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Fine mapping of powdery mildew and stripe rust resistance genes Pm5V/Yr5V transferred from Dasypyrum villosum into wheat without yield penalty

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Abstract

Key message

The novel wheat powdery mildew and stripe rust resistance genes Pm5V/Yr5V are introgressed from Dasypyrum villosum and fine mapped to a narrowed region in 5VS, and their effects on yield-related traits were characterized.

Abstract

The powdery mildew and stripe rust seriously threaten wheat production worldwide. Dasypyrum villosum (2n = 2x = 14, VV), a relative of wheat, is a valuable resource of resistance genes for wheat improvement. Here, we describe a platform for rapid introgression of the resistance genes from D. villosum into the wheat D genome. A complete set of new wheat-D. villosum V (D) disomic substitution lines and 11 D/V Robertsonian translocation lines are developed and characterized by molecular cytogenetic method. A new T5DL·5V#5S line NAU1908 shows resistance to both powdery mildew and stripe rust, and the resistances associated with 5VS are confirmed to be conferred by seedling resistance gene Pm5V and adult-plant resistance gene Yr5V, respectively. We flow-sort chromosome arm 5VS and sequence it using the Illumina NovaSeq 6000 system that allows us to generate 5VS-specific markers for genetic mapping of Pm5V/Yr5V. Fine mapping shows that Pm5V and Yr5V are closely linked and the location is narrowed to an approximately 0.9 Mb region referencing the sequence of Chinese Spring 5DS. In this region, a NLR gene in scaffold 24,874 of 5VS orthologous to TraesCS5D02G044300 is the most likely candidate gene for Pm5V. Soft- and hard-grained T5DL·5V#5S introgressions confer resistance to both powdery mildew and stripe rust in diverse wheat genetic backgrounds without yield penalty. Meanwhile, significant decrease in plant height and increase in yield were observed in NIL-5DL·5V#5S compared with that in NIL-5DL·5DS. These results indicate that Pm5V/Yr5V lines might have the potential value to facilitate wheat breeding for disease resistance.

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Data availability

Data supporting the findings of this work are available within the paper and its Supplementary Information files. The plant materials and datasets generated and analyzed during the present study are available from the corresponding authors upon reasonable request.

References

  • Al-Kaff N, Knight E, Bertin I, Foote T, Hart N, Griffiths S, Moore G (2008) Detailed dissection of the chromosomal region containing the Ph1 locus in wheat Triticum aestivum: with deletion mutants and expression profiling. Ann Bot 101:863–872

    Article  CAS  Google Scholar 

  • Bhave M, Morris CF (2008) Molecular genetics of puroindolines and related genes: allelic diversity in wheat and other grasses. Plant Mol Biol 66:205–219

    Article  CAS  Google Scholar 

  • Chen F, Jia HY, Zhang XJ, Qiao LY, Li X, Zheng J, Guo HJ, Powers C, Yan LL, Chang ZJ (2019) Positional cloning of PmCH1357 reveals the origin and allelic variation of the Pm2 gene for powdery mildew resistance in wheat. Crop J 7:771–783

    Article  Google Scholar 

  • Feuillet C, Langridge P, Waugh R (2008) Cereal breeding takes a walk on the wild side. Trends Genet 24:24–32

    Article  CAS  Google Scholar 

  • Gaurav K, Arora S, Silva P, Sánchez-Martín J, Horsnell R, Gao LL, Brar GS, Widrig V, Raupp WJ, Singh N, Wu SY, Kale SM, Chinoy C, Nicholson P, Quiroz-Chvez J, Simmonds J, Hayta S, Smedley MA, Harwood W, Pearce S, Gilbert D, Kangara N, Gardener C, Forner-Martnez M, Liu JQ, Yu GT, Boden SA, Pascucci A, Ghosh S, Hafeez AN, O’Hara T, Waites J, Cheema J, Steuernagel B, Patpour M, Justesen AF, Liu SY, Rudd JC, Avni R, Sharon A, Steiner B, Kirana RP, Buerstmayr H, Mehrabi AA, Nasyrova FY, Chayut N, Matny O, Steffenson BJ, Sandhu N, Chhuneja P, Lagudah E, Elkot AF, Tyrrell S, Bian XD, Davey RP, Simonsen M, Schauser L, Tiwari VK, Randy KH, Hucl P, Li AL, Liu DC, Mao L, Xu S, Brown-Guedira G, Faris J, Dvorak J, Luo MC, Krasileva K, Lux T, Artmeier S (2022) Population genomic analysis of Aegilops tauschii identifies targets for bread wheat improvement. Nat Biotechnol 40:422–431

    Article  CAS  Google Scholar 

  • Gill BS, Friebe BR, White FF (2011) Alien introgressions represent a rich source of genes for crop improvement. Proc Nat Acad Sci USA 108:7657–7658

    Article  CAS  Google Scholar 

  • Giorgi D, Farina A, Grosso V, Gennaro A, Ceoloni C, Lucrett S (2013) FISHIS: fluorescence in situ hybridization in suspension and chromosome flow sorting made easy. PLoS One 8:e57994

    Article  CAS  Google Scholar 

  • Gradzielewska A (2006) The genus Dasypyrum — part 2. Dasypyrum villosum — a wild species used in wheat improvement. Euphytica 152:441–454

    Article  Google Scholar 

  • Hafeez AN, Arora S, Ghosh S, Gilbert D, Bowden RL, Wulff BBH (2021) Creation and judicious application of a wheat resistance gene atlas. Mol Plant 14:1053–1070

    Article  CAS  Google Scholar 

  • Hickey LT, Hafeez AN, Robinson H, Jackson SA, Leal-Bertioli SCM, Tester M, Gao CX, Godwin ID, Hayes BJ, Wulff BBH (2019) Breeding crops to feed 10 billion. Nat Biotechnol 37:744–754

    Article  CAS  Google Scholar 

  • Hurni S, Brunner B, Buchmann G, Herren G, Jordan T, Krukowski P, Wicker T, Yahiaoui N, Mago R, Keller B (2013) Rye Pm8 and wheat Pm3 are orthologous genes and show evolutionary conservation of resistance function against powdery mildew. Plant J 76:957–969

    Article  CAS  Google Scholar 

  • Jordan T, Seeholzer S, Schwizer S, Töller A, Somssich IE, Keller B (2011) The wheat Mla homologue TmMla1 exhibits an evolutionarily conserved function against powdery mildew in both wheat and barley. Plant J 65:610–621

    Article  CAS  Google Scholar 

  • King J, Grewal S, Yang CY, Hubbart S, Scholefield D, Ashling S, Edwards KJ, Allen MA, Burridge A, Bloor C, Davassi A, da Silva GJ, Chalmers K, King IP (2017) A step change in the transfer of interspecifc variation into wheat from Amblyopyrum muticum. Plant Biotech J 15:217–226

    Article  CAS  Google Scholar 

  • Li GW, Wang LJ, Yang JP, He H, Jin HB, Li XM, Ren TH, Ren ZL, Li F, Han X, Zhao XG, Dong LL, Li YW, Song ZP, Yan ZH, Zheng NN, Shi CL, Wang ZH, Yang SL, Xiong ZJ, Zhang ML, Sun GH, Zheng X, Gou MY, Ji CM, Du JK, Zheng HK, Doleel J, Deng XW, Stein N, Yang QH, Zhang KP, Wang DW (2021) A high-quality genome assembly highlights rye genomic characteristics and agronomically important genes. Nat Genet 53:574–584

    Article  CAS  Google Scholar 

  • Lukaszewski AJ (2000) Manipulation of the 1RS.1BL translocation in wheat by induced homoeologous recombination. Crop Sci 40:216–225

    Article  CAS  Google Scholar 

  • Luo M, Xie LQ, Chakraborty S, Wang AH, Matny O, Jugovich M, Kolmer JA, Richardson T, Bhatt D, Hoque M, Patpour M, Sørensen C, Ortiz D, Dodds P, Steuernagel B, Wulff BBH, Upadhyaya NM, Mago R, Periyannan S, Lagudah E, Freedman R, Lynne Reuber T, Steffenson BJ, Ayliffe M (2021) A five-transgene cassette confers broad-spectrum resistance to a fungal rust pathogen in wheat. Nat Biotechnol 39:561–566

    Article  CAS  Google Scholar 

  • Mago R, Zhang P, Vautrin S, Šimková H, Bansal U, Luo MC, Rouse M, Karaoglu H, Periyannan S, Kolmer J, Jin Y, Ayliffe MA, Bariana H, Park RF, McIntosh R, Doležel J, Bergès H, Spielmeyer W, Lagudah ES, Ellis JG, Dodds PN (2015) The wheat Sr50 gene reveals rich diversity at a cereal disease resistance locus. Nat Plant 1:15186

    Article  CAS  Google Scholar 

  • Marcussen T, Sandve SR, Heier L, Spannagl M, Pfeifer M, Jakobsen KS, Wulff BBH, Steuernagel B, Mayer KF, Olsen OA (2014) Ancient hybridizations among the ancestral genomes of bread wheat. Science 345:1250092

    Article  Google Scholar 

  • Mirzaghaderi G, Mason AS (2019) Broadening the bread wheat D genome. Theor Appl Genet 132:1295–1307

    Article  CAS  Google Scholar 

  • De Pace C, Vaccino P, Cionini G, Pasquini M, Bizzarri M, Qualset CO (2011) Dasypyrum. In: Kole C (ed) Wild crop relatives: genomic and breeding resources, cereals, vol 1, chapter 4. Springer, Heidelberg, pp 185–292

  • Periyannan S, Moore J, Ayliffe M, Bansal U, Wang X, Huang L, Deal K, Luo M, Kong X, Bariana H, Mago R, McIntosh R, Dodds P, Dvorak J, Lagudah E (2013) The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science 341:786–788

    Article  CAS  Google Scholar 

  • Peterson RF, Campbell AB, Hannah AE (1948) A diagrammatic scale for estimating rust intensity on leaves and stems of cereals. Can J Res 26:496–500

    Article  Google Scholar 

  • Praz CR, Bourras S, Zeng F, Sánchez-Martín J, Menardo F, Xue M, Yang L, Roffler S, Böni R, Herren G, McNally KE, Ben-David R, Parlange F, Oberhaensli S, Flückiger S, Schäfer LK, Wicker T, Yu D, Keller B (2017) AvrPm2 encodes an RNase-like avirulence effector which is conserved in the two different specialized forms of wheat and rye powdery mildew fungus. New Phytolog 213:1301–1314

    Article  CAS  Google Scholar 

  • Sánchez-Martín J, Steuernagel B, Ghosh S, Herren G, Hurni S, Adamski N, Vrána J, Kubaláková M, Krattinger SG, Wicker T, Doležel J, Keller B, Wulff BBH (2016) Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol 17:221

    Article  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  Google Scholar 

  • Sheng BQ, Duan XY (1991) Modification on the evaluation methods of 0–9 level of powdery mildew infection on wheat. Biotech J Agric Sci 9:37–39

    Google Scholar 

  • Subbarao GV, Kishii M, Bozal-Leorri A, Ortiz-Monasterio I, Gao X, Ibba MI, Karwat H, Gonzalez-Moro MB, Gonzalez-Murua C, Yoshihashi T, Tobita S, Kommerell V, Braun HJ, Iwanaga M (2021) Enlisting wild grass genes to combat nitrification in wheat farming: a nature-based solution. Proc Nat Acad Sci USA 118:e2106595118

    Article  CAS  Google Scholar 

  • Tadesse W, Sanchez-Garcia M, Assefa SG, Amri A, Bishaw Z, Ogbonnaya FC, Baum M (2019) Genetic gains in wheat breeding and its role in feeding the world. Crop Breed Genet Genom 1:e190005

    Google Scholar 

  • Vrána J, Kubaláková M, Simková H, Cíhalíková J, Lysák MA, Dolezel J (2000) Flow-sorting of mitotic chromosomes in common wheat (Triticum aestivum L.). Genetics 156:2033–2041

    Article  Google Scholar 

  • Wang X, Cao AZ, Yu CM, Wang DW, Wang XE, Chen PD (2010) Establishment of an effective virus induced gene silencing system with BSMV in Haynaldia villosa. Mol Biol Rep 37:967–972

    Article  Google Scholar 

  • Wang H, Sun S, Ge W, Zhao L, Hou B, Wang K, Lyu Z, Chen L, Xu S, Guo J, Li M, Su P, Li X, Wang G, Bo C, Fang X, Zhuang W, Cheng X, Wu J, Dong L, Chen W, Li W, Xiao G, Zhao J, Hao Y, Xu Y, Gao Y, Liu W, Liu Y, Yin H, Li J, Li X, Zhao Y, Wang X, Ni F, Ma X, Li A, Xu SS, Bai G, Nevo E, Gao C, Ohm H, Kong L (2020) Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat. Science 368:eaba5435

    Article  CAS  Google Scholar 

  • Watson A, Ghosh S, Williams MJ, Cuddy WS, Simmonds J, Rey MD, Asyraf Md Hatta M, Hinchliffe A, Steed A, Reynolds D, Adamski NM, Breakspear A, Korolev A, Rayner T, Dixon LE, Riaz A, Martin W, Ryan M, Edwards D, Batley J, Raman H, Carter J, Rogers C, Domoney C, Moore G, Harwood W, Nicholson P, Dieters MJ, DeLacy IH, Zhou J, Uauy C, Boden SA, Park RF, Wulff BBH, Hickey LT (2018) Speed breeding is a powerful tool to accelerate crop research and breeding. Nat Plants 4:23–29

    Article  Google Scholar 

  • Xing L, Hu P, Liu J, Witek K, Zhou S, Xu J, Zhou W, Gao L, Huang Z, Zhang R, Wang X, Chen P, Wang H, Jones JDG, Karafiátová M, Vrána J, Bartoš J, Doležel J, Tian Y, Wu Y, Cao A (2018) Pm21 from Haynaldia villosa encodes a CC-NBS-LRR protein conferring powdery mildew resistance in wheat. Mol Plant 11:874–878

    Article  CAS  Google Scholar 

  • Zhang RQ, Cao YP, Wang XE, Feng YG, Chen PD (2010) Development and characterization of a Triticum aestivum-D. villosum T5VS.5DL translocation line with soft grain texture. J Cereal Sci 51:220–225

    Article  CAS  Google Scholar 

  • Zhang RQ, Sun BX, Chen J, Cao AZ, Xing LP, Feng YG, Lan CX, Chen PD (2016) Pm55, a developmental-stage and tissue-specific powdery mildew resistance gene introgressed from Dasypyrum villosum into common wheat. Theor Appl Genet 129:975–1984

    Article  Google Scholar 

  • Zhang XD, Wei X, Xiao J, Yuan CX, Wu YF, Cao AZ, Xing LP, Chen PD, Zhang SZ, Wang XE, Wang HY (2017) Whole genome development of intron targeting (IT) markers specific for Dasypyrum villosum chromosomes based on next-generation sequencing technology. Mol Breed 37:11

    Article  CAS  Google Scholar 

  • Zhang RQ, Fan YL, Kong LN, Wang ZJ, Wu JZ, Xing LP, Cao AZ, Feng YG (2018) Pm62, an adult-plant powdery mildew resistance gene introgressed from Dasypyrum villosum chromosome arm 2VL into wheat. Theor Appl Genet 131:2613–2620

    Article  CAS  Google Scholar 

  • Zhang RQ, Xiong CX, Mu HQ, Yao RN, Meng XR, Kong LN, Xing LP, Wu JZ, Feng YG, Cao AZ (2021) Pm67, a new powdery mildew resistance gene transferred from Dasypyrum villosum chromosome 1V to common wheat (Triticum aestivum L.). Crop J 9:882–888

    Article  Google Scholar 

  • Zhou SS, Zhang JP, Chen YH, Liu WH, Lu YQ, Yang XM, Li XQ, Jia JZ, Liu X, Li LH (2018) Construction of Agropyron Gaertn. genetic linkage maps using a wheat 660 K SNP array reveals a homoeologous relationship with the wheat genome. Plant Biotech J 16:818–827

    Article  CAS  Google Scholar 

  • Zhou Y, Bai SL, Li H, Su GL, Zheng DL, Ma FF, Zhao XP, Nie F, Li JY, Chen LY, Lv LL, Zhu LL, Fan RX, Ge YF, Shaheen A, Guo GH, Zhang Z, Ma JC, Liang HH, Qiu XL, Hu JM, Sun T, Hou JY, Xu HX, Xue SL, Jiang WK, Huang JL, Li SP, Zou CS, Song CP (2021) Introgressing the Aegilops tauschii genome into wheat as a basis for cereal improvement. Nat Plants 7:774–786

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to Prof. Xiue Wang and Zengjun Qi from Nanjing Agricultural University for advice and support during this research. We thank Prof. Robert McIntosh, University of Sydney, for reviewing the manuscript. We also thank Zdeňka Dubská and Jitka Weiserová for the assistance with preparation of samples for chromosome sorting and Mahmoud Said and István Molnár for checking the purity in flow-sorted chromosome fractions. Many thanks to Prof. Caixia Lan of Huazhong Agricultural University, Hubei, China for providing Pst races and assistance with stripe rust tests; Drs. Jizhong Wu and Xuemin Yang, Jiangsu Academy of Agricultural Science, Nanjing for assistance with grain hardness and other trait evaluations. Tests of introgression lines with 25 Bgt isolates were performed by Prof. Yilin Zhou, Institute of Plant Protection, Chinese Academy of Agricultural Science, Beijing.

Funding

This work was supported by the Special Fund for Independent Innovation of Agricultural Science and Technology in Jiangsu (No. CX (19)1001); the National Natural Science Foundation of China (31971938, 31871619); The “JBGS” Project of Seed Industry Revitalization in Jiangsu Province (JBGS (2021) 013); and the ERDF project “Plants as a Tool for Sustainable Global Development” (No. CZ.02.1.01/0.0/0.0/16_019/0000827).

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  1. Ruiqi Zhang, Chuntian Lu, Xiangru Meng have contributed equally.

Authors and Affiliations

  1. College of Agronomy of Nanjing Agricultural University/National Key Laboratory of Crop Genetics and Germplasm Enhancement /JCIC-MCP, Nanjing, 210095, People’s Republic of China

    Ruiqi Zhang, Chuntian Lu, Xiangru Meng, Yali Fan, Jie Du, Runran Liu, Yigao Feng, Liping Xing, Yiwei Wang, Huanqing Mu, Bingxiao Sun, Fu Hou, Ruonan Yao, Chuanxi Xiong, Yang Wang, Peidu Chen & Aizhong Cao

  2. Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany of the Czech Academy of Sciences, Šlechtitelů 31, 77900, Olomouc, Czech Republic

    Petr Cápal, Kateřina Holušová & Jaroslav Doležel

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  1. Ruiqi Zhang
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Contributions

RZ designed the study. CL, XM, YF, JD, RL, YF, LX, PC, KH, JD, YW, HM, BS, FH, RY, CX and YW performed the research. RZ, CL and XM analyzed the data. RZ, PC and AC wrote the paper. All authors read and approved the final manuscript.

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Correspondence to Ruiqi Zhang.

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Patent applications based on this work have been filed by R.Z, L.X. and A.C. Other authors claim no competing interests.

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The authors declare that the experiments comply with the current laws of the country in which they were performed.

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Communicated by Steven S. Xu.

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Zhang, R., Lu, C., Meng, X. et al. Fine mapping of powdery mildew and stripe rust resistance genes Pm5V/Yr5V transferred from Dasypyrum villosum into wheat without yield penalty. Theor Appl Genet 135, 3629–3642 (2022). https://doi.org/10.1007/s00122-022-04206-9

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