A CNL protein in wild emmer wheat confers powdery mildew resistance.

Powdery mildew, a fungal disease caused by Blumeria graminis f. sp. tritici (Bgt), has a serious impact on wheat production. Loss of resistance in cultivars prompts a continuing search for new sources of resistance. Wild emmer wheat (Triticum turgidum ssp. dicoccoides, WEW), the progenitor of both modern tetraploid and hexaploid wheats, harbors many powdery mildew resistance genes. We report here the positional cloning and functional characterization of Pm41, a powdery mildew resistance gene derived from WEW, which encodes a coiled-coil, nucleotide-binding and leucine-rich repeat protein (CNL). Mutagenesis and stable genetic transformation confirmed the function of Pm41 against Bgt infection in wheat. We demonstrated that Pm41 was present at a very low frequency (1.81%) only in southern WEW populations. It was absent in other WEW populations, domesticated emmer, durum, and common wheat, suggesting that the ancestral Pm41 was restricted to its place of origin and was not incorporated into domesticated wheat. Our findings emphasize the importance of conservation and exploitation of the primary WEW gene pool, as a valuable resource for discovery of resistance genes for improvement of modern wheat cultivars.

[1]  Sanzhen Liu,et al.  A rare single nucleotide variant in Pm5e confers powdery mildew resistance in common wheat. , 2020, The New phytologist.

[2]  J. Dvorak,et al.  A rare gain of function mutation in a wheat tandem kinase confers resistance to powdery mildew , 2020, Nature Communications.

[3]  S. Sehgal,et al.  A spontaneous wheat-Aegilops longissima translocation carrying Pm66 confers resistance to powdery mildew , 2020, Theoretical and Applied Genetics.

[4]  Lingli Dong,et al.  Wheat powdery mildew resistance gene Pm64 derived from wild emmer (Triticum turgidum var. dicoccoides) is tightly linked in repulsion with stripe rust resistance gene Yr5 , 2019 .

[5]  Arthur T. O. Melo,et al.  Durum wheat genome highlights past domestication signatures and future improvement targets , 2019, Nature Genetics.

[6]  T. Fahima,et al.  Wheat tandem kinases provide insights on disease-resistance gene flow and host-parasite co-evolution. , 2019, The Plant journal : for cell and molecular biology.

[7]  J. Dvorak,et al.  Improved Genome Sequence of Wild Emmer Wheat Zavitan with the Aid of Optical Maps , 2019, G3: Genes, Genomes, Genetics.

[8]  L. Paulin,et al.  Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family , 2018, Nature Communications.

[9]  B. Keller,et al.  Evolutionary divergence of the rye Pm17 and Pm8 resistance genes reveals ancient diversity , 2018, Plant Molecular Biology.

[10]  Jonathan D. G. Jones,et al.  Shifting the limits in wheat research and breeding using a fully annotated reference genome , 2018, Science.

[11]  Jonathan D. G. Jones,et al.  Pm21 from Haynaldia villosa Encodes a CC-NBS-LRR Protein Conferring Powdery Mildew Resistance in Wheat. , 2018, Molecular plant.

[12]  Hongjie Li,et al.  Pm21, Encoding a Typical CC-NBS-LRR Protein, Confers Broad-Spectrum Resistance to Wheat Powdery Mildew Disease. , 2018, Molecular plant.

[13]  D. Tang,et al.  The NB-LRR gene Pm60 confers powdery mildew resistance in wheat. , 2018, The New phytologist.

[14]  R. V. D. van der Hoorn,et al.  Defended to the Nines: 25 Years of Resistance Gene Cloning Identifies Nine Mechanisms for R Protein Function[OPEN] , 2018, Plant Cell.

[15]  Axel Himmelbach,et al.  Wild emmer genome architecture and diversity elucidate wheat evolution and domestication , 2017, Science.

[16]  M. Luo,et al.  Molecular mapping of YrTZ2, a stripe rust resistance gene in wild emmer accession TZ-2 and its comparative analyses with Aegilops tauschii , 2017, bioRxiv.

[17]  B. Steuernagel,et al.  Rapid gene isolation in barley and wheat by mutant chromosome sequencing , 2016, Genome Biology.

[18]  J. Dubcovsky,et al.  Distribution and haplotype diversity of WKS resistance genes in wild emmer wheat natural populations , 2016, Theoretical and Applied Genetics.

[19]  J. Patrick,et al.  A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat , 2015, Nature Genetics.

[20]  T. Komari,et al.  Wheat (Triticum aestivum L.) transformation using immature embryos. , 2015, Methods in molecular biology.

[21]  M. Moscou,et al.  Strategies for transferring resistance into wheat: from wide crosses to GM cassettes , 2014, Front. Plant Sci..

[22]  B. Keller,et al.  The powdery mildew resistance gene Pm8 derived from rye is suppressed by its wheat ortholog Pm3. , 2014, The Plant journal : for cell and molecular biology.

[23]  Hadi Quesneville,et al.  Structural and functional partitioning of bread wheat chromosome 3B , 2014, Science.

[24]  D. Zhang,et al.  Comparative genetic mapping and genomic region collinearity analysis of the powdery mildew resistance gene Pm41 , 2014, Theoretical and Applied Genetics.

[25]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[26]  T. Wicker,et al.  Rye Pm8 and wheat Pm3 are orthologous genes and show evolutionary conservation of resistance function against powdery mildew. , 2013, The Plant journal : for cell and molecular biology.

[27]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[28]  A. Tiedemann,et al.  Climate change and potential future risks through wheat diseases: a review , 2012, European Journal of Plant Pathology.

[29]  Damon Lisch,et al.  How important are transposons for plant evolution? , 2012, Nature Reviews Genetics.

[30]  Y. Matsuoka Evolution of polyploid triticum wheats under cultivation: the role of domestication, natural hybridization and allopolyploid speciation in their diversification. , 2011, Plant & cell physiology.

[31]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[32]  H. M. Alexander,et al.  TIR-NBS-LRR genes are rare in monocots: evidence from diverse monocot orders , 2009, BMC Research Notes.

[33]  E. Nevo,et al.  Molecular identification of a new powdery mildew resistance gene Pm41 on chromosome 3BL derived from wild emmer (Triticum turgidum var. dicoccoides) , 2009, Theoretical and Applied Genetics.

[34]  C. Xie,et al.  Identification and genetic mapping of pm42, a new recessive wheat powdery mildew resistance gene derived from wild emmer (Triticum turgidum var. dicoccoides) , 2009, Theoretical and Applied Genetics.

[35]  J. Dubcovsky,et al.  A Kinase-START Gene Confers Temperature-Dependent Resistance to Wheat Stripe Rust , 2009, Science.

[36]  B. Keller,et al.  A Putative ABC Transporter Confers Durable Resistance to Multiple Fungal Pathogens in Wheat , 2009, Science.

[37]  A. Blanco,et al.  Molecular mapping of the novel powdery mildew resistance gene Pm36 introgressed from Triticum turgidum var. dicoccoides in durum wheat , 2008, Theoretical and Applied Genetics.

[38]  Yuling Bai,et al.  Natural genetic resources of Arabidopsis thaliana reveal a high prevalence and unexpected phenotypic plasticity of RPW8-mediated powdery mildew resistance. , 2008, The New phytologist.

[39]  Bruce D. Smith,et al.  The Molecular Genetics of Crop Domestication , 2006, Cell.

[40]  J. Dubcovsky,et al.  A NAC Gene Regulating Senescence Improves Grain Protein, Zinc, and Iron Content in Wheat , 2006, Science.

[41]  E. Nevo,et al.  Genetic diversity for drought resistance in wild emmer wheat and its ecogeographical associations , 2005 .

[42]  B. Keller,et al.  Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. , 2004, The Plant journal : for cell and molecular biology.

[43]  S. Kianian,et al.  Mapping genes for grain protein concentration and grain yield on chromosome 5B of Triticum turgidum (L.) var. dicoccoides , 2004, Euphytica.

[44]  E. Nevo,et al.  Variation for resistance to head blight caused by Fusarium graminearum in wild emmer (Triticum dicoccoides) originating from Israel , 2003, Euphytica.

[45]  M. Feldman,et al.  A new powdery mildew resistance gene: Introgression from wild emmer into common wheat and RFLP-based mapping , 2000, Euphytica.

[46]  R. Khanna-Chopra,et al.  Evaluation of heat stress tolerance in irrigated environment of T. aestivum and related species. I. Stability in yield and yield components , 1999, Euphytica.

[47]  T. E. Miller,et al.  The introduction into bread wheat of a major gene for resistance to powdery mildew from wild emmer wheat , 1991, Euphytica.

[48]  E. Nevo,et al.  Molecular characterization of a novel powdery mildew resistance gene Pm30 in wheat originating from wild emmer , 2004, Euphytica.

[49]  B. Keller,et al.  Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Blake C. Meyers,et al.  Genome-Wide Analysis of NBS-LRR–Encoding Genes in Arabidopsis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009308. , 2003, The Plant Cell Online.

[51]  E. Nevo,et al.  Evolution of Wild Emmer and Wheat Improvement: Population Genetics, Genetic Resources, and Genome Organization of Wheat’s Progenitor, Triticum dicoccoides , 2002 .

[52]  Professor Eviatar Nevo,et al.  Evolution of Wild Emmer and Wheat Improvement , 2002, Springer Berlin Heidelberg.

[53]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[54]  E. Nevo,et al.  Genetic Resources for Salt Tolerance in the Wild Progenitors of Wheat (Triticum dicoccoides) and Barley (Hordeum spontaneum) in Israel , 1993 .

[55]  Q. Zhuang,et al.  Present status of wheat breeding and related genetic study in China. , 1993 .

[56]  M. Baum,et al.  Wide Crosses in Cereals , 1992 .