Extensive Genetic Variation at the Sr22 Wheat Stem Rust Resistance Gene Locus in the Grasses Revealed Through Evolutionary Genomics and Functional Analyses
In the last 20 years, severe wheat stem rust outbreaks have been recorded in Africa, Europe, and Central Asia. This previously well controlled disease, caused by the fungus Puccinia graminis f. sp. tritici, has reemerged as a major threat to wheat cultivation. The stem rust (Sr) resistance gene Sr22...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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The American Phytopathological Society
2020-11-01
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| Series: | Molecular Plant-Microbe Interactions |
| Subjects: | |
| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI-01-20-0018-R |
| _version_ | 1819081397757804544 |
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| author | M. Asyraf Md. Hatta Sreya Ghosh Naveenkumar Athiyannan Terese Richardson Burkhard Steuernagel Guotai Yu Matthew N. Rouse Michael Ayliffe Evans S. Lagudah Guru V. Radhakrishnan Sambasivam K. Periyannan Brande B. H. Wulff |
| author_facet | M. Asyraf Md. Hatta Sreya Ghosh Naveenkumar Athiyannan Terese Richardson Burkhard Steuernagel Guotai Yu Matthew N. Rouse Michael Ayliffe Evans S. Lagudah Guru V. Radhakrishnan Sambasivam K. Periyannan Brande B. H. Wulff |
| author_sort | M. Asyraf Md. Hatta |
| collection | DOAJ |
| description | In the last 20 years, severe wheat stem rust outbreaks have been recorded in Africa, Europe, and Central Asia. This previously well controlled disease, caused by the fungus Puccinia graminis f. sp. tritici, has reemerged as a major threat to wheat cultivation. The stem rust (Sr) resistance gene Sr22 encodes a nucleotide-binding and leucine-rich repeat receptor which confers resistance to the highly virulent African stem rust isolate Ug99. Here, we show that the Sr22 gene is conserved among grasses in the Triticeae and Poeae lineages. Triticeae species contain syntenic loci with single-copy orthologs of Sr22 on chromosome 7, except Hordeum vulgare, which has experienced major expansions and rearrangements at the locus. We also describe 14 Sr22 sequence variants obtained from both Triticum boeoticum and the domesticated form of this species, T. monococcum, which have been postulated to encode both functional and nonfunctional Sr22 alleles. The nucleotide sequence analysis of these alleles identified historical sequence exchange resulting from recombination or gene conversion, including breakpoints within codons, which expanded the coding potential at these positions by introduction of nonsynonymous substitutions. Three Sr22 alleles were transformed into wheat cultivar Fielder and two postulated resistant alleles from Schomburgk (hexaploid wheat introgressed with T. boeoticum segment carrying Sr22) and T. monococcum accession PI190945, respectively, conferred resistance to P. graminis f. sp. tritici race TTKSK, thereby unequivocally confirming Sr22 effectiveness against Ug99. The third allele from accession PI573523, previously believed to confer susceptibility, was confirmed as nonfunctional against Australian P. graminis f. sp. tritici race 98-1,2,3,5,6.[Graphic: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license. |
| first_indexed | 2024-12-21T20:00:08Z |
| format | Article |
| id | doaj.art-63cd4a4c018248c19d13a65e0416a07d |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-12-21T20:00:08Z |
| publishDate | 2020-11-01 |
| publisher | The American Phytopathological Society |
| record_format | Article |
| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-63cd4a4c018248c19d13a65e0416a07d2022-12-21T18:51:59ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062020-11-0133111286129810.1094/MPMI-01-20-0018-RExtensive Genetic Variation at the Sr22 Wheat Stem Rust Resistance Gene Locus in the Grasses Revealed Through Evolutionary Genomics and Functional AnalysesM. Asyraf Md. Hatta0Sreya Ghosh1Naveenkumar Athiyannan2Terese Richardson3Burkhard Steuernagel4Guotai Yu5Matthew N. Rouse6Michael Ayliffe7Evans S. Lagudah8Guru V. Radhakrishnan9Sambasivam K. Periyannan10Brande B. H. Wulff11John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United KingdomJohn Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United KingdomCommonwealth Scientific and Industrial Research Organization (CSIRO), Agriculture and Food, General Post Office Box 1700, Canberra, ACT 2601, AustraliaCommonwealth Scientific and Industrial Research Organization (CSIRO), Agriculture and Food, General Post Office Box 1700, Canberra, ACT 2601, AustraliaJohn Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United KingdomJohn Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United KingdomUnited States Department of Agriculture–Agricultural Research Service Cereal Disease Laboratory, St. Paul, MN 55108, U.S.A.Commonwealth Scientific and Industrial Research Organization (CSIRO), Agriculture and Food, General Post Office Box 1700, Canberra, ACT 2601, AustraliaCommonwealth Scientific and Industrial Research Organization (CSIRO), Agriculture and Food, General Post Office Box 1700, Canberra, ACT 2601, AustraliaJohn Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United KingdomCommonwealth Scientific and Industrial Research Organization (CSIRO), Agriculture and Food, General Post Office Box 1700, Canberra, ACT 2601, AustraliaJohn Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United KingdomIn the last 20 years, severe wheat stem rust outbreaks have been recorded in Africa, Europe, and Central Asia. This previously well controlled disease, caused by the fungus Puccinia graminis f. sp. tritici, has reemerged as a major threat to wheat cultivation. The stem rust (Sr) resistance gene Sr22 encodes a nucleotide-binding and leucine-rich repeat receptor which confers resistance to the highly virulent African stem rust isolate Ug99. Here, we show that the Sr22 gene is conserved among grasses in the Triticeae and Poeae lineages. Triticeae species contain syntenic loci with single-copy orthologs of Sr22 on chromosome 7, except Hordeum vulgare, which has experienced major expansions and rearrangements at the locus. We also describe 14 Sr22 sequence variants obtained from both Triticum boeoticum and the domesticated form of this species, T. monococcum, which have been postulated to encode both functional and nonfunctional Sr22 alleles. The nucleotide sequence analysis of these alleles identified historical sequence exchange resulting from recombination or gene conversion, including breakpoints within codons, which expanded the coding potential at these positions by introduction of nonsynonymous substitutions. Three Sr22 alleles were transformed into wheat cultivar Fielder and two postulated resistant alleles from Schomburgk (hexaploid wheat introgressed with T. boeoticum segment carrying Sr22) and T. monococcum accession PI190945, respectively, conferred resistance to P. graminis f. sp. tritici race TTKSK, thereby unequivocally confirming Sr22 effectiveness against Ug99. The third allele from accession PI573523, previously believed to confer susceptibility, was confirmed as nonfunctional against Australian P. graminis f. sp. tritici race 98-1,2,3,5,6.[Graphic: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-01-20-0018-Rplant biotechnologyresistance geneSr22stem rustUg99wheat |
| spellingShingle | M. Asyraf Md. Hatta Sreya Ghosh Naveenkumar Athiyannan Terese Richardson Burkhard Steuernagel Guotai Yu Matthew N. Rouse Michael Ayliffe Evans S. Lagudah Guru V. Radhakrishnan Sambasivam K. Periyannan Brande B. H. Wulff Extensive Genetic Variation at the Sr22 Wheat Stem Rust Resistance Gene Locus in the Grasses Revealed Through Evolutionary Genomics and Functional Analyses Molecular Plant-Microbe Interactions plant biotechnology resistance gene Sr22 stem rust Ug99 wheat |
| title | Extensive Genetic Variation at the Sr22 Wheat Stem Rust Resistance Gene Locus in the Grasses Revealed Through Evolutionary Genomics and Functional Analyses |
| title_full | Extensive Genetic Variation at the Sr22 Wheat Stem Rust Resistance Gene Locus in the Grasses Revealed Through Evolutionary Genomics and Functional Analyses |
| title_fullStr | Extensive Genetic Variation at the Sr22 Wheat Stem Rust Resistance Gene Locus in the Grasses Revealed Through Evolutionary Genomics and Functional Analyses |
| title_full_unstemmed | Extensive Genetic Variation at the Sr22 Wheat Stem Rust Resistance Gene Locus in the Grasses Revealed Through Evolutionary Genomics and Functional Analyses |
| title_short | Extensive Genetic Variation at the Sr22 Wheat Stem Rust Resistance Gene Locus in the Grasses Revealed Through Evolutionary Genomics and Functional Analyses |
| title_sort | extensive genetic variation at the sr22 wheat stem rust resistance gene locus in the grasses revealed through evolutionary genomics and functional analyses |
| topic | plant biotechnology resistance gene Sr22 stem rust Ug99 wheat |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI-01-20-0018-R |
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