Abstract
Key message
A major stripe rust resistance QTL was mapped to a 0.4 centimorgan (cM) genetic region on the long arm of chromosome 7B, using combined genome-wide linkage mapping and bulk segregant analysis.
Abstract
The German winter wheat cv. Centrum has displayed high levels of adult plant stripe rust resistance (APR) in field environments for many years. Here, we used the combined genome-wide linkage mapping and pool-extreme genotyping to characterize the APR resistance. One hundred and fifty-one F2:7 recombinant inbred lines derived from a cross between susceptible landrace Mingxian 169 and Centrum were evaluated for stripe rust resistance in multiple environments and genotyped by the wheat 35K single nucleotide polymorphism (SNP) array. Three stable quantitative trait loci (QTL) were identified using QTL analysis across five field environments. To saturate the major QTL, the wheat 660K SNP array was also used to genotype bulked extremes. A major QTL named QYrcen.nwafu-7BL from Centrum was mapped in a 0.4 cM genetic interval flanking by AX-94556751 and AX-110366788 across a 2 Mb physical genomic region, explaining 19.39-42.81% of the total phenotypic variation. It is likely a previously uncharacterized QTL based on pedigree analysis, reaction response, genotyping data and map comparison. The SNP markers closely linked with QYrcen.nwafu-7BL were converted to KASP markers and validated in a subset of 120 wheat lines. A 211 F2 breeding population from a cross of an elite cultivar Xinong 979 with Centrum were developed for marker-based selection. Three selected lines with desirable agronomic traits and the positive alleles of both KASP markers showed acceptable resistance which should be used as resistance donors in wheat breeding programs. The other QTL QYrcen.nwafu-1AL and QYrcen.nwafu-4AL with additive effects could enhance the level of resistance conferred by QYrcen.nwafu-7BL.
Similar content being viewed by others
References
Allen AM, Winfield MO, Burridge AJ, Downie RC, Benbow HR, Barker GL, Wilkinson PA, Coghill J, Waterfall C, Davassi A, Scopes G, Pirani A, Webster T, Brew F, Bloor C, Griffiths S, Bentley AR, Alda M, Jack P, Phillips AL, Edwards KJ (2017) Characterization of a wheat breeders’ Array suitable for high-throughput SNP genotyping of global accessions of hexaploid bread wheat (Triticum aestivum). Plant Biotechnol J 15:390–401
Badea A, Eudes F, Graf RJ, Laroche A, Gaudet DA, Sadasivaiah RS (2008) Phenotypic and marker-assisted evaluation of spring and winter wheat germplasm for resistance to fusarium head blight. Euphytica 164:803–819
Bai BB, Liu TG, Liu B, Gao L, Chen WQ (2017) High relative parasitic fitness of G22 derivatives is associated with the epidemic potential of wheat stripe rust in China. Plant Dis 102:483–487
Basnet BR, Ibrahim AMH, Chen X, Singh RP, Mason ER, Bowden RL, Liu S, Hays DB, Devkota RN, Subramanian NK, Rudd JC (2014) Molecular mapping of stripe rust resistance in hard red winter wheat TAM 111 adapted to the U.S. high plains. Crop Sci 54:1361–1373
Bulli P, Zhang J, Chao S, Chen X, Pumphrey M (2016) Genetic architecture of resistance to stripe rust in a global winter wheat germplasm collection. G3 6:2237–2253
Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A, See D, Bai G, Pumphrey M, Tomar L, Wong D, Kong S, Reynolds M, da Silva ML, Bockelman H, Talbert L, Anderson JA, Dreisigacker S, Baenziger S, Carter A, Korzun V, Morrell PL, Dubcovsky J, Morell MK, Sorrells ME, Hayden MJ, Akhunov E (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci U S A 110:8057–8062
Chen XM (2005) Epidemiology and control of stripe rust (Puccinia striiformis f. sp. tritici) on wheat. Can J Plant Pathol 27:314–337
Chen XM (2013) High-temperature adult-plant resistance, key for sustainable control of stripe rust. Am J Plant Sci 04:608–627
Chen XM (2014) Integration of cultivar resistance and fungicide application for control of wheat stripe rust. Can J Plant Pathol 36:311–326
Chen JL, Chu C, Souza EJ, Guttieri MJ, Chen XM, Xu S, Hole D, Zemetra R (2012) Genome-wide identification of QTL conferring high-temperature adult-plant (HTAP) resistance to stripe rust (Puccinia striiformis f. sp. tritici) in wheat. Mol Breed 29:791–800
Cui F, Zhang N, Fan XL, Zhang W, Zhao CH, Yang LJ, Pan RQ, Chen M, Han J, Zhao XQ, Ji J, Tong YP, Zhang HX, Jia JZ, Zhao GY, Li JM (2017) Utilization of a Wheat660K SNP array-derived high-density genetic map for high-resolution mapping of a major QTL for kernel number. Sci Rep 7:3788
Ellis JG, Lagudah ES, Spielmeyer W, Dodds PN (2014) The past, present and future of breeding rust resistant wheat. Front Plant Sci 5:641
Feng J, Wang M, See DR, Chao S, Zheng YL, Chen X (2018) Characterization of novel gene Yr79 and four additional QTL for all-stage and high-temperature adult-plant resistance to stripe rust in spring wheat PI 182103. Phytopathology 108:737–747
Han DJ, Zhang PY, Wang QL, Zeng QD, Wu JH et al (2012) Identification and evaluation of resistance to stripe rust in 1980 wheat landraces and abroad germplasm. Sci Agric Sin 45:5013–5023
Han DJ, Wang QL, Chen XM, Zeng QD, Wu JH et al (2015) Emerging Yr26-virulent races of Puccinia striiformis f. sp. tritici are threatening wheat production in the Sichuan Basin, China. Plant Dis 99:754–760
He ZH, Lan CX, Chen XM, Zou YC, Zhuang QS, Xia XC (2011) Progress and perspective in research of adult-plant resistance to stripe rust and powdery mildew in wheat. Sci Agric Sin 44:2193–2215
Herrera-Foessel SA, Singh RP, Lillemo M, Huerta-Espino J, Bhavani S, Singh S, Lan C, Calvo-Salazar V, Lagudah ES (2014) Lr67/Yr46 confers adult plant resistance to stem rust and powdery mildew in wheat. Theor Appl Genet 127:781–789
Herrera-Foessel SA, Singh RP, Lan CX, Huerta-Espino J, Calvo-Salazar V, Bansal UK, Bariana HS, Lagudah ES (2015) Yr60, a gene conferring moderate resistance to stripe rust in wheat. Plant Dis 4:508–511
Imtiaz M, Ahmad M, Cromey MG, Griffin WB, Hampton JG (2004) Detection of molecular markers linked to the durable adult plant stripe rust resistance gene Yr18 in bread wheat (Triticum aestivum L.). Plant Breed 123:401–404
Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Lan CX, Zhang YL, Herrera-Foessel SA, Basnet BR, Huerta-Espino J, Lagudah ES, Singh RP (2015) Identification and characterization of pleiotropic and co-located resistance loci to leaf rust and stripe rust in bread wheat cultivar Sujata. Theor Appl Genet 128:549–561
Li Y, Niu YC (2007) Identification of molecular markers for wheat stripe rust resistance gene Yr6. Acta Agric Boreali-Sin 22:189–192
Li ZF, Zheng TC, He ZH, Li GQ, Xu SC, Li XP, Yang GY, Singh RP, Xia XC (2006) Molecular tagging of stripe rust resistance gene YrZH84 in Chinese wheat line Zhou 8425B. Theor Appl Genet 112:1098–1103
Lin F, Chen XM (2007) Genetics and molecular mapping of genes for race-specific all-stage resistance and non-race-specific high-temperature adult-plant resistance to stripe rust in spring wheat cultivar Alpowa. Theor Appl Genet 114:1277–1287
Lin F, Xu SC, Zhang LJ, Miao Q, Zhai Q, Li N (2004) SSR marker of wheat stripe rust resistance gene Yr2. J Trit Crops 25:17–19
Line RF, Qayoum A (1992) Virulence, aggressiveness, evolution, and distribution of races of Puccinia striiformis (the cause of stripe rust of wheat) in North America 1968–1987. US Department of Agriculture Technical Bulletin
Maccaferri M, Zhang J, Bulli P, Abate Z, Chao S, Cantu D, Bossolini E, Chen X, Pumphrey M, Dubcovsky J (2015) A genome-wide association study of resistance to stripe rust (f. sp.) in a worldwide collection of hexaploid spring wheat (L.). G3 (Bethesda) 5(3):449–465
McDonald BA, Linde C (2002) The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica 124:163–180
McIntosh RA, Wellings CR, Park RF (1995) Wheat rusts: an atlas of resistance genes. CSIRO Publishing, East Melbourne, pp 20–26
McIntosh RA, Mu JM, Han DJ, Kang ZS (2018) Wheat stripe rust resistance gene Yr24/Yr26: a retrospective review. Crop J 6:321–329
Meng L, Li H, Zhang L, Wang J (2015) QTL IciMapping: Integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop J 3:269–283
Nematollahi G, Mohler V, Wenzel G, Zeller FJ, Hsam SLK (2008) Microsatellite mapping of powdery mildew resistance allele Pm5d from common wheat line IGV1-455. Euphytica 159:307–313
Peterson RF, Campbell AB, Hannah AE (1948) A diagrammatic scale for estimating rust intensity on leaves and stems of cereals. Can J Res Sect C 26:496–500
Ramburan VP, Pretorius ZA, Louw JH, Boyd LA, Smith PH, Boshoff WH, Prins R (2004) A genetic analysis of adult plant resistance to stripe rust in the wheat cultivar Kariega. Theor Appl Genet 108:1426–1433
Randhawa M, Bansal U, Valarik M, Klocova B, Dolezel J, Bariana H (2013) Molecular mapping of stripe rust resistance gene Yr51 in chromosome 4AL of wheat. Theor Appl Genet 127:317–324
Rasheed A, Wen W, Gao FM, Zhai SN, Jin H, Liu J, Guo Q, Zhang Y, Dreisigacker S, Xia XC, He ZH (2016) Development and validation of KASP assays for genes underpinning key economic traits in bread wheat. TAG Theoretical and Applied Genetics Theoretische und angewandte Genetik 129:1843–1860
Ren RS, Wang MN, Chen XM, Zhang ZJ (2012a) Characterization and molecular mapping of Yr52 for high-temperature adult-plant resistance to stripe rust in spring wheat germplasm PI 183527. Theor Appl Genet 125:847–857
Ren Y, He ZH, Li J, Lillemo M, Wu L, Bai B, Lu Q, Zhu H, Zhou G, Du J, Lu Q, Xia XC (2012b) 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 125:1211–1221
Ren Y, Singh RP, Basnet BR, Lan CX, Huerta-Espino J, Lagudah ES, Ponce-Molina LJ (2017) Identification and mapping of adult plant resistance loci to leaf rust and stripe rust in common wheat cultivar Kundan. Plant Dis 101:456–463
Rosewarne GM, Singh RP, Huerta-Espino J, Rebetzke G (2008) Quantitative trait loci for slow-rusting resistance in wheat to leaf rust and stripe rust identified with multi-environment analysis. Theor Appl Genet 116:1027–1034
Semagn K, Babu R, Hearne S, Olsen M (2013) Single nucleotide polymorphism genotyping using Kompetitive Allele Specific PCR (KASP): overview of the technology and its application in crop improvement. Mol Breed 33:1–14
Singh RP, Julio HE, Harindra MW (2005) Genetics and breeding for durable resistance to leaf and stripe rusts in wheat. Turk J Agric 29:121–127
Singh RP, Huerta-Espino J, Bhavani S, Herrera-Foessel SA, Singh D, Singh PK, Velu G, Mason RE, Jin Y, Njau P, Crossa J (2010) Race non-specific resistance to rust diseases in CIMMYT spring wheats. Euphytica 179:175–186
Singh A, Pandey MP, Singh AK, Knox RE, Ammar K, Clarke JM, Clarke FR, Singh RP, Pozniak CJ, Depauw RM, McCallum BD, Cuthbert RD, Randhawa HS, Fetch TG Jr (2013) Identification and mapping of leaf, stem and stripe rust resistance quantitative trait loci and their interactions in durum wheat. Mol Breed 31:405–418
Singh RP, Herrera-Foessel S, Huerta-Espino J, Singh S, Bhavani S, Lan C, Basnet BR (2014) Progress towards genetics and breeding for minor genes based resistance to Ug99 and other rusts in CIMMYT high-yielding spring wheat. J Integr Agric 13:255–261
Song WN, Ko L, Henry RJ (1994) Polymorphisms in the α-amy1 gene of wild and cultivated barley revealed by the polymerase chain reaction. Theor Appl Genet 89:509–513
Sourdille P, Singh S, Cadalen T, Brown-Guedira GL, Gay G, Qi L, Gill BS, Dufour P, Murigneux A, Bernard M (2004) Microsatellite-based deletion bin system for the establishment of genetic-physical map relationships in wheat (Triticum aestivum L.). Funct Integr Genomics 4:12–25
Tang C, Xu Q, Zhao M, Wang X, Kang Z (2018) Understanding the lifestyles and pathogenicity mechanisms of obligate biotrophic fungi in wheat: The emerging genomics era. Crop J 6:60–67
Vazquez MD, Peterson CJ, Riera-Lizarazu O, Chen XM, Heesacker A, Ammar K, Crossa J, Mundt C (2012) Genetic analysis of adult plant, quantitative resistance to stripe rust in wheat cultivar ‘Stephens’ in multi-environment trials. Theor Appl Genet 124:1–11
Vazquez MD, Zemetra R, Peterson CJ, Chen XM, Heesacker A, Mundt CC (2015) Multi-location wheat stripe rust QTL analysis: genetic background and epistatic interactions. Theor Appl Genet 128:1307–1318
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wan AM, Chen XM, He ZH (2007) Wheat stripe rust in China. Aust J Agric Res 58:605–619
Wang JK (2009) Inclusive composite interval mapping of quantitative trait genes. Acta Agron Sin 35:239–245
Wang N, Wang QL, Qiu HC, Zeng QD, Wang XJ, Kang ZS, Han DJ (2010) Characterization and inheritance of resistance to stripe rust in a wheat cultivar centrum. J Trit Crops 32:784–788
Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, International Wheat Genome Sequencing C, Lillemo M, Mather D, Appels R, Dolferus R, Brown-Guedira G, Korol A, Akhunova AR, Feuillet C, Salse J, Morgante M, Pozniak C, Luo MC, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796
Wellings CR (2011) Global status of stripe rust: a review of historical and current threats. Euphytica 179:129–141
Winfield MO, Wilkinson PA, Allen AM, Barker GL, Coghill JA, Burridge A, Hall A, Brenchley RC, D’Amore R, Hall N, Bevan MW, Richmond T, Gerhardt DJ, Jeddeloh JA, Edwards KJ (2012) Targeted re-sequencing of the allohexaploid wheat exome. Plant Biotechnol J 10:733–742
Wu J, Wang Q, Xu L, Chen X, Li B, Mu J, Zeng Q, Huang L, Han D, Kang Z (2018) Combining single nucleotide polymorphism genotyping array with bulked segregant analysis to map a gene controlling adult plant resistance to stripe rust in wheat line 03031-1-5 H62. Phytopathology 108:103–113
Xu H, Zhang J, Zhang P, Qie Y, Niu Y, Li H, Ma P, Xu Y, An D (2014) Development and validation of molecular markers closely linked to the wheat stripe rust resistance gene YrC591 for marker-assisted selection. Euphytica 198:317–323
Yao Q, Song YX, Zhou RH, Fu TH, Jia JZ (2009) Quantitative trait loci for adult-plant resistance against yellow rust in a wheat-derived recombinant inbred line population. Sci Agric Sin 42:4234–4241
Zeng SM, Luo Y (2006) Long-distance spread and interregional epidemics of wheat stripe rust in China. Plant Dis 90:980–988
Zeng QD, Shen C, Yuan FP, Wang QL, Wu JH et al (2015) The resistance evaluation of the Yr genes to the main prevalent pathotypes of Puccinia striiformis f. sp. tritici in China. Acta Phytopathol Sin 45:641–650
Zhou XL, Wang MN, Chen XM, Lu Y, Kang ZS, Jing JX (2014) Identification of Yr59 conferring high-temperature adult-plant resistance to stripe rust in wheat germplasm PI 178759. Theor Appl Genet 127:935–945
Acknowledgements
The authors are grateful to Prof. X. M. Chen, US Department of Agriculture, for critical review of this manuscript. This study was financially supported by the National Science Foundation for Young Scientists in China (Grant 31701421), the National Key Research and Development Program of China (Grant No. 2016YFE0108600), and the earmarked fund for Modern Agro-industry Technology Research System (No. CARS-3-1-11).
Author information
Authors and Affiliations
Contributions
JMM conducted the experiments, analyzed the data and wrote the manuscript. SH, QLW and JHW assisted in analyzing the data. QLW, QDZ and DJH identified the resistant parental line, made the cross and participated in field experiments. SH, MFD, SJL and SZY participated in field experiments and contributed to genotyping. DJ Han and ZS Kang conceived and directed the project and revised the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical standards
I declare on behalf of my co-authors that the work described is original, previously unpublished research and not under consideration for publication elsewhere. The experiments in this study comply with the current laws of China.
Additional information
Communicated by Evans Lagudah.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mu, J., Huang, S., Liu, S. et al. Genetic architecture of wheat stripe rust resistance revealed by combining QTL mapping using SNP-based genetic maps and bulked segregant analysis. Theor Appl Genet 132, 443–455 (2019). https://doi.org/10.1007/s00122-018-3231-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-018-3231-2