, 215:67 | Cite as

Response of Japanese wheat varieties to three pathotypes of wheat yellow mosaic virus

  • Hisayo KojimaEmail author
  • Takahide Sasaya
  • Koichi Hatta
  • Masako Seki
  • Shunsuke Oda
  • Chikako Kiribuchi-Otobe
  • Toshiyuki Takayama
  • Yumiko Fujita
  • Makiko Chono
  • Hitoshi Matsunaka
  • Zenta Nishio


Yellow mosaic disease, caused by wheat yellow mosaic virus (WYMV), is one of the most serious diseases of winter wheat (Triticum aestivum L.) in Japan. WYMV pathotype I is distributed mainly in western and central Japan, pathotype II in northern Japan, and pathotype III on a part of the southern island of Japan. Major resistance genes and quantitative trait loci for WYMV were previously identified on wheat chromosomes 2DL, 3BS, and 5AL. We evaluated a total of 165 modern Japanese wheat varieties, released by the Ministry of Agriculture, Forestry and Fisheries, for response to the three pathotypes in field trials, and genotyped them using microsatellite markers associated with the three WYMV resistance genes. Based on the data, we propose a model for the relationship between the three resistance genes and WYMV pathotypes. The results strongly suggest that the resistance conferred by the gene on 5AL has broken down with emergence of pathotype III, which may be derived from pathotype I.


Disease resistance Resistance breakdown ELISA test Triticum aestivum 



The authors are grateful to Dr. T. Ohki and Dr. O. Netsu for technical advice. We thank members of the Institute of Crop Science, NARO for technical assistance. This work was supported in part by ‘Development of Crop Production Technology for All Year Round Multi-utilization of Paddy Fields’ from the Ministry of Agriculture, Forestry and Fisheries, Japan and ‘Research Grant from NARO Gender Equality Program’.

Supplementary material

10681_2019_2387_MOESM1_ESM.xlsx (11 kb)
Supplementary material 1 (XLSX 10 kb)
10681_2019_2387_MOESM2_ESM.xlsx (28 kb)
Supplementary material 2 (XLSX 28 kb)


  1. Adams MJ (1991) The distribution of Barley Yellow Mosaic-Virus (BaYMV) and Barley Mild Mosaic-Virus (BaMMV) in UK winter barley samples, 1987–1990. Plant Pathol 40:53–58CrossRefGoogle Scholar
  2. Graner A, Bauer E (1993) RFLP mapping of the ym4 virus resistance gene in barley. Theor Appl Genet 86:689–693CrossRefGoogle Scholar
  3. 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 98:285–290CrossRefGoogle Scholar
  4. 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 156:36–41Google Scholar
  5. 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 84:627–630CrossRefGoogle Scholar
  6. Hariri D, Meyer M, Prud’homme H (2003) Characterization of a new barley mild mosaic virus pathotype in France. Eur J Plant Pathol 109:921–928CrossRefGoogle Scholar
  7. Inouye T (1969) Filamentous particles as the causal agent of yellow mosaic disease of wheat (cited in Namba et al. (1998) Arch Virol 143:631–643). Nogaku Kenkyu 53:61–68Google Scholar
  8. 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 149:1469–1480CrossRefGoogle Scholar
  9. 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 6:449–458CrossRefGoogle Scholar
  10. Kashiwazaki S, Ogawa K, Usugi T, Omura T, Tsuchizaki T (1989) Characterization of several strains of barley yellow mosaic virus. Ann Phytopathol Soc Jpn 55:16–25CrossRefGoogle Scholar
  11. 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 134:373–378CrossRefGoogle Scholar
  12. Kusume T, Tamada T, Hattori H, Tsuchiya T, Kubo K, Abe H, Namba S, Tsuchizaki T, Kishi K, Kasiwazaki S (1997) Identification of a new Wheat yellow mosaic virus strain with specific pathogenicity towards major wheat cultivars grown in Hokkaido. Ann Phytopathol Soc Jpn 63:107–109CrossRefGoogle Scholar
  13. Liu W, Nie H, Wang S, Li X, He Z, Han C, Wang J, Chen X, Li L, Yu J (2005) Mapping a resistance gene in wheat cultivar Yangfu 9311 to yellow mosaic virus, using microsatellite markers. Theor Appl Genet 111:651–657CrossRefGoogle Scholar
  14. Lu X, Kashiwazaki S, Tamura M, Namba S (1998) The 3’ terminal sequence of RNA1 of Wheat spindle streak mosaic virus Canadian isolate (WSSMV-C). Eur J Plant Pathol 104:765–768CrossRefGoogle Scholar
  15. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326CrossRefGoogle Scholar
  16. Namba S, Kashiwazaki S, Lu X, Tamura M, Tsuchizaki T (1998) Complete nucleotide sequence of Wheat yellow mosaic bymovirus genomic RNAs. Arch Virol 143:631–643CrossRefGoogle Scholar
  17. Netsu O, Ohki T, Kojima H, Oda S, Aoki E, Yoshioka T, Yanagisawa T, Ishikawa K, Sasaya T (2011) Development of serological diagnosis by ELISA for specific detection of four soil-borne viruses in wheat (Triticum aestivum) and barley (Hordeum vulgare). Proc Kanto Tosan Plant Prot Soc 58:13–17 (in Japanese) Google Scholar
  18. Nishio Z, Kojima H, Hayata A, Iriki N, Tabiki T, Ito M, Yamauchi H, Murray TM (2010) Mapping a gene conferring resistance to Wheat yellow mosaic virus in European winter wheat cultivar ‘Ibis’ (Triticum aestivum L.). Euphytica 176:223–229CrossRefGoogle Scholar
  19. Nolt BL, Romaine CP, Smith SH, Cole H Jr (1981) Further evidence for the association of Polymyxa graminis with the transmission of Wheat spindle streak mosaic virus. Phytopathology 71:1269–1272Google Scholar
  20. 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 104:313–319CrossRefGoogle Scholar
  21. Ohto Y (2005) Study on the ecology of wheat yellow mosaic disease. Bull Natl Agric Res Cent Tohoku Reg 104:17–74 (in Japanese) Google Scholar
  22. Ohto Y (2006) Studies on the pathotypes of Japanese isolates of Wheat yellow mosaic virus and their distribution in Japan. Bull Natl Agric Res Cent Tohoku Reg 105:73–96 (in Japanese) Google Scholar
  23. Ordon F, Perovic D (2013) Virus resistance in barley. In: Varshney RK, Tuberosa R (eds) Translational genomics for crop breeding, vol 1, 1st edn. Biotic Stresses, Wiley, pp 63–75CrossRefGoogle Scholar
  24. Ordon F, Ahlemeyer J, Werner K, Köhler W, Friedt W (2005) Molecular assessment of genetic diversity in winter barley and its use in breeding. Euphytica 146:21–28CrossRefGoogle Scholar
  25. Ordon F, Habekuss A, Kastirr U, Rabenstein F, Kühne T (2009) Virus resistance in cereals: sources of resistance, genetics and breeding. J Phytopathol 157:535–545CrossRefGoogle Scholar
  26. Paux E, Sourdille P, Salse J, Saintenac C, Choulet F, Leroy P, Korol A, Michalak M, Kiwanians S, Spielmeyer W, Lagudah E, Somers D, Kilian A, Alaux M, Vautrin S, Bergès H, Eversole K, Appels R, Safar J, Simkova H, Dolezel J, Bernard M, Feuillet C (2008) A physical map of the 1-gigabase bread wheat chromosome 3B. Science 322:101–104CrossRefGoogle Scholar
  27. Sawada E (1927) Control of wheat yellow mosaic virus (cited in Namba et al. (1998) Arch Virol 143:631–643). J Plant Prot 14:444–449Google Scholar
  28. Slykhuis JT, Barr DJS (1978) Confirmation of Polymyxa graminis as a vector of Wheat spindle streak mosaic virus. Phytopathology 68:639–643CrossRefGoogle Scholar
  29. Somers DJ, Isaac P (2004) SSRs from the wheat microsatellite consortium.
  30. Stein N, Perovic D, Kumlehn J, Pellio B, Stracke S, Ordon F, Graner A (2005) The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J 42:912–922CrossRefGoogle Scholar
  31. Steyer S, Kummert J, Froidmont F (1995) Characterization of a resistance-breaking BaYMV isolate from Belgium. Agronomie 15:433–438CrossRefGoogle Scholar
  32. Suzuki T, Nitta-Murai M, 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 128:1569–1578CrossRefGoogle Scholar
  33. 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 127:1625–1634CrossRefGoogle Scholar
  34. 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 111:2104–2109CrossRefGoogle Scholar
  35. 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 124:177–188CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Hisayo Kojima
    • 1
    • 2
    Email author
  • Takahide Sasaya
    • 3
  • Koichi Hatta
    • 4
  • Masako Seki
    • 5
  • Shunsuke Oda
    • 4
  • Chikako Kiribuchi-Otobe
    • 1
    • 2
  • Toshiyuki Takayama
    • 6
  • Yumiko Fujita
    • 1
  • Makiko Chono
    • 1
  • Hitoshi Matsunaka
    • 7
  • Zenta Nishio
    • 7
    • 8
  1. 1.Institute of Crop ScienceNAROTsukubaJapan
  2. 2.University of TsukubaTsukubaJapan
  3. 3.NARO HeadquartersTsukubaJapan
  4. 4.Hokkaido Agricultural Research CenterNAROMemuro, KasaiJapan
  5. 5.Central Region Agricultural Research CenterNAROJouetsuJapan
  6. 6.Tohoku Agricultural Research CenterNAROMoriokaJapan
  7. 7.Kyushu Okinawa Agricultural Research CenterNAROChikugoJapan
  8. 8.Tokyo University of AgricultureAtsugiJapan

Personalised recommendations