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Bulked segregant RNA-sequencing (BSR-seq) identified a novel rare allele of eIF4E effective against multiple isolates of BaYMV/BaMMV

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Abstract

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A novel rare allele of the barley host factor gene eIF4E for BaMMV/BaYMV infection was identified in an Iranian landrace that showed broad resistance to barley yellow mosaic virus disease, and molecular markers facilitating efficient selection were developed.

Abstract

The soil-borne yellow mosaic virus disease caused by different strains of barley yellow mosaic virus (BaYMV) and barley mild mosaic virus (BaMMV) is a major threat to winter barley (Hordeum vulgare) production in Europe and East Asia. However, the exploration of resistant germplasm or casual genes for barley breeding is rather limited in relation to the rapid diversification of viral strains. Here, we identified an Iranian barley landrace ‘HOR3298,’ which represented complete resistance to BaYMV and BaMMV. In contrast to rym4 and rym5, which act as the predominant source in Europe and East Asia for breeding resistant cultivars over decades and which have been overcome by several virulent isolates, this landrace showed broad-spectrum resistance to multiple isolates of BaYMV/BaMMV in the fields of Germany and China. By employment of bulked segregant RNA sequencing, test for allelism, and haplotype analysis, a recessive resistance gene in ‘HOR3298’ was genetically mapped coincident with the host factor eukaryotic translation initiation factor 4E (eIF4E, causal gene of rym4 and rym5). The eIF4EHOR3298 allele encoded for a novel haplotype that contained an exclusive nucleotide mutation (G565A) in the coding sequence. The easily handled markers were developed based on the exclusively rare variation, providing precise selection of this allele. Thus, this work provided a novel reliable resistance source and the feasible marker-assisted selection assays that can be used in breeding for barley yellow mosaic virus disease resistance in cultivated barley.

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References

  • Achon MA, Ratti C, Rubies-Autonell C (2003) Occurrence of barley mild mosaic virus on barley in Spain. Plant Dis 87:1004

    Article  CAS  PubMed  Google Scholar 

  • Bauer E, Weyen J, Schiemann A, Graner A, Ordon F (1997) Molecular mapping of novel resistance genes against barley mild mosaic virus (BaMMV). Theor Appl Genet 95:1263–1269

    Article  CAS  Google Scholar 

  • Charron C, Nicolai M, Gallois JL, Robaglia C, Moury BT, Palloix A, Caranta C (2008) Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J 54:56–68

    Article  CAS  PubMed  Google Scholar 

  • Chen JP, Adams MJ, Zhu FT, Shi C, Chen H (1992) Responses of some Asian and European barley cultivars to UK and Chinese isolates of soil-borne barley mosaic viruses. Ann Appl Biol 121:9

    Google Scholar 

  • Chen JP, Adams MJ, Zhu FT, Wang ZQ, Chen J, Huang SZ, Zhang ZC (1996) Response of foreign barley cultivars to barley yellow mosaic virus at different sites in China. Plant Pathol 45:1117–1125

    Article  Google Scholar 

  • Chen J, Shi NN, Cheng Y, Diao A, Chen JP, Wilson TMA, Antoniw JF, Adams MJ (1999) Molecular analysis of barley yellow mosaic virus isolates from China. Virus Res 64:13–21

    Article  CAS  PubMed  Google Scholar 

  • Gotz R, Friedt W (1993) Resistance to the Barley yellow mosaic virus complex—differential genotypic reactions and genetics of BaMMV-resistance of barley (Hordeum vulgare L.). Plant Breed 111:125–131

    Article  Google Scholar 

  • Graner A, Streng S, Kellermann A, Schiemann A, Bauer E, Waugh R, Pellio B, Ordon F (1999) Molecular mapping and genetic fine-structure of the rym5 locus encoding resistance to different strains of the barley yellow mosaic virus complex. Theor Appl Genet 98:285–290

    Article  CAS  Google Scholar 

  • Habekuß A, Kuhne T, Kramer I, Rabenstein F, Ehrig F, Ruge-Wehling B, Huth W, Ordon F (2008) Identification of barley mild mosaic virus isolates in Germany breaking rym5 resistance. J Phytopathol 156:36–41

    Google Scholar 

  • Hariri D, Meyer M, Le Gouis J, Bahrman N, Fouchard M, Forget C, Andre A (2000) Characterisation of BaYMV and BaMMV pathotypes in France. Eur J Plant Pathol 106:365–372

    Article  CAS  Google Scholar 

  • Hariri D, Meyer M, Prud’homme H (2003) Characterization of a new barley mild mosaic virus pathotype in France. Eur J Plant Pathol 109:921–928

    Article  CAS  Google Scholar 

  • Hofinger BJ, Russell JR, Bass CG, Baldwin T, Dos Reis M, Hedley PE, Li YD, Macaulay M, Waugh R, Hammond-Kosack KE, Kanyuka K (2011) An exceptionally high nucleotide and haplotype diversity and a signature of positive selection for the eIF4E resistance gene in barley are revealed by allele mining and phylogenetic analyses of natural populations. Mol Ecol 20:3653–3668

    CAS  PubMed  Google Scholar 

  • Hosseini A, Jafarpour B, Moghadam EM, Mehrvar M, Aghl MZ, Autonell CR, Ratti C (2014) Occurrence of soil-borne cereal viruses and molecular characterization of the coat protein gene of barley yellow mosaic virus Isolates from Iran. J Plant Pathol 96:391–396

    Google Scholar 

  • Iida Y, Konishi T (1994) Linkage analysis of the rym6 resistance gene to Japanese strain II of barley yellow mosaic virus (BaYMV-II) in barley. Breed Sci 44:191–194

    Google Scholar 

  • Jatayev S, Kurishbayev A, Zotova L, Khasanova G, Serikbay D, Zhubatkanov A, Botayeva M, Zhumalin A, Turbekova A, Soole K, Langridge P, Shavrukov Y (2017) Advantages of Amplifluor-like SNP markers over KASP in plant genotyping. BMC Plant Biol 17:254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jezewska M, Trzmiel K (2009) First report of barley yellow mosaic virus infecting barley in Poland. Plant Pathol 58:784

    Article  Google Scholar 

  • Jost M, Taketa S, Mascher M, Himmelbach A, Yuo T, Shahinnia F, Rutten T, Druka A, Schmutzer T, Steuernagel B, Beier S, Taudien S, Scholz U, Morgante M, Waugh R, Stein N (2016) A homolog of blade-on-petiole 1 and 2 (BOP1/2) controls internode length and homeotic changes of the barley inflorescence. Plant Physiol 171:1113–1127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kai H, Takata K, Tsukazaki M, Furusho M, Baba T (2012) Molecular mapping of Rym17, a dominant and rym18 a recessive barley yellow mosaic virus (BaYMV) resistance genes derived from Hordeum vulgare L. Theor Appl Genet 124:577–583

    Article  CAS  PubMed  Google Scholar 

  • Kaiser R, Friedt W (1992) Gene for resistance to barley mild mosaic virus in German winter barley located on chromosome-3L. Plant Breed 108:169–172

    Article  Google Scholar 

  • Kanyuka K, Ward E, Adams MJ (2003) Polymyxa graminis and the cereal viruses it transmits: a research challenge. Mol Plant Pathol 4:393–406

    Article  CAS  PubMed  Google Scholar 

  • Kanyuka K, McGrann G, Alhudaib K, Hariri D, Adams MJ (2004) Biological and sequence analysis of a novel European isolate of barley mild mosaic virus that overcomes the barley rym5 resistance gene. Arch Virol 149:1469–1480

    Article  CAS  PubMed  Google Scholar 

  • Kanyuka K, Druka A, Caldwell DG, Tymon A, McCallum N, Waugh R, Adams MJ (2005) Evidence that the recessive bymovirus resistance locus rym4 in barley corresponds to the eukaryotic translation initiation factor 4E gene. Mol Plant Pathol 6:449–458

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Landmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357-U121

    Google Scholar 

  • Kühne T (2009) Soil-borne viruses affecting cereals-known for long but still a threat. Virus Res 141:174–183

    Article  CAS  PubMed  Google Scholar 

  • Kühne T, Shi N, Proeseler G, Adams MJ, Kanyuka K (2003) The ability of a bymovirus to overcome the rym4-mediated resistance in barley correlates with a codon change in the VPg coding region on RNA1. J Gen Virol 84:2853–2859

    Article  CAS  PubMed  Google Scholar 

  • Li G, Qian W, Zhang S, Zhang S, Li F, Zhang H, Fang Z, Wu J, Wang X, Sun R (2018) Variability in eukaryotic initiation factor iso4E in Brassica rapa influences interactions with the viral protein linked to the genome of Turnip mosaic virus. Sci Rep 8:13588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu SZ, Yeh CT, Tang HM, Nettleton D, Schnable PS (2012) Gene mapping via bulked segregant RNA-seq (BSR-seq). PLoS ONE 7:e36406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lüpken T, Stein N, Perovic D, Habekuss A, Kramer I, Hahnel U, Steuernagel B, Scholz U, Zhou R, Ariyadasa R, Taudien S, Platzer M, Martis M, Mayer K, Friedt W, Ordon F (2013) Genomics-based high-resolution mapping of the BaMMV/BaYMV resistance gene rym11 in barley (Hordeum vulgare L.). Theor Appl Genet 126:1201–1212

    Article  CAS  PubMed  Google Scholar 

  • Mascher M, Jost M, Kuon JE, Himmelbach A, Assfalg A, Beier S, Scholz U, Graner A, Stein N (2014) Mapping-by-sequencing accelerates forward genetics in barley. Genome Biol 15:R78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, Radchuk V, Dockter C, Hedley PE, Russell J, Bayer M, Ramsay L, Liu H, Haberer G, Zhang XQ, Zhang QS, Barrero RA, Li L, Taudien S, Groth M, Felder M, Hastie A, Simkova H, Stankova H, Vrana J, Chan S, Munoz-Amatrian M, Ounit R, Wanamaker S, Bolser D, Colmsee C, Schmutzer T, Aliyeva-Schnorr L, Grasso S, Tanskanen J, Chailyan A, Sampath D, Heavens D, Clissold L, Cao SJ, Chapman B, Dai F, Han Y, Li H, Li X, Lin CY, McCooke JK, Tan C, Wang PH, Wang SB, Yin SY, Zhou GF, Poland JA, Bellgard MI, Borisjuk L, Houben A, Dolezel J, Ayling S, Lonardi S, Kersey P, Lagridge P, Muehlbauer GJ, Clark MD, Caccamo M, Schulman AH, Mayer KFX, Platzer M, Close TJ, Scholz U, Hansson M, Zhang GP, Braumann I, Spannagl M, Li CD, Waugh R, Stein N (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427–433

    Article  CAS  PubMed  Google Scholar 

  • McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neff MM, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18:613–615

    Article  CAS  PubMed  Google Scholar 

  • Nishigawa H, Hagiwara T, Yumoto M, Sotome T, Kato T, Natsuaki T (2008) Molecular phylogenetic analysis of barley yellow mosaic virus. Arch Virol 153:1783–1786

    Article  CAS  PubMed  Google Scholar 

  • Okada Y, Kashiwazaki S, Kanatani R, Arai S, Ito K (2003) Effects of barley yellow mosaic disease resistant gene rym1 on the infection by strains of barley yellow mosaic virus and barley mild mosaic virus. Theor Appl Genet 106:181–189

    Article  CAS  PubMed  Google Scholar 

  • Ordon F, Ahlemeyer J, Werner K, Kohler W, Friedt W (2005) Molecular assessment of genetic diversity in winter barley and its use in breeding. Euphytica 146:21–28

    Article  CAS  Google Scholar 

  • Pellio B, Streng S, Bauer E, Stein N, Perovic D, Schiemann A, Friedt W, Ordon F, Graner A (2005) High-resolution mapping of the rym4/rym5 locus conferring resistance to the barley yellow mosaic virus complex (BaMMV, BaYMV, BaYMV-2) in barley (Hordeum vulgare ssp. vulgare L.). Theor Appl Genet 110:283–293

    Article  CAS  PubMed  Google Scholar 

  • Perovic D, Kramer I, Habekuss A, Perner K, Pickering R, Proeseler G, Kanyuka K, Ordon F (2014) Genetic analyses of BaMMV/BaYMV resistance in barley accession HOR4224 result in the identification of an allele of the translation initiation factor 4e (Hv-eIF4E) exclusively effective against barley mild mosaic virus (BaMMV). Theor Appl Genet 127:1061–1071

    Article  CAS  PubMed  Google Scholar 

  • Plumb RT, Lennon EA, Gutteridge RA (1986) The effects of infection by barley yellow mosaic virus on the yield and components of yield of barley. Plant Pathol 35:314–318

    Article  Google Scholar 

  • Rasheed A, Wen W, Gao F, Zhai S, Jin H, Liu J, Guo Q, Zhang Y, Dreisigacker S, Xia X, He Z (2016) Development and validation of KASP assays for genes underpinning key economic traits in bread wheat. Theor Appl Genet 129:1843–1860

    Article  CAS  PubMed  Google Scholar 

  • Rolland M, Villemot J, Marais A, Theil S, Faure C, Cadot V, Valade R, Vitry C, Rabenstein F, Candresse T (2017) Classical and next generation sequencing approaches unravel bymovirus diversity in barley crops in France. PLoS ONE 12:e0188495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruge B, Linz A, Pickering R, Proeseler G, Greif P, Wehling P (2003) Mapping of Rym14 Hb, a gene introgressed from Hordeum bulbosum and conferring resistance to BaMMV and BaYMV in barley. Theor Appl Genet 107:965–971

    Article  CAS  PubMed  Google Scholar 

  • Ruge-Wehling B, Linz A, Habekuss A, Wehling P (2006) Mapping of Rym16 Hb, the second soil-borne virus-resistance gene introgressed from Hordeum bulbosum. Theor Appl Genet 113:867–873

    Article  CAS  PubMed  Google Scholar 

  • Shao M, Bai G, Rife TW, Poland J, Lin M, Liu S, Chen H, Kumssa T, Fritz A, Trick H, Li Y, Zhang G (2018) QTL mapping of pre-harvest sprouting resistance in a white wheat cultivar Danby. Theor Appl Genet 131:1683–1697

    Article  PubMed  Google Scholar 

  • Stein N, Perovic D, Kumlehn J, Pellio B, Stracke S, Streng S, Ordon F, Graner A (2005) The eukaryotic translation initiation factor 4E confers multiallelic recessive bymovirus resistance in Hordeum vulgare (L.). Plant J 42:912–922

    Article  CAS  PubMed  Google Scholar 

  • Stracke S, Presterl T, Stein N, Perovic D, Ordon F, Graner A (2007) Effects of introgression and recombination on haplotype structure and linkage disequilibrium surrounding a locus encoding bymovirus resistance in barley. Genetics 175:805–817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi R, Hayashi J, Inouye T, Moriya I, Hirao C (1973) Studies on resistance to yellow mosaic disease in barley. I. Tests for varietal reactions and genetic analysis of resistance to the disease. Ber Ohara Inst Landwirtsch Biol 16:1–17

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thind AK, Wicker T, Simkova H, Fossati D, Moullet O, Brabant C, Vrana J, Dolezel J, Krattinger SG (2017) Rapid cloning of genes in hexaploid wheat using cultivar-specific long-range chromosome assembly. Nat Biotechnol 35:793–796

    Article  CAS  PubMed  Google Scholar 

  • Wang AM, Krishnaswamy S (2012) Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol Plant Pathol 13:795–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Xie JZ, Zhang HZ, Guo BM, Ning SZ, Chen YX, Lu P, Wu QH, Li MM, Zhang DY, Guo GH, Zhang Y, Liu DC, Zou SK, Tang JW, Zhao H, Wang XC, Li J, Yang WY, Cao TJ, Yin GH, Liu ZY (2017) Mapping stripe rust resistance gene YrZH22 in Chinese wheat cultivar Zhoumai 22 by bulked segregant RNA-Seq (BSR-Seq) and comparative genomics analyses. Theor Appl Genet 130:2191–2201

    Article  CAS  PubMed  Google Scholar 

  • Yang P, Perovic D, Habekuss A, Zhou RN, Graner A, Ordon F, Stein N (2013) Gene-based high-density mapping of the gene rym7 conferring resistance to barley mild mosaic virus (BaMMV). Mol Breed 32:27–37

    Article  CAS  Google Scholar 

  • Yang P, Habekuss A, Ordon F, Stein N (2014a) Analysis of bymovirus resistance genes on proximal barley chromosome 4HL provides the basis for precision breeding for BaMMV/BaYMV resistance. Theor Appl Genet 127:1625–1634

    Article  PubMed  Google Scholar 

  • Yang P, Lupken T, Habekuss A, Hensel G, Steuernagel B, Kilian B, Ariyadasa R, Himmelbach A, Kumlehn J, Scholz U, Ordon F, Stein N (2014b) Protein disulfide isomerase like 5-1 is a susceptibility factor to plant viruses. Proc Natl Acad Sci USA 111:2104–2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang P, Habekuss A, Hofinger BJ, Kanyuka K, Kilian B, Graner A, Ordon F, Stein N (2017) Sequence diversification in recessive alleles of two host factor genes suggests adaptive selection for bymovirus resistance in cultivated barley from East Asia. Theor Appl Genet 130:331–344

    Article  CAS  PubMed  Google Scholar 

  • You Y, Shirako Y (2013) Evaluation of host resistance to barley yellow mosaic virus infection at the cellular and whole-plant levels. Plant Pathol 62:226–232

    Article  CAS  Google Scholar 

  • Zheng T, Cheng Y, Chen JP, Antoniw JF, Adams MJ (1999) The occurrence of barley mild mosaic virus (BaMMV) in China and the nucleotide sequence of its coat protein gene. J Phytopathol 147:229–234

    Article  CAS  Google Scholar 

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Acknowledgements

We gratefully acknowledge IPK Genebank and National Crop Genebank of China for kindly providing the barley accessions, Prof. Nils Stein (IPK-Gatersleben, Germany) for productive discussion, Prof. Rugen Xu (Yangzhou University, China) for providing BaYMV/BaMMV carrying soil, Ms. Haiying Guan (CAAS), Ms. Mary Ziems (IPK), Ms. Jelena Perovic (IPK) and Ms. Dörte Grau (JKI) for excellent technical support. This work was financially supported by National Key R&D Program of China (2018YFD1000702, 2018YFD1000700) to P. Yang and J. Liu, Fundamental Research Funds for Central Non-Profit of Institute of Crop Sciences of CAAS (S2018YC01, S2018PY04) and Agricultural Science and Technology Innovation Program of CAAS to P. Yang, and part of the collaborative project ‘‘Plant KBBE II-ViReCrop’’ by a Grant (FKZ 0315708) of the German Ministry of Education and Research (BMBF) to F. Ordon.

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  1. Lijie Shi and Congcong Jiang contributed equally to this work.

Authors and Affiliations

  1. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China

    Lijie Shi, Congcong Jiang, Qiang He, Jun Liu, Jing Zhang & Ping Yang

  2. Federal Research Centre for Cultivated Plants, Institute for Resistance Research and Stress Tolerance, Julius Kuehn-Institute (JKI), 06484, Quedlinburg, Germany

    Antje Habekuß & Frank Ordon

  3. College of Agronomy, Sichuan Agricultural University, Chengdu, 611130, China

    Lijie Shi & Zongyun Feng

  4. Institute of Agricultural Sciences of Coastal Area Jiangsu, Yancheng, 224002, China

    Haiye Luan & Huiquan Shen

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  1. Lijie Shi
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  2. Congcong Jiang
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Access to the BSR-seq reads data: https://www.ncbi.nlm.nih.gov/Traces/study/?acc=PRJNA514114.

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Suppl. Fig. 1

Snapshot of multiple alignment of eIF4EHOR3298 and other eIF4E haplotypes (TIFF 1608 kb)

Suppl. Fig. 2

The developed dCAPS marker (A) and KASP marker (B), which could be used for selection of the eIF4EHOR3298 allele in both homozygotes and heterozygotes. The allele discrimination of KASP marker was called after 35 cycles of amplification (JPEG 770 kb)

Suppl. Table 1

The primers used in this study (PDF 185 kb)

Suppl. Table 2

The diversity panel of 498 Chinese barley landraces/historical cultivars (PDF 402 kb)

Suppl. Table 3

Output of the BSR-seq in resistant and susceptible bulks of F2 segregants derived from ‘HOR3298’ x ‘W757/612’ (PDF 96 kb)

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Shi, L., Jiang, C., He, Q. et al. Bulked segregant RNA-sequencing (BSR-seq) identified a novel rare allele of eIF4E effective against multiple isolates of BaYMV/BaMMV. Theor Appl Genet 132, 1777–1788 (2019). https://doi.org/10.1007/s00122-019-03314-3

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