Abstract
Main conclusion
Fine mapping of wheat powdery mildew-resistance gene Pm4e to a 0.19 cM interval with sequence-based markers provides the foundation for map-based cloning and marker-assisted selection with breeder-friendly markers.
Powdery mildew caused by Blumeria graminis f. sp. tritici is a wheat foliar disease that poses a serious threat to global wheat production. Pm4 is a resistance gene locus that has played a key role in controlling this disease in wheat production and a few resistance alleles of this locus have been identified. We have previously mapped the Pm4e allele to a 6.7 cM interval on chromosome 2AL. In this study, Pm4e was delimited to a 0.19 cM interval flanked by Xwgrc763 and Xwgrc865, through employment of a larger segregating population, derived from the cross of resistant parent D29 with susceptible parent Yangmai 158 (Y158), and enrichment of the genetic interval with markers developed on Chinese Spring (C.S.) survey sequence. In this interval, Pm4e co-segregated with a few markers, some of which were either D29-dominant or Y158-dominant, implying great sequence variation in the interval between D29 and Y158. Most of these co-segregation markers could not differentiate the Pm4 alleles from each other. Survey of 55 wheat cultivars with four co-dominant markers showed that the Pm4e-co-segregating loci always co-exist. Annotation of the Pm4e interval-corresponding C.S. sequence revealed more than a dozen resistance gene analogs clustered in a 2.4 Mb region, although C.S. is susceptible to the Pm4e-avirulent isolate Bgt2. This study has established the foundation for map-based cloning of Pm4e. Moreover, some of the co-dominant markers developed in this study could help in marker-assisted transfer of Pm4e into elite cultivars.
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Change history
05 September 2018
Unfortunately, the style of the units was incorrectly published (“cm” instead of “cM”) throughout the original article.
References
Bhullar NK, Zhang ZQ, Wicker T, Keller B (2010) Wheat gene banks as a source of new alleles of the powdery mildew resistance gene Pm3: a large scale allele mining project. BMC Plant Bio 10:88
Briggle LW (1966) Transfer of resistance to Erysiphe graminis f. sp. tritici from Khapli emmer and Yuma durum to hexaploid wheat. Crop Sci 6:459–461
Cloutier S, McCallum BD, Loutre C, Banks TW, Wicker T, Feuillet C, Keller B, Jordan MC (2007) Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol Biol 65:93–106
Duan S, Xu Y, Wu X (2002) Research progress of pathogen virulence, resistance genes and resistance breeding of wheat powdery mildew. J Triticeae Crops 22:83–86 (in Chinese)
Everts KL, Leath S (1992) Effect of early season powdery mildew on development, survival, and yield contribution of tillers of winter wheat. Phytopathology 82:1273–1278
Fu BS, Yang C, Li N, Ma HQ, Kong ZX, Zhang LX, Jia HY, Ma ZQ (2013) pmX: a recessive powdery mildew resistance gene at the Pm4 locus identified in wheat landrace Xiaohongpi. Theor Appl Genet 126:913–921
Hao Y, Liu A, WangY Feng D, Gao J, Li X, Liu S, Wang H (2008) Pm23: a new allele of Pm4 located on chromosome 2AL in wheat. Theor Appl Genet 117:1205–1212
He H, Zhu S, Zhao R, Jiang Z, Ji Y, Ji J, Qui D, Li H, Bie T (2018) Pm21, encoding a typical CC-NBS-LRR protein, confers broad-spectrum resistance to wheat powdery mildew disease. Mol Plant 11:879–882
Huang XQ, Hsam SLK, Zeller FJ (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 Breed 116:233–238
Huang XQ, Hsam SLK, Zeller FJ, Wenzel G, Mohler V (2000) Molecular mapping of the wheat powdery mildew resistance gene Pm24 and marker validation for molecular breeding. Theor Appl Genet 101:407–414
Huang XQ, Wang LX, Xu MX, Röder MS (2003) Microsatellite mapping of the powdery mildew resistance gene Pm5e in common wheat (Triticum aestivum L.). Theor Appl Genet 106:858–865
Koller T, Brunner S, Herren G, Hurni S, Keller B (2018) Pyramiding of transgenic Pm3 alleles in wheat results in improved powdery mildew resistance in the field. Theor Appl Genet 131:861–871
Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Li N, Jia HY, Kong ZX, Tang WB, Ding YX, Liang JC, Ma HQ, Ma ZQ (2017) Identification and marker-assisted transfer of a new powdery mildew resistance gene at the Pm4 locus in common wheat. Mol Breed 37:79
Liang JC, Fu BS, Tang WB, Khan NU, Li N, Ma ZQ (2016) Fine mapping of two powdery mildew resistance genes located at the Pm1 cluster. Plant Genome. https://doi.org/10.3835/plantgenome2015.09.0084
Lincoln SE, Daly MJ, Lander ES (1993) Constructing linkage maps with MAPMAKER/Exp version 3. 0: a tutorial reference manual, vol 3. Whitehead Institute for Medical Res, Cambridge
Liu W, Koo DH, Xia Q, Li C, Bai F, Song Y, Friebe B, Gill BS (2017) Homoeologous recombination-based transfer and molecular cytogenetic mapping of powdery mildew-resistant gene Pm57 from Aegilops searsii into wheat. Theor Appl Genet 30:841–848
Ma ZQ, Sorrells ME, Tanksley SD (1994) RFLP markers linked to powdery mildew resistance genes Pm1, Pm2, Pm3 and Pm4 in wheat. Genome 37:871–875
Ma ZQ, Wei JB, Chen SH (2004) PCR-based markers for the powdery mildew resistance gene Pm4a in wheat. Theor Appl Genet 109:140–145
Ma PT, Xu HX, Xu YF, Li LH, Qie YM, Luo QL, Zhang XT, Li XQ, Zhou YL, An DG (2015) Molecular mapping of a new powdery mildew resistance gene Pm2b in Chinese breeding line KM2939. Theor Appl Genet 128:613–622
McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Xia XC (2017) Catalogue of gene symbols for wheat: 2017 Supplement. https://shigen.nig.ac.jp/wheat/komugi/genes/macgene/supplement2017.pdf. Accessed 4 Aug 2018
Michelmore RW, Paran I, Kesseli RV (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. Proc Natl Acad Sci USA 88:9828–9832
Niu JS, Wang BQ, Wang YH, Cao AZ, Qi ZJ, Shen TM (2008) Chromosome location and microsatellite markers linked to a powdery mildew resistance gene in wheat line “Lankao 90(6)”. Plant Breed 127:346–349
Niu JS, Jia HY, Yin J, Wang BQ, Ma ZQ, Shen TM (2010) Development of an STS marker linked to powdery mildew resistance genes PmLK906 and Pm4a by gene chip hybridization. Agric Sci China 9:331–336
Periyannan S, Moore J, Ayliffe M, Bansal U, Wang XJ, Huang L, Deal K, Luo MC, Kong XY, Bariana H, Mago R, McIntosh R, Dodds P, Dvorak J, Lagudah E (2013) The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science 341:786–788
Sánchez MJ, Steuernage B, Ghosh S, Herren G, Hurni S, Adamski N, Vrána J, Kubaláková M, Krattinger SG, Wicker T, Doležel J, Keller B, Wulff BBH (2016) Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol 17:221
Santos FR, Pena SD, Epplen JT (1993) Genetic and population study of a Y-linked tetranucleotide repeat DNA polymorphism with a simple non-isotopic technique. Hum Genet 90:655–656
Schmolke M, Mohler V, Hartl L, Zeller FJ, Hsam SLK (2012) A new powdery mildew resistance allele at the Pm4 wheat locus transferred from einkorn (Triticum monococcum). Mol Breed 29:449–456
Srichumpa P, Brunner S, Keller B, Yahiaoui N (2005) Allelic series of four powdery mildew resistance genes at the Pm3 locus in hexaploid bread wheat. Plant Physiol 139:885–895
Sun HG, Hu JH, Song W, Qiu D, Cui L, Wu PP, Zhang HJ, Liu HW, Yang L, Qu YF, Li YH, Li T, Cheng W, Zhou Y, Liu ZY, Li JT, Li HJ (2018) Pm61: a recessive gene for resistance to powdery mildew in wheat landrace Xuxusanyuehuang identified by comparative genomics analysis. Theor Appl Genet. https://doi.org/10.1007/s00122-018-3135-1
Tan CC, Li GQ, Cowger C, Carver BF, Xu XY (2018) Characterization of Pm59, a novel powdery mildew resistance gene in Afghanistan wheat landrace PI 181356. Theor Appl Genet 131:1145–1152
The TT, McIntosh RA, Bennett EGA (1979) Cytogenetical studies in wheat. IX. Monosomic analyses, telocentric mapping and linkage relationships of genes Sr21, Pm4 and Mle. Aust J Biol Sci 32:115–125
Wei FS, Gobelman-Werner K, Morroll SM, Kurth J, Mao L, Wing R, Leister D, Schulze-Lefert P, Wise RP (1999) The Mla (powdery mildew) resistance cluster is associated with three NBS-LRR gene families and suppressed recombination within a 240-kb DNA interval on chromosome 5S (1HS) of barley. Genetics 153:1929–1948
Wiersma AT, Pulman JA, Brown LK, Cowger C, Olson EL (2017) Identification of Pm58 from Aegilops tauchii. Theor Appl Genet 130:1123–1133
Wu PP, Xie JZ, Hu JH, Qiu D, Liu ZY, Li JT, Li MM, Zhang HJ, Li Yang, Liu HW, Zhou Y, Zhang ZJ, Li HJ (2018) Development of molecular markers linked to powdery mildew resistance gene Pm4b by combining SNP discovery from transcript sequencing data with bulked segregant analysis (BSR-Seq) in wheat. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00095
Xu HX, Yao GQ, Xiong L, Yang LL, Jiang YM, Fu BS, Zhao WF, Zhang ZZ, Zhang CQ, Ma ZQ (2008) Identification and mapping of pm2026: a recessive powdery mildew resistance gene in an einkorn (Triticum monococcum L.) accession. Theor Appl Genet 117:471–477
Xue F, Wang CY, Li C, Duan XY, Zhou YL, Zhao NJ, Wang YJ, Ji WQ (2012) Molecular mapping of a powdery mildew resistance gene in common wheat landrace Baihulu and its allelism with Pm24. Theor Appl Genet 125:1425–1432
Yahiaoui N, Srichumpa P, Dudler R, Keller B (2004) Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. Plant J 37:528–538
Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat Vrn2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644
Yao GQ, Zhang JJ, Yang LL, Xu HX, Jiang YM, Xiong L, Zhang CQ, Zhang ZZ, Ma ZQ, Sorrells ME (2007) Genetic mapping of two powdery mildew resistance genes in einkorn (Triticum monococcum L.) accessions. Theor Appl Genet 114:351–358
Zhang R, Sun B, Chen J, Cao A, Xing L, Feng Y, Lan C, Chen P (2016) Pm55, a developmental-stage and tissue-specific powdery mildew resistance gene introgressed from Dasypyrum villosum into common wheat. Theor Appl Genet 129:1975–1984
Zhao CZ, Li YH, Dong HT, Geng MM, Liu WH, Li F, Ni ZF, Wang XJ, Xie CJ, Sun QX (2016) Molecular cloning, functional verification, and evolution of TmPm3, the powdery mildew resistance gene of Triticum monococcum L. Genet Mol Res 15(2):gmr.15028056
Zhu Z, Zhou R, Kong X, Dong Y, Jia J (2005) Microsatellite markers linked to two powdery mildew resistance genes introgressed from Triticum carthlicum accession PS5 into common wheat. Genome 48:585–590
Zou SH, Wang H, Li YW, Kong ZS, Tang DZ (2017) The NB-LRR gene Pm60 confers powdery mildew resistance in wheat. N Phytol 218:298–309
Acknowledgements
This project was partially supported by National Key Research and Development Program (2016YFD0101802), NSFC Funds 30025030, 30771344, 30771165 and 31501302, Fundamental Research Fund for the Central Universities (KJQN201633), Jiangsu Collaborative Innovation Initiative for Modern Crop Production, ‘111’ project B08025, Innovation Team Program for Jiangsu Universities (2014). The first author also acknowledges the financial support from Chinese Scholarship Council for Ph. D program.
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The original version of this article was revised: The incorrect units has been corrected.
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Ullah, K.N., Li, N., Shen, T. et al. Fine mapping of powdery mildew resistance gene Pm4e in bread wheat (Triticum aestivum L.). Planta 248, 1319–1328 (2018). https://doi.org/10.1007/s00425-018-2990-y
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DOI: https://doi.org/10.1007/s00425-018-2990-y