Abstract
Key message
We identified TdPm60 alleles from wild emmer wheat (WEW), an ortholog of Pm60 from T. urartu, which constitutes a strong candidate for PmG16 mildew resistance. Deployment of PmG16 in Israeli modern bread wheat cultivar Ruta improved the resistance to several local Bgt isolates.
Abstract
Wild emmer wheat (WEW), the tetraploid progenitor of durum and bread wheat, is a valuable genetic resource for resistance to powdery mildew fungal disease caused by Blumeria graminis f. sp. tritici (Bgt). PmG16 gene, derived from WEW, confers high resistance to most tested Bgt isolates. We mapped PmG16 to a 1.4-cM interval between the flanking markers uhw386 and uhw390 on Chromosome 7AL. Based on gene annotation of WEW reference genome Zavitan_V1, 34 predicted genes were identified within the ~ 3.48-Mb target region. Six genes were annotated as associated with disease resistance, of which TRIDC7AG077150.1 was found to be highly similar to Pm60, previously cloned from Triticum urartu, and resides in the same syntenic region. The functional molecular marker (FMM) for Pm60 (M-Pm60-S1) co-segregated with PmG16, suggesting the Pm60 ortholog from WEW (designated here as TdPm60) as a strong candidate for PmG16. Sequence alignment identified only eight SNPs that differentiate between TdPm60 and TuPm60. Furthermore, TdPm60 was found to be present also in the WEW donor lines of the powdery mildew resistance genes MlIW172 and MlIW72, mapped to the same region of Chromosome 7AL as PmG16, suggesting that TdPm60 constitutes a candidate also for these genes. Furthermore, screening of additional 230 WEW accessions with Pm60 specific markers revealed 58 resistant accessions from the Southern Levant that harbored TdPm60, while none of the susceptible accessions showed the presence of this gene. Deployment of PmG16 in Israeli modern bread wheat cultivar Ruta conferred resistance against several local Bgt isolates.
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07 July 2021
A Correction to this paper has been published: https://doi.org/10.1007/s00122-021-03894-z
References
Asif M, Iqbal M, Randhawa H, Spaner D (2014) Wheat: The miracle cereal. Managing and breeding wheat for organic systems. Springer, Cham, pp 1–7
Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H, Hale I, Mascher M, Spannagl M, Wiebe K, Jordan KW (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357(6346):93–97
Ben-David R, Xie W, Peleg Z, Saranga Y, Dinoor A, Fahima T (2010) Identification and mapping of PmG16, a powdery mildew resistance gene derived from wild emmer wheat. Theor Appl Genet 121(3):499–510
Bhullar NK, Street K, Mackay M, Yahiaoui N, Keller B (2009) Unlocking wheat genetic resources for the molecular identification of previously undescribed functional alleles at the Pm3 resistance locus. Proc Natl Acad Sci 106(23):9519–9524
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10(1):421
Chhuneja P, Yadav B, Stirnweis D, Hurni S, Kaur S, Elkot AF, Keller B, Wicker T, Sehgal S, Gill BS, Singh K (2015) Fine mapping of powdery mildew resistance genes PmTb7A. 1 and PmTb7A. 2 in Triticum boeoticum (Boiss.) using the shotgun sequence assembly of chromosome 7AL. Theor Appl Genetics 128(10):2099–2111
DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7(12):1243–1249
Distelfeld A, Uauy C, Fahima T, Dubcovsky J (2006) Physical map of the wheat high-grain protein content gene Gpc-B1 and development of a high-throughput molecular marker. New Phytol 169(4):753–763
Fatiukha A, Deblieck M, Klymiuk V, Merchuk-Ovnat L, Peleg Z, Ordon F, Fahima T, Korol AB, Saranga Y and Krugman T (2019) Genomic architecture of phenotypic plasticity of complex traits in tetraploid wheat in response to water stress. bioRxiv, 565820
Feldman M, Kislev ME (2007) Domestication of emmer wheat and evolution of free-threshing tetraploid wheat. Israel J Plant Sci 55(3–4):207–221
Han J, Zhang L, Li G, Zhang H, Xie C, Yang Z, Sun Q, Liu Z (2009) Molecular mapping of powdery mildew resistance gene MlWE18 in wheat originated from wild emmer (Triticum turgidum van dicoccoides). Acta Agron Sin 35(10):1791–1797
He H, Zhu S, Zhao R, Jiang Z, Ji Y, Ji J, Qiu 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(6):879–882
Hewitt T, Mueller MC, Molnár I, Mascher M, Holušová K, Šimková H, Kunz L, Zhang J, Li J, Bhatt D, Sharma R, Schudel S, Yu G, Steuernagel B, Periyannan S, Wulff B, Ayliffe M, McIntosh R, Keller B, Lagudah E, Zhang P (2020) A highly differentiated region of wheat chromosome 7AL encodes a Pm1a immune receptor that recognises its corresponding AvrPm1a effector from Blumeria graminis. New Phytol. https://doi.org/10.1111/nph.17075
Hsam SLK, Zeller FJ (1997) Evidence of allelism between genes Pm8 and Pm17 and chromosomal location of powdery mildew and leaf rust resistance genes in the common wheat cultivar ‘Amigo.’ Plant Breeding 116(2):119–122
Hsam SLK, Huang XQ, Ernst F, Hartl L, Zeller FJ (1998) Chromosomal location of genes for resistance to powdery mildew in common wheat (Triticum aestivum L. em Thell.) 5 Alleles at the Pm1 locus. Theor Appl Genet 96(8):1129–1134
Huang L, Raats D, Sela H, Klymiuk V, Lidzbarsky G, Feng L, Krugman T, Fahima T (2016) Evolution and adaptation of wild emmer wheat populations to biotic and abiotic stresses. Annu Rev Phytopathol 54:279–301
Hurni S, Brunner S, Buchmann G, Herren G, Jordan T, Krukowski P, Wicker T, Yahiaoui N, Mago R, Keller B (2013) Rye Pm8 and wheat Pm3 are orthologous genes and show evolutionary conservation of resistance function against powdery mildew. Plant J 76(6):957–969
Ji X, Xie C, Ni Z, Yang T, Nevo E, Fahima T, Liu Z, Sun Q (2008) Identification and genetic mapping of a powdery mildew resistance gene in wild emmer (Triticum dicoccoides) accession IW72 from Israel. Euphytica 159(3):385–390
Jupe F, Pritchard L, Etherington GJ, MacKenzie K, Cock PJ, Wright F, Sharma SK, Bolser D, Bryan GJ, Jones JD, Hein I (2012) Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genomics 13(1):75
Kahle D, Wickham H (2013) ggmap: Spatial visualization with ggplot2. The R Journal 5(1):144–161
Klymiuk V, Yaniv E, Huang L, Raats D, Fatiukha A, Chen S, Feng L, Frenkel Z, Krugman T, Lidzbarsky G, Chang W (2018) Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family. Nat Commun 9(1):1–12
Klymiuk V, Fatiukha A, Huang L, Wei Z, Kis-Papo T, Saranga Y, Krugman T, Fahima T (2019) Durum wheat as a bridge between wild emmer wheat genetic resources and bread wheat. Applications of Genetic and Genomic Research in Cereals. Woodhead Publishing, UK, pp 201–230
Klymiuk V, Fatiukha A, Raats D, Bocharova V, Huang L, Feng L, Jaiwar S, Pozniak C, Coaker G, Dubcovsky J, Fahima T (2020) Three previously characterized resistances to yellow rust are encoded by a single locus Wtk1. J Exp Bot 71(9):2561–2572
Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323(5919):1360–1363
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Li N, Wen Z, Wang J, Fu B, Liu J, Xu H, Kong Z, Zhang L, Jia H, Ma Z (2014) Transfer and mapping of a gene conferring later-growth-stage powdery mildew resistance in a tetraploid wheat accession. Mol Breeding 33(3):669–677
Li M, Dong L, Li B, Wang Z, Xie J, Qiu D, Li Y, Shi W, Yang L, Wu Q, Chen Y (2020) A CNL protein in wild emmer wheat confers powdery mildew resistance. New Phytol 228:1027–1037
Liang J, Fu B, Tang W, Khan NU, Li N, Ma Z (2016) Fine mapping of two wheat powdery mildew resistance genes located at the Pm1 cluster. Plant Genome 9(2):1–9
Ling H, Ma B, Shi X, Liu H, Dong L, Sun H, Cao Y, Gao Q, Zheng S, Li Y, Yu Y (2018) Genome sequence of the progenitor of wheat A subgenome Triticum urartu. Nature 557(7705):424–428
Lu P, Guo L, Wang Z, Li B, Li J, Li Y, Qiu D, Shi W, Yang L, Wang N, Guo G (2020) A rare gain of function mutation in a wheat tandem kinase confers resistance to powdery mildew. Nat Commun 11(1):1–11
Maccaferri M, Harris NS, Twardziok SO, Pasam RK, Gundlach H, Spannagl M, Ormanbekova D, Lux T, Prade VM, Milner SG, Himmelbach A (2019) Durum wheat genome highlights past domestication signatures and future improvement targets. Nat Genet 51(5):885–895
Maxwell JJ, Lyerly JH, Cowger C, Marshall D, Brown-Guedira G, Murphy JP (2009) MlAG12: a Triticum timopheevii-derived powdery mildew resistance gene in common wheat on chromosome 7AL. Theor Appl Genet 119(8):1489–1495
McIntosh RA, Dubcovsky J, Rogers WJ et al (2019) Catalogue of gene symbols for wheat: 2019 Supplement. Annul Wheat Newsletter 65:98–109
Moore JW, Herrera-Foessel S, Lan C, Schnippenkoetter W, Ayliffe M, Huerta-Espino J, Lillemo M, Viccars L, Milne R, Periyannan S, Kong X (2015) A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat Genet 47(12):1494–1498
Neu C, Stein N, Keller B (2002) Genetic mapping of the Lr20 Pm1 resistance locus reveals suppressed recombination on chromosome arm 7AL in hexaploid wheat. Genome 45(4):737–744
Ouyang S, Zhang D, Han J, Zhao X, Cui Y, Song W, Huo N, Liang Y, Xie J, Wang Z, Wu Q (2014) Fine physical and genetic mapping of powdery mildew resistance gene MlIW172 originating from wild emmer (Triticum dicoccoides). PloS One 9(6):e100160
Peleg Z, Saranga Y, Suprunova T, Ronin Y, Röder MS, Kilian A, Korol AB, Fahima T (2008) High-density genetic map of durum wheat × wild emmer wheat based on SSR and DArT markers. Theor Appl Genet 117(1):103
Porebski S, Bailey LG, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Report 15:8–15
Qiu Y, Zhou R, Kong X, Zhang S, Jia J (2005) Microsatellite mapping of a Triticum urartu Tum. derived powdery mildew resistance gene transferred to common wheat (Triticum aestivum L.). Theor Appl Genet 111(8):1524–1531
Sánchez-Martín J, Steuernagel B, Ghosh S, Herren G, Hurni S, Adamski N, Vrána J, Kubaláková M, Krattinger SG, Wicker T, Doležel J (2016) Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol 17(1):221
Sánchez-Martín J, Widrig V, Herren G, Wicker T, Zbinden H, Gronnier J, Spörri L, Praz CR, Heuberger M, Kolodziej MC, Isaksson J, Steuernagel B, Karafiátová M, Doležel J, Zipfel C, Keller B (2021) Wheat Pm4 resistance to powdery mildew is controlled by alternative splice variants encoding chimeric proteins. Nat Plants 7(3):327–341
Sela H, Ezrati S, Ben-Yehuda P, Manisterski J, Akhunov E, Dvorak J, Breiman A, Korol A (2014) Linkage disequilibrium and association analysis of stripe rust resistance in wild emmer wheat (Triticum turgidum ssp. dicoccoides) population in Israel. Theor Appl Genet 127(11):2453–2463
Shen J, Araki H, Chen L, Chen J, Tian D (2006) Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana. Genetics 172(2):1243–1250
Shen Q, Li Y, Zhao F, and Zhou L (2018) Development and application of specific molecular markers for identification of powdery mildew resistance gene Pm60. China patent CN 108950057A
Singh RP, Singh PK, Rutkoski J, Hodson DP, He X, Jørgensen LN, Hovmøller MS, Huerta-Espino J (2016) Disease impact on wheat yield potential and prospects of genetic control. Annu Rev Phytopathol 54:303–322
Steuernagel B, Witek K, Krattinger SG, Ramirez-Gonzalez RH, Schoonbeek HJ, Yu G, Baggs E, Witek AI, Yadav I, Krasileva KV, Jones JD (2020) The NLR-Annotator tool enables annotation of the intracellular immune receptor repertoire. Plant Physiol 183(2):468–482
Tang D, Zou S (2017) Wheat powdery mildew resistant gene PmR2 and its clone and application. China patent CN201710632539.2A
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants: H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11(6):1187–1194
Van Ooijen JW (2006) JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen, Netherlands, p 33
van Wees S (2008) Phenotypic analysis of Arabidopsis mutants: trypan blue stain for fungi, oomycetes, and dead plant cells. Cold Spring Harbor Protocols 8: pdb-prot4982
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78
Walkowiak S, Gao L, Monat C, Haberer G, Kassa MT, Brinton J et al (2020) Multiple wheat genomes reveal global variation in modern breeding. Nature 588:277–283
Wei Z, Klymiuk V, Bocharova V, Pozniak C, Fahima T (2020) A post-haustorial defense mechanism is mediated by the powdery mildew resistance gene, PmG3M, derived from wild emmer wheat. Pathogens 9(6):418
Wicker T, Yahiaoui N, Keller B (2007) Illegitimate recombination is a major evolutionary mechanism for initiating size variation in plant resistance genes. Plant J 51(4):631–641
Xie W, Ben-David R, Zeng B, Distelfeld A, Röder MS, Dinoor A, Fahima T (2012) Identification and characterization of a novel powdery mildew resistance gene PmG3M derived from wild emmer wheat, Triticum Dicoccoides. Theor Appl Genet 124(5):911–922
Xie J, Guo G, Wang Y, Hu T, Wang L, Li J, Qiu D, Li Y, Wu Q, Lu P, Chen Y et al (2020) A rare single nucleotide variant in Pm5e confers powdery mildew resistance in common wheat. New Phytol 228:1011–1026
Xing L, Hu P, Liu J, Witek K, Zhou S, Xu J, Zhou W, Gao L, Huang Z, Zhang R, Wang X (2018) Pm21 from Haynaldia villosa encodes a CC-NBS-LRR protein conferring powdery mildew resistance in wheat. Mol Plant 11(6):874–878
Xu X, Li Q, Ma Z, Fan J, Zhou Y (2018) Molecular mapping of powdery mildew resistance gene PmSGD in Chinese wheat landrace Shangeda using RNA-seq with bulk segregant analysis. Mol Breeding 38(3):23
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(4):528–538
Yahiaoui N, Kaur N, Keller B (2009) Independent evolution of functional Pm3 resistance genes in wild tetraploid wheat and domesticated bread wheat. Plant J 57(5):846–856
Yao G, Zhang J, Yang L, Xu H, Jiang Y, Xiong L, Zhang C, Zhang Z, Ma Z, Sorrells ME (2007) Genetic mapping of two powdery mildew resistance genes in einkorn (Triticum monococcum L.) accessions. Theor Appl Genet 114(2):351–358
Young ND, Tanksley SD (1989) Restriction fragment length polymorphism maps and the concept of graphical genotypes. Theor Appl Genet 77(1):95–101
Zhang L, Zheng X, Qiao L, Qiao L, Wang ZJ, Zheng J (2018) Analysis of three types of resistance gene analogs in PmU region from Triticum urartu. J Integr Agric 17(12):2601–2611
Zhang D, Zhu K, Dong L, Liang Y, Li G, Fang T, Guo G, Wu Q, Xie J, Chen Y, Lu P et al (2019) 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. Crop J 7(6):761–770
Zhao F, Li Y, Yang B, Yuan H, Jin C, Zhou L, Pei H, Zhao L, Li Y, Zhou Y, Xie J, Shen Q (2020) Powdery mildew disease resistance and marker-assisted screening at the Pm60 locus in wild diploid wheat Triticum urartu. Crop J 8(2):252–259
Zhou Y, Zhao X, Li Y, Xu J, Bi A, Kang L, Xu D, Chen H, Wang Y, Wang Y, Liu S, Jiao C, Lu H, Wang J, Yin C, Jiao Y, Lu F (2020) Triticum population sequencing provides insights into wheat adaptation. Nat Genet 52:1412–1422
Zhu T, Wang L, Rodriguez JC, Deal KR, Avni R, Distelfeld A, McGuire PE, Dvorak J, Luo MC (2019) Improved genome sequence of wild emmer wheat Zavitan with the aid of optical maps. G3: Genes Genomes Genetics 9(3):619–624
Zou S, Wang H, Li Y, Kong Z, Tang D (2018) The NB-LRR gene Pm60 confers powdery mildew resistance in wheat. New Phytol 218(1):298–309
Acknowledgements
Y.L. was supported by a fellowship provided by the Planning and Budgeting Committee (PBC) of the Israel Council for Higher Education for Outstanding Post-doctoral Fellows from China and India—from 2018 to 2021. Z.W. was supported by the China Scholarship Council for financial support and the University of Haifa Graduate School. The authors wish to thank Dr. Meng Xu for the development of the geographic distribution map, Dr. Tamar Kis-papo and Souad Khalifa for their technical support, Dr. Imad Shams and Tamar Lotan Labs for assistance in microscopy works, and Dr. Rajib Roychowdhury for critical reading and English editing of the manuscript.
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This study was supported by the Israel Science Foundation, grant number 1719/08 and 1366/18.
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TF, YL, and ZW conceived and designed the study; ZW, AF, and YL developed the critical RILs; AF, ZW, and YL performed data analysis of genotyping by 15 K wheat SNP arrays of Trait Genetics®; HW, ZW, SJ, and YL were involved in marker development and analysis; YL, ZW, and SJ done microscopic observations; ZW, YL, SH, and SJ done phenotyping; YL and SJ contributed to sequencing; TK and YL performed germplasm selection; AF, YL, and HS done bioinformatic analysis of Pm60 locus; YL and TF wrote the manuscript; AF, HS, ZW, TK, and TF reviewed and edited the manuscript; TF was involved in coordination and funding acquisition.
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Li, Y., Wei, ZZ., Fatiukha, A. et al. TdPm60 identified in wild emmer wheat is an ortholog of Pm60 and constitutes a strong candidate for PmG16 powdery mildew resistance. Theor Appl Genet 134, 2777–2793 (2021). https://doi.org/10.1007/s00122-021-03858-3
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DOI: https://doi.org/10.1007/s00122-021-03858-3