Abstract
Wheat blast, a devastating disease having spread recently from South America to Asia and Africa, is caused by Pyricularia oryzae (synonym of Magnaporthe oryzae) pathotype Triticum, which first emerged in Brazil in 1985. Rmg8 and Rmg7, genes for resistance to wheat blast found in common wheat and tetraploid wheat, respectively, recognize the same avirulence gene, AVR-Rmg8. Here we show that an ancestral resistance gene, which had obtained an ability to recognize AVR-Rmg8 before the differentiation of Triticum and Aegilops, has expanded its target pathogens. Molecular cloning revealed that Rmg7 was an allele of Pm4, a gene for resistance to wheat powdery mildew on 2AL, whereas Rmg8 was its homoeologue on 2BL ineffective against wheat powdery mildew. Rmg8 variants with the ability to recognize AVR-Rmg8 were distributed not only in Triticum spp. but also in Aegilops speltoides, Aegilops umbellulata and Aegilops comosa. This result suggests that the origin of resistance gene(s) recognizing AVR-Rmg8 dates back to the time before differentiation of A, B, S, U and M genomes, that is, ~5 Myr before the emergence of its current target, the wheat blast fungus. Phylogenetic analyses suggested that, in the evolutionary process thereafter, some of their variants gained the ability to recognize the wheat powdery mildew fungus and evolved into genes controlling dual resistance to wheat powdery mildew and wheat blast.
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Data availability
Sequence data were deposited in the GenBank/EMBL database under the accession numbers LC779671, LC779672, LC779673 and LC779674. All plasmids, plant lines and fungal strains used or generated in this work are available from the corresponding author upon request. The databases used in the present study were the reference genome of Chinese Spring (https://wheat-urgi.versailles.inra.fr/Seq-Repository/Assemblies) and the reference genome of T. durum cultivar Svevo (https://plants.ensembl.org/Triticum_turgidum /Info/Index). Source data are provided with this paper. Any additional data supporting the findings in the present study are available from the corresponding author upon request.
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Acknowledgements
We thank I. Chuma (Obihiro University of Agriculture and Veterinary Medicine, Japan), K. Nakajima (Mie Prefecture Agricultural Research Institute, Japan), A. Ohta (Kyoto University, Japan), K. Uchihashi (Hyogo Prefectural Technology Center for Agriculture, Japan), H. Tsujimoto (Tottori University, Japan) and T. Kataoka (National Agricultural Research Center for Kyushu Okinawa Region, Japan) for providing powdery-mildewed wheat leaves collected in fields. We also thank T. Islam (Bangabandhu Sheikh Mujibur Rahman Agricultural University, Bangladesh) for personal communication on field tests of Rmg8 carriers in his country and P. Nicholson (John Innes Centre, UK) for suggestions on the manuscript. Aegilops spp. accessions were provided by the National BioResource Project–Wheat with support in part by the National BioResource Project of the MEXT, Japan. Computations were partially performed on the NIG supercomputer owned by the National Institute of Genetics, Research Organization of Information and Systems. This research was supported by the research program on development of innovative technology grants (JPJ007097) from the project of the Bio-oriented Technology Research Advancement Institution (BRAIN) (provided for Y. Tosa); a grant from Agriculture, Forestry and Fisheries Research Council Secretariat (International collaborative research project for solving global issues); Ministry of Agriculture, Forestry and Fisheries (MAFF), Japan (provided for Y. Tosa); and Kobe University Strategic International Collaborative Research Grant (Type B Fostering Joint Research) (provided for S.A.).
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Contributions
K.M. performed molecular mapping and crossing of Aegilops accessions. M. Shimizu and R.T. selected transcripts of candidate genes. F.A. and M.K.-K. performed wheat transformation. C.N., Y. Takahashi, M. Shibata, M.Y., M.I., and Z.S. performed screening of germplasms and their molecular analyses. S.N., H.H., M.F., M.T., K.H., N.M., Y.M., and K.K. provided germplasms and scientific advice. S.A. performed the other experiments including the protoplast assay and summarized the data. S.A. and Y. Tosa designed the research and wrote the manuscript.
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Nature Plants thanks Tzion Fahima, Tofazzal Islam, Yinghui Li and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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Extended data
Extended Data Fig. 1 Search for Rmg8 candidate genes through association analyses of expressed genes with susceptible F2:3 lines.
a, An outline of screening of candidate genes. b, A list of Rmg8 candidate genes. NBS, Nucleotide-binding site; NLR, Nucleotide-binding site and leucine-rich repeat; RLK, Receptor-like kinase.
Extended Data Fig. 2 Reactions of T1 transformants carrying Rmg8-V1 and Rmg8-V2.
T1 individuals derived from transformation of Fielder with the Rmg8-V1 CDS (Fielder+Rmg8-V1) or with Rmg8-V2 CDS (Fielder+Rmg8-V2) were inoculated with Br48, Br48ΔA8, and Br48ΔA8+eI, and incubated for five days. Presence (+)/absence (-) of the transgene confirmed by PCR with the HPT primers are shown below the panels.
Extended Data Fig. 3 PCR products amplified with KM200 primers.
Genomic DNAs of common wheat (S-615, Sch) and tetraploid wheat (St24, Tat14) were subjected to amplification with KM200 primers, and resulting amplicons were run on a 2% gel for 30 min. The 424 bp fragment is amplified from both of the Rmg8 carrier and the Rmg7 carrier, but not from the noncarriers. The 350 bp fragment is amplified from all cultivars/accessions irrespective of their genotypes, and can be used as an indicator of successful PCR reactions.
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Supplementary Table 1.
Source data
Source Data Fig. 1a
Segregation data of the markers.
Source Data Fig. 1b
Unprocessed gel image.
Source Data Fig. 4
Sequence data of Rmg8 variants.
Source Data Extended Data Fig. 3
Unprocessed gel image.
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Asuke, S., Morita, K., Shimizu, M. et al. Evolution of wheat blast resistance gene Rmg8 accompanied by differentiation of variants recognizing the powdery mildew fungus. Nat. Plants 10, 971–983 (2024). https://doi.org/10.1038/s41477-024-01711-1
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DOI: https://doi.org/10.1038/s41477-024-01711-1
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