Fine mapping of powdery mildew resistance gene PmTm4 in wheat using comparative genomics

doi:10.1016/S2095-3119(16)61377-1

摘要/Abstract

Abstract: Powdery mildew, caused by Blumeria graminis f. sp. tritici, is one of the most severe wheat diseases. Mining powdery mildew resistance genes in wheat cultivars and their appliance in breeding program is a promising way to control this disease. Genetic analysis revealed that a single dominant resistance gene named PmTm4 originated from Chinese wheat line Tangmai 4 confers resistance to prevailing isolates of B. graminis f. sp. tritici isolate E09. Detailed comparative genomics analyses helped to develop closely linked markers to PmTm4 and a fine genetic map was constructed using large F₂ population, in which PmTm4 was located into a 0.66-cM genetic interval. The orthologous subgenome region of PmTm4 in Aegilops tauschii was identified, and two resistance gene analogs (RGA) were characterized from the corresponding sequence scaffolds of Ae. tauschii draft assembly. The closely linked markers and identified Ae. tauschii orthologs in the mapping interval provide an entry point for chromosome landing and map-based cloning of PmTm4.

Key words: powdery mildew resistance gene, PmTm4, genetic mapping, comparative genomic analysis

XIE Jing-zhong, WANG Li-li, WANG Yong, ZHANG Huai-zhi, ZHOU Sheng-hui, WU Qiu-hong, CHEN Yong-xing, WANG Zhen-zhong, WANG Guo-xin, ZHANG De-yun, ZHANG Yan, HU Tie-zhu, LIU Zhi-yong. [J]. Journal of Integrative Agriculture, 2017, 16(03): 540-550.

XIE Jing-zhong, WANG Li-li, WANG Yong, ZHANG Huai-zhi, ZHOU Sheng-hui, WU Qiu-hong, CHEN Yong-xing, WANG Zhen-zhong, WANG Guo-xin, ZHANG De-yun, ZHANG Yan, HU Tie-zhu, LIU Zhi-yong. Fine mapping of powdery mildew resistance gene PmTm4 in wheat using comparative genomics[J]. Journal of Integrative Agriculture, 2017, 16(03): 540-550.

参考文献

Alam M A, Xue F, Wang C, Ji W. 2011. Powdery mildew resistance genes in wheat: Identification and genetic analysis. Journal of Molecular Biology Research, 1, 20–39.
Allen G C, Flores-Vergara M A, Krasynanski S, Kumar S, Thompson W F. 2006. A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nature Protocols, 1, 2320–2325.
Ariyadasa R, Mascher M, Nussbaumer T, Schulte D, Frenkel Z, Poursarebani N, Zhou R, Steuernagel B, Gundlach H, Taudien S, Felder M, Platzer M, Himmelbach A, Schmutzer T, Hedley P E, Muehlbauer G J, Scholz U, Korol A, Mayer K F, Waugh R, et al. 2014. A sequence-ready physical map of barley anchored genetically by two million single-nucleotide polymorphisms. Plant Physiology, 164, 412–423.
Belova T, Zhan B, Wright J, Caccamo M, Asp T, Simkova H, Kent M, Bendixen C, Panitz F, Lien S, Dolezel J, Olsen O A, Sandve S R. 2013. Integration of mate pair sequences to improve shotgun assemblies of flow-sorted chromosome arms of hexaploid wheat. BMC Genomics, 14, 222.
Borrill P, Adamski N, Uauy C. 2015. Genomics as the key to unlocking the polyploid potential of wheat. New Phytologist, 208, 1008–1022.
Brenchley R, Spannagl M, Pfeifer M, Barker G L, D’Amore R, Allen A M, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo M C, Sehgal S, Gill B, Kianian S, et al. 2012. Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature, 491, 705–710.
Brutnell T P, Bennetzen J L, Vogel J P. 2015. Brachypodium distachyon and Setaria viridis: Model genetic systems for the grasses. Annual Review of Plant Biology, 66, 465–485.
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden T L. 2009. BLAST+: Architecture and applications. BMC Bioinformatics, 10, 421.
Catalan P, Muller J, Hasterok R, Jenkins G, Mur L A, Langdon T, Betekhtin A, Siwinska D, Pimentel M, Lopez-Alvarez D. 2012. Evolution and taxonomic split of the model grass Brachypodium distachyon. Annals of Botany, 109, 385–405.
Cavanagh C R, Chao S, Wang S, Huang B E, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira G L, Akhunova A, See D, Bai G, Pumphrey M, Tomar L, Wong D, Kong S, Reynolds M, da Silva M L, Bockelman H, Talbert L, et al. 2013. Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proceedings of the National Academy of Sciences of the United States of America, 110, 8057–8062.
Chapman J A, Mascher M, Buluc A, Barry K, Georganas E, Session A, Strnadova V, Jenkins J, Sehgal S, Oliker L, Schmutz J, Yelick K A, Scholz U, Waugh R, Poland J A, Muehlbauer G J, Stein N, Rokhsar D S. 2015. A whole-genome shotgun approach for assembling and anchoring the hexaploid bread wheat genome. Genome Biology, 16, 26.
Choulet F, Alberti A, Theil S, Glover N, Barbe V, Daron J, Pingault L, Sourdille P, Couloux A, Paux E, Leroy P, Mangenot S, Guilhot N, Le Gouis J, Balfourier F, Alaux M, Jamilloux V, Poulain J, Durand C, Bellec A, et al. 2014. Structural and functional partitioning of bread wheat chromosome 3B. Science, 345, 1249721.
Coordinators N R. 2016. Database resources of the National Center for Biotechnology Information. Nucleic Acids Research, 44, D7–D19.
Cowger C, Miranda L, Griffey C, Hall M, Murphy J P, Maxwell J. 2012. In: Sharma I, ed., Disease Resistance in Wheat. CAB International, Wallingford. pp. 84–120.
CRP (Consultative Group for International Agricultural Research). 2014. Global wheat science and partnerships for food security and nutrition. CGIAR Research Program on Wheat Annual Report 2014. [2015-09-08]. https://slate.adobe.com/a/J6KpK/
FAO (Food and Agriculture Organization). 2015a. Cereals and us: Time to renew an ancient bond. In: Save and Grow in Practice: Maize, Rice, Wheat, Chapter 1. [2015-12-02]. http://www.fao.org/ag/save-and-grow/MRW/en/1/index.html
FAO (Food and Agriculture Organization). 2015b. Online statistical database: Food balance. FAOSTAT. [2015-12-02]. http://faostat3.fao.org/download/FB/*/E
Fischer S, Brunk B P, Chen F, Gao X, Harb O S, Iodice J B, Shanmugam D, Roos D S, Stoeckert Jr C J. 2011. Using OrthoMCL to assign proteins to OrthoMCL-DB groups or to cluster proteomes into new ortholog groups. Current Protocols in Bioinformatics, 35, 6–12.
Fu B, Chen Y, Li N, Ma H, Kong Z, Zhang L, Jia H, Ma Z. 2013. pmX: A recessive powdery mildew resistance gene at the Pm4 locus identified in wheat landrace Xiaohongpi. Theoretical and Applied Genetics, 126, 913–921.
Herrera-Foessel S A, Lagudah E S, Huerta-Espino J, Hayden M J, Bariana H S, Singh D, Singh R P. 2011. New slow-rusting leaf rust and stripe rust resistance genes Lr67 and Yr46 in wheat are pleiotropic or closely linked. Theoretical and Applied Genetics, 122, 239–249.
Hsam S L K, Huang X Q, Zeller F J. 2000. Chromosomal location of powdery mildew resistance genes in Chinese wheat (Triticum aestivum L. em. Thell.) landraces Xiaobaidong and Fuzhuang 30. Journal of Genetics & Breeding, 54, 311–317.
Hsam S L K, Huang X Q, Zeller F J. 2001. Chromosomal location of genes for resistance to powdery mildew in common wheat (Triticum aestivum L. em Thell.) 6. Alleles at the Pm5 locus. Theoretical and Applied Genetics, 102, 127–133.
Hu T Z, Li H J, Xie C J, You M S, Yang Z M, Sun Q X, Liu Z Y. 2008. Molecular mapping and chromosomal location of powdery mildew resistance gene in wheat cultivar Tangmai 4.

Acta Agronomica Sinica, 34, 1193–1198.
Huang X Q, Hsam S L K, Zeller F J. 1997. Identification of powdery mildew resistance genes in common wheat (Triticum aestivum L. em Thell.). IX. Cultivars, land races and breeding lines grown in China. Plant Breeding, 116, 233–238.
Huang X Q, Röder M S. 2011. High-density genetic and physical bin mapping of wheat chromosome 1D reveals that the powdery mildew resistance gene Pm24 is located in a highly recombinogenic region. Genetica, 139, 1179–1187.
Huang X Q, Wang L X, Xu M X, Roder M S. 2003. Microsatellite mapping of the powdery mildew resistance gene Pm5e in common wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 106, 858–865.
IBGSC (International Barley Genome Sequencing Consortium), Mayer K F, Waugh R, Brown J W, Schulman A, Langridge P, Platzer M, Fincher G B, Muehlbauer G J, Sato K, Close T J, Wise R P, Stein N. 2012. A physical, genetic and functional sequence assembly of the barley genome. Nature, 491, 711–716.
IBI (International Brachypodium Initiative). 2010. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature, 463, 763–768.
IRGSP (International Rice Genome Sequencing Project). 2005. The map-based sequence of the rice genome. Nature, 436, 793–800.
IWGSC (International Wheat Genome Sequencing Consortium). 2014. A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science, 345, 1251788.
Jia J, Zhao S, Kong X, Li Y, Zhao G, He W, Appels R, Pfeifer M, Tao Y, Zhang X, Jing R, Zhang C, Ma Y, Gao L, Gao C, Spannagl M, Mayer K F, Li D, Pan S, Zheng F, et al. 2013. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature, 496, 91–95.
Kersey P J, Allen J E, Christensen M, Davis P, Falin L J, Grabmueller C, Hughes D S T, Humphrey J, Kerhornou A, Khobova J, Langridge N, McDowall M D, Maheswari U, Maslen G, Nuhn M, Ong C K, Paulini M, Pedro H, Toneva I, Tuli M A, et al. 2014. Ensembl Genomes 2013: Scaling up access to genome-wide data. Nucleic Acids Research, 42, D546–D552.
Lander E S, Green P, Abrahamson J, Barlow A, Daly M J, Lincoln S E, Newberg L A. 1987. MAPMAKER: An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics, 1, 174–181.
Li H J, Conner R L, McCallum B D, Chen X M, Su H, Wen Z Y, Chen Q, Jia X. 2004. Resistance of Tangmai 4 wheat to powdery mildew, stem rust, leaf rust, and stripe rust and its chromosome composition. Canadian Journal of Plant Science, 84, 1015–1023.
Liang Y, Zhang D Y, Ouyang S, Xie J, Wu Q, Wang Z, Cui Y, Lu P, Zhang D, Liu Z J, Zhu J, Chen Y X, Zhang Y, Luo M C, Dvorak J, Huo N, Sun Q, Gu Y Q, Liu Z. 2015. Dynamic evolution of resistance gene analogs in the orthologous genomic regions of powdery mildew resistance gene MlIW170 in Triticum dicoccoides and Aegilops tauschii. Theoretical and Applied Genetics, 128, 1617–1629.
Ling H Q, Zhao S, Liu D, Wang J, Sun H, Zhang C, Fan H, Li D, Dong L, Tao Y, Gao C, Wu H, Li Y, Cui Y, Guo X, Zheng S, Wang B, Yu K, Liang Q, Yang W, et al. 2013. Draft genome of the wheat A-genome progenitor Triticum urartu. Nature, 496, 87–90.
Liu R H, Meng J L. 2003. MapDraw: A microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data. Hereditas (Beijing), 25, 317–321.
Liu Z, Sun Q, Ni Z, Yang T, McIntosh R A. 1999. Development of SCAR markers linked to the Pm21 gene conferring resistance to powdery mildew in common wheat. Plant Breeding, 118, 215–219.
Lu P, Liang Y, Li D, Wang Z, Li W, Wang G, Wang Y, Zhou S, Wu Q, Xie J, Zhang D, Chen Y, Li M, Zhang Y, Sun Q, Han C, Liu Z. 2016. Fine genetic mapping of spot blotch resistance gene Sb3 in wheat (Triticum aestivum). Theoretical and Applied Genetics, 129, 577–589.
Luo M C, Gu Y Q, You F M, Deal K R, Ma Y, Hu Y, Huo N, Wang Y, Wang J, Chen S, Jorgensen C M, Zhang Y, McGuire P E, Pasternak S, Stein J C, Ware D, Kramer M, McCombie W R, Kianian S F, Martis M M, et al. 2013. A 4-gigabase physical map unlocks the structure and evolution of the complex genome of Aegilops tauschii, the wheat D-genome progenitor. Proceedings of the National Academy of Sciences of the United States of America, 110, 7940–7945.
Ma H, Kong Z, Fu B, Li N, Zhang L, Jia H, Ma Z. 2011. Identification and mapping of a new powdery mildew resistance gene on chromosome 6D of common wheat. Theoretical and Applied Genetics, 123, 1099–1106.
Mandadi K K, Scholthof K B. 2015. Genome-wide analysis of alternative splicing landscapes modulated during plant-virus interactions in Brachypodium distachyon. The Plant Cell, 27, 71–85.
McIntosh R A, Dubcovsky J, Rogers W J, Morris C. 2013. Catalogue of gene symbols for wheat: 2013–2014. In: Proceedings of the 12th International Wheat Genetics Symposium, Yokohama, Japan.
Michelmore R W, Paran I, Kesseli R V. 1991. Identification of markers linked to disease-resistance genes by bulked segregant analysis: A rapid method to detect markers in specific genomic regions by using segregating populations. Proceedings of the National Academy of Sciences of the United States of America, 88, 9828–9832.
Mochida K, Kawaura K, Shimosaka E, Kawakami N, Shin I T, Kohara Y, Yamazaki Y, Ogihara Y. 2006. Tissue expression map of a large number of expressed sequence tags and its application to in silico screening of stress response genes in common wheat. Molecular Genetics and Genomics, 276, 304–312.
Moore J W, Herrera-Foessel S, Lan C, Schnippenkoetter W, Ayliffe M, Huerta-Espino J, Lillemo M, Viccars L, Milne R, Periyannan S, Kong X, Spielmeyer W, Talbot M, Bariana H, Patrick J W, Dodds P, Singh R, Lagudah E. 2015. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nature Genetics, 47, 1494–1498.
Nematollahi G, Mohler V, Wenzel G, Zeller F J. 2008. Microsatellite mapping of powdery mildew resistance allele Pm5d from common wheat line IGV1–455. Euphytica, 159, 307–313.
Ouyang S, Zhang D, Han J, Zhao X, Cui Y, Song W, Huo N, Liang Y, Xie J, Wang Z, Wu Q, Chen Y X, Lu P, Zhang D Y, Wang L, Sun H, Yang T, Keeble-Gagnere G, Appels R, Dolezel J, et al. 2014. Fine physical and genetic mapping of powdery mildew resistance gene MlIW172 originating from wild emmer (Triticum dicoccoides). PLOS ONE, 9, e100160.
Paterson A H, Bowers J E, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti A K, Chapman J, Feltus F A, Gowik U, Grigoriev I V, et al. 2009. The sorghum bicolor genome and the diversification of grasses. Nature, 457, 551–556.
Poursarebani N, Ariyadasa R, Zhou R, Schulte D, Steuernagel B, Martis M M, Graner A, Schweizer P, Scholz U, Mayer K, Stein N. 2013. Conserved synteny-based anchoring of the barley genome physical map. Functional & Integrative Genomics, 13, 339–350.
Qin B, Cao A, Wang H, Chen T, You F M, Liu Y, Ji J, Liu D, Chen P, Wang X E. 2011. Collinearity-based marker mining for the fine mapping of Pm6, a powdery mildew resistance gene in wheat. Theoretical and Applied Genetics, 123, 207–218.
R Development Core Team. 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. [2014-11-20]. http://www.R-project.org/
Wang Z, Cui Y, Chen Y, Zhang D, Liang Y, Zhang D, Wu Q, Xie J, Ouyang S, Li D, Huang Y, Lu P, Wang G, Yu M, Zhou S, Sun Q, Liu Z. 2014. Comparative genetic mapping and genomic region collinearity analysis of the powdery mildew resistance gene Pm41. Theoretical and Applied Genetics, 127, 1741–1751.
Wang Z, Li H, Zhang D, Guo L, Chen J, Chen Y, Wu Q, Xie J, Zhang Y, Sun Q, Dvorak J, Luo M C, Liu Z. 2015. Genetic and physical mapping of powdery mildew resistance gene MlHLT in Chinese wheat landrace Hulutou. Theoretical and Applied Genetics, 128, 365–373.
Wu H, Qin J, Han J, Zhao X, Ouyang S, Liang Y, Zhang D, Wang Z, Wu Q, Xie J, Cui Y, Peng H, Sun Q, Liu Z. 2013. Comparative high-resolution mapping of the wax inhibitors Iw1 and Iw2 in hexaploid wheat. PLOS ONE, 8, e84691.
Xiao M, Song F, Jiao J, Wang X, Xu H, Li H. 2013. Identification of the gene Pm47 on chromosome 7BS conferring resistance to powdery mildew in the Chinese wheat landrace Hongyanglazi. Theoretical and Applied Genetics, 126, 1397–1403.
Xue F, Wang C, Li C, Duan X, Zhou Y, Zhao N, Wang Y, Ji W. 2012. Molecular mapping of a powdery mildew resistance gene in common wheat landrace Baihulu and its allelism with Pm24. Theoretical and Applied Genetics, 125, 1425–1432.
Xue F, Zhai W W, Duan X Y, Zhou Y L, Ji W Q. 2009. Microsatellite mapping of a powdery mildew resistance gene in wheat landrace Xiaobaidong. Acta Agronomica Sinica, 35, 1806–1811. (in Chinese)
You F M, Huo N, Gu Y Q, Luo M C, Ma Y, Hane D, Lazo G R, Dvorak J, Anderson O D. 2008. BatchPrimer3: A high throughput web application for PCR and sequencing primer design. BMC Bioinformatics, 9, 253.
Zeng X, Long H, Wang Z, Zhao S, Tang Y, Huang Z, Wang Y, Xu Q, Mao L, Deng G, Yao X, Li X, Bai L, Yuan H, Pan Z, Liu R, Chen X, WangMu Q, Chen M, Yu L, et al. 2015. The draft genome of Tibetan hulless barley reveals adaptive patterns to the high stressful Tibetan Plateau. Proceedings of the National Academy of Sciences of the United States of America, 112, 1095–1100.
Zhang D, Ouyang S H, Wang L L, Cui Y, Wu Q H, Liang Y, Wang Z Z, Xie J Z, Zhang D Y, Wang Y, Chen Y X, Liu Z Y. 2015. Comparative genetic mapping revealed powdery mildew resistance gene MlWE4 derived from wild emmer is located in same genomic region of Pm36 and Ml3D232 on chromosome 5BL. Journal of Integrative Agriculture, 14, 603–609.
Zhang H, Guan H, Li J, Zhu J, Xie C, Zhou Y, Duan X, Yang T, Sun Q, Liu Z. 2010. Genetic and comparative genomics mapping reveals that a powdery mildew resistance gene Ml3D232 originating from wild emmer co-segregates with an NBS-LRR analog in common wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 121, 1613–1621.
Zhou R, Zhu Z, Kong X, Huo N, Tian Q, Li P, Jin C, Dong Y, Jia J. 2005. Development of wheat near-isogenic lines for powdery mildew resistance. Theoretical and Applied Genetics, 110, 640–648.
Zhu Y L, Wang L M, Wang H G. 2008. Studies on SSR molecular marker of wheat powdery mildew resistance gene Pm5e. Molecular Plant Breeding, 6, 1080–1084.