Kohei Machines, Takako Suzuki https://orcid.org/0000-0002-8325-5791, Youko Six https://orcid.org/0000-0003-3575-4059, Yoko Yamashita https://orcid.org/0000-0003-2510-4220, Hongjing Zhu https://orcid.org/0000-0002-4794-2340, Taiichi Ogawa https://orcid.org/0000-0002-7635-6594, Masaru Ohta https://orcid.org/0000-0003-2384-0320, Kohei tomorrow https://orcid.org/0000-0003-1827-2445, Wenjing Xu https://orcid.org/0000-0002-9240-8120, Daichi Takahashi https://orcid.org/0000-0003-2118-5318, Taiga Miyazaki, Akemi Tagiri https://orcid.org/0000-0002-6445-2335, Chihiro Soma https://orcid.org/0000-0001-6943-047X, Harukuni Octopus https://orcid.org/0000-0001-8003-3731, Shuhei Nasuda https://orcid.org/0000-0002-9019-8692, Romain de oliveira https://orcid.org/0000-0003-0017-6308, Stephen Paul https://orcid.org/0000-0002-3094-7129, Guoxiong Chen https://orcid.org/0000-0002-3687-4012, Mohammad Pourkheirandish https://orcid.org/0000-0003-4337-3600, Jianzhong Wu https://orcid.org/0000-0002-4033-852X, Cheng Liu https://orcid.org/0000-0003-3354-8817 [email protected]and Takao Komatsuda https://orcid.org/0000-0001-8195-249X [email protected]Authors Info & Affiliations
Edited by David Baulcombe, University of Cambridge, Cambridge, United Kingdom; received September 5, 2022; accepted January 30, 2023
March 10, 2023
120 (11) e2214968120
Significance
The infection with Wheat yellow mosaic virus causes significant economic loss in yield globally, but the basis of genetic resistance to this virus is poorly understood. We report the isolation of the resistance gene Ym2 using a positional cloning approach, supported by transgenic complementation. A sequence analysis across related species suggests that Ym2 was inherited not from Aegilops speltoides (a species closely related to the donor of the bread wheat B genome), but rather from the more distant relativeAegilops sharonensis. The analysis has provided novel information as to how the Ym2 region arose during the course of the evolution of cultivated wheat.
Abstract
Wheat yellow mosaic virus (WYMV) is a pathogen transmitted into its host’s roots by the soil-borne vector Polymyxa grass. Ym1 and Ym2 genes protect the host from the significant yield losses caused by the virus, but the mechanistic basis of these resistance genes remains poorly understood. Here, it has been shown that Ym1 and Ym2 act within the root either by hindering the initial movement of WYMV from the vector into the root and/or by suppressing viral multiplication. A mechanical inoculation experiment on the leaf revealed that the presence of Ym1 reduced viral infection incidence, rather than viral titer, while that of Ym2 was ineffective in the leaf. To understand the basis of the root specificity of the Ym2 product, the gene was isolated from bread wheat using a positional cloning approach. The candidate gene encodes a CC-NBS-LRR protein and it correlated allelic variation with respect to its sequence with the host’s disease response. Ym2 (B37500) and its paralog (B35800) are found in the near-relatives, respectively, Aegilops sharonensiss andAegilops speltoides (a close relative of the donor of bread wheat’s B genome), while both sequences, in a concatenated state, are present in several accessions of the latter species. Structural diversity in Ym2 has been generated via translocation and recombination between the two genes and enhanced by the formation of a chimeric gene resulting from an intralocus recombination event. The analysis has revealed how the Ym2 region has evolved during the polyploidization events leading to the creation of cultivated wheat.
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Data, Materials, and Software Availability
All data are available in the manuscript, the supplementary materials, or at publicly accessible repositories. These data in the public repositories include sequence data of BACs for cv. Hokushin LC709268 to LC709270 and for cv. Madsen LC709271 to LC709274; RNA-seq BioProject PRJDB13850 (Runs DRR391476 to DRR391486); Ym2 genome LC717504, transcript LC717505 and Ym2 paralogous 3B35800 genome LC717506; Bobwhite S26 genes LC742127 to LC742130; WYMV RNAs LC718993 to LC718996; variation at Ym2 in wheat varieties LC651679 to LC651777.
Acknowledgments
We thank Robert McIntosh (University of Sydney) for editing the manuscript. This research was financially supported by Genomics for Agricultural Innovation Program of the Ministry of Agriculture, Forestry and Fisheries (MAFF) of Japan Grant TRS1003 (to T.S., J.W. and T.K.); Innovation Program 2021 and 2022 of the National Agriculture and Food Research Organization (NARO) (to Y.O.); Youth Taishan Scholar Project of Shandong Province tsqn201812123 (to C.L.); Double Hundred Talent Program of Department of Science & Technology of Shandong Province WST2020012 (to. T.K.); and Leading Talent Research Startup Fee of Shandong Academy of Agricultural Sciences CXGC2021B01 (to. T.K.).
Author contributions
K.M., T.S., J.W., G.C., M.P., C.L., and T.K. designed research; K.M., T.S., Y.O., Y.Y., H.Z., T.O., M.O., K.D., W.X., D.T., T.M., A.T., C.S., H.H., S.N., R.D.O., E.P., G.C., J.W., C.L., and T.K. performed research; K.M. and T.K. analyzed data; and K.M., W.X., G.C., M.P., C.L., and T.K. wrote the paper.
Competing interests
The authors declare no competing interest.
Supporting Information
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Information & Authors
Information
Published in
Proceedings of the National Academy of Sciences
Vol. 120 | No. 11
March 14, 2023
Classifications
Copyright
Data, Materials, and Software Availability
All data are available in the manuscript, the supplementary materials, or at publicly accessible repositories. These data in the public repositories include sequence data of BACs for cv. Hokushin LC709268 to LC709270 and for cv. Madsen LC709271 to LC709274; RNA-seq BioProject PRJDB13850 (Runs DRR391476 to DRR391486); Ym2 genome LC717504, transcript LC717505 and Ym2 paralogous 3B35800 genome LC717506; Bobwhite S26 genes LC742127 to LC742130; WYMV RNAs LC718993 to LC718996; variation at Ym2 in wheat varieties LC651679 to LC651777.
Submission history
Received: September 5, 2022
Accepted: January 30, 2023
Published online: March 10, 2023
Published in issue: March 14, 2023
Keywords
- molecular evolution
- recombination
- wild relatives
- plant breeding
- Bymovirus
Acknowledgments
We thank Robert McIntosh (University of Sydney) for editing the manuscript. This research was financially supported by Genomics for Agricultural Innovation Program of the Ministry of Agriculture, Forestry and Fisheries (MAFF) of Japan Grant TRS1003 (to T.S., J.W. and T.K.); Innovation Program 2021 and 2022 of the National Agriculture and Food Research Organization (NARO) (to Y.O.); Youth Taishan Scholar Project of Shandong Province tsqn201812123 (to C.L.); Double Hundred Talent Program of Department of Science & Technology of Shandong Province WST2020012 (to. T.K.); and Leading Talent Research Startup Fee of Shandong Academy of Agricultural Sciences CXGC2021B01 (to. T.K.).
Author Contributions
K.M., T.S., J.W., G.C., M.P., C.L., and T.K. designed research; K.M., T.S., Y.O., Y.Y., H.Z., T.O., M.O., K.D., W.X., D.T., T.M., A.T., C.S., H.H., S.N., R.D.O., E.P., G.C., J.W., C.L., and T.K. performed research; K.M. and T.K. analyzed data; and K.M., W.X., G.C., M.P., C.L., and T.K. wrote the paper.
Competing Inter ests
The authors declare no competing interest.
Notes
This article is a PNAS Direct Submission.
Authors
Affiliations
Kohei Machines
Institute of Crop Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan
Hokkaido Research Organization, Agricultural Research Department, Chuo Agricultural Experiment Station, Naganuma, Hokkaido 069-1395, Japan
Institute of Crop Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan
Graduate School of Horticulture, Chiba University, Matsudo, Chiba 271-8510 Japan
Hokkaido Research Organization, Agricultural Research Department, Chuo Agricultural Experiment Station, Naganuma, Hokkaido 069-1395, Japan
Institute of Crop Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan
Graduate School of Horticulture, Chiba University, Matsudo, Chiba 271-8510 Japan
Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8634, Japan
Institute of Crop Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan
Hokkaido Research Organization, Agricultural Research Department, Chuo Agricultural Experiment Station, Naganuma, Hokkaido 069-1395, Japan
Crop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, Shandong 250100, China
Shandong Wheat Technology Innovation Center, Jinan, Shandong 250100, China
Institute of Crop Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan
Department of Bioengineering, Nagaoka University of Technology, Nagaoka, Niigata 940-2188, Japan
Taiga Miyazaki
Institute of Crop Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan
Department of Bioengineering, Nagaoka University of Technology, Nagaoka, Niigata 940-2188, Japan
Institute of Crop Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan
Hokkaido Research Organization, Agricultural Research Department, Chuo Agricultural Experiment Station, Naganuma, Hokkaido 069-1395, Japan
Hokkaido Research Organization, Agricultural Research Department, Chuo Agricultural Experiment Station, Naganuma, Hokkaido 069-1395, Japan
Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
Université Clermont Auvergne, National Research Institute for Agriculture, Food & Environment (INRAE), Genetics, Diversity & Ecophysiology of Cereals, 63000 Clermont-Ferrand, France
Gencovery 69009 Lyon, France
Université Clermont Auvergne, National Research Institute for Agriculture, Food & Environment (INRAE), Genetics, Diversity & Ecophysiology of Cereals, 63000 Clermont-Ferrand, France
VetAgro Sup, 63370 Lempdes, France
Institute of Crop Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan
Key Laboratory of Stress Physiology and Ecology in Cold and Arid Regions of Gansu Province, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou 730000, China
School of Agriculture and Food, The University of Melbourne, Parkville, VIC 3010, Australia
Institute of Crop Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan
Institute of Crop Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan
Crop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, Shandong 250100, China
Shandong Wheat Technology Innovation Center, Jinan, Shandong 250100, China
Institute of Crop Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan
Crop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, Shandong 250100, China
Shandong Wheat Technology Innovation Center, Jinan, Shandong 250100, China
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