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Identification of a suppressor for the wheat stripe rust resistance gene Yr81 in Chinese wheat landrace Dahongpao

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Abstract

Key message

Combined with BSE-Seq analysis and multiple genetic populations, three genes involved in stripe rust resistance were identified in Chinese wheat landrace Dahongpao, including a novel suppressor on 2BS.

Abstract

Dahongpao (DHP), a landrace of hexaploid wheat in China, exhibits a high degree of stripe rust resistance in the field for many years. In this study, bulked segregant analysis coupled with exome capture sequencing (BSE-Seq) was used to identify genes encoding stripe rust resistance in multiple genetic populations from the cross between DHP and a susceptible hexaploid Australian cultivar, Avocet S (AvS). The most effective QTL in DHP was Yr18, explaining up to 53.08% of phenotypic variance in the F2:3 families. To identify additional genes, secondary mapping populations SP1 and SP2 were produced by crossing AvS with two resistant lines derived from F2:3 families lacking Yr18. An all-stage resistance gene, Yr.DHP-6AS, was identified via BSE-Seq analysis of SP1. Combined the recombinant plants from both SP1 and SP2, Yr.DHP-6AS was located between KP6A_1.66 and KP6A_8.18, corresponding to the same region as Yr81. In addition, secondary mapping populations SP3 and SP4 were developed by selfing a segregating line from F2:3 families lacking Yr18. A novel suppressor gene on chromosome 2BS was identified from DHP for effectively suppressing the resistance of Yr.DHP-6AS in the SP3 and SP4. As a result, the wheat lines carrying both Yr18 and Yr.DHP-6AS show higher level of stripe rust resistance than DHP, providing an effective and simple combination for developing new wheat cultivars with ASR and APR genes. Further, the newly developed KASP markers, KP6A_1.99 and KP6A_5.22, will facilitate the application of Yr.DHP-6AS in wheat breeding via marker-assisted selection.

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Availability of data and material

The datasets supporting the conclusions of this study are included in this published article and its supplementary information files. Sequence data have been submitted to National Genomics Data Center (NGDS) under Bioproject no. PRJCA011980. All the materials, including the resistant Chinese wheat landrace "Dahongpao" (DHP), used in this study are deposited at Triticeae Research Institute, Sichuan Agricultural University.

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References

  • Athiyannan N, Abrouk M, Boshoff WHP, Cauet S, Rodde N, Kudrna D, Mohammed N, Bettgenhaeuser J, Botha KS, Derman SS, Wing RA, Prins R, Krattinger S (2022a) Long-read genome sequencing of bread wheat facilitates disease resistance gene cloning. Nat Genet 54:227–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Athiyannan N, Zhang P, McIntosh R, Chakraborty S, Hewitt T, Bhatt D, Forrest K, Upadhyaya N, Steuernagel B, Arora S, Huerta J, Hayden M, Wulff BBH, Ayliffe M, Hickey LT, Laugdah E, Periyannan S (2022b) Haplotype variants of the stripe rust resistance gene Yr28 in Aegilops tauschii. Theor Appl Genet 135:4327–4336

    Article  CAS  PubMed  Google Scholar 

  • Bansal UK, Hayden MJ, Keller B, Wellings CR, Bariana HS (2009) Relationship between wheat rust resistance genes Yr1 and Sr48 and a microsatellite marker. Plant Pathol 58:1039–1043

    Article  CAS  Google Scholar 

  • Cao J, Xu Z, Fan X, Zhou Q, Ji G, Wang F, Feng B, Wang T (2020) Genetic mapping and utilization analysis of stripe rust resistance genes in a Tibetan wheat (Triticum aestivum L.) landrace Qubaichun. Genet Resour Crop Evol 67:1765–1775

    Article  CAS  Google Scholar 

  • Chen XM (2014) Integration of cultivar resistance and fungicide application for control of wheat stripe rust. Can J Plant Pathol 36:311–326

    Article  CAS  Google Scholar 

  • Chen XM (2020) Pathogens which threaten food security: Puccinia striiformis, the wheat stripe rust pathogen. Food Secur 12:239–251

    Article  Google Scholar 

  • Chen XM, Kang ZS (2017) Stripe rust. Springer Netherlands, Dordrecht, p 520

    Book  Google Scholar 

  • Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:884–890

    Article  Google Scholar 

  • Dong CH, Zhang LC, Chen ZX, Xia C, Gu YQ, Wang JR, Li DP, Xie ZC, Zhang Q, Zhang XY, Gui LX, Liu X, Kong XY (2020) Combining a new exome capture panel with an effective varBScore algorithm accelerates BSA-based gene cloning in wheat. Front Plant Sci 11:1249

    Article  PubMed  PubMed Central  Google Scholar 

  • Fang T, Lei L, Li G, Powers C, Hunger RM, Carver BF, Yang LL (2020) Development and deployment of KASP markers for multiple alleles of Lr34 in wheat. Theor Appl Genet 113:2183–2195

    Article  Google Scholar 

  • Feng J, Sun JL, Shah SJA, Wang FT, Yao Q, Guo QY, Lin RM, Xu SC (2022) Identification of a stripe rust resistance gene YrSF in Chinese wheat (Triticum aestivum L.) landrace Sifangmai. Plant Breed 141(4):549–557

    Article  CAS  Google Scholar 

  • Fu DL, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen XM, Sela H, Fahima T, Dubcovsky J (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 3:1357–1360

    Article  Google Scholar 

  • Gessese M, Bariana H, Wong D, Hayden M, Bansal U (2019) Molecular mapping of stripe rust resistance gene Yr81 in a common wheat landrace Aus27430. Plant Dis 103:1166–1171

    Article  CAS  PubMed  Google Scholar 

  • Hiebert CW, Moscou MJ, Hewitt T, Steuernagel B, Hernández-Pinzón I, Green P, Pujol V, Zhang P, Rouse MN, Jin Y, Mclntosh RA, Upadhyaya N, Zhang JP, Bhavani S, Vrána J, Karafiátová M, Huang L, Fetch T, Doležel J, Wulff BBH, Lagudah E, Spielmeyer W (2020) Stem rust resistance in wheat is suppressed by a subunit of the mediator complex. Nat Commun 11:1123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurni S, Brunner S, Stirnweis D, Herren G, Peditto D, McIntosh RA, Keller B (2014) The powdery mildew resistance gene Pm8 derived from rye is suppressed by its wheat ortholog Pm3. Plant J 79:904–913

    Article  CAS  PubMed  Google Scholar 

  • Jiang YF, Duan LY, Guan FN, Yao FJ, Long L, Wang YQ, Zhao XY, Li H, Li W, Xu Q, Jiang QT, Wang JR, Wei YM, Ma J, Kang HY, Qi PF, Deng M, Zheng YL, Chen GY (2022) Exome sequencing from bulked segregant analysis identifies an all stage stripe rust resistance gene on 1AL in Chinese wheat landrace ‘Xiaohemai.’ Plant Dis 106:1209–1215

    Article  CAS  PubMed  Google Scholar 

  • Kankwatsa P, Singh D, Thomson PC, Babiker EM, Bonman JM, Newcomb M, Park RF (2017) 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 Breed 37:113

    Article  Google Scholar 

  • Klymiuk V, Yaniv E, Huang L, Raats D, Fatiukha A, Chen S, Feng L, Frenkel Z, Krugman T, Lidzbarsky G, Chang W, Jääskeläinen MJ, Schudoma C, Paulin L, Laine P, Bariana H, Sela H, Saleem K, Sørensen CK, Hovmøller MS, Distelfeld A, Chalhoub B, Dubcovsky J, Korol AB, Schulman AH, Fahima T (2018) Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family. Nat Commun 9:3735

    Article  PubMed  PubMed Central  Google Scholar 

  • Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363

    Article  CAS  PubMed  Google Scholar 

  • Lan CX, Liang SS, Zhou XC, Zhou G, Lu QL, Xia XC, He ZH (2010) Identification of genomic regions controlling adult-plant stripe rust resistance in Chinese landrace Pingyuan 50 through bulked segregant analysis. Phytopathology 100:313–318

    Article  PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li ZQ, Zeng SM (2020) Wheat rusts in China. China Agricultural Press, China

    Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Li P, Li G, Zhang YW, Zuo JF, Liu JY, Zhang YM (2022) A combinatorial strategy to identify various types of QTLs for quantitative traits using extreme phenotype individuals in an F2 population. Plant Commun 3(3):100319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Department of Agriculture Technical Bulletin U.S. No. 1788. http://naldc.nal.usda.gov/download/CAT92983836/PDF

  • Liu L, Wang MN, Zhang ZW, See DR, Chen XM (2020) Identification of stripe rust resistance loci in U.S. spring eheat cultivars and breeding lines using genome-wide association mapping and Yr gene markers. Plant Dis 104:2181–2192

    Article  CAS  PubMed  Google Scholar 

  • Long L, Yao FJ, Guan FN, Cheng YK, Duan LY, Zhao XY, Li H, Pu ZE, Li W, Jiang QT, Wei YM, Ma J, Kang HY, Dai SF, Qi PF, Xu Q, Deng M, Zheng YL, Jiang YF, Chen GY (2021) A stable QTL on chromosome 5BL combined with Yr18 conferring high-level adult-plant resistance to stripe rust in Chinese wheat landrace Anyuehong. Phytopathology 111:1594–1601

    Article  CAS  PubMed  Google Scholar 

  • Lu HF, Lin T, Klein J, Wang SH, Qi JJ, Zhou Q, Sun JJ, Zhang ZH, Weng YQ, Huang SW (2014) QTL-seq identifies an early flowering QTL located near Flowering Locus T in cucumber. Theor Appl Genet 127:1491–1499

    Article  PubMed  Google Scholar 

  • Ma DF, Li Q, Tang MS, Chao KX, Li JC, Wang BT, Jing JX (2015) Mapping of gene conferring adult plant resistance to stripe rust in Chinese wheat landrace Baidatou. Mol Breed 35:157–165

    Article  Google Scholar 

  • Marchal C, Zhang J, Zhang P, Fenwick P, Steuernagel B, Adamski NM, Boyd L, McIntosh R, Wulff BBH, Berry S, Lagudah E, Uauy C (2018) BED-domain-containing immune receptors confer diverse resistance spectra to yellow rust. Nat Plants 4:662–668

    Article  CAS  PubMed  Google Scholar 

  • McCormick RF, Truong SK, Mullet JE (2015) RIG: Recalibration and interrelation of genomic sequence data with the GATK. G3 (bethesda) 5:655–665

    Article  PubMed  Google Scholar 

  • McIntosh RA, Dubcovsky J, Rogers WJ, Xia XC, Raupp WJ (2020) Catalogue of gene symbols for wheat: 2020 supplement. https://wheat.pw.usda.gov/GG3/wgc

  • McIntosh R, Mu JM, Han DJ, Kang ZS (2018) Wheat stripe rust resistance gene Yr24/Yr26: a retrospective review. Crop J 6:321–329

    Article  Google Scholar 

  • Meng L, Li HH, Zhang LY, Wang JK (2015) QTL IciMapping: Integrated software for genetic linkage map construction and quantitative trait locus mapping in bi-parental populations. Crop J 3:269–283

    Article  Google Scholar 

  • Moore JW, Herrera-Foessel S, Lan C, Schnippenkoetter W, Aylife M, Huerta-Espino J, Lillemo M, Viccars L, Milne R, Periyannan S, Kong XY, Spielmeyer W, Talbot M, Bariana H, Patrick JW, Dodds P, Singh R, Lagudah E (2015) A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat Genet 47:1494–1498

    Article  CAS  PubMed  Google Scholar 

  • Narasimhan V, Danecek P, Scally A, Xue Y, Tyler-Smith C, Durbin R (2016) BCFtools/RoH: a hidden Markov model approach for detecting autozygosity from next-generation sequencing data. Bioinformatics 32:1749–1751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pang YL, Liu CX, Lin M, Ni F, Li WH, Cai J, Zhang ZL, Zhu HQ, Liu JX, Wu JJ, Bai GH, Liu SB (2022) Mapping QTL for adult-plant resistance to stripe rust in a Chinese wheat landrace. Int J Mol Sci 23(17):9662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramirez-Gonzalez RH, Uauy C, Caccamo M (2015) PolyMarker: a fast polyploid primer design pipeline. Bioinformatics 31:2038–2039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3:430–439

    Article  PubMed  Google Scholar 

  • Stewart CN, Via LE (1993) A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. Biotechniques 14:748–751

    CAS  PubMed  Google Scholar 

  • Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S, Innan H, Cano LM, Kamoun S, Terauchi R (2013) QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74:174–183

    Article  CAS  PubMed  Google Scholar 

  • Tene M, Adhikari E, Cobo N, Jordan KW, Matny O, Blanco IAD, Roter J, Ezrati S, Govta L, Manisterski J, Yehuda PB, Chen XM, Steffenson B, Akhunov E, Sela H (2022) GWAS for stripe rust resistance in wild emmer wheat (Triticum dicoccoides) population: obstacles and solutions. Crop Sci 2(1):42–61

    Google Scholar 

  • Van Ooijen JW (2006) JoinMap® 4.0, Software for the calculation of genetic linkage maps in experimental populations Kyazma BV, Wageningen, The Netherlands.

  • Wan AM, Zhao ZH, Chen XM, He ZH, Jin SL, Jia QZ, Yao G, Yang JX, Wang BT, Li GB, Bi YQ, Yuan ZY (2004) Wheat stripe rust epidemic and virulence of Puccinia striiformis f. sp. tritici in China in 2002. Plant Dis 88:896–904

    Article  PubMed  Google Scholar 

  • Wang Z, Ren JD, Du ZY, Che MZ, Zhang YB, Quan W, Jiang X, Ma Y, Zhao Y, Zhang ZJ (2019) Identification of a major QTL on chromosome arm 2AL for reducing yellow rust severity from a Chinese wheat landrace with evidence for durable resistance. Theor Appl Genet 132:457–471

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Zou S, Li Y, Lin F, Tang D (2020) An ankyrin-repeat and WRKY-domain-containing immune receptor confers stripe rust resistance in wheat. Nat Commun 11:1353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YQ, Liang FY, Guan FN, Yao FJ, Long L, Zhao XY, Duan LY, Wu Y, Li H, Li W, Jiang QT, Wei YM, Ma J, Qi PF, Deng M, Zheng YL, Kang HY, Jiang YF, Chen GY (2021) Molecular mapping and analysis of an excellent quantitative trait loci conferring adult-plant resistance to stripe rust in Chinese wheat landrace Gaoxianguangtoumai. Front Plant Sci 12:756557

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu L, Xia XC, Rosewarne GM, Zhu HZ, Li SZ, Zhang ZY, He ZH (2015) Stripe rust resistance gene Yr18 and its suppressor gene in Chinese wheat landraces. Plant Breed 134(6):634–640

    Article  CAS  Google Scholar 

  • Wu XL, Wang JW, Cheng YK, Ye XL, Li W, Pu ZE, Jiang QT, Wei YM, Deng M, Zheng YL, Chen GY (2016) Inheritance and molecular mapping of an all-stage stripe rust resistance gene derived from the Chinese common wheat land race ‘Yilongtuomai.’ J Hered 107:463–470

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Wang YQ, Yao FJ, Long L, Li J, Li H, Pu ZE, Li W, Jiang QT, Wang JR, Wei YM, Ma J, Kang HY, Qi PF, Dai SF, Deng M, Zheng YL, Jiang YF, Chen GY (2020) Molecular mapping of a novel QTL conferring adult plant resistance to stripe rust in Chinese wheat landrace ‘Guangtoumai.’ Plant Dis 105:1919–1925

    Article  Google Scholar 

  • Yang EN, Rosewarne GM, Herrera-Foessel SA, Huerta-Espino J, Tang ZX, Sun CF, Ren ZL, Singh RP (2013) QTL analysis of the spring wheat “Chapio” identifies stable stripe rust resistance despite inter-continental genotype × environment interactions. Theor Appl Genet 126:1721–1732

    Article  CAS  PubMed  Google Scholar 

  • Yao FJ, Zhang XM, Ye XL, Li J, Long L, Yu C, Li J, Wang YQ, Wu Y, Wang JR, Jiang QT, Li W, Ma J, Wei YM, Zheng YL, Chen GY (2019) Characterization of molecular diversity and genome-wide association study of stripe rust resistance at the adult plant stage in northern Chinese wheat landraces. BMC Genet 20:38–53

    Article  PubMed  PubMed Central  Google Scholar 

  • Yao FJ, Guan FN, Duan LY, Long L, Tang H, Jiang YF, Li H, Jiang QT, Wang JR, Qi PF, Kang HY, Li W, Ma J, Pu ZE, Deng M, Wei YM, Zheng YL, Chen XM, Chen GY (2021) Genome-Wide association analysis of stable stripe rust resistance loci in a Chinese wheat landrace Panel using the 660K SNP array. Front Plant Sci 12:783830

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang HY, Wang Z, Ren JD, Du ZY, Quan W, Zhang YB, Zhang ZJ (2017) A QTL with major effect on reducing stripe rust severity detected from a Chinese wheat landrace. Plant Dis 101:1533–1539

    Article  CAS  PubMed  Google Scholar 

  • Zhang CZ, Huang L, Zhang HF, Hao QQ, Lyu B, Wang MN, Epstein L, Liu M, Kou CL, Qi J, Chen FJ, Li MK, Gao G, Ni F, Zhang LQ, Hao M, Wang JR, Chen XM, Luo MC, Zheng YL, Wu JJ, Liu DC, Fu DL (2019a) An ancestral NB-LRR with duplicated 3′ UTRs confers stripe rust resistance in wheat and barley. Nat Commun 10:4023–4034

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang HW, Wang X, Pan QC, Li P, Liu YJ, Lu XD, Zhong WS, Li MQ, Li J, Wang PX, Li DD, Liu Y, Li Q, Yang F, Zhang YM, Wang GY, Li L (2019b) QTG-Seq accelerates QTL fine mapping through QTL partitioning and whole-genome sequencing of bulked segregant samples. Mol Plant 12:426–437

    Article  PubMed  Google Scholar 

  • Zhang LC, Dong CH, Chen ZX, Gui LX, Chen C, Li DP, Xie ZC, Zhang Q, Zhang XY, Xia C, Liu X, Kong XY, Wang JR (2021) WheatGmap: a comprehensive platform for wheat gene mapping and genomic studies. Mol Plant 14:187–190

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful to Prof. Qiu-Zhen Jia (Plant Protection Research Institute, Gansu Academy of Agricultural Sciences, Lanzhou, P. R. China) for providing the stripe rust races, and Prof. Li-Hui Li and Xiu-Quan Li (Chinese Academy of Agricultural Sciences) for providing plant materials.

Funding

We acknowledge financial support from financial support from the Major Program of National Agricultural Science and Technology of China (Grant Number NK20220607), the National Natural Science Foundation of China (Grant Number 32272059) and the Science and Technology Department of Sichuan Province (Grant Numbers 2022ZDZX0014, 2021YFYZ0002 and 2021YJ0297).

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HLJ carried out the experiment, analyzed the data, and drafted the manuscript; HPZ and XYZ carried out the experiment and analyzed the data; LL, FNG, YPW, LYH, XYZ, YQW and HL carried out the phenotypic evaluation; WL, QTJ, YMW, JM, PFQ, MD, HYK and YLZ participated in the field experiment; GYC and YFJ designed and carried out the experiment, formulated the questions, analyzed the data and revised the manuscript. All authors have reviewed and approved the final manuscript.

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Correspondence to Guoyue Chen or Yunfeng Jiang.

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Communicated by Evans Lagudah.

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Jin, H., Zhang, H., Zhao, X. et al. Identification of a suppressor for the wheat stripe rust resistance gene Yr81 in Chinese wheat landrace Dahongpao. Theor Appl Genet 136, 67 (2023). https://doi.org/10.1007/s00122-023-04347-5

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