A segment of Triticum militinae chromosome 7G harbors a gene(s) conferring powdery mildew resistance which is effective at both the seedling and the adult plant stages when transferred into bread wheat (T. aestivum). The introgressed segment replaces a piece of wheat chromosome arm 4AL. An analysis of segregating materials generated to positionally clone the gene highlighted that in a plant heterozygous for the introgression segment, only limited recombination occurs between the introgressed region and bread wheat 4A. Nevertheless, 75 genetic markers were successfully placed within the region, thereby confining the gene to a 0.012 cM window along the 4AL arm. In a background lacking the Ph1 locus, the localized rate of recombination was raised 33-fold, enabling the reduction in the length of the region containing the resistance gene to a 480 kbp stretch harboring 12 predicted genes. The substituted segment in the reference sequence of bread wheat cv. Chinese Spring is longer (640 kbp) and harbors 16 genes. A comparison of the segments' sequences revealed a high degree of divergence with respect to both their gene content and nucleotide sequence. Of the 12 T. militinae genes, only four have a homolog in cv. Chinese Spring. Possible candidate genes for the resistance have been identified based on function predicted from their sequence.

Biological and Environmental Science and Engineering Division King Abdullah University of Science and Technology Thuwal 23955 6900 Kingdom of Saudi Arabia

Department of Chemistry and Biotechnology Tallinn University of Technology Akadeemia tee 15 19086 Tallinn Estonia

Institute of Experimental Botany of the Czech Academy of Sciences Centre of the Region Haná for Biotechnological and Agricultural Research Šlechtitelů 31 78371 Olomouc Czech Republic

Limagrain Central Europe Cereals s r o Hrubčice 111 79821 Bedihošť Czech Republic

Zobrazit více v PubMed

Abrouk M, Balcárková B, Šimková H, Komínková E, Martis M, Jakobson I, Timofejeva L, Rey E, Vrána J, Kilian A, Järve K, Doležel J, Valárik M. The in silico identification and characterization of a bread wheat/Triticum militinae introgression line. Plant Biotechnol J. 2017;15:249–256. doi: 10.1111/pbi.12610. PubMed DOI PMC

Altschul SA, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H, Hale I, Mascher M, Spannagl M, Wiebe K, Jordan KW, Golan G, Deek J, Ben-Zvi B, Ben-Zvi G, Himmelbach A, MacLachlan RP, Sharpe AG, Fritz A, Ben-Davis R, Budak H, Fahima T, Korol A, Faris JD, Hernandez A, Mikel MA, Levy AA, Steffenson B, Maccaferri M, Tuberosa R, Cattivelli L, Faccioli P, Ceriotti A, Kashkush K, Pourkheirandish M, Komatsuda T, Eilam T, Sela H, Sharon A, Ohad N, Chamovitz DA, Mayer KFX, Stein N, Ronen G, Peleg Z, Pozniak CJ, Akhunov ED, Distelfeld A. Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science. 2017;357:93–97. doi: 10.1126/science.aan0032. PubMed DOI

Bariana HS, Hayden MJ, Ahmed NU, Bell JA, Sharp PJ, McIntosh RA. Mapping of durable adult plant and seedling resistances to stripe rust and stem rust diseases in wheat. Aust J Agric Res. 2001;52:1247–1255. doi: 10.1071/AR01040. DOI

Boisvert S, Laviolette F, Corbeil J. Ray: simultaneous assembly of reads from a mix of high-throughput sequencing technologies. J Comput Biol. 2010;17:1519–1533. doi: 10.1089/cmb.2009.0238. PubMed DOI PMC

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, Gaspin C, Safar J, Dolezel J, Rogers J, Vandepoele K, Aury JM, Mayer K, Berges H, Quesneville H, Wincker P, Feuillet C. Structural and functional partitioning of bread wheat chromosome 3B. Science. 2014;345:1249721. doi: 10.1126/science.1249721. PubMed DOI

Conner RL, Kuzyk AD, Su H. Impact of powdery mildew on the yield of soft white spring wheat cultivars. Can J Plant Sci. 2003;83:725–728. doi: 10.4141/P03-043. DOI

Devos KM, Dubcovsky J, Dvorak J, Chinoy CN, Gale MD. Structural evolution of wheat chromosomes 4A, 5A, and 7B and its impact on recombination. Theor Appl Genet. 1995;91:282–288. doi: 10.1007/BF00220890. PubMed DOI

Dorofeyev VF, Jakubtsiner MM, Rudenko MI, Migushova EF, Udachin RA, Merezhko AF, Semenova LV, Novikova MV, Gradchaninova OD, Shitova IP (1976) The wheats of the world. In: Brezhnev DD, Dorofeyev VF (eds), Kolos Publication, Leningrad, 487 pp. (in Russian)

Feuillet C, Langridge P, Waugh R. Cereal breeding takes a walk on the wild side. Trends Genet. 2008;24:24–32. doi: 10.1016/j.tig.2007.11.001. PubMed DOI

Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A. The Pfam protein database: towards a more sustainable future. Nucleic Acids Res. 2016;44:D279–D285. doi: 10.1093/nar/gkv1344. PubMed DOI PMC

Gornicki P, Zhu H, Wang J, Challa GS, Zhang Z, Gill BS, Li W. The chloroplast view of the evolution of polyploid wheat. New Phytol. 2014;204:704–714. doi: 10.1111/nph.12931. PubMed DOI

Hayashi N, Inoue H, Kato T, Funao T, Shirota M, Shimizu T, Kanamori H, Yamane H, Hayano-Saito Y, Matsumoto T, Yano M, Takatsuji H. Durable panicle blast-resistance gene Pb1 encodes an atypical CC-NBS-LRR protein and was generated by acquiring a promoter through local genome duplication. Plant J. 2010;64:498–510. doi: 10.1111/j.1365-313X.2010.04348.x. PubMed DOI

Hernandez P, Martis M, Dorado G, Pfeifer M, Gálvez S, Schaaf S, Jouve N, Šimková H, Valárik M, Doležel J, Mayer KFX. Next-generation sequencing and syntenic integration of flow-sorted arms of wheat chromosome 4A exposes the chromosome structure and gene content. Plant J. 2012;69:377–386. doi: 10.1111/j.1365-313X.2011.04808.x. PubMed DOI

Huang L, Brooks SA, Li W, Fellers JP, Trick HN, Gill BS. Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics. 2003;164:664–665. PubMed PMC

Hurni S, Brunner S, Buchmann G, Herren G, Jordan T, Krukowski P, Wicker T, Yahiaoui N, Mago R, Keller B. Rye Pm8 and wheat Pm3 are orthologous genes and show evolutionary conservation of resistance function against powdery mildew. Plant J. 2013;76:957–969. doi: 10.1111/tpj.12345. PubMed DOI

Islamov B, Peusha H, Jakobson I, Järve K (2015) Triticum militinae introgressions into bread wheat affect host responses to powdery mildew challenge. In: Poster session presented at 14th international cereal rusts and powdery mildews conference, Helsingør, Denmark, 5–8 July 2015

Ivaničová Z, Jakobson I, Reis D, Šafář J, Milec Z, Abrouk M, Doležel J, Järve K, Valárik M. Characterization of new allele influencing flowering time in bread wheat introgressed from Triticum militinae. New Biotechnol. 2016;33:718–727. doi: 10.1016/j.nbt.2016.01.008. PubMed DOI

IWGSC A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science. 2014;345:1251788. doi: 10.1126/science.1251788. PubMed DOI

IWGSC Shifting the limits in wheat research and breeding through a fully annotated and anchored reference genome sequence. Science. 2018;361:eaar7191. doi: 10.1126/science.aar7191. PubMed DOI

Jakobson I, Peusha H, Timofejeva L, Järve K. Adult plant and seedling resistance to powdery mildew in a Triticum aestivum × Triticum militinae hybrid line. Theor Appl Genet. 2006;112:760–769. doi: 10.1007/s00122-005-0181-2. PubMed DOI

Jakobson I, Reis D, Tiidema A, Peusha H, Timofejeva L, Valárik M, Kladivová M, Šimková H, Doležel J, Järve K. Fine mapping, phenotypic characterization and validation of non-race-specific resistance to powdery mildew in a wheat-Triticum militinae introgression line. Theor Appl Genet. 2012;125:609–623. doi: 10.1007/s00122-012-1856-0. PubMed DOI

Järve K, Peusha HO, Tsymbalova J, Tamm S, Devos KM, Enno TM. Chromosome location of a Triticum timopheevi-derived powdery mildew resistance gene transferred to common wheat. Genome. 2000;43:377–381. doi: 10.1139/g99-141. PubMed DOI

Järve K, Jakobson I, Enno T. Tetraploid wheat species Triticum timopheevi and Triticum militinae in common wheat improvement. Acta Agron Hung. 2002;50:463–477. doi: 10.1556/AAgr.50.2002.4.9. DOI

Jia J, Devos KM, Chao S, Miller TE, Reader SM, Gale MD. RFLP-based maps of the homoeologous group-6 chromosomes of wheat and their application in the tagging of Pm12, a powdery mildew resistance gene transferred from Aegilops speltoides to wheat. Theor Appl Genet. 1996;92:559–565. doi: 10.1007/BF00224558. PubMed DOI

King J, Grewal S, Yang C, Hubbart-Edwards S, Scholefield D, Ashling S, Broomfield D, Howells C, King IP (2017) A step change in the transfer of interspecific variation into wheat from its wild relatives. In: Buerstmayr H, Lang-Mladek C, Steiner B, Michel S, Buerstmayr M, Lemmens M, Vollmann J, Grausgruber H (eds) Proceedings of the 13th international wheat genetics symposium, Tulln, Austria, 23–28 April 2017. BOKU-University of Natural Resources and Life Sciences, Vienna, p. 40

Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science. 2009;323:1360–1363. doi: 10.1126/science.1166453. PubMed DOI

La Camera S, Balagué C, Geoffroy P, Legrand M, Feussner I, Roby D, Heitz T. The Arabidopsis patatin-like protein 2 (PLP2) plays an essential role in cell death execution and differentially affects biosynthesis of oxylipins and resistance to pathogens. Mol Plant Microbe Interaction. 2009;22:469–481. doi: 10.1094/MPMI-22-4-0469. PubMed DOI

Leath S, Bowen KL. Effects of powdery mildew, triadimenol seed treatment and triadimenol foliar sprays on yield of winter wheat in North Carolina. Phytopathology. 1989;79:152–155. doi: 10.1094/Phyto-79-152. DOI

Leroy P, Guilhot N, Sakai H, Bernard A, Choulet F, Theil S, Reboux S, Amano N, Flutre T, Pelegrin C, Ohyanagi H, Seidel M, Giacomoni F, Reichstadt M, Alaux M, Gicquello E, Legeai F, Cerutti L, Numa H, Tanaka T, Mayer K, Itoh T, Quesneville H, Feuillet C. TriAnnot: a versatile and high performance pipeline for the automated annotation of plant genomes. Front Plant Sci. 2011;3:1–14. PubMed PMC

Li ZK, Luo LJ, Mei HW, Paterson AH, Zhao XH, Zhong DB, Wang YP, Yu XQ, Zhu L, Tabien R, Stansel JW, Ying CS. A “defeated” rice resistance gene acts as a QTL against a virulent strain of Xanthomonas oryzae pv. oryzae. Mol Gen Genet. 1999;261:58–63. doi: 10.1007/s004380050941. PubMed DOI

Lillemo M, Lu Q (2015) A meta analysis of partial resistance loci to powdery mildew in wheat. In: Paper presented at 14th international cereal rusts and powdery mildews conference, Helsingør, Denmark, 5–8 July 2015

Lukaszewski AJ. Physical distribution of translocation breakpoints in homoeologous recombinants induced by the absence of the Ph1 gene in wheat and triticale. Theor Appl Genet. 1995;90:714–719. doi: 10.1007/BF00222138. PubMed DOI

Lukaszewski AJ. Introgressions between wheat and rye. In: Molnár-Láng M, Ceoloni C, Doležel J, editors. Alien introgression in wheat. New York: Springer; 2015. pp. 163–190.

Luo MC, Yang ZL, Kota RS, Dvořák J. Recombination of chromosome 3Am and 5Am of Triticum monococcum with homeologous chromosomes 3A and 5A of wheat: the distribution of recombination across chromosomes. Genetics. 2000;154:1301–1308. PubMed PMC

Lutz J, Limpert E, Bartos P, Zeller FJ. Identification of powdery mildew resistance genes in common wheat (Triticum aestivum L.) Plant Breed. 1992;108:33–39. doi: 10.1111/j.1439-0523.1992.tb00097.x. DOI

Mago R, Tabe L, Vautrin S, Šimková H, Kubaláková M, Upadhyaya N, Berges H, Kong X, Breen J, Doležel J, Appels R, Ellis JG, Spielmeyer W. Major haplotype divergence including multiple germin-like protein genes, at the wheat Sr2 adult plant stem rust resistance locus. BMC Plant Biol. 2014;14:379. doi: 10.1186/s12870-014-0379-z. PubMed DOI PMC

Mago R, Vautrin S, Šimková H, Bansal U, Luo MC, Rouse M, Karaoglu H, Periyannan S, Kolmer J, Jin Y, Ayliffe MA, Bariana H, Park RF, McIntosh R, Doležel J, Bergès H, Spielmeyer W, Lagudah ES, Ellis JG, Dodds PN. The wheat Sr50 gene reveals rich diversity at a cereal disease resistance locus. Nat Plants. 2015;1:15186. doi: 10.1038/nplants.2015.186. PubMed DOI

Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45:D200–D203. doi: 10.1093/nar/gkw1129. PubMed DOI PMC

Michaels SD, Amasino RM. A robust method for detecting single-nucleotide changes as polymorphic markers by PCR. Plant J. 1999;14:381–385. doi: 10.1046/j.1365-313X.1998.00123.x. PubMed DOI

Michelmore RW, Meyers BC. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 1998;8:1113–1130. doi: 10.1101/gr.8.11.1113. PubMed DOI

Mondal S, Rutkoski JE, Velu G, Singh PK, Crespo-Herrera LA, Guzmán C, Bhavani S, Lan C, He X, Singh RP. Harnessing diversity in wheat to enhance grain yield, climate resilience, disease and insect pest resistance and nutrition through conventional and modern breeding approaches. Front Plant Sci. 2016;7:991. doi: 10.3389/fpls.2016.00991. PubMed DOI PMC

Periyannan S, Moore J, Ayliffe M, Bansal U, Wang X, Huang L, Deal K, Luo M, Kong X, Bariana H, Mago R, McIntosh R, Dodds P, Dvorak J, Lagudah E. The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science. 2013;341:786–788. doi: 10.1126/science.1239028. PubMed DOI

Rajaraman J, Douchkov D, Hensel G, Stefanoto FL, Gordon A, Ereful N, Caldararu OF, Petrescu AJ, Kumlehn J, Boyd LA, Schweizer P. An LRR/malectin receptor-like kinase mediates resistance to non-adapted and adapted powdery mildew fungi in barley and wheat. Front Plant Sci. 2016;7:1836. doi: 10.3389/fpls.2016.01836. PubMed DOI PMC

Riley R, Chapman V. Genetic control of the cytologically diploid behavior of hexaploid wheat. Nature. 1958;182:713–715. doi: 10.1038/182713a0. DOI

Roberts MA, Reader SM, Dalgliesh C, Miller TE, Foote TN, Fish LJ, Snape JW, Moore G. Induction and characterization of Ph1 wheat mutants. Genetics. 1999;153:1909–1918. PubMed PMC

Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier MH, Leroy P, Ganal MW. A microsatellite map of wheat. Genetics. 1998;149:2007–2023. PubMed PMC

Saintenac C, Zhang W, Salcedo A, Rouse MN, Trick HN, Akhunov E, Dubcovsky J. Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science. 2013;341:783–786. doi: 10.1126/science.1239022. PubMed DOI PMC

Sánchez-Martín J, Steuernagel B, Ghosh S, Herren G, Hurni S, Adamski N, Vrána J, Kubaláková M, Krattinger SG, Wicker T, Doležel J, Keller B, Wulff BBH. Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol. 2016;17:221. doi: 10.1186/s13059-016-1082-1. PubMed DOI PMC

Sears ER. Induced mutant with homoeologous pairing in common wheat. Can J Genet Cytol. 1977;19:585–593. doi: 10.1139/g77-063. DOI

Sekhwal MK, Li PC, Lam I, Wang XE, Cloutier S, You FM. Disease resistance gene analogs in plants. Int J Mol Sci. 2015;16:19248–19290. doi: 10.3390/ijms160819248. PubMed DOI PMC

Šimková H, Svensson JT, Condamine P, Hřibová E, Suchánková P, Bhat PR, Bartoš J, Šafář J, Close TJ, Doležel J. Coupling amplified DNA from flow-sorted chromosomes to high-density SNP mapping in barley. BMC Genom. 2008;9:294. doi: 10.1186/1471-2164-9-294. PubMed DOI PMC

Šimková H, Šafář J, Kubaláková M, Suchánková P, Číhalíková J, Robert-Quatre H, Azhaguvel P, Weng Y, Peng J, Lapitan NLV, Ma Y, You FM, Luo M, Bartoš J, Doležel J. BAC libraries from wheat chromosome 7D: efficient tool for positional cloning of aphid resistance genes. J Biomed Biotechnol. 2011;2011:302543. PubMed PMC

Steuernagel B, Periyannan SK, Hernández-Pinzón I, Witek K, Rouse MN, Yu G, Hatta A, Ayliffe M, Bariana H, Jones JDG, Lagudah ES, Wulff BBH. Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nat Biotechnol. 2016;34:652–655. doi: 10.1038/nbt.3543. PubMed DOI

Thind AK, Wicker T, Šimková H, Fossati D, Moullet O, Brabant C, Vrána J, Doležel J, Krattinger S. Rapid cloning of genes in hexaploid wheat using cultivar-specific long-range chromosome assembly. Nat Biotechnol. 2017;35:793–796. doi: 10.1038/nbt.3877. PubMed DOI

Tiwari VK, Wang S, Sehgal S, Vrána J, Friebe B, Kubaláková M, Chhuneja P, Doležel J, Akhunov E, Kalia B, Sabir J, Gill BS. SNP discovery for mapping alien introgressions in wheat. BMC Genom. 2014;15:273. doi: 10.1186/1471-2164-15-273. PubMed DOI PMC

Tsõmbalova J, Karafiátová M, Vrána J, Kubaláková M, Peusha H, Jakobson I, Järve M, Valárik M, Doležel J, Järve K. A haplotype specific to North European wheat (Triticum aestivum L.) Genet Resour Crop Evol. 2016;64:653–664. doi: 10.1007/s10722-016-0389-9. DOI

Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. Primer3: new capabilities and interfaces. Nucleic Acids Res. 2012;40:e115. doi: 10.1093/nar/gks596. PubMed DOI PMC

Valárik M, Linkiewicz AM, Dubcovsky J. A microcolinearity study at the earliness per se gene Eps-Am 1 region reveals an ancient duplication that preceded the wheat-rice divergence. Theor Appl Genet. 2006;112:945–957. doi: 10.1007/s00122-005-0198-6. PubMed DOI

Valkoun JJ. Wheat pre-breeding using wild progenitors. Euphytica. 2001;119:17–23. doi: 10.1023/A:1017562909881. DOI

van der Biezen EA, Jones JDG. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol. 1998;8:R226–R227. doi: 10.1016/S0960-9822(98)70145-9. PubMed DOI

Wicker T, Yahiaoui N, Guyot R, Schlagenhauf E, Liu ZD, Dubcovsky J, Keller B. Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and Am genomes of wheat. Plant Cell. 2003;15:1186–1197. doi: 10.1105/tpc.011023. PubMed DOI PMC

Winfield MO, Allen AM, Burridge AJ, Barker GLA, Benbow HR, Wilkinson PA, Coghill J, Waterfall C, Davassi A, Scopes G, Pirani A, Webster T, Brew F, Bloor C, King J, West C, Griffiths S, King I, Bentley AR, Edwards KJ. High-density SNP genotyping array for hexaploid wheat and its secondary and tertiary gene pool. Plant Biotechnol J. 2016;14:1195–1206. doi: 10.1111/pbi.12485. PubMed DOI PMC

Ye ZM, Ting JPY. NLR, the nucleotide-binding domain leucine-rich repeat containing gene family. Curr Opin Immunol. 2008;20:3–9. doi: 10.1016/j.coi.2008.01.003. PubMed DOI

Zamir D. Improving plant breeding with exotic genetic libraries. Nat Rev Genet. 2001;2:983–989. doi: 10.1038/35103590. PubMed DOI

The chromatin determinants and Ph1 gene effect at wheat sites with contrasting recombination frequency

Identification, High-Density Mapping, and Characterization of New Major Powdery Mildew Resistance Loci From the Emmer Wheat Landrace GZ1

Powdery Mildew Resistance Phenotypes of Wheat Gene Bank Accessions