5.9
CiteScore
5.9
Impact Factor
Volume 49 Issue 8
Aug.  2022
Turn off MathJax
Article Contents
Article Navigation >  Journal of Genetics and Genomics  > 2022  >  49(8): 787-795

Functional characterization of powdery mildew resistance gene MlIW172, a new Pm60 allele and its allelic variation in wild emmer wheat

doi: 10.1016/j.jgg.2022.01.010
  •  

    a. State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China;

  •  

    b. College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 100049, China;

  •  

    c. Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing University of Agriculture, Beijing 102206, China;

  •  

    d. Institute of Evolution and the Department of Evolutionary and Environmental Biology, University of Haifa, Mt. Carmel, Haifa 3498838, Israel;

  •  

    e. The National Engineering Laboratory of Crop Molecular Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China

Funds:

We are grateful to Profs. Qixin Sun and Tsomin Yang, China Agricultural University, China, for their advice and support during the research. Many thanks to Profs. Zhengqiang Ma and Haiyan Jia of Nanjing Agricultural University, China, for information exchange. This work was financially supported by National Science Foundation of China (31971876, U21A20224) and Scientific Research Project of Beijing Municipal Commission of Education (KM201910020014).

  • Received Date: 2021-11-27
  • Accepted Date: 2022-01-29
  • Rev Recd Date: 2022-01-26
  • Publish Date: 2022-02-12
    Abstract
  • Wild emmer wheat (Triticum dicoccoides, WEW) is an immediate progenitor of both the cultivated tetraploid and hexaploid wheats and it harbors rich genetic diversity against powdery mildew caused by Blumeria graminis f. sp. tritici (Bgt). A powdery mildew resistance gene MlIW172 originated from WEW accession IW172 (G-797-M) is fine mapped in a 0.048 centimorgan (cM) genetic interval on 7AL, corresponding to a genomic region spanning 233kb, 1Mb and 800kb in Chinese Spring, WEW Zavitan, and T.urartu G1812, respectively. MlIW172 encodes a typical NLR protein NLRIW172 and physically locates in an NBS-LRR gene cluster. NLR is subsequently identified as a new allele of Pm60, and its function is validated by EMS mutagenesis and transgenic complementation. Haplotype analysis of the Pm60 alleles reveals diversifications in sequence variation in the locus and presence and absence variations (PAV) in WEW populations. Four common single nucleotide variations (SNV) are detected between the Pm60 alleles from WEW and T.urartu, indicative of speciation divergence between the two different wheat progenitors. The newly identified Pm60 alleles and haplotypes in WEW are anticipated to be valuable for breeding powdery mildew resistance wheat cultivars via marker-assisted selection.
    • FullText(HTML)
  • loading
    • References(60)
  • Allen, G.C., Flores-Vergara, M.A., Krasnyanski, S., Kumar, S., Thompson, W.F., 2006. A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat. Protoc. 1, 2320-2325
    Arora, S., Steuernagel, B., Gaurav, K., Chandramohan, S., Long, Y.M., Matny, O., Johnson, R., Enk, J., Periyannan, S., Singh, N., et al., 2019. Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nat. Biotechnol. 37, 139-143
    Bayer, P.E., Golicz, A.A., Scheben, A., Batley, J., Edwards, D., 2020. Plant pan-genomes are the new reference. Nat. Plants 6, 914-920
    Ben-David, R., Xie, W.L., 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, 499-510
    Bialas, A., Zess, E.K., Concepcion, J.C.D.L., Franceschetti, M., Pennington, H.G., Yoshida, K., Upson, J.L., Chanclud, E., Wu, C.H., Langner, T., 2018. Lessons in effector and NLR biology of plant-microbe system. Mol. Plant Microbe In. 31, 34-45
    Fu, D.L., Uauy, C., Distelfeld, A., Blechl, A., Epstein, L., Chen, X.M., Sela, H., Fahima, T., Dubcovsky, J., 2009. A novel kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323, 1357-1360
    Gaurav, K., Arora, S., Silva, P., Sanchez-Martin, J., Horsnell, R., Gao, L.L., Brar, G.S., Widrig, V., Raupp, W.J., Singh, N., et al., 2021. Population genomic analysis of Aegilops tauschii identifies targets for bread wheat improvement. Nat. Biotechnol. doi.org/10.1038/s41587-021-01058-4
    Golicz, A.A., Bayer, P.E., Barker, G.C., Edger, P.P., Kim, H., Martinez, P.A., Chan, C.K.K., Severn-Ellis, A., McCombie, W.R., Parkin, I.A.P., et al., 2016. The pangenome of an agronomically important crop plant Brassica oleracea. Nat. Commun. 7, 13390
    Hafeez, A.N., Arora, S., Ghosh, S., Gilbert, D., Bowden, R.L., Wulff, B.B.H., 2021. Creation and judicious application of a wheat resistance gene atlas. Mol. Plant 14, 1053-1070
    Hewitt, T., Mueller, M.C., Molnar, I., Mascher M., Holosova K., Simkova H., Kunz, L., Zhang, J.P., Li, J.B., Bhatt, D., et al., 2020. A highly differentiated region of wheat chromosome 7AL encodes a Pm1a immune receptor that recognize its corresponding AvrPm1a effector from Blumeria graminis. New Phytol. 229, 2812-2826
    Huang L., Sela H., Feng L., Chen Q., Krugman T., Yan J., Dubcovsky J. Fahima, T., 2016. Distribution and haplotype diversity of WKS resistance genes in wild emmer wheat natural populations. Theor. Appl. Genet. 129, 921-934
    Ishida, Y., Tsunashima, M., Hiei, Y., Komari, T., 2015. Wheat (Triticum aestivum L.) transformation using immature embryos. Methods Mol. Biol. 1223, 189-198
    Jayakodi, M., Padmarasu, S., Haberer, G., Bonthala, V.S., Gundlach, H., Monat, C., Lux, T., Kamal, N., Lang, D., Himmelbach, A., et al., 2020. The barley pan-genome reveals the hidden legacy of mutation breeding. Nature 588, 284-289
    Ji, X.L., Xie, C.J., Ni, Z.F., Yang, T., Nevo, E., Fahina, T., Liu, Z.Y., Sun, Q.X., 2008. Identification and genetic mapping of a powdery mildew resistance gene in wild emmer (Triticum dicoccoides) accession IW72 from Israel. Euphytica 159, 385-390
    Klymiuk V., Fatiukha A., Fahima T., 2019. Wheat tandem kinase provide insights on disease-resistance gene flow and host-parasite co-evolution. Plant J. 98, 667-679
    Klymiuk, V., Yaniv, E., Huang, L., Raats, D., Fatiukha, A., Chen, S.S., Feng, L.H., Frenkel, Z., Krugman, T., Lidzbarsky, G., et al., 2018. Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family. Nat. Commun. 9, 3735
    Krattinger, S.G., Lagudah, E.S., Spielmeyer, W., Singh, R.P., Huerta-Espino, J., McFadden, H., Bossolini, E. Selter, L.L., Keller, B., 2009. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323, 1360-1363
    Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7:molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874
    Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., et al., 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948
    Li, G.Q., Cowger, C., Wang, X.W., Carver, B.F., Xu, X.Y., 2019. Characterization of Pm65, a new powdery mildew resistance gene on chromosome 2AL of a facultative wheat cultivar. Theor. Appl. Genet. 132, 2625-2632
    Li, M.M., Dong, L.L., Li, B.B., Wang, Z.Z., Xie, J.Z., Qiu, D., Li, Y.H., Shi, W.Q., Yang, L.J., Wu, Q.H., et al., 2020. A NLR protein in wild emmer wheat confers powdery mildew resistance. New Phytol. 228, 1027-1037
    Li, Y.H., Wei, Z.Z., Fatiukha, A., Jaiwar, S., Wang, H.C., Hasan, S., Liu, Z.Y., Sela, H., Krugman, T., Fahima, T., 2021. 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
    Liang, J.C., Fu, B.S., Tang, W.B., Khan, N.U., Li, N., Ma, Z.Q., 2016. Fine mapping of two wheat powdery mildew resistance genes located at the Pm1 cluster. Plant Genome 9, 1-9
    Liang, Y., Zhang, D.Y., Ouyang, S.H., Xie, J.Z., Wu, Q.H., Wang, Z.Z., Cui, Y., Lu, P., Zhang, D., Liu, Z.J., et al., 2015. Dynamic evolution of resistance gene analogs in the orthologous genomic regions of powdery mildew resistance gene MlIW170 in Triticum dicoccoides and Aegilops tauschii. Theor. Appl. Genet. 128, 1617-1629
    Lincoln, L., Lander, E., 1993. Constructing Genetic Linkage Maps with MAPMAKER/EXP Version 3.0:A tutorial and reference manual. Cambridge, Lander ES, 1-9
    Livak, K.J., Schmittgen, T.D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods (San Diego, Calif.) 25, 402-408
    Lu, P., Guo, L., Wang, Z.Z., Li, B.B., Li, J., Li, Y.H., Qiu, D., Shi. W.Q., Yang, L.J., Wang, N., et al., 2020. A rare gain of function mutation in a wheat tandem kinase confers resistance to powdery mildew. Nat. Commun. 11, 680
    Luo, S., Zhang, Y., Hu, Q., Chen, J.J., Li, K.P., Liu, C., Liu, H., Wang, W., Kuang, H.H., 2012. Dynamic nucleotide-binding site and leucine-rich repeat-encoding genes in the grass family. Plant Physiol. 159, 197-210
    Ma, S.W., Wang, M., Wu, J.H., Guo, W.L., Chen, Y.M., Li, G.W., Wang, Y.P., Shi, W.M., Xia, G.M., et al., 2021. WheatOmics:a platform combining multiple omics data to accelerate functional genomics studies in wheat. Mol. Plant 14, 1965-1968
    Marchal, C., Zhang, J.P., Zhang, P., Fenwick, P., Steuernagel, B., Adamski, N.M., Boyd, L., McIntosh, R., Wulff, B.B.H., Berry, S., et al., 2018. BED-domain-containing immune receptors confer diverse resistance spectra to yellow rust. Nat. Plants 4, 662-668
    McIntosh, R.A., Dubcovsky, J., Rogers, W.J., Xia, X.C., Raupp, W.J., 2021. Catalogue of gene symbols for wheat:2021 supplement. Annu Wheat Newsletter 67, 104-113
    Meyers, B.C., Kozik, A., Griego, A., Kuang, H.H., Michelmore, R.W., 2003. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15, 809-834
    Montenegro, J.D., Golicz, A.A., Bayer, P.E., Hurgobin, B., Lee, H., Chan, C.K., Visendi, P., Lai, K., Dolezel, J., Batley, J., et al., 2017. The pangenome of hexaploid bread wheat. 90, 1007-1013
    Monosi, B., Wisser, R.J., Pennill, L., Hulbert, S.H., 2004. Full-genome analysis of resistance gene homologues in rice. Theor. Appl. Genet. 109, 1434-1447
    Moseman, J.G., Nevo, E., Morshidy, M.A.E., Zohary, D., 1984. Resistance of Triticum dicoccoides to infection with Erysiphe graminis tritici. Euphytica 33, 41-47
    Narusaka, M., Shirasu, K., Noutoshi, Y., Kubo, Y., Shiraishi, T., Iwabuchi, M., Narusaka1, Y., 2009. RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J. 60, 218-226
    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, 737-744
    Nevo, E., Korol, A.B., Beiles, A., Fahima, T., 2002. Evolution of wild emmer and wheat improvement:population genetics, genetic resources, and genome organization of wheat's progenitor, Triticum dicoccoides. Berlin, Germany:Springer-Verlag
    Ouyang, S.H., Zhang, D., Han, J., Zhao, X.J., Cui, Y., Song, W., Huo, N.X., Liang, Y., Xie, J.Z., Wang, Z.Z., et al., 2014. Fine physical and genetic mapping of powdery mildew resistance gene MlIW172 originating from wild emmer (Triticum dicoccoides). PLoS ONE 9, e100160
    Qiu, Y.C., Zhou, R.H., Kong, X.Y., Zhang, S.S., Jia, J.Z., 2005. Microsatellite mapping of a Triticum urartu Tum. derived powdery mildew resistance gene transferred to common wheat (Triticum aestivum L.). Theor. Appl. Genet. 111, 1524-1531
    Sanchez-Martin, J., Steuernagel, B., Ghosh, S., Herren, G., Hurni, S., Adamski, N., Vrana, J., Kubalakova, M., Krattinger, S.G., Wicker, T., et al., 2016. Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol. 17, 221
    Sanchez-Martin, J., and Keller, B., 2021. NLR immune receptors and diverse types of non-NLR proteins control race-specific resistance in Triticeae. Curr Opin Plant Biol. 62, 102053
    Sanchez-Martin, J., Widrig, V., Herren, G., Wicker, T., Zbinden, H., Gronnier, G., Sporri, L., Praz, C.R., Heuberger, M., Kolodziej, M., et al., 2021. Wheat Pm4 resistance to powdery mildew is controlled by alternative splice variants encoding chimeric proteins. Nature Plants 7, 327-341
    Sears, E.R., Briggle, L.W., 1969. Mapping gene Pm1 for resistance to Erysiphe graminis f. sp. tritici on chromosome 7A of wheat. Crop Sci. 9, 96-97
    Steuernagel, B., Periyannan, S.K., Hernandez-Pinzon, I., Witek, K., Rouse, M.N., Yu, G.T., Hatta, A., Ayliffe, M., Bariana, H., Jones, J.D.G., et al., 2016. Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nat. Biotechnol. 34, 652-655
    Thind, A.K., Wicker, T., Krattinger, S.G., (2017) Rapid identification of rust resistance genes through cultivar-specific de novo chromosome assemblies. In:Periyannan S. (eds) Wheat Rust Diseases. Methods Mol. Biol. 1659, 245-255
    Tian, D., Traw, M., Chen, J., Kreitman, M., Bergelson, J., 2003. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423, 74-77
    Van de Weyer, A.-L., Monteiro, F., Furzer, O.J., Nishimura, M.T., Cevik, V., Witek, K., Jones, J.D.G., Dangl, J.L., Weigel, D., Bemm, F., 2019. A species-wide inventory of NLR genes and alleles in Arabidopsis thaliana. Cell 178, 1260-1272
    Walkowiak, S., Gao, L.L., Monat, C., Haberer, G., Kassa, M.T., Brinton, J., Ramirez-Gonzalez R.H. Kolodziej, M.C., Delorean, E., Thambugala, D., et al., 2020. Multiple wheat genomes reveal global variation in modern breeding. Nature 588, 277-283
    Wu, Q.H., Zhao, F., Chen, Y.X., Zhang, P.P., Zhang, H.Z., Guo, G.H., Xie, J.Z., Dong, L.L., Lu, P., Li, M.M., et al., 2021. Bulked segregant CGT-Seq-facilitated map-based cloning of a powdery mildew resistance gene originating from wild emmer wheat (Triticum dicoccoides). Plant Biotechnol. J. 19, 1288-1290
    Xie, J.Z., Guo, G.H., Wang, Y., Hu, T.Z., Wang, L.L., Li, J.T., Qiu, D., Li, Y.H., Wu, Q.H., Lu, P., et al., 2020. A rare single nucleotide variant in Pm5e confers powdery mildew resistance in common wheat. New Phytol. 228, 1011-1026
    Xing, L.P., Hu, P., Liu, J.Q., Witek, K., Zhou, S., Xu, J.F., Zhou, W.H., Gao, L., Huang, Z.P., Zhang, R.Q., et al., 2018. Pm21 from Haynaldia villosa encodes a CC-NBS-LRR protein conferring powdery mildew resistance in wheat. Mol. Plant 11, 874-878
    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 hexaploidy wheat. Plant J. 37, 528-538
    Yao, G.Q., Zhang, J.L., Yang, L.L., Xu, H.X., Jiang, Y.M., Xiong, L., Zhang, C.Q., Zhang, Z.Z., Ma, Z.Q., Sorrells, M.E., 2007. Genetic mapping of two powdery mildew resistance genes in einkorn (Triticum monococcum L.) accessions. Theor. Appl. Genet. 114, 351-358
    Yao, W., Li, G., Zhao, H., Wang, G., Lian, X., Xie, W., 2015. Exploring the rice dispensable genome using a metagenome-like assembly strategy. Genome Biol. 16, 1-20
    Zhang, D.Y., Zhu, K.Y., Dong, L.L., Liang, Y., Li, G.Q., Fang, T.L., Guo, G.H., Wu, Q.H., Xie, J.Z. Chen, Y.X., 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, 761-770
    Zhang, L., Zheng, X.W., Qiao, L.Y., Qiao, L., Zhao, J.J., Wang, J.M., Zheng, J., 2018. Analysis of three types of resistance gene analogs in PmU region from Triticum Urartu. J. Integr. Agr. 17, 2601-2611
    Zhao, F.K., Li, Y.H., Yang, B.J., Yuan, H.B., Jin, C., Zhou, L.X., Pei, H.C. Zhao, L.F., Li, Y.W., Zhou, Y.L., et al., 2020. Powdery mildew disease resistance and marker-assisted screening at the Pm60 locus in wild diploid wheat Triticum urartu. Crop J. 8, 252-259
    Zhu, K.Y., Li, M.M., Wu, H.B., Zhang, D.Y., Dong, L.L., Wu, Q.H., Chen, Y.X., Xie, J.Z., Lu, P., Guo, G.H., et al., 2021. Fine mapping of powdery mildew resistance gene MlWE74 derived from wild emmer wheat (Triticum turgidum ssp. Dicoccoides) in n NBS-LRR gene cluster. Theor. Appl. Genet. https://doi.org/10.1007/s00122-021-04027-2
    Zou, S.H., Wang, H., Li, Y.W., Kong, Z.S., Tang, D.Z., 2018. The NB-LRR gene Pm60 confers powdery mildew resistance in wheat. New Phytol. 218, 298-309
    • Relative Articles
    • Supplements(0)
    • Cited By
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索
    Get Citation
    PDF

    Article Metrics

    Article views (500) PDF downloads (51) Cited by ()
    Proportional views
    Related

    Editorial Office

    Journal of Genetics and Genomics

    京ICP备09063187号-7

    No.1, West Beichen Road, Chaoyang District, Beijing 100101, P.R.China

    +86-10-64806528+86-10-64807786jgg@genetics.ac.cn

    Supported by: Beijing Renhe Information Technology Co. Ltd  

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return