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Bymovirus-induced yellow mosaic diseases in barley and wheat: viruses, genetic resistances and functional aspects

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Abstract

Bymovirus-induced yellow mosaic diseases seriously threaten global production of autumn-sown barley and wheat, which are two of the presently most important crops around the world. Under natural field conditions, the diseases are caused by infection of soil-borne plasmodiophorid Polymyxa graminis-transmitted bymoviruses of the genus Bymovirus of the family Potyviridae. Focusing on barley and wheat, this article summarizes the achievements on taxonomy, geography and host specificity of these disease-conferring viruses, as well as the genetics of resistance in barley, wheat and wild relatives. Moreover, based on recent progress of barley and wheat genomics, germplasm resources and large-scale sequencing, the exploration and isolation of corresponding resistant genes from wheat and barley as well as relatives, no matter what a large and complicated genome is present, are becoming feasible and are discussed. Furthermore, the foreseen advances on cloning of the resistance or susceptibility-encoding genes, which will provide the possibility to explore the functional interaction between host plants and soil-borne viral pathogens, are discussed as well as the benefits for marker-assisted resistance breeding in barley and wheat.

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References

  • Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M, Innan H, Cano L, Kamoun S, Terauchi R (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174–178

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Achon MA, Marsiñach M, Ratti C, Rubies-Autonell C (2005) First report of Barley yellow mosaic virus in barley in Spain. Plant Dis 89:105

    CAS  PubMed  Google Scholar 

  • Adams MJ, Swaby AG, Jones P (1988) Confirmation of the transmission of Barley yellow mosaic virus (BaYMV) by the fungus Polymyxa graminis. Ann Appl Biol 112:133–141

    Google Scholar 

  • Adams MJ, Jones DR, O’Neill TM, Hill SA (1993) The effect of cereal break crops on Barley mild mosaic virus. Ann Appl Biol 123:37–45

    Google Scholar 

  • Ahlawat Y, Majumdar A, Chenulu V (1976) First record of wheat spindle streak mosaic in India. Plant Dis Rep 60:782–783

    Google Scholar 

  • Andika IB, Zheng SL, Tan ZL, Sun LY, Kondo H, Zhou XP, Chen JP (2013) Endoplasmic reticulum export and vesicle formation of the movement protein of Chinese wheat mosaic virus are regulated by two transmembrane domains and depend on the secretory pathway. Virology 435:493–503

    CAS  PubMed  Google Scholar 

  • Arai Y, Yamaguchi M, Oyama M, Oozeki M, Sekiwa T, Sotome T, Kato T (2018) Evaluation of barley cultivars carrying rym1 to rym15 genes against Japanese BaYMV strains, and its utilization for resistant breeding. Bull Tochigi Agr Exp Stn 77:1–12

    Google Scholar 

  • Arora S, Steuernagel B, Gaurav K, Chandramohan S, Long Y, Matny O, Johnson R, Enk J, Periyannan S, Singh N, Asyraf MHM, Athiyannan N, Cheema J, Yu G, Kangara N, Ghosh S, Szabo LJ, Poland J, Bariana H, Jones JDG, Bentley AR, Ayliffe M, Olson E, Xu SS, Steffenson BJ, Lagudah E, Wulff BBH (2019) Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nat Biotechnol 37:139–143

    CAS  PubMed  Google Scholar 

  • Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H, Hale I, Mascher M, Spannagl M, Wiebe K, Jordan KW, Golan G, Deek J, Ben-Zvi B, Ben-Zvi G, Himmelbach A, MacLachlan RP, Sharpe AG, Fritz A, Ben-David R, Budak H, Fahima T, Korol A, Faris JD, Hernandez A, Mikel MA, Levy AA, Steffenson B, Maccaferri M, Tuberosa R, Cattivelli L, Faccioli P, Ceriotti A, Kashkush K, Pourkheirandish M, Komatsuda T, Eilam T, Sela H, Sharon A, Ohad N, Chamovitz DA, Mayer KFX, Stein N, Ronen G, Peleg Z, Pozniak CJ, Akhunov ED, Distelfeld A (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357:93–97

    CAS  PubMed  Google Scholar 

  • Bakardjieva N, Krasteva C, Habekuß A, Rabenstein F (2004) Detection of cereal viruses and study of aphid population in Bulgaria. Bulg J Agric Sci 10:161–164

    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

    CAS  Google Scholar 

  • Baulcombe D (2005) RNA silencing. Trends Biochem Sci 30:290–293

    CAS  PubMed  Google Scholar 

  • Beier S, Himmelbach A, Colmsee C, Zhang X-Q, Barrero RA, Zhang Q, Li L, Bayer M, Bolser D, Taudien S, Groth M, Felder M, Hastie A, Šimková H, Staňková H, Vrána J, Chan S, Muñoz-Amatriaín M, Ounit R, Wanamaker S, Schmutzer T, Aliyeva-Schnorr L, Grasso S, Tanskanen J, Sampath D, Heavens D, Cao S, Chapman B, Dai F, Han Y, Li H, Li X, Lin C, McCooke JK, Tan C, Wang S, Yin S, Zhou G, Poland JA, Bellgard MI, Houben A, Doležel J, Ayling S, Lonardi S, Langridge P, Muehlbauer GJ, Kersey P, Clark MD, Caccamo M, Schulman AH, Platzer M, Close TJ, Hansson M, Zhang G, Braumann I, Li C, Waugh R, Scholz U, Stein N, Mascher M (2017) Construction of a map-based reference genome sequence for barley, Hordeum vulgare L. Sci Data 4:170044

    CAS  PubMed  PubMed Central  Google Scholar 

  • Botticella E, Sestili F, Hernandez-Lopez A, Phillips A, Lafiandra D (2011) High resolution melting analysis for the detection of EMS induced mutations in wheat SBEIIa genes. BMC Plant Biol 11:156

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brakke MK, Estes AP, Schuster ML (1965) Transmission of Soil-borne wheat mosaic virus. Phytopathology 55:79–86

    Google Scholar 

  • Braselton JP (1995) Current status of the plasmodiophorids. Crit Rev Microbiol 21:263–275

    CAS  PubMed  Google Scholar 

  • Cadle-Davidson L, Bergstrom GC (2004) The effects of post planting environment on the incidence of soilborne viral diseases in winter cereals. Phytopathology 94:527–534

    CAS  PubMed  Google Scholar 

  • Cadle-Davidson L, Schindelbeck RR, van Es HM, Gray SM, Bergstrom GC (2003) Using air pressure cells to evaluate the effect of soil environment on the transmission of soilborne viruses of wheat. Phytopathol 93:1131–1136

    CAS  Google Scholar 

  • Caldwell DG, McCallum N, Shaw P, Muehlbauer GJ, Marshall DF, Waugh R (2004) A structured mutant population for forward and reverse genetics in Barley (Hordeum vulgare L.). Plant J 40:143–150

    CAS  PubMed  Google Scholar 

  • Campbell RN (1996) Fungal transmission of plant viruses. Annu Rev Phytopathol 34:87–108

    CAS  PubMed  Google Scholar 

  • Carrington JC, Jensen PE, Schaad MC (1998) Genetic evidence for an essential role for potyvirus CI protein in cell-to-cell movement. Plant J 14:393–400

    CAS  PubMed  Google Scholar 

  • Carroll JE, Bergstrom GC, Gray SM (2002) Assessing the resistance of winter wheat to wheat spindle streak mosaic bymovirus. Can J Plant Pathol 24:465–470

    Google Scholar 

  • Cartwright E, Rosnefl A, Peerenboorn E, Steinbiß H, Antoniw J, Adams M (1996) Barley mild mosaic virus: deletions, duplications and transmission. In: Proceedings of 3rd symposium of international working group of plant viruses with fungal vectors, Dundee, UK pp 9–12

  • Charron C, Nicolaï M, Gallois J-L, Robaglia C, Moury B, 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

    CAS  PubMed  Google Scholar 

  • Chen JP (1993) Occurrence of fungally transmitted wheat mosaic viruses in China. Ann Appl Biol 123:55–61

    Google Scholar 

  • Chen JP (2005) Progress and prospects of studies on Polymyxa graminis and its transmitted cereal viruses in China. Prog Nat Sci 15:481–490

    CAS  Google Scholar 

  • Chen JP, Ruan YL (1992) Research advance on Barley yellow mosaic viruses and their fungal vector Polymyxa graminis L. Virol Sin 7:1–10

    Google Scholar 

  • Chen JP, Adams M, Zhu F, 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 121:631–639

    Google Scholar 

  • Chen JP, Adams M, Zhu F, Wang Z, Chen J, Huang S, Zhang Z (1996) Response of foreign barley cultivars to Barley yellow mosaic virus at different sites in China. Plant Pathol 45:1117–1125

    Google Scholar 

  • Chen J, Sohn A, Chen JP, Lei J, Cheng Y, Schulze S, Steinbiss HH, Antoniw JF, Adams MJ (1999) Molecular comparisons amongst wheat bymovirus isolates from Asia, North America and Europe. Plant Pathol 48:642–647

    CAS  Google Scholar 

  • Chen L, Huang L, Min D, Phillips A, Wang S, Madgwick PJ, Parry MAJ, Hu YG (2012) Development and characterization of a new TILLING population of common bread wheat (Triticum aestivum L.). PLoS ONE 7:e41570

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen M, Sun L, Wu H, Chen J, Ma Y, Zhang X, Du L, Cheng S, Zhang B, Ye X, Pang J, Zhang X, Li L, Andika IB, Chen J, Xu H (2014) Durable field resistance to wheat yellow mosaic virus in transgenic wheat containing the antisense virus polymerase gene. Plant Biotechnol J 12:447–456

    CAS  PubMed  Google Scholar 

  • Colasuonno P, Incerti O, Lozito ML, Simeone R, Gadaleta A, Blanco A (2016) DHPLC technology for high-throughput detection of mutations in a durum wheat TILLING population. BMC Genet 17:43

    PubMed  PubMed Central  Google Scholar 

  • Colmsee C, Beier S, Himmelbach A, Schmutzer T, Stein N, Scholz U, Mascher M (2015) BARLEX: the barley draft genome explorer. Mol Plant 8:964–966

    CAS  PubMed  Google Scholar 

  • Dai K, Zhao R, Shi M, Xiao J, Yu Z, Jia Q, Wang Z, Yuan C, Sun H, Cao A, Zhang R, Chen P, Li Y, Wang H, Wang X (2020) Dissection and cytological mapping of chromosome arm 4VS by the development of wheat-Haynaldia villosa structural aberration library. Theor Appl Genet 133:217–226

    CAS  PubMed  Google Scholar 

  • Dessens JT, Meyer M (1995) Characterization of fungally and mechanically transmitted isolates of Barley mild mosaic virus: two strains in competition. Virology 212:383–391

    CAS  PubMed  Google Scholar 

  • Dessens JT, Nguyen M, Meyer M (1995) Primary structure and sequence analysis of RNA2 of a mechanically transmitted Barley mild mosaic virus isolate: an evolutionary relationship between bymo- and furoviruses. Arch Virol 140:325–333

    CAS  PubMed  Google Scholar 

  • Driskel BA, Hunger RM, Payton ME, Verchot-Lubicz J (2002) Response of hard red winter wheat to soilborne wheat mosaic virus using novel inoculation methods. Phytopathology 92:347–354

    PubMed  Google Scholar 

  • Elkot AFA, Chhuneja P, Kaur S, Saluja M, Keller B, Singh K (2015) Marker assisted transfer of two powdery mildew resistance genes PmTb7A.1 and PmTb7A.2 from Triticum boeoticum (Boiss.) to Triticum aestivum (L.). PLoS ONE 10:e0128297

    PubMed  PubMed Central  Google Scholar 

  • Erath W, Bauer E, Kastirr U, Schmidt M, Korzun V, Schmiedchen B, Wilde P, Schön CC (2016) Oligogenic control of resistance to soil-borne viruses SBCMV and WSSMV in rye (Secale cereale L.). Plant Breed 135:552–559

    CAS  Google Scholar 

  • Faccini N, Scudellari D, Stanca AM (2001) Characterization, diffusion and means of struggle: the virosis of barley in Emilia-Romagna. Inf Agrar 57:56–57

    Google Scholar 

  • Fatakhun A, Pavlenko L, Bobyr A (1987) The pathogen of Barley yellow mosaic virus in the Ukraine. Mikrobiol Z 49:76–80

    Google Scholar 

  • Foulds IJ, Lea VJ, Sidebottom C, James CM, Boulton RE, Brears T, Slabas AR, Jack PL, Stratford R (1993) Cloning and sequence analysis of the coat protein gene of Barley mild mosaic virus. Virus Res 27:79–89

    CAS  PubMed  Google Scholar 

  • Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323:1357–1360

    CAS  PubMed  PubMed Central  Google Scholar 

  • Furusho M, Baba T, Yamaguchi O, Yoshida T, Hamachi Y, Yoshikawa R, Mizuta K, Yoshino M (1999) Breeding of a new malting barley cultivar Houshun by the Bulbosum method. Breed Sci 49:281–284

    Google Scholar 

  • Gerechter-Amitai ZK, Wahl I, Vardi A, Zohary D (1971) Transfer of stem rust seedling resistance from wild diploid einkorn to tetraploid durum wheat by means of a triploid hybrid bridge. Euphytica 20:281–285

    Google Scholar 

  • Gottwald S, Bauer P, Komatsuda T, Lundqvist U, Stein N (2009) TILLING in the two-rowed barley cultivar ‘Barke’ reveals preferred sites of functional diversity in the gene HvHox1. BMC Res Notes 2:258

    PubMed  PubMed Central  Google Scholar 

  • Götz 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

    Google Scholar 

  • Graner A, Bauer E (1993) RFLP mapping of the Ym4 virus-resistance gene in barley. Theor Appl Genet 86:689–693

    CAS  PubMed  Google Scholar 

  • Graner A, Streng S, Kellermann A, Proeseler G, Schiemann A, Peterka H, Ordon F (1999a) Molecular mapping of genes conferring resistance to soil-borne viruses in barley: an approach to promote understanding of host-pathogen interactions. Z Pflanzenk Pflanzen 106:405–410

    CAS  Google Scholar 

  • Graner A, Streng S, Kellermann A, Schiemann A, Bauer E, Waugh R, Pellio B, Ordon F (1999b) 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

    CAS  Google Scholar 

  • Habekuß A, Kühne 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 

  • Han C, Li D, Xing Y, Zhu K, Tian Z, Cai Z, Yu J, Liu Y (2000) Wheat yellow mosaic virus widely occurring in wheat (Triticum aestivum) in China. Plant Dis 84:627–630

    PubMed  Google Scholar 

  • Hariri D, Courtillot M, Zaoui P, Lapierre H (1987) Multiplication of Soilborne wheat mosaic virus (SBWMV) in wheat roots infected by a soil carrying SBWMV and Wheat yellow mosaic virus (WYMV). Agronomie 7:789–796

    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

    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

    CAS  Google Scholar 

  • Hariri D, Gouis J, Ordon F, Adams M (2004) Cereals mosaic virus transmitted by Polymyxa graminis. Phytoma 41–45

  • Hibino H, Usugi T, Saito Y (1981) Comparative electron microscopy of inclusions associated with five soil-borne filamentous viruses of cereals. Ann Phytopathol Soc Jpn 47:510–519

    Google Scholar 

  • Hill SA, Evans EJ (1980) New or unusual records of plant diseases and pests: Barley yellow mosaic virus. Plant Pathol 29:197–199

    Google Scholar 

  • Hill SA, Walpole BJ (1989) National and local spread of Barley yellow mosaic virus in the United Kingdom. EPPO Bull 19:555–562

    Google Scholar 

  • Hipper C, Brault V, Ziegler-Graff V, Revers F (2013) Viral and cellular factors involved in phloem transport of plant viruses. Front Plant Sci 4:154

    PubMed  PubMed Central  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 

  • Holtz Y, Bonnefoy M, Viader V, Ardisson M, Rode NO, Poux G, Roumet P, Marie-Jeanne V, Ranwez V, Santoni S, Gouache D, David J (2017) Epistatic determinism of durum wheat resistance to the Wheat spindle streak mosaic virus. Theor Appl Genet 130:1491–1505

    PubMed  PubMed Central  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 

  • Huth W (2002) The soil-borne viruses of wheat and rye in Europe: an increasing problem but solvable by agronomic measures and cultivation of resistant varieties. Ges Pflanzen 54:51–57

    Google Scholar 

  • Huth W, Lesemann D-E (1978) One for the Federal Republic new virose of winter barley. Nachrichtenbl Dt Pflanzenschutzd 30:184–185

    Google Scholar 

  • Huth W, Lesemann DE, Paul HL (1984) Barley yellow mosaic virus: purification, electron microscopy, serology, and other properties of two types of the virus. J Phytopathol 111:37–54

    Google Scholar 

  • Huth W, Götz R, Lesemann DE (2007) Different types of resistance to soil-borne viruses of wheat. Ges Pflanzen 59:29–39

    Google Scholar 

  • Iida Y, Ban T, Konishi T (1999) Linkage analysis of the rym6 resistance gene to Japanese strain II of Barley yellow mosaic virus (BaYMV-II) in barley. Barley Genet Newsl 29:31–32

    Google Scholar 

  • Ikata S, Kawai I (1940) Studies on wheat yellow mosaic disease. Noji Kairyo Shiryo 154:1–123

    Google Scholar 

  • Inouye T (1969) Filamentous particles as the causal agent of yellow mosaic disease of wheat. Nogaku Kenkyu 53:61–68

    Google Scholar 

  • International Wheat Genome Sequencing Consortium (IWGSC) (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788

    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

    PubMed  Google Scholar 

  • Jeong W, Lee DY, Park S, Rhee SG (2008) ERp16, an endoplasmic reticulum-resident thiol-disulfide oxidoreductase—biochemical properties and role in apoptosis induced by endoplasmic reticulum stress. J Biol Chem 283:25557–25566

    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

    Google Scholar 

  • Jia J, Zhao S, Kong X, Li Y, Zhao G, He W, Appels R, Pfeifer M, Tao Y, Zhang X, Jing R, Zhang C, Ma Y, Gao L, Gao C, Spannagl M, Mayer KFX, Li D, Pan S, Zheng F, Hu Q, Xia X, Li J, Liang Q, Chen J, Wicker T, Gou C, Kuang H, He G, Luo Y, Keller B, Xia Q, Lu P, Wang J, Zou H, Zhang R, Xu J, Gao J, Middleton C, Quan Z, Liu G, Wang J, Yang H, Liu X, He Z, Mao L, Wang J, International Wheat Genome Sequencing C (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95

    CAS  PubMed  Google Scholar 

  • Jiang J, Laliberte JF (2011) The genome-linked protein VPg of plant viruses: a protein with many partners. Curr Opin Virol 1:347–354

    CAS  PubMed  Google Scholar 

  • Jiang S, Wu B, Jiang L, Zhang M, Lu Y, Wang S, Yan F, Xin X (2019) Triticum aestivum heat shock protein 23.6 interacts with the coat protein of wheat yellow mosaic virus. Virus Genes 55:209–217

    CAS  PubMed  Google Scholar 

  • Jo Y, Bae J-Y, Kim S-M, Choi H, Lee BC, Cho WK (2018) Barley RNA viromes in six different geographical regions in Korea. Sci Rep 8:13237

    PubMed  PubMed Central  Google Scholar 

  • Johnston PA, Timmerman-Vaughan GM, Farnden KJF, Pickering R (2009) Marker development and characterisation of Hordeum bulbosum introgression lines: a resource for barley improvement. Theor Appl Genet 118:1429–1437

    PubMed  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    CAS  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

    CAS  PubMed  Google Scholar 

  • Kang BC, Yeam I, Jahn MM (2005) Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621

    CAS  PubMed  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

    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

    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

    CAS  PubMed  Google Scholar 

  • Kapooria R, Ndunguru J, Clover GG (2000) First reports of Soilborne wheat mosaic virus and Wheat spindle streak mosaic virus in Africa. Plant Dis 84:921

    CAS  PubMed  Google Scholar 

  • Kashiwazaki S (1996) The complete nucleotide sequence and genome organization of Barley mild mosaic virus (Na1 strain). Arch Virol 141:2077–2089

    CAS  PubMed  Google Scholar 

  • Kashiwazaki S, Ogawa K, Usugi T, Omura T, Tsuchizaki T (1989) Characterization of several strains of Barley yellow mosaic virus. Ann Phytopathol Soc Jpn 55:16–25

    Google Scholar 

  • Katis N, Tzavella-Klonari K, Adams MJ (1997) Occurrence of barley yellow mosaic and barley mild mosaic bymoviruses in Greece. Eur J Plant Pathol 103:281–284

    Google Scholar 

  • Khan AA, Bergstrom GC, Nelson JC, Sorrells ME (2000) Identification of RFLP markers for resistance to wheat spindle streak mosaic bymovirus (WSSMV) disease. Genome 43:477–482

    CAS  PubMed  Google Scholar 

  • Kim HS, Baek SB, Kim DW, Hwang JJ, Kim SJ (2011) Evaluation and verification of barley genotypes with known genes for resistance to Barley yellow mosaic virus and Barley mild mosaic virus under field conditions in South Korea. Plant Pathol J 27:324–332

    Google Scholar 

  • Kojima H, Nishio Z, Kobayashi F, Saito M, Sasaya T, Kiribuchi-Otobe C, Seki M, Oda S, Nakamura T (2015) Identification and validation of a quantitative trait locus associated with Wheat yellow mosaic virus pathotype I resistance in a Japanese wheat variety. Plant Breed 134:373–378

    CAS  Google Scholar 

  • Konishi T, Ban T, Iida Y, Yoshimi R (1997) Genetic analysis of disease resistance to all strains of BaYMV in a Chinese barley landrace, Mokusekko 3. Theor Appl Genet 94:871–877

    Google Scholar 

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

    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

    PubMed  Google Scholar 

  • Kurowska M, Labocha-Pawłowska A, Gnizda D, Maluszynski M, Szarejko I (2012) Molecular analysis of point mutations in a barley genome exposed to MNU and gamma rays. Mutat Res 738–739:52–70

    PubMed  Google Scholar 

  • Langenberg WG (1985) Immunoelectron microscopy of Wheat spindle streak and Soil-borne wheat mosaic virus doubly infected wheat. J Ultrastruct Res 92:72–79

    Google Scholar 

  • Langenberg WG, Van Der Wal D (1986) Identification of Barley yellow mosaic virus by immuno-electron microscopy in barley but not in Polymyxa graminis or Lagena radicicola. Neth J Plant Pathol 92:133–136

    Google Scholar 

  • Le Gouis J, Devaux P, Werner K, Hariri D, Bahrman N, Beghin D, Ordon F (2004) rym15 from the Japanese cultivar Chikurin Ibaraki 1 is a new Barley mild mosaic virus (BaMMV) resistance gene mapped on chromosome 6H. Theor Appl Genet 108:1521–1525

    PubMed  Google Scholar 

  • Lee KJ, Choi MK, Lee WH, Rajkumar M (2006) Molecular analysis of Korean isolate of Barley yellow mosaic virus. Virus Genes 32:171–176

    PubMed  Google Scholar 

  • Li H, Shirako Y (2015) Association of VPg and eIF4E in the host tropism at the cellular level of Barley yellow mosaic virus and Wheat yellow mosaic virus in the genus Bymovirus. Virology 476:159–167

    CAS  PubMed  Google Scholar 

  • Li L, Yang X, Li X, Dong Y, Chen X (1998) Introduction of desirable genes from Agropyron cristatum into common wheat by intergeneric hybridization. Sci Agric Sin 31:1–5

    CAS  Google Scholar 

  • Li D, Yan L, Su N, Han C, Hou Z, Yu J, Liu Y (1999) The nucleotide sequence of a Chinese isolate of Wheat yellow mosaic virus and its comparison with a Japanese isolate. Arch Virol 144:2201–2206

    CAS  PubMed  Google Scholar 

  • Li H, Kondo H, Kühne T, Shirako Y (2016) Barley yellow mosaic virus VPg is the determinant protein for breaking eIF4E-mediated recessive resistance in barley plants. Front Plant Sci 7:1449

    PubMed  PubMed Central  Google Scholar 

  • Li L, Andika IB, Xu Y, Zhang Y, Xin X, Hu L, Sun Z, Hong G, Chen Y, Yan F, Yang J, Li J, Chen J (2017) Differential characteristics of viral siRNAs between leaves and roots of wheat plants naturally infected with Wheat yellow mosaic virus, a soil-borne virus. Front Microbiol 8:1802

    PubMed  PubMed Central  Google Scholar 

  • Ling H-Q, Zhao S, Liu D, Wang J, Sun H, Zhang C, Fan H, Li D, Dong L, Tao Y, Gao C, Wu H, Li Y, Cui Y, Guo X, Zheng S, Wang B, Yu K, Liang Q, Yang W, Lou X, Chen J, Feng M, Jian J, Zhang X, Luo G, Jiang Y, Liu J, Wang Z, Sha Y, Zhang B, Wu H, Tang D, Shen Q, Xue P, Zou S, Wang X, Liu X, Wang F, Yang Y, An X, Dong Z, Zhang K, Zhang X, Luo M-C, Dvorak J, Tong Y, Wang J, Yang H, Li Z, Wang D, Zhang A, Wang J (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496:87–90

    CAS  PubMed  Google Scholar 

  • Ling H-Q, Ma B, Shi X, Liu H, Dong L, Sun H, Cao Y, Gao Q, Zheng S, Li Y, Yu Y, Du H, Qi M, Li Y, Lu H, Yu H, Cui Y, Wang N, Chen C, Wu H, Zhao Y, Zhang J, Li Y, Zhou W, Zhang B, Hu W, van Eijk MJT, Tang J, Witsenboer HMA, Zhao S, Li Z, Zhang A, Wang D, Liang C (2018) Genome sequence of the progenitor of wheat A subgenome Triticum urartu. Nature 557:424–428

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu WH, Nie H, Wang SB, Li X, He ZT, Han CG, Wang JR, Chen XL, Li LH, Yu JL (2005a) Mapping a resistance gene in wheat cultivar Yangfu 9311 to yellow mosaic virus, using microsatellite markers. Theor Appl Genet 111:651–657

    CAS  PubMed  Google Scholar 

  • Liu WH, Nie H, He ZT, Chen XL, Han YP, Wang JR, Li X, Han CG, Yu JL (2005b) Mapping of a wheat resistance gene to yellow mosaic disease by amplified fragment length polymorphism and simple sequence repeat markers. J Integr Plant Biol 47:1133–1139

    CAS  Google Scholar 

  • Liu C, Suzuki T, Mishina K, Habekuss A, Ziegler A, Li C, Sakuma S, Chen G, Pourkheirandish M, Komatsuda T (2016) Wheat yellow mosaic virus resistance in wheat cultivar Madsen acts in roots but not in leaves. J Gen Plant Pathol 82:261–267

    CAS  Google Scholar 

  • Luo M-C, Gu YQ, Puiu D, Wang H, Twardziok SO, Deal KR, Huo N, Zhu T, Wang L, Wang Y, McGuire PE, Liu S, Long H, Ramasamy RK, Rodriguez JC, Van SL, Yuan L, Wang Z, Xia Z, Xiao L, Anderson OD, Ouyang S, Liang Y, Zimin AV, Pertea G, Qi P, Bennetzen JL, Dai X, Dawson MW, Müller H-G, Kugler K, Rivarola-Duarte L, Spannagl M, Mayer KFX, Lu F-H, Bevan MW, Leroy P, Li P, You FM, Sun Q, Liu Z, Lyons E, Wicker T, Salzberg SL, Devos KM, Dvořák J (2017) Genome sequence of the progenitor of the wheat D genome Aegilops tauschii. Nature 551:498–502

    CAS  PubMed  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

    PubMed  Google Scholar 

  • Maroquin C, Cavelier M, Rassel A (1982) First observations on barley mosaic virus in Belgium. Bull Rech Agron Gembloux 17:157–176

    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

    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 X-Q, Zhang Q, Barrero RA, Li L, Taudien S, Groth M, Felder M, Hastie A, Šimková H, Staňková H, Vrána J, Chan S, Muñoz-Amatriaín 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 S, Chapman B, Dai F, Han Y, Li H, Li X, Lin C, McCooke JK, Tan C, Wang P, Wang S, Yin S, Zhou G, Poland JA, Bellgard MI, Borisjuk L, Houben A, Doležel J, Ayling S, Lonardi S, Kersey P, Langridge P, Muehlbauer GJ, Clark MD, Caccamo M, Schulman AH, Mayer KFX, Platzer M, Close TJ, Scholz U, Hansson M, Zhang G, Braumann I, Spannagl M, Li C, Waugh R, Stein N (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427–433

    CAS  PubMed  Google Scholar 

  • Maule AJ (2008) Plasmodesmata: structure, function and biogenesis. Curr Opin Plant Biol 11:680–686

    CAS  PubMed  Google Scholar 

  • McKinney HH (1923) Investigations of the rosette disease of wheat and its control. J Agric Res 23:771–800

    Google Scholar 

  • McKinney HH, Eckerson SH, Webb RW (1923) The intracellular bodies associated with the rosette disease and a mosaic like leaf mottling of wheat. J Agric Res 26:605–608

    Google Scholar 

  • Miedaner T, Korzun V (2012) Marker-assisted selection for disease resistance in wheat and barley breeding. Phytopathology 102:560–566

    PubMed  Google Scholar 

  • Milner SG, Jost M, Taketa S, Mazón ER, Himmelbach A, Oppermann M, Weise S, Knüpffer H, Basterrechea M, König P, Schüler D, Sharma R, Pasam RK, Rutten T, Guo G, Xu D, Zhang J, Herren G, Müller T, Krattinger SG, Keller B, Jiang Y, González MY, Zhao Y, Habekuß A, Färber S, Ordon F, Lange M, Börner A, Graner A, Reif JC, Scholz U, Mascher M, Stein N (2019) Genebank genomics highlights the diversity of a global barley collection. Nat Genet 51:319–326

    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

    CAS  PubMed  Google Scholar 

  • Nishio Z, Kojima H, Hayata A, Iriki N, Tabiki T, Ito M, Yamauchi H, Murray TD (2010) Mapping a gene conferring resistance to Wheat yellow mosaic virus in European winter wheat cultivar ‘Ibis’ (Triticum aestivum L.). Euphytica 176:223–229

    CAS  Google Scholar 

  • Nissan-Azzouz F, Graner A, Friedt W, Ordon F (2005) Fine-mapping of the BaMMV, BaYMV-1 and BaYMV-2 resistance of barley (Hordeum vulgare) accession PI1963. Theor Appl Genet 110:212–218

    CAS  PubMed  Google Scholar 

  • Ohki T, Netsu O, Kojima H, Sakai J, Onuki M, Maoka T, Shirako Y, Sasaya T (2014) Biological and genetic diversity of Wheat yellow mosaic virus (Genus Bymovirus). Phytopathology 104:313–319

    CAS  PubMed  Google Scholar 

  • Ohki T, Sasaya T, Maoka T (2019) Cylindrical inclusion protein of Wheat yellow mosaic virus is involved in differential infection of wheat cultivars. Phytopathology 109:1475–1480

    PubMed  Google Scholar 

  • Ohto Y (2006) Studies on the pathotypes of Japanese isolates of Wheat yellow mosaic virus and their distribution in Japan. Bull Natl Agric Res Center Tohoku Reg 105:73–96

    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

    CAS  PubMed  Google Scholar 

  • Olivera PD, Rouse MN, Jin Y (2018) Identification of new sources of resistance to wheat stem rust in Aegilops spp. in the tertiary genepool of wheat. Front Plant Sci 9:1719

    PubMed  PubMed Central  Google Scholar 

  • Ordon F, Friedt W (1993) Mode of inheritance and genetic diversity of BaMMV resistance of exotic barley germplasms carrying genes different from Ym4. Theor Appl Genet 86:229–233

    CAS  PubMed  Google Scholar 

  • Ordon F, Perovic D (2013) Chapter 5: Virus resistance in barley. In: Varshney RK, Tuberosa R (eds) Translational genomics for crop breeding: biotic stress, vol 1, 1st edn. Wiley, Hoboken, pp 63–75

    Google Scholar 

  • Ordon F, Bauer E, Friedt W, Graner A (1995) Marker-based selection for the ym4 BaMMV-resistance gene in barley using RAPDs. Agronomie 15:481–485

    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

    CAS  Google Scholar 

  • Ordon F, Habekuß A, Kastirr U, Rabenstein F, Kühne T (2009) Virus resistance in cereals: sources of resistance, genetics and breeding. J Phytopathol 157:535–545

    Google Scholar 

  • Pankin A, Campoli C, Dong X, Kilian B, Sharma R, Himmelbach A, Saini R, Davis SJ, Stein N, Schneeberger K, von Korff M (2014) Mapping-by-sequencing identifies HvPHYTOCHROME C as a candidate gene for the early maturity 5 locus modulating the circadian clock and photoperiodic flowering in barley. Genetics 198:383–396

    PubMed  PubMed Central  Google Scholar 

  • Park J, Seo J, Kim Y, Kim J (2005) Occurrence of viral diseases in barley fields and responses of resistant genes to BaYMV-Ik and BaMMV. Korean J Crop Sci 50:197–204

    Google Scholar 

  • Pasquini M, Infantino A, Iori A, Rubies-Autonell C, Santori A, Vallega V (2006) Emerging wheat diseases: present situation in Italy. Inf Fitopatol 56:3–10

    Google Scholar 

  • Paull JG, Pallotta MA, Langridge P, The TT (1994) RFLP markers associated with Sr22 and recombination between chromosome 7A of bread wheat and the diploid species Triticum boeoticum. Theor Appl Genet 89:1039–1045

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Periyannan SK, Bansal UK, Bariana HS, Pumphrey M, Lagudah ES (2011) A robust molecular marker for the detection of shortened introgressed segment carrying the stem rust resistance gene Sr22 in common wheat. Theor Appl Genet 122:1–7

    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

    CAS  PubMed  Google Scholar 

  • Perovic D, Kopahnke D, Habekuß A, Ordon F, Serfling A (2019) Chapter 7: Marker-based harnessing of genetic diversity to improve resistance of barley to fungal and viral diseases. In: Miedaner T, Korzun V (eds) Applications of genetic and genomic research in cereals. Woodhead Publishing, Cambridge, pp 137–164

    Google Scholar 

  • Pfeifer M, Kugler KG, Sandve SR, Zhan B, Rudi H, Hvidsten TR, Mayer KF, Olsen OA (2014) Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345:1250091

    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

    Google Scholar 

  • Proeseler G, Stanarius A (1983) Nachweis des Weizenspindelstrichelmosaik-virus (Wheat spindle streak mosaic virus) in der DDR. Arch Phytopathol Pflanzensch 19:345–349

    Google Scholar 

  • Qi D, Innes RW (2013) Recent advances in plant NLR structure, function, localization, and signaling. Front Immunol 4:348

    PubMed  PubMed Central  Google Scholar 

  • Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, Davey M, Jacobs J, van Ex F, Pasha A, Khedikar Y, Robinson SJ, Cory AT, Florio T, Concia L, Juery C, Schoonbeek H, Steuernagel B, Xiang D, Ridout CJ, Chalhoub B, Mayer KFX, Benhamed M, Latrasse D, Bendahmane A, Wulff BBH, Appels R, Tiwari V, Datla R, Choulet F, Pozniak CJ, Provart NJ, Sharpe AG, Paux E, Spannagl M, Bräutigam A, Uauy C (2018) The transcriptional landscape of polyploid wheat. Science 361:eaar6089

    PubMed  Google Scholar 

  • Rawat N, Sehgal SK, Joshi A, Rothe N, Wilson DL, McGraw N, Vadlani PV, Li W, Gill BS (2012) A diploid wheat TILLING resource for wheat functional genomics. BMC Plant Biol 12:205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rawat N, Schoen A, Singh L, Mahlandt A, Wilson DL, Liu S, Lin G, Gill BS, Tiwari VK (2018) TILL-D: an Aegilops tauschii TILLING resource for wheat improvement. Front Plant Sci 9:1665

    PubMed  PubMed Central  Google Scholar 

  • Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45

    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

    PubMed  PubMed Central  Google Scholar 

  • Rotenberg D, Bockus WW, Whitfield AE, Hervey K, Baker KD, Ou Z, Laney AG, De Wolf ED, Appel JA (2016) Occurrence of viruses and associated grain yields of paired symptomatic and nonsymptomatic tillers in Kansas winter wheat fields. Phytopathology 106:202–210

    PubMed  Google Scholar 

  • Ruan YL, Jin DD, Xu RG, Gao DS, Feng ZJ, Ma YM (1984) The identification of resistance in barley varieties to the Barley yellow mosaic virus (BaYMV). Acta Phytophy Sin 11:217–222

    Google Scholar 

  • Rubies-Autonell C, Vallega V (1987) Observations on a mixed Soil-borne wheat mosaic virus and Wheat spindle streak mosaic virus infection in durum wheat (Triticum durum Desf). J Phytopathol 119:111–121

    Google Scholar 

  • Ruge B, Linz A, Pickering R, Proeseler G, Greif P, Wehling P (2003) Mapping of Rym14Hb, a gene introgressed from Hordeum bulbosum and conferring resistance to BaMMV and BaYMV in barley. Theor Appl Genet 107:965–971

    CAS  PubMed  Google Scholar 

  • Ruge-Wehling B, Linz A, Habekuß A, Wehling P (2006) Mapping of Rym16Hb, the second soil-borne virus-resistance gene introgressed from Hordeum bulbosum. Theor Appl Genet 113:867–873

    CAS  PubMed  Google Scholar 

  • Saeki K, Miyazaki C, Hirota N, Saito A, Ito K, Konishi T (1999) RFLP mapping of BaYMV resistance gene rym3 in barley (Hordeum vulgare). Theor Appl Genet 99:727–732

    CAS  PubMed  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

    PubMed  PubMed Central  Google Scholar 

  • Schenk P, Steinbiß H-H, Müller B, Schmitz K (1993) Association of two Barley yellow mosaic virus (RNA 2) encoded proteins with cytoplasmic inclusion bodies revealed by immunogold localisation. Protoplasma 173:113–122

    CAS  Google Scholar 

  • Schlichter U, Sohn A, Peerenboom E, Schell J, Steinbiß HH (1993) Molecular analysis of the capsid protein gene of a German isolate of Barley mild mosaic virus. Plant Cell Rep 12:237–240

    CAS  PubMed  Google Scholar 

  • Schoelz JE, Harries PA, Nelson RS (2011) Intracellular transport of plant viruses: finding the door out of the cell. Mol Plant 4:813–831

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sears RG, Martin TJ, McCluskey PJ, Paulsen GM, Heer WF, Long JH, Witt MD, Brown-Guedira G (2001a) Registration of ‘Betty’ wheat. Crop Sci 41:1366–1367

    Google Scholar 

  • Sears RG, Martin TJ, McCluskey PJ, Paulsen GM, Heer WF, Long JH, Witt MD, Brown-Guedira G (2001b) Registration of ‘Heyne’ wheat. Crop Sci 41:1367

    Google Scholar 

  • Shi LJ, Jiang CC, He Q, Habekuß A, Ordon F, Luan HY, Shen HQ, Liu J, Feng ZY, Zhang J, Yang P (2019) 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

    CAS  PubMed  Google Scholar 

  • Signoret PA, Alliot B, Poinso B (1977) Presence en France du WSSMV. Ann Phytopathol 9:377–379

    Google Scholar 

  • Slade AJ, Fuerstenberg SI, Loeffler D, Steine MN, Facciotti D (2005) A reverse genetic, nontransgenic approach to wheat crop improvement by TILLING. Nat Biotechnol 23:75–81

    CAS  PubMed  Google Scholar 

  • Slykhuis J (1960) Evidence of soil-borne mosaic of wheat in Ontario. Can J Plant Dis Surv 40:43

    Google Scholar 

  • Sorrells ME, Benscher D, Bergstrom GC (2004) Registration of ‘Richland’ wheat. Crop Sci 44:1472–1473

    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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sun LY, Jing B, Andika IB, Hu YC, Sun BJ, Xiang R, Kondo H, Chen JP (2013) Nucleo-cytoplasmic shuttling of VPg encoded by Wheat yellow mosaic virus requires association with the coat protein. J Gen Virol 94:2790–2802

    CAS  PubMed  Google Scholar 

  • Sun L, Andika IB, Shen J, Yang D, Chen J (2014) The P2 of Wheat yellow mosaic virus rearranges the endoplasmic reticulum and recruits other viral proteins into replication-associated inclusion bodies. Mol Plant Pathol 15:466–478

    CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki T, Murai MN, Hayashi T, Nasuda S, Yoshimura Y, Komatsuda T (2015) Resistance to Wheat yellow mosaic virus in Madsen wheat is controlled by two major complementary QTLs. Theor Appl Genet 128:1569–1578

    CAS  PubMed  Google Scholar 

  • Szunics L, Pocsai E, Szunics L, Vida G (1989) Viral diseases on cereals in central Hungary. Acta Agron Hung 48:237–250

    Google Scholar 

  • Szurman-Zubrzycka ME, Zbieszczyk J, Marzec M, Jelonek J, Chmielewska B, Kurowska MM, Krok M, Daszkowska-Golec A, Guzy-Wrobelska J, Gruszka D, Gajecka M, Gajewska P, Stolarek M, Tylec P, Sega P, Lip S, Kudełko M, Lorek M, Gorniak-Walas M, Malolepszy A, Podsiadlo N, Szyrajew KP, Keisa A, Mbambo Z, Todorowska E, Gaj M, Nita Z, Orlowska-Job W, Maluszynski M, Szarejko I (2018) HorTILLUS: a rich and renewable source of induced mutations for forward/reverse genetics and pre-breeding programs in barley (Hordeum vulgare L.). Front Plant Sci 9:216

    PubMed  PubMed Central  Google Scholar 

  • Takagi H, Oli MT, Abe A, Yoshida K, Uemura A, Yaegashi H, Obara T, Oikawa K, Utsushi H, Kanzaki E, Mitsuoka C, Natsume S, Kosugi S, Kanzaki H, Matsumura H, Urasaki N, Kamoun S, Terauchi R (2015) MutMap accelerates breeding of a salt-tolerant rice cultivar. Nat Biotechnol 33:445–449

    CAS  PubMed  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 16:1–17

    Google Scholar 

  • Takata K, Kai H, Uchimura Y, Tsukazaki M, Furusho M, Baba T (2012) Selection of DNA markers closely linked to the resistance gene rym7t against Barley yellow mosaic disease. Breed Res 14:43–49

    Google Scholar 

  • Talamè V, Bovina R, Sanguineti MC, Tuberosa R, Lundqvist U, Salvi S (2008) TILLMore, a resource for the discovery of chemically induced mutants in barley. Plant Biotechnol J 6:477–485

    PubMed  Google Scholar 

  • The TT (1973) Chromosome location of genes conditioning stem rust resistance transferred from diploid to hexaploid wheat. Nat New Biol 241:256

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Timpe U, Kühne T (1994) The complete nucleotide sequence of RNA2 of Barley mild mosaic virus (BaMMV). Eur J Plant Pathol 100:233–241

    CAS  Google Scholar 

  • Tiwari VK, Wang S, Danilova T, Koo DH, Vrána J, Kubaláková M, Hribova E, Rawat N, Kalia B, Singh N, Friebe B, Doležel J, Akhunov E, Poland J, Sabir JSM, Gill BS (2015) Exploring the tertiary gene pool of bread wheat: sequence assembly and analysis of chromosome 5 Mg of Aegilops geniculata. Plant J 84:733–746

    CAS  PubMed  Google Scholar 

  • Uauy C, Paraiso F, Colasuonno P, Tran RK, Tsai H, Berardi S, Comai L, Dubcovsky J (2009) A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biol 9:115

    PubMed  PubMed Central  Google Scholar 

  • Uauy C, Wulff BBH, Dubcovsky J (2017) Combining traditional mutagenesis with new high-throughput sequencing and genome editing to reveal hidden variation in polyploid wheat. Annu Rev Genet 51:435–454

    CAS  PubMed  Google Scholar 

  • Vaianopoulos C, Legreve A, Lorca C, Moreau V, Steyer S, Maraite H, Bragard C (2006) Widespread occurrence of Wheat spindle streak mosaic virus in Belgium. Plant Dis 90:723–728

    CAS  PubMed  Google Scholar 

  • Verchot J, Driskel BA, Zhu Y, Hunger RM, Littlefield LJ (2001) Evidence that Soilborne wheat mosaic virus moves long distance through the xylem in wheat. Protoplasma 218:57–66

    CAS  PubMed  Google Scholar 

  • Wang AM (2015) Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Annu Rev Phytopathol 53:45–66

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Tang S, Zhan Q, Hou Q, Zhao Y, Zhao Q, Feng Q, Zhou C, Lyu D, Cui L, Li Y, Miao J, Zhu C, Lu Y, Wang Y, Wang Z, Zhu J, Shangguan Y, Gong J, Yang S, Wang W, Zhang J, Xie H, Huang X, Han B (2019) Dissecting a heterotic gene through GradedPool-Seq mapping informs a rice-improvement strategy. Nat Commun 10:2982

    PubMed  PubMed Central  Google Scholar 

  • Wei TY, Zhang CW, Hong JA, Xiong RY, Kasschau KD, Zhou XP, Carrington JC, Wang AM (2010) Formation of complexes at plasmodesmata for Potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Pathol 6:e1000962

    Google Scholar 

  • Wendler N, Mascher M, Nöh C, Himmelbach A, Scholz U, Ruge-Wehling B, Stein N (2014) Unlocking the secondary gene-pool of barley with next-generation sequencing. Plant Biotechnol J 12:1122–1131

    CAS  PubMed  Google Scholar 

  • Wendler N, Mascher M, Himmelbach A, Johnston P, Pickering R, Stein N (2015) Bulbosum to Go: a toolbox to utilize Hordeum vulgare/bulbosum introgressions for breeding and beyond. Mol Plant 8:1507–1519

    CAS  PubMed  Google Scholar 

  • Werner K, Friedt W, Laubach E, Waugh R, Ordon F (2003a) Dissection of resistance to soil-borne yellow-mosaic-inducing viruses of barley (BaMMV, BaYMV, BaYMV-2) in a complex breeders’ cross by means of SSRs and simultaneous mapping of BaYMV/BaYMV-2 resistance of var. ‘Chikurin Ibaraki 1’. Theor Appl Genet 106:1425–1432

    CAS  PubMed  Google Scholar 

  • Werner K, Rönicke S, Le Gouis J, Friedt W, Ordon F (2003b) Mapping of a new BaMMV-resistance gene derived from the variety ‘Taihoku A’. J Plant Dis Prot 110(3):304–311

    CAS  Google Scholar 

  • Werner K, Friedt W, Ordon F (2005) Strategies for pyramiding resistance genes against the Barley yellow mosaic virus complex (BaMMV, BaYMV, BaYMV-2). Mol Breed 16:45–55

    CAS  Google Scholar 

  • Wicker T, Schulman AH, Tanskanen J, Spannagl M, Twardziok S, Mascher M, Springer NM, Li Q, Waugh R, Li C, Zhang G, Stein N, Mayer KFX, Gundlach H (2017) The repetitive landscape of the 5100 Mbp barley genome. Mob DNA 8:22

    PubMed  PubMed Central  Google Scholar 

  • Wiese M, Shari E, Clayton J, Ellingboe A (1970) Occurrence of wheat streak mosaic and a new variegation disorder, wheat spindle streak mosaic, in Michigan wheat. Plant Dis Rep 54:635–637

    Google Scholar 

  • Winfield MO, Allen AM, Burridge AJ, Barker GLA, Benbow HR, Wilkinson PA, Coghill J, Waterfall C, Davassi A, Scopes G, Pirani A, Webster T, Brew F, Bloor C, King J, West C, Griffiths S, King I, Bentley AR, Edwards KJ (2016) High-density SNP genotyping array for hexaploid wheat and its secondary and tertiary gene pool. Plant Biotechnol J 14:1195–1206

    CAS  PubMed  Google Scholar 

  • Wu J, Yang XM, Wang H, Li HJ, Li LH, Li XQ, Liu WH (2006) The introgression of chromosome 6P specifying for increased numbers of florets and kernels from Agropyron cristatum into wheat. Theor Appl Genet 114:13–20

    CAS  PubMed  Google Scholar 

  • Xie L, Song XJ, Liao ZF, Wu B, Yang J, Zhang H, Hong J (2019) Endoplasmic reticulum remodeling induced by Wheat yellow mosaic virus infection studied by transmission electron microscopy. Micron 120:80–90

    CAS  PubMed  Google Scholar 

  • Xu Y, Hu L, Li L, Zhang Y, Sun B, Meng X, Zhu T, Sun Z, Hong G, Chen Y, Yan F, Yang J, Li J, Chen J (2018) Ribotypes of polymyxa graminis in wheat samples infected with soilborne wheat viruses in China. Plant Dis 102:948–954

    CAS  PubMed  Google Scholar 

  • Yan F, Sun L, Shang Y, Chen J (2013) Occurrence of cereal viral diseases and their control in China. Plant Prot 39:33–37

    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

    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

    PubMed  Google Scholar 

  • Yang P, Lüpken 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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • You Y, Shirako Y (2010) Bymovirus reverse genetics: requirements for RNA2-encoded proteins in systemic infection. Mol Plant Pathol 11:383–394

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang C, Machray GC, Cruz SS, Wilson TMA (2005a) Soil-borne wheat mosaic virus (SBWMV) 37 kDa protein rescues cell-to-cell and long-distance movement of an immobile tobacco mosaic virus mutant in Nicotiana benthamiana, a non-host of SBWMV. J Phytopathol 153:5–10

    CAS  Google Scholar 

  • Zhang QP, Li Q, Wang X, Wang HY, Lang SP, Wang YN, Wang SL, Chen PD, Liu DJ (2005b) Development and characterization of a Triticum aestivum-Haynaldia villosa translocation line T4VS 4DL conferring resistance to Wheat spindle streak mosaic virus. Euphytica 145:317–320

    CAS  Google Scholar 

  • Zhao RH, Wang HY, Xiao J, Bie TD, Cheng SH, Jia Q, Yuan CX, Zhang RQ, Cao AZ, Chen PD, Wang X (2013) Induction of 4VS chromosome recombinants using the CS ph1b mutant and mapping of the Wheat yellow mosaic virus resistance gene from Haynaldia villosa. Theor Appl Genet 126:2921–2930

    CAS  PubMed  Google Scholar 

  • Zhao G, Zou C, Li K, Wang K, Li T, Gao L, Zhang X, Wang H, Yang Z, Liu X, Jiang W, Mao L, Kong X, Jiao Y, Jia J (2017) The Aegilops tauschii genome reveals multiple impacts of transposons. Nat Plant 3:946–955

    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

    CAS  Google Scholar 

  • Zhou X, Cao M (1985) Screening tests of barley cultivars for resistance to Barley yellow mosaic virus. Acta Phytophy Sin 12:217–223

    Google Scholar 

  • Zhu X, Wang H, Guo J, Wu Z, Cao A, Bie T, Nie M, You FM, Cheng Z, Xiao J, Liu Y, Cheng S, Chen P, Wang X (2012) Mapping and validation of quantitative trait loci associated with wheat yellow mosaic Bymovirus resistance in bread wheat. Theor Appl Genet 124:177–188

    PubMed  Google Scholar 

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Acknowledgements

We apologize to the researchers whose related work was not mentioned here due to the space constraints. The authors thank the handling editor Dr. T. Komatsuda (National Institute of Agrobiological Sciences, Japan) for reproductive comments, Dr. H. Luan from Yancheng Institute of Agricultural Science in Jiangsu, China, and Dr. A. Ziegler from Julius Kühn-Institute (JKI) in Germany for kindly providing photographs with diseased symptom. The authors gratefully thank three anonymous reviewers for many valuable comments. This work was financially supported by National Key R&D Program of China to P. Yang and J. Kan (Grant: 2018YFD1000703/2018YFD1000700), Fundamental Research Funds for Central Non-Profit of Institute of Crop Sciences of CAAS (Grant: S2018PY04) and Agricultural Science and Technology Innovation Program of CAAS to P. Yang, and China Postdoctoral Science Foundation to C. Jiang (Grant: 2018M631643).

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Author notes

  1. Congcong Jiang and Jinhong Kan contributed equally to this work.

Authors and Affiliations

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

    Congcong Jiang, Jinhong Kan & Ping Yang

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

    Frank Ordon & Dragan Perovic

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  1. Congcong Jiang
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  2. Jinhong Kan
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  3. Frank Ordon
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  4. Dragan Perovic
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  5. Ping Yang
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Contributions

PY conceived the ideas, CJ, JK and PY compiled the literature sources and wrote the manuscript, and FO and DP contributed to checking genetic data, critical reading and language editing.

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Correspondence to Ping Yang.

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Jiang, C., Kan, J., Ordon, F. et al. Bymovirus-induced yellow mosaic diseases in barley and wheat: viruses, genetic resistances and functional aspects. Theor Appl Genet 133, 1623–1640 (2020). https://doi.org/10.1007/s00122-020-03555-7

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