Abstract
Powdery mildew, caused by Blumeria graminis f. sp. tritici (Bgt), is a severe disease that affects the yield and quality of wheat. Popularization of resistant cultivars in production is the preferred strategy to control this disease. In the present study, the Chinese wheat breeding line Jimai 809 showed excellent agronomic performance and high resistance to powdery mildew at the whole growth stage. To dissect the genetic basis for this resistance, Jimai 809 was crossed with the susceptible wheat cultivar Junda 159 to produce segregation populations. Genetic analysis showed that a single dominant gene, temporarily designated PmJM809, conferred the resistance to different Bgt isolates. PmJM809 was then mapped on the chromosome arm 2BL and flanked by the markers CISSR02g-1 and CIT02g-13 with genetic distances 0.4 and 0.8 cM, respectively, corresponding to a physical interval of 704.12–708.24 Mb. PmJM809 differed from the reported Pm genes on chromosome arm 2BL in origin, resistance spectrum, physical position and/or genetic diversity of the mapping interval, also suggesting PmJM809 was located on a complex interval with multiple resistance genes. To analyze and screen the candidate gene(s) of PmJM809, six genes related to disease resistance in the candidate interval were evaluated their expression patterns using an additional set of wheat samples and time-course analysis post-inoculation of the Bgt isolate E09. As a result, four genes were speculated as the key candidate or regulatory genes. Considering its comprehensive agronomic traits and resistance findings, PmJM809 was expected to be a valuable gene resource in wheat disease resistance breeding. To efficiently transfer PmJM809 into different genetic backgrounds, 13 of 19 closely linked markers were confirmed to be suitable for marker-assisted selection. Using these markers, a series of wheat breeding lines with harmonious disease resistance and agronomic performance were selected from the crosses of Jimai 809 and several susceptible cultivars.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data supporting the findings of this study are included in the paper or are available from the corresponding authors on request.
References
Han GH, Cao LJ, Yan HW, Gu TT, Shi ZP, Li XQ, Li LH, An DG (2023) Development and identification of a wheat-rye breeding line for harmonious improvement between powdery mildew resistance and high yield potential. Plant Dis 107:2453–2459. https://doi.org/10.1094/PDIS-12-22-2817-RE
Ji JH, Qin B, Wang HY, Cao AZ, Chen AZ, Wang SL, Chen PD, Zhuang LF, Du Y, Liu DJ, Wang XE (2008) STS markers for powdery mildew resistance gene Pm6 in wheat. Theor Appl Genet 163:159–165. https://doi.org/10.1007/s10681-007-9578-0
He HG, Zhu SY, Zhao RH, Jiang ZN, Ji YY, Ji J, Qiu D, Li HJ, 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. https://doi.org/10.1016/j.molp.2018.03.004
Helguera M, Khan IA, Kolmer J, Lijavetzky D, Zhong-qi L, Dubcovsky J (2003) PCR assays for the Lr37-Yr17-Sr38 cluster of rust resistance genes and their use to develop isogenic hard red spring wheat lines. Crop Sci 43:1839–1847. https://doi.org/10.2135/cropsci2003.1839
Hewitt T, Müller MC, Molnár I, Mascher M, Holušová K, Šimková H, Kunz L, Zhang JP, Li JB, Bhatt D, Sharma R, Schudel S, Yu GT, Steuernagel B, Periyannan S, Wulff B, Ayliffe M, McIntosh R, Keller B, Lagudah E, Zhang P (2021) A highly differentiated region of wheat chromosome 7AL encodes a Pm1a immune receptor that recognizes its corresponding AvrPm1a effector from Blumeria graminis. New Phytol 229:2812–2826. https://doi.org/10.1111/nph.17075
Hickey LT, Hafeez AN, Robinson H, Jackson SA, Leal-Bertioli SCM, Tester M, Gao CX, Godwin ID, Hayes BJ, Wulff BBH (2009) Breeding crops to feed 10 billion. Nat Biotechnol 37:744–754. https://doi.org/10.1038/s41587-019-0152-9
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. https://doi.org/10.1007/s00122-002-1146-3
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 76:957–969. https://doi.org/10.1111/tpj.12345
Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugen 12:172–175. https://doi.org/10.1111/j.1469-1809.1943.tb02321.x
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 323:1360–1363. https://doi.org/10.1126/science.1166453
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181. https://doi.org/10.1016/0888-7543(87)90010-3
Li MM, Dong LL, Li BB, Wang ZZ, Xie JZ, Qiu D, Li YH, Shi WQ, Yang LJ, Wu QH, Chen YX, Lu P, Guo GH, Zhang HZ, Zhang PP, Zhu KY, Li YW, Zhang Y, Wang RG, Yuan CG, Liu W, Yu DZ, Luo MC, Fahima T, Nevo E, Li H, Liu Z (2020a) A CNL protein in wild emmer wheat confers powdery mildew resistance. New Phytol 228:1027–1037. https://doi.org/10.1111/nph.16761
Li YH, Shi XH, Hu JH, Wu PP, Qiu D, Qu YF, Xie JZ, Wu QH, Zhang HJ, Yang L, Liu HW, Zhou Y, Liu ZY, Li HJ (2020b) Identification of a recessive gene PmQ conferring resistance to powdery mildew in wheat landrace Qingxinmai using BSR-Seq analysis. Plant Dis 104:743–751. https://doi.org/10.1094/PDIS-08-19-1745-RE
Li YH, Wei ZZ, Sela H, Govta L, Klymiuk V, Roychowdhury R, Chawla HS, Ens J, Wiebe K, Bocharova V, Ben-David R, Pawar PB, Zhang YQ, Jaiwar S, Molnár I, Doležel J, Coaker G, Pozniak CJ, Fahima T (2023) Dissection of a rapidly evolving wheat resistance gene cluster by long-read genome sequencing accelerated the cloning of Pm69. Plant Commun 5:100646. https://doi.org/10.1016/j.xplc.2023.100646
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lu P, Guo L, Wang ZZ, Li BB, Li J, Li YH, Qiu D, Shi WQ, Yang LJ, Wang N, Guo GH, Xie JZ, Wu QH, Chen YX, Li MM, Zhang HZ, Dong LL, Zhang PP, Zhu KY, Yu DZ, Zhang Y, Deal KR, Huo NX, Liu CM, Luo MC, Dvorak J, Gu YQ, Li HJ, Liu ZY (2020) A rare gain of function mutation in a wheat tandem kinase confers resistance to powdery mildew. Nat Commun 11:680. https://doi.org/10.1038/s41467-020-14294-0
Ma PT, Wu LR, Xu YF, Xu HX, Zhang X, Wang WR, Liu C, Wang B (2021) Bulked segregant RNA-Seq provides distinctive expression profile against powdery mildew in the wheat genotype YD588. Front Plant Sci 12:764978. https://doi.org/10.3389/fpls.2021.764978
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 U S A 88:9828–9832. https://doi.org/10.1073/pnas.88.21.9828
Moore JW, Herrera-Foessel S, Lan CX, Schnippenkoetter W, Ayliffe M, Huerta-Espino J, Lillemo M, Viccars L, Milne R, Periyannan S, Kong XY, Spielmeyer W, Talbot M, Bariana H, Patrick JW, Dodds P, Singh R, Lagudah E (2015) A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat Genet 47:1494–1498. https://doi.org/10.1038/ng.3439
Mu YJ, Gong WP, Qie YM, Liu XQ, Li LZ, Sun NN, Liu W, Guo J, Han R, Yu ZY, Xiao LN, Su FY, Zhang WJ, Wang JC, Han GH, Ma PT (2022) Identification of the powdery mildew resistance gene in wheat breeding line Yannong 99102–06188 via bulked segregant exome capture sequencing. Front Plant Sci 13:1005627. https://doi.org/10.3389/fpls.2022.1005627
Qin B, Cao AZ, Wang HY, Chen TT, You FM, Liu YY, Ji JH, Liu DJ, Chen PD, Wang XE (2011) Collinearity-basedmarker mining for the fine mapping of Pm6, a powdery mildew resistance gene in wheat. Theor Appl Genet 123:207–18. https://doi.org/10.1007/s00122-011-1577-9
Sánchez-Martín J, Steuernagel B, Ghosh S, Herre 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. https://doi.org/10.1186/s13059-016-1082-1
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 7:327–341. https://doi.org/10.1038/s41477-021-00869-2
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. https://doi.org/10.1007/BF00202486
Sharp PJ, Kreis M, Shewry PR, Gale MD (1988) Location of β-amylase sequences in wheat and its relatives. Theor Appl Genet 75:286–290. https://doi.org/10.1007/BF00303966
Si QM, Zhang XX, Duan XY, Sheng BQ, Zhou YL (1992) On gene analysis and classification of powdery mildew (Erysiphe graminis f. sp. tritici) resistant wheat varieties. Acta Phytopathol Sin 22:349–355. https://doi.org/10.13926/j.cnki.apps.1992.04.021
Singh SP, Hurni S, Ruinelli M, Brunner S, Sanchez-Martin J, Krukowski P, Peditto D, Buchmann G, Zbinden H, Keller B (2018) Evolutionary divergence of the rye Pm17 and Pm8 resistance genes reveals ancient diversity. Plant Mol Biol 98:249–260. https://doi.org/10.1007/s11103-018-0780-3
Tan CC, Li GQ, Cowger C, Carver BF, Xu XY (2019) Characterization of Pm63, a powdery mildew resistance gene in Iranian landrace PI 628024. Theor Appl Genet 132:1137–1144. https://doi.org/10.1007/s00122-018-3265-5
Wan WT, Xiao JX, Li ML, Tang X, Wen MX, Cheruiyot AK, Li YB, Wang HY, Wang XE (2020) Fine mapping of wheat powdery mildew resistance gene Pm6 using 2B/2G homoeologous recombinants induced by the ph1b mutant. Theor Appl Genet 133:1265–1275. https://doi.org/10.1007/s00122-020-03546-8
Wang CM, Zheng Q, Li LH, Niu YC, Wang HB, Li B, Zhang XT, Xu YF, An DG (2009) Molecular cytogenetic characterization of a new T2BL · 1RS wheat-rye chromosome translocation line resistant to stripe rust and powdery mildew. Plant Dis 93:124–129. https://doi.org/10.1094/PDIS-93-2-0124
Wang WR, He HG, Gao HM, Xu HX, Song WY, Zhang X, Zhang LP, Song JC, Liu C, Liu KC, Ma PT (2021) Characterization of the powdery mildew resistance gene in wheat breeding line KN0816 and its evaluation in marker-assisted selection. Plant Dis 105:4042–4050. https://doi.org/10.1094/PDIS-05-21-0896-RE
Wang B, Meng T, Xiao B, Yu TY, Yue TY, Jin YL, Ma PT (2023) Fighting wheat powdery mildew: from genes to fields. Theor Appl Genet 136:196. https://doi.org/10.1007/s00122-023-04445-4
Wang YJ, Abrouk M, Gourdoupis S, Koo DH, Karafiátová M, Molnár I, Holušová K, Doležel J, Athiyannan N, Cavalet-Giorsa E, Jaremko Ł, Poland J, Krattinger SG (2023) An unusual tandem kinase fusion protein confers leaf rust resistance in wheat. Nat Genet 55:914–920. https://doi.org/10.1038/s41588-023-01401-2
Wu PP, Hu JH, Zou ZW, Qiu D, Qu YF, Li YH, Li T, Zhang HJ, Yang L, Liu HW, Zhou YQ, Zhang ZJ, Li JT, Liu ZY, Li HJ (2019) Fine mapping of the wheat powdery mildew resistance gene Pm52 using comparative genomics analysis and the Chinese spring reference genomic sequence. Theor Appl Genet 132:1451–1461. https://doi.org/10.1007/s00122-019-03291-7
Wu YN, Yu XT, Zhang X, Yan LJ, Gao L, Hao YQ, Wang XY, Xue SL, Qu YF, Hu TZ, Fu BS, Zhou Y, Li SP, Li HJ, Li CX, Ma PT, Xu HX (2021) Characterization of PmDGM conferring powdery mildew resistance in Chinese wheat landrace Duanganmang. Plant Dis 105:3127–3133. https://doi.org/10.1094/PDIS-12-20-2719-RE
Wu LR, Zhu T, He HG, Cao XY, Li HS, Xu HX, Jia MS, Zhang LP, Song JC, Mirzaghaderi G, Liu C, Ma PT (2022) Genetic dissection of the powdery mildew resistance in wheat breeding line LS5082 using BSR-Seq. Crop J 10:1120–1130. https://doi.org/10.1016/j.cj.2021.12.008
Xie JZ, Guo GH, Wang Y, Hu TZ, Wang LL, Li JT, Qiu D, Li YH, Wu QH, Lu P, Chen YX, Dong LL, Li MM, Zhang HZ, Zhang PP, Zhu KY, Li BB, Deal KR, Huo NX, Zhang Y, Luo MC, Liu SZ, Gu YQ, Li HJ, Liu ZY (2020) A rare single nucleotide variant in Pm5e confers powdery mildew resistance in common wheat. New Phytol 228:1011–1026. https://doi.org/10.1111/nph.16762
Xing LP, Hu P, Liu JQ, Witek K, Zhou S, Xu JF, Zhou WH, Gao L, Huang ZP, Zhang RQ, Wang XE, Chen PD, Wang HY, Jones JDG, Karafiátová M, Vrána J, Bartoš J, Doležel J, Tian YC, Wu YF, Cao AZ (2018) Pm21 from Haynaldia villosa encodes a CC-NBS-LRR protein conferring powdery mildew resistance in wheat. Mol Plant 11:874–878. https://doi.org/10.1016/j.molp.2018.02.013
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. https://doi.org/10.1046/j.1365-313x.2003.01977.x
Yang H, Zhong SF, Chen C, Yang H, Chen W, Tan FQ, Zhang M, Chen WQ, Ren TH, Li Z, Luo PG (2021) Identification and cloning of a CC-NBS-NBS-LRR Gene as a candidate of Pm40 by integrated analysis of both the available transcriptional data and published linkage mapping. Int J Mol Sci 22:10239. https://doi.org/10.3390/ijms221910239
Yu GT, Matny O, Gourdoupis S, Rayapuram N, Aljedaani FR, Wang YL, Nürnberger T, Johnson R, Crean EE, Saur IML, Gardener C, Yue YJ, Kangara N, Steuernagel B, Hayta S, Smedley M, Harwood W, Patpour M, Wu SY, Poland J, Jones JDG, Reuber TL, Ronen M, Sharon A, Rouse MN, Xu S, Holušová K, Bartoš J, Molnár I, Karafiátová M, Hirt H, Blilou I, Jaremko Ł, Doležel J, Steffenson BJ, Wulff BBH (2023) The wheat stem rust resistance gene Sr43 encodes an unusual protein kinase. Nat Genet 55:921–926. https://doi.org/10.1038/s41588-023-01402-1
Zhan HX, Li GR, Zhang XJ, Li X, Guo HJ, Gong WP, Jia JQ, Qiao LY, Ren YK, Yang ZJ, Chang ZJ (2014) Chromosomal location and comparative genomics analysis of powdery mildew resistance gene Pm51 in a putative wheat-Thinopyrum ponticum introgression line. PLoS One 9:e113455. https://doi.org/10.1371/journal.pone.0113455
Zhang DY, Zhu KY, Dong LL, Liang Y, Li GQ, Fang TL, Guo GH, Wu QH, Xie JZ, Chen YX, Lu P, Li MM, Zhang HZ, Wang ZZ, Zhang Y, Sun QX, Liu ZY (2019) Wheat powdery mildew resistance gene Pm64 derived from wild emmer (Triticumturgidum var. dicoccoides) is tightly linked in repulsion with stripe rust resistancegene Yr5. Crop J 7:761–770. https://doi.org/10.1016/j.cj.2019.03.003
Zhang X, Wang WR, Liu C, Zhu SY, Gao HM, Xu HX, Zhang LP, Song JC, Song WY, Liu KC, He HG, Ma PT (2021) Diagnostic KASP markers of wheat broad-spectrum powdery mildew resistance genes Pm21, PmV, and Pm12 developed for high throughput marker-assisted selection. Plant Dis 105:2844–2850. https://doi.org/10.1094/PDIS-02-21-0308-RE
Zhang WJ, Yu ZY, Wang DM, Xiao LN, Su FY, Mu YJ, Zheng JP, Li LZ, Yin Y, Yu TY, Jin YL, Ma PT (2023) Characterization and identification of the powdery mildew resistance gene in wheat breeding line ShiCG15-009. BMC Plant Biol 23:113. https://doi.org/10.1186/s12870-023-04132-y
Zhao ZH, Sun HG, Song W, Lu M, Huang J, Wu LF, Wang XM, Li HJ (2013) Genetic analysis and detection of the gene MlLX99 on chromosome 2BL conferring resistance to powdery mildew in the wheat cultivar Liangxing 99. Theor Appl Genet 126:3081–9. https://doi.org/10.1007/s00122-013-2194-6
Zhu ZD, Zhou RH, Kong XY, Dong YC, Jia JZ (2005) Microsatellite markers linked to 2 powdery mildew resistance genes introgressed from Triticum carthlicum accession PS5 into common wheat. Genome 48:585–590. https://doi.org/10.1139/g05-016
Zhu SY, Liu C, Gong SJ, Chen ZZ, Chen R, Liu TL, Liu RK, Du HN, Guo R, Li GY, Li MM, Fan RC, Liu ZY, Shen QH, Gao AL, Ma PT, He HG (2022) Pm12 and Pm21 are orthologous genes originated from different wild relatives of wheat and show evolutionary conservation but divergent powdery mildew resistance. Plant Commun 4:100472. https://doi.org/10.1016/j.xplc.2022.100472
Zhu SY, Du HN, Su FY, Wang J, Meng QF, Liu TL, Guo R, Chen ZZ, Li HH, Liu WX, Ma PT, He HG (2023) Molecular cytogenetics analyses of two new wheat-rye 6RL translocation lines with resistance to wheat powdery mildew. Crop J 11:584–592. https://doi.org/10.1016/j.cj.2022.07.017
Zou JW, Qiu D, Sun YL, Zheng CX, Li JT, Wu PP, Wu XF, Wang XM, Zhou Y, Li HJ (2017) Pm52: effectiveness of the gene conferring resistance to powdery mildew in wheat cultivar Liangxing 99. Acta Agron Sin 43:332–342. https://doi.org/10.3724/SP.J.1006.2017.00332
Zou SH, Wang H, Li YW, Kong ZS, Tang DZ (2018) The NB-LRR gene Pm60 confers powdery mildew resistance in wheat. New Phytol 218:298–309. https://doi.org/10.1111/nph.14964
Acknowledgements
We are grateful to Prof. Hongxing Xu, School of Life Sciences, Henan University, for providing the Blumeria graminis f. sp. tritici (Bgt) isolates.
Funding
This research was financially supported by the National Natural Science Foundation of China (32072053, 32301923), Key Research and Development Project of Yantai City (2022XCZX092, 2023ZDCX023) and Co-construction State Key Laboratory of Wheat and Maize Crop Science (SKL2022KF09).
Author information
Authors and Affiliations
Contributions
PM and YJ conceived the research. YZ, GH, YQ, BX, JW and ZQ performed the experiments. XH, RL, JZ and LS analyzed the data. YZ and YQ performed the phenotypic assessment. JS and YZ developed the experimental materials. YJ wrote the manuscript. All authors approved the final manuscript.
Corresponding authors
Ethics declarations
Ethics approval
We declare that these experiments comply with the ethical standards in China.
Conflict of interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhao, Y., Han, G., Qie, Y. et al. Characterization of the powdery mildew resistance locus in wheat breeding line Jimai 809 and its breeding application. Mol Breeding 44, 28 (2024). https://doi.org/10.1007/s11032-024-01467-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-024-01467-8