse MN, Singh S, Singh RP, Bhavani S, Huerta-Espino J, Sorrells ME (2014) A consensus map for Ug99 stem rust resistance loci in wheat. Theor Appl Genet 127(7):1561–1581
Zwer P, Park R, McIntosh R (1992) Wheat stem rust in Australia dash 1969-1985. Crop Pasture Sci 43(3):399–431
Acknowledgements
The authors greatly appreciate the research material and technical support provided by the following institutions and individuals. The Plant Breeding Institute (PBI) of the University of Sydney provided the facilities, equipment, and areas for the research. The USDA-National Small Grains Collection provided seeds and genotypic data of the wheat landraces. Dr. Urmil Bansal, Ms. Kate Vincent, and Ms. Naeela Qureshi provided the APR-linked molecular markers and helped in the analyses. The contribution of Prof. Colin Wellings in the stripe rust data interpretation is greatly appreciated. Mr. M. Williams, Mr. J. Roake, Mr. K. Kandel, and Ms. M. Pietilainen supported in establishment and management of greenhouse and field experiments.
Author information
Authors and Affiliations
Contributions
PK, DS, and RP designed the research studies, characterized seedling and adult plant resistance existing in the wheat landraces, and mapped SNP markers significantly associated with resistance. MN, EB, and MB provided germplasm and carried out wheat landrace genotyping. PK, PT, and EB carried out genome wide association analyses. PK and DS with help from all other coauthors wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Funding
This study was jointly funded by Bill & Melinda Gates Foundation, USA, and in collaboration with the University of Sydney Australia, World Bank, and Government of Uganda through the National Agricultural Research Organization (NARO) Uganda under the Agricultural Technology and Agribusiness Advisory Services (ATAAS) Project.
Rights and permissions
About this article
Cite this article
Kankwatsa, P., Singh, D., Thomson, P.C. et al. Characterization and genome-wide association mapping of resistance to leaf rust, stem rust and stripe rust in a geographically diverse collection of spring wheat landraces. Mol Breeding 37, 113 (2017). https://doi.org/10.1007/s11032-017-0707-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-017-0707-8