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Characterization of a new gene for resistance to wheat powdery mildew on chromosome 1RL of wild rye Secale sylvestre

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PmSESY, a new wheat powdery mildew resistance gene was characterized and genetically mapped to the terminal region of chromosome 1RL of wild rye Secale sylvestre.

Abstract

The genus Secale is an important resource for wheat improvement. The Secale species are usually considered as non-adapted hosts of Blumeria graminis f. sp. tritici (Bgt) that causes wheat powdery mildew. However, as a wild species of cultivated rye, S. sylvestre is rarely studied. Here, we reported that 25 S. sylvestre accessions were susceptible to isolate BgtYZ01, whereas the other five confer effective resistance to all the tested isolates of Bgt. A population was then constructed by crossing the resistant accession SESY-01 with the susceptible accession SESY-11. Genetic analysis showed that the resistance in SESY-01 was controlled by a single dominant gene, temporarily designated as PmSESY. Subsequently, combining bulked segregant RNA-Seq (BSR-Seq) analysis with molecular analysis, PmSESY was mapped into a 1.88 cM genetic interval in the terminus of the long arm of 1R, which was closely flanked by markers Xss06 and Xss09 with genetic distances of 0.87 cM and 1.01 cM, respectively. Comparative mapping demonstrated that the corresponding physical region of the PmSESY locus was about 3.81 Mb in rye cv. Lo7 genome, where 30 disease resistance-related genes were annotated, including five NLR-type disease resistance genes, three kinase family protein genes, three leucine-rich repeat receptor-like protein kinase genes and so on. This study gives a new insight into S. sylvestre that shows divergence in response to Bgt and reports a new powdery mildew resistance gene that has potential to be used for resistance improvement in wheat.

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References

  • Cuadrado A, Jouve N (2002) Evolutionary trends of different repetitive DNA sequences during speciation in the genus Secale. J Hered 93:339–345

    Article  CAS  Google Scholar 

  • Chen PD, Qi LL, Zhou B, Zhang SZ, Liu DJ (1995) Development and molecular cytogenetic analysis of wheat-Haynaldia villosa 6VS/6AL translocation lines specifying resistance to powdery mildew. Theor Appl Genet 91:1125–1128

    Article  CAS  Google Scholar 

  • Dracatos PM, Bartoš J, Elmansour H, Singh D, Karafiátová M, Zhang P, Steuernagel B, Svačina R, Cobbin JCA, Clark B et al (2019) The coiled-coil NLR Rph1, confers leaf rust resistance in barley cultivar Sudan. Plant Physiol 179:1362–1372

    Article  CAS  Google Scholar 

  • Feuillet C, Langridge P, Waugh R (2007) Cereal breeding takes a walk on the wild side. Trends Genet 24:24–32

    Article  Google Scholar 

  • Friebe B, Heun M, Tuleen N, Zeller FJ, Gill BS (1994) Cytogenetically monitored transfer of powdery mildew resistance from rye into wheat. Crop Sci 34:621–625

    Article  Google Scholar 

  • Fu S, Chen L, Wang Y, Li M, Yang Z, Qiu L, Yan B, Ren Z, Tang Z (2015) Oligonucleotide probes for ND-FISH analysis to identify rye and wheat chromosomes. Sci Rep 5:10552

    Article  Google Scholar 

  • Han F, Lamb JC, Birchler A (2006) High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize. Proc Natl Acad Sci USA 103:3238–3243

    Article  CAS  Google Scholar 

  • Hao M, Liu M, Luo J, Fan C, Yi Y, Zhang L, Yuan Z, Ning S, Zheng Y, Liu D (2018) Introgression of powdery mildew resistance gene Pm56 on rye chromosome arm 6RS into wheat. Front Plant Sci 9:1040

    Article  Google Scholar 

  • He H, Ji Y, Zhu S, Li B, Zhao R, Jiang Z, Bie T (2017) Genetic, physical and comparative mapping of the powdery mildew resistance gene Pm21 originating from Dasypyrum villosum. Front Plant Sci 8:1914

    Article  Google Scholar 

  • He H, Liu R, Ma P, Du H, Zhang H, Wu Q, Yang L, Gong S, Liu T, Huo N et al (2020) Characterization of Pm68, a new powdery mildew resistance gene on chromosome 2BS of Greek durum wheat TRI 1796. Theor Appl Genet. https://doi.org/10.1007/s00122-020-03681-2

    Article  PubMed  PubMed Central  Google Scholar 

  • He H, Zhu S, Zhao R, Jiang Z, Ji Y, Ji J, Qiu D, Li H, Bie T (2018) Pm21, encoding a typical CC-NBS-LRR protein, confers broad-spectrum resistance to wheat powdery mildew disease. Mol Plant 11:879–882

    Article  CAS  Google Scholar 

  • He R, Chang Z, Yang Z, Yuan Z, Zhan H, Zhang X, Liu J (2009) Inheritance and mapping of powdery mildew resistance gene Pm43 introgressed from Thinopyrum intermedium into wheat. Theor Appl Genet 118:1173–1180

    Article  CAS  Google Scholar 

  • International Wheat Genome Sequencing Consortium (IWGSC) (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  • Li H, Dong Z, Xia Q, Tian X, Sehgal S, Koo DH, Friebe B, Ma P, Liu W (2020) A spontaneous wheat-Aegilops longissima translocation carrying Pm66 confers resistance to powdery mildew. Theor Appl Genet 133:1149–1159

    Article  CAS  Google Scholar 

  • Li H, Zhou Y, Xin W, Wei Y, Zhang J, Guo L (2019) Wheat breeding in northern China: achievements and technical advances. Crop J 7:718–729

    Article  CAS  Google Scholar 

  • Li J, Chen Q, Zhang P, Lang T, Hoxha S, Li G, Yang Z (2019) Comparative FISH and molecular identification of new stripe rust resistant wheat-Thinopyrum intermedium ssp. trichophorum introgression lines. Crop J 7:819–829

    Article  Google Scholar 

  • Li L, Liu J, Xue X, Li C, Yang Z, Li T (2018) CAPS/dCAPS Designer: a web-based high-throughput dCAPS marker design tool. Sci China Life Sci 61:992–995

    Article  CAS  Google Scholar 

  • Li Y, Shi X, Hu J, Wu P, Qiu D, Qu Y, Xie J, Wu Q, Zhang H, Yang L et al (2020) Identification of a recessive gene PmQ conferring resistance to powdery mildew in wheat landrace Qingxinmai using BSR-Seq analysis. Plant Dis 104:743–751

    Article  CAS  Google Scholar 

  • Li Z, Ren Z, Tan F, Tang Z, Ren T (2016) Molecular cytogenetic characterization of new wheat-rye 1R(1B) substitution and translocation lines from a Chinese Secale cereal L. Aigan with resistance to stripe rust. PLoS One 11:e0163642

    Article  Google Scholar 

  • Lott GK, Johnson BR, Bonow RH, Land BR, Hoy RR (2009) g-PRIME: a free, Windows based data acquisition and event analysis software package for physiology in classrooms and research labs. J Undergrad Neurosci Educ 8:A50–A54

    PubMed  PubMed Central  Google Scholar 

  • Luo P, Luo H, Chang Z, Zhang H, Zhang M, Ren Z (2009) Characterization and chromosomal location of Pm40 in common wheat: a new gene for resistance to powdery mildew derived from Elytrigia intermedium. Theor Appl Genet 118:1059–1064

    Article  CAS  Google Scholar 

  • Ma P, Xu H, Xu Y, Li L, Qie Y, Luo Q, Zhang X, Li X, Zhou Y, An D (2015) Molecular mapping of a new powdery mildew resistance gene Pm2b in Chinese breeding line KM2939. Theor Appl Genet 128:613–622

    Article  CAS  Google Scholar 

  • Martis MM, Zhou R, Haseneyer G, Schmutzer T, Vrána J, Kubaláková M, König S, Kugler KG, Scholz U, Hackauf B et al (2013) Reticulate evolution of the rye genome. Plant Cell 25:3685–3698

    Article  CAS  Google Scholar 

  • McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Xia XC (2017) Catalogue of gene symbols for wheat: 2017 supplement (KOMUGI Wheat Genetic Resource Database). https://shigen.nig.ac.jp/wheat/komugi/genes/symbolClassList.jsp

  • Menardo F, Praz CR, Wyder S, Ben-David R, Bourras S, Matsumae H, McNally KE, Parlange F, Riba A, Roffler S et al (2016) Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nat Genet 48:201–205

    Article  Google Scholar 

  • Menardo F, Wicker T, Keller B (2017) Reconstructing the evolutionary history of powdery mildew lineages (Blumeria graminis) at different evolutionary time scales with NGS data. Genome Biol Evol 9:446–456

    Article  Google Scholar 

  • Petersen G, Seberg O (1998) Molecular characterization and sequence polymorphism of the alcohol dehydrogenase 1 gene in Hordeum vulgare L. Euphytica 102:57–63

    Article  CAS  Google Scholar 

  • Petersen G, Seberg O, Aagesen L, Frederiksen S (2004) An empirical test of the treatment of indels during optimization alignment based on the phylogeny of the genus Secale (Poaceae). Mol Phylogenet Evol 30:733–742

    Article  CAS  Google Scholar 

  • Rabanus-Wallace MT, Hackauf B, Mascher M, Lux T, Wicker T, Gundlach H, Báez M, Houben A, Mayer KFX, Guo L et al (2019) Chromosome-scale genome assembly provides insights into rye biology, evolution, and agronomic potential. bioRxiv. https://doi.org/10.1101/2019.12.11.869693

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

    Article  Google Scholar 

  • Singh SP, Hurni S, Ruinelli M, Brunner S, Sanchez-Martin J, Krukowski P, Peditto D, Buchmann G, Zbinden H, Keller B (2018) Evolutionary divergence of the rye Pm17 and Pm8 resistance genes reveals ancient diversity. Plant Mol Biol 98:249–260

    Article  CAS  Google Scholar 

  • Steuernagel B, Periyannan SK, Hernández-Pinzón I, Witek K, Rouse MN, Yu G, Hatta A, Ayliffe M, Bariana H, Jones JDG et al (2016) Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nat Biotechnol 34:652–655

    Article  CAS  Google Scholar 

  • Tang Z, Yang Z, Fu S (2014) Oligonucleotides replacing the roles of repetitive sequences pAs1, pSc119.2, pTa-535, pTa71, CCS1, and pAWRC.1 for FISH analysis. J Appl Genet 55:313–318

    Article  CAS  Google Scholar 

  • Tang ZX, Ross K, Ren ZL, Yang ZJ, Zhang HY, Chikmawati T, Miftahudin GJP (2011) Secale, Chapter 8. In: Kole C (ed) Wild crop relatives: genomic and breeding resources. Cereals, Springer, Berlin, pp 367–396

  • Troch V, Audenaert K, Wyand RA, Haesaert G, Höfte M, Brown JKM (2014) Formae speciales of cereal powdery mildew: close or distant relatives. Mol Plant Pathol 15:304–314

    Article  Google Scholar 

  • Wu P, Xie J, Hu J, Qiu D, Liu Z, Li T, Li M, Zhang H, Yang L, Liu H et al (2018) Development of molecular markers linked to powdery mildew resistance gene Pm4b by combining SNP discovery from transcriptome sequencing data with bulked segregant analysis (BSR-Seq) in wheat. Front Plant Sci 9:95

    Article  Google Scholar 

  • Yang Z, Li G, Jiang H, Ren Z (2001) Expression of nucleolus, endosperm storage proteins and disease resistance in an amphiploid between Aegilops tauschii and Secale silvestre. Euphytica 119:317–321

    Article  Google Scholar 

  • Zeller FJ, Kong L, Hartl L, Mohler V, Hsam SLK (2002) Chromosomal location of genes for resistance to powdery mildew in common wheat (Triticum aestivum L. em Thell.). 7. Gene Pm29 in line Pova. Euphytica 123:187–194

    Article  CAS  Google Scholar 

  • Zhan H, Li G, Zhang X, Li X, Guo H, Gong W, Jia J, Qiao L, Ren Y, Yang Z, Chang Z (2014) Chromosomal location and comparative genomics analysis of powdery mildew resistance gene Pm51 in a putative wheat-Thinopyru ponticum introgresion line. PLoS ONE 9:e113455

    Article  Google Scholar 

  • Zhang R, Fan Y, Kong L, Wang Z, Wu J, Xing L, Cao A, Feng Y (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 R, Sun B, Chen J, Cao A, Xing L, Feng Y, Lan C, Chen P (2016) Pm55, a developmental-stage and tissue-specific powdery mildew resistance gene introgressed from Dasypyrum villosum into common wheat. Theor Appl Genet 129:1975–1984

    Article  CAS  Google Scholar 

  • Zhang S, Zhang R, Song G, Gao J, Li W, Han X, Chen M, Li Y, Li G (2018) Targeted mutagenesis using the Agrobacterium tumefaciens-mediated CRISPR-Cas9 system in common wheat. BMC Plant Biol 18:302

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by grants from Jiangsu Agricultural Science and Technology Innovation Fund [CX(19)2042], State Key Laboratory of Plant Cell and Chromosome Engineering (PCCE-KF-2019-04), Priority Academic Program Development of Jiangsu Higher Education Institutions, Jiangsu Education Department, National Natural Science Foundation of China (31872009), Leading Talents Plan of Hubei Academy of Agricultural Sciences (L2018013), Taishan Scholars Project (tsqn201812123) and State Key Laboratory of Crop Biology in Shandong Agricultural University (2020KF07). The authors are thankful to National Centre for Plant Genetic Resources, Polish Genebank (NCPGR), Genebank Information System of the IPK Gatersleben (GBIS-IPK) and Germplasm Resources Information Network (GRIN) for providing Secale sylvestre accessions. The authors are also grateful to Prof. Robert McIntosh (The University of Sydney, Australia) for constructive comments on this manuscript and Prof. Hongjie Li (Chinese Academy of Agricultural Sciences, China) for editing this manuscript.

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HH and SZ conceived and designed the experiments. HH, HD, RL, TL, LY, SG, ZT, HD, CL, RH, WS, and LW performed the experiments. HH and SZ analyzed the data and wrote the paper.

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Correspondence to Huagang He or Shanying Zhu.

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Communicated by Beat Keller.

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He, H., Du, H., Liu, R. et al. Characterization of a new gene for resistance to wheat powdery mildew on chromosome 1RL of wild rye Secale sylvestre. Theor Appl Genet 134, 887–896 (2021). https://doi.org/10.1007/s00122-020-03739-1

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