Abstract
Wheat resistance genes Rwt3 and Rwt4 constitute a host-specificity barrier against non-wheat pathotypes of the blast fungus, Pyricularia oryzae. To understand the origin of these host-specificity resistance genes, we examined their distribution in Aegilops tauschii, a wild wheat progenitor species with the D genome, using synthetic hexaploid lines derived from crosses between Triticum turgidum cv. Langdon and 54 Ae. tauschii accessions, which cover the native ranges and lineages of the species. Infection assays with transformants carrying their corresponding avirulence genes (PWT3 and PWT4) revealed different distribution patterns of the two resistance genes. Rwt3 was present in the TauL1 and TauL2 lineages with wider geographic distribution, while Rwt4 was mainly present in the TauL2 and TauL3 lineages with narrow geographic distribution. Rwt3 and Rwt4 co-occurred exclusively in a TauL2 sublineage that has been suggested to be a probable donor of the D genome to common wheat. This result suggests that Rwt3 and Rwt4 in common wheat is likely to have been derived from Ae. tauschii individual(s) carrying both genes and that the common ancestor of common wheat had both genes when it was established through amphidiploidization.
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References
Ayliffe M, Sørensen CK (2019) Plant nonhost resistance: paradigms and new environments. Curr Opin Plant Biol 50:104–113
Cook DE, Mesarich CH, Thomma BPHJ (2015) Understanding plant immunity as a surveillance system to detect invasion. Annu Rev Phytopathol 53:541–563
Cruz CD, Valent B (2017) Wheat blast disease: danger on the move. Trop Plant Pathol 42:210–222
de Vries S, Stukenbrock EH, Rose LE (2020) Rapid evolution in plant–microbe interactions—an evolutionary genomics perspective. New Phytol 226:1256–1262
Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548
Frantzeskakis L, Di Pietro A, Rep M, Schirawski J, Wu C-H, Panstruga R (2020) Rapid evolution in plant–microbe interactions—a molecular genomics perspective. New Phytol 225:1134–1142
Hirata K, Tosa Y, Nakayashiki H, Mayama S (2005) Significance of PWT4–Rwt4 interaction in the species specificity of Avena isolates of Magnaporthe oryzae on wheat. J Gen Plant Pathol 71:340–344
Inoue Y, Vy TTP, Yoshida K, Asano H, Mitsuoka C, Asuke S, Anh VL, Cumagun CJR, Chuma I, Terauchi R, Kato K, Mitchell T, Valent B, Farman M, Tosa Y (2017) Evolution of the wheat blast fungus through functional losses in a host specificity determinant. Science 357:80–83
Jones JDG, Vance RE, Dangl JL (2016) Intracellular innate immune surveillance devices in plants and animals. Science 354:aaf6395
Kajimura T, Murai K, Takumi S (2011) Distinct genetic regulation of flowering time and grain-filling period based on empirical study of D-genome diversity in synthetic hexaploid wheat lines. Breed Sci 61:130–141
Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of Triticum vulgare. Agric Hort 19:889–890 (in Japanese)
Kihara H, Lilienfeld F (1949) A new synthesized 6x-wheat. Proceedings of the 8th international congress of genetics. Hereditas, pp 307–319 (Supplement)
Matsuoka Y, Takumi S (2017) The role of reproductive isolation in allopolyploid speciation patterns: empirical insights from the progenitors of common wheat. Sci Rep 7:16004
Matsuoka Y, Takumi S, Kawahara T (2007) Natural variation for fertile triploid F1 hybrid formation in allohexaploid wheat speciation. Theor Appl Genet 115:509–518
Matsuoka Y, Nasuda S, Ashida Y, Nitta M, Tsujimoto H, Takumi S, Kawahara T (2013) Genetic basis for spontaneous hybrid genome doubling during allopolyploid speciation of common wheat shown by natural variation analyses of the paternal species. PLoS ONE 8:e68310
Matsuoka Y, Takumi S, Kawahara T (2015) Intraspecific lineage divergence and its association with reproductive trait change during species range expansion in central Eurasian wild wheat Aegilops tauschii Coss. (Poaceae). BMC Evol Biol 15:213
McFadden ES, Sears ER (1944) The artificial synthesis of Triticum spelta. Rec Genet Soc Am 13:26–27
Mizuno N, Yamasaki M, Matsuoka Y, Kawahara T, Takumi S (2010) Population structure of wild wheat D-genome progenitor Aegilops tauschii Coss.: implications for intraspecific lineage diversification and evolution of common wheat. Mol Ecol 19:999–1013
Nesbitt M, Samuel D (1996) From staple crop to extinction? The archaeology and history of hulled wheats. In: Padulosi S, Hammer K, Heller J (eds) Hulled wheats: promoting the conservation and use of underutilized and neglected crops. Int Plant Genet Resources Institute, Rome, pp 41–100
Nishijima R, Iehisa JCM, Matsuoka Y, Takumi S (2014) The cuticular wax inhibitor locus Iw2 in wild diploid wheat Aegilops tauschii: phenotypic survey, genetic analysis, and implications for the evolution of common wheat. BMC Plant Biol 14:246
Takabayashi N, Tosa Y, Oh HS, Mayama S (2002) A gene-for-gene relationship underlying the species-specific parasitism of Avena/Triticum isolates of Magnaporthe grisea on wheat cultivars. Phytopathology 92:1182–1188
Takumi S, Naka Y, Morihiro H, Matsuoka Y (2009) Expression of morphological and flowering time variation through allopolyploidization: an empirical study with 27 wheat synthetics and their parental Aegilops tauschii accessions. Plant Breed 128:585–590
Tsunewaki K (1966) Comparative gene analysis of common wheat and its ancestral species, II. Waxiness, growth habit and awnedness. Jpn J Bot 37:175–229
Van de Weyer A-L, Monteiro F, Furzer OJ, Nishimura MT, Cevik V, Witek K, Jones JDG, Dangl JL, Weigel D, Bemm F (2019) A species-wide inventory of NLR genes and alleles in Arabidopsis thaliana. Cell 178:1260-1272.e14
Vy TTP, Hyon G-S, Nga NTT, Inoue Y, Chuma I, Tosa Y (2014) Genetic analysis of host–pathogen incompatibility between Lolium isolates of Pyricularia oryzae and wheat. J Gen Plant Pathol 80:59–65
Acknowledgments
We express our sincere gratitude to Dr. S. Takumi, Kobe University, for providing the synthetic hexaploid lines and valuable suggestions. He was to be a coauthor of this article, but passed away before we started writing the manuscript. We also thank Dr. M. Moscou, The Sainsbury Laboratory, Norwich UK, for useful suggestions on the title of this article.
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Inoue, Y., Vy, T.T.P., Asuke, S. et al. Origin of host-specificity resistance genes of common wheat against non-adapted pathotypes of Pyricularia oryzae inferred from D-genome diversity in synthetic hexaploid wheat lines. J Gen Plant Pathol 87, 201–208 (2021). https://doi.org/10.1007/s10327-021-00990-2
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DOI: https://doi.org/10.1007/s10327-021-00990-2