Abstract
Key message
A stable QTL QPm.caas-3BS for adult-plant resistance to powdery mildew was mapped in an interval of 431 kb, and candidate genes were predicted based on gene sequences and expression profiles.
Abstract
Powdery mildew is a devastating foliar disease occurring in most wheat-growing areas. Characterization and fine mapping of genes for powdery mildew resistance can benefit marker-assisted breeding. We previously identified a stable quantitative trait locus (QTL) QPm.caas-3BS for adult-plant resistance to powdery mildew in a recombinant inbred line population of Zhou8425B/Chinese Spring by phenotyping across four environments. Using 11 heterozygous recombinants and high-density molecular markers, QPm.caas-3BS was delimited in a physical interval of approximately 3.91 Mb. Based on re-sequenced data and expression profiles, three genes TraesCS3B02G014800, TraesCS3B02G016800 and TraesCS3B02G019900 were associated with the powdery mildew resistance locus. Three gene-specific kompetitive allele-specific PCR (KASP) markers were developed from these genes and validated in the Zhou8425B derivatives and Zhou8425B/Chinese Spring population in which the resistance gene was mapped to a 0.3 cM interval flanked by KASP14800 and snp_50465, corresponding to a 431 kb region at the distal end of chromosome 3BS. Within the interval, TraesCS3B02G014800 was the most likely candidate gene for QPm.caas-3BS, but TraesCS3B02G016300 and TraesCS3B02G016400 were less likely candidates based on gene annotations and sequence variation between the parents. These results not only offer high-throughput KASP markers for improvement of powdery mildew resistance but also pave the way to map-based cloning of the resistance gene.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The authors declare that all data and materials support their published claims and comply with field standards.
Code availability
The authors declare that software application or custom code supports their published claims and complies with field standards.
Abbreviations
- APR:
-
Adult-plant resistance
- ASR:
-
All-stage resistance
- Bgt :
-
Blumeria graminis f. sp. tritici
- BLUE:
-
Best linear unbiased estimate
- FPKM:
-
Fragments per kilobase per million reads
- KASP:
-
Kompetitive allele-specific PCR
- MDS:
-
Maximum disease severity
- NIL:
-
Near-isogenic line
- PCR:
-
Polymerase chain reaction
- qPCR:
-
Quantitative real-time PCR
- QTL:
-
Quantitative trait locus
- RIL:
-
Recombinant inbred line
- SNP:
-
Single nucleotide polymorphism
References
Ashikari M, Sakakibara H, Lin SY, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745. https://doi.org/10.1126/science.1113373
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-David 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 (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357:93–97. https://doi.org/10.1126/science.aan0032
Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45:399–436. https://doi.org/10.1146/annurev.phyto.45.062806.094427
Boni R, Chauhan H, Hensel G, Roulin A, Sucher J, Kumlehn J, Brunner S, Krattinger SG, Keller B (2018) Pathogen-inducible Ta-Lr34res expression in heterologous barley confers disease resistance without negative pleiotropic effects. Plant Biotechnol J 16:245–253. https://doi.org/10.1111/pbi.12765
Brenchley R, Spannagl M, Pfeifer M, Barker GL, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo NX, Luo MC, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KFX, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shot gun sequencing. Nature 491:705–710. https://doi.org/10.1038/nature11650
Chen XM (2005) Epidemiology and control of stripe rust (Puccinia striiformis f. sp. tritici) on wheat. Can J Plant Pathol 27:314–337. https://doi.org/10.1080/07060660509507230
Chen YM, Song WJ, Xie XM, Wang ZH, Guan PF, Peng HR, Jiao YN, Ni ZF, Sun QX, Guo WL (2020) A collinearity-incorporating homology inference strategy for connecting emerging assemblies in Triticeae tribe as a pilot practice in the plant pangenomic Era. Mol Plant 13:1694–1708. https://doi.org/10.1016/j.molp.2020.09.019
Cloutier S, McCallum BD, Loutre C, Banks TW, Wicker T, Feuillet C, Keller B, Jordan MC (2007) Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol Biol 65:93–106. https://doi.org/10.1007/s11103-007-9201-8
D’Auria JC (2006) Acyltransferases in plants: a good time to be BAHD. Curr Opin Plant Biol 9:331–340. https://doi.org/10.1016/j.pbi.2006.03.016
Daetwyler HD, Pong-Wong R, Villanueva B, Woolliams JA (2010) The impact of genetic architecture on genome-wide evaluation methods. Genetics 185:1021–1031. https://doi.org/10.1534/genetics.110.116855
Feuillet C, Travella S, Stein N, Albar L, Nublat A, Keller B (2003) Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc Natl Acad Sci USA 100:15253–15258. https://doi.org/10.1073/pnas.2435133100
Gao HY, Niu JS, Li SP (2018) Impacts of wheat powdery mildew on grain yield & quality and its prevention and control methods. Am J Agric Forestry 6:141–147. https://doi.org/10.11648/j.ajaf.20180605.14
Gaurav K, Arora S, Silva P, Sanchez-Martin J, Horsnell R, Gao L, Brar GS, Widrig V, Raupp J, Singh N, Wu S (2021) Evolution of the bread wheat D-subgenome and enriching it with diversity from Aegilops tauschii. bioRxiv. https://doi.org/10.1101/2021.01.31.428788v1.full
Guo WL, Xin MM, Wang ZH, Yao YY, Hu ZR, Song WJ, Yu KH, Chen YM, Wang XB, Guan PF, Appels R, Peng HR, Ni ZF, Sun QX (2020) Origin and adaptation to high altitude of Tibetan semi-wild wheat. Nat Commun 11:5085. https://doi.org/10.1038/s41467-020-18738-5
He HG, Zhu SY, Zhao RH, Jiang ZN, Ji YY, Ji J, Qiu D, Li HJ, Bie TD (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
He HG, Liu RK, Ma PT, Du HN, Zhang HH, Wu QH, Yang LJ, Gong SJ, Liu TL, Huo NX, Gu YQ, Zhu SY (2020) Characterization of Pm68, a new powdery mildew resistance gene on chromosome 2BS of Greek durum wheat TRI 1796. Theor Appl Genet 134:53–62. https://doi.org/10.1007/s00122-020-03681-2
Hewitt T, Mueller MC, Molnar I, Mascher M, Holusova K, Simkova 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 (2020) 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
Holland JB (2007) Genetic architecture of complex traits in plants. Curr Opin Plant Biol 10:156–161. https://doi.org/10.1016/j.pbi.2007.01.003
Hsu F, Kent WJ, Clawson H, Kuhn RM, Diekhans M, Haussler D (2006) The UCSC known genes. Bioinformatics 22:1036–1046. https://doi.org/10.1093/bioinformatics/btl048
Huang L, Brooks SA, Li W, Fellers JP, Trick HN, Gill BS (2003) Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics 164:655–664. https://doi.org/10.1093/genetics/164.2.655
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
International Wheat Genome Sequencing Consortium (IWGSC) (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191. https://doi.org/10.1126/science.aar7191
Jia AL, Ren Y, Gao FM, Yin GH, Liu JD, Guo L, Zheng JZ, He ZH, Xia XC (2018) Mapping and validation of a new QTL for adult-plant resistance to powdery mildew in Chinese elite bread wheat line Zhou8425B. Theor Appl Genet 131:1063–1071. https://doi.org/10.1007/s00122-018-3058-x
Juroszek P, von Tiedemann A (2013) Climate change and potential future risks through wheat diseases: a review. Eur J Plant Pathol 136:21–33. https://doi.org/10.1007/s10658-012-0144-9
Kang YC, Barry K, Cao FB, Zhou MX (2020) Genome-wide association mapping for adult resistance to powdery mildew in common wheat. Mol Biol Rep 47:1241–1256. https://doi.org/10.1007/s11033-019-05225-4
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
Krattinger SG, Sucher J, Selter LL, Chauhan H, Zhou B, Tang MZ, Upadhyaya NM, Mieulet D, Guiderdoni E, Weidenbach D, Schaffrath U, Lagudah ES, Keller B (2016) The wheat durable, multipathogen resistance gene Lr34 confers partial blast resistance in rice. Plant Biotechnol J 14:1261–1268. https://doi.org/10.1111/pbi.12491
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
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 HJ, Liu ZY (2020) A CNL protein in wild emmer wheat confers powdery mildew resistance. New Phytol 228:1027–1037. https://doi.org/10.1111/nph.16761
Lin F, Chen XM (2007) Genetics and molecular mapping of genes for race-specific all-stage resistance and non-race-specific high-temperature adult-plant resistance to stripe rust in spring wheat cultivar Alpowa. Theor Appl Genet 114:1277–1287. https://doi.org/10.1007/s00122-007-0518-0
Liu N, Bai GH, Lin M, Xu XY, Zheng WM (2017) Genome-wide association analysis of powdery mildew resistance in US winter wheat. Sci Rep 7:11743. https://doi.org/10.1038/s41598-017-11230-z
Liu Z, Wang Q, Wan H, Yang F, Wei H, Xu Z, Ji H, Xia X, Li J, Yang W (2021) QTL mapping for adult-plant resistance to powdery mildew in Chinese elite common wheat Chuanmai104. Cereal Res Commun 49:99108. https://doi.org/10.1007/s42976-020-00082-5
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lu YM, Lan CX, Liang SS, Zhou XC, Liu D, Zhou G, Lu LQ, Jing JX, Wang MN, Xia XC, He ZH (2009) QTL mapping for adult-plant resistance to stripe rust in Italian common wheat cultivars Libellula and Strampelli. Theor Appl Genet 119:1349–1359. https://doi.org/10.1007/s00122-009-1139-6
Lu P, Liang Y, Li DL, Wang ZZ, Li WB, Wang GX, Wang Y, Zhou SH, Wu QH, Xie JZ, Zhang DY, Chen YX, Li MM, Zhang Y, Sun QX, Han CG, Liu ZY (2016) Fine genetic mapping of spot blotch resistance gene Sb3 in wheat (Triticum aestivum). Theor Appl Genet 129:577–589. https://doi.org/10.1007/s00122-015-2649-z
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
Maccaferri M, Harris NS, Twardziok SO, Pasam RK, Gundlach H, Spannagl M, Ormanbekova D, Lux T, Prade VM, Milner SG, Himmelbach A, Mascher M, Bagnaresi P, Faccioli P, Cozzi P, Lauria M, Lazzari B, Stella A, Manconi A, Gnocchi M, Moscatelli M, Avni R, Deek J, Biyiklioglu S, Frascaroli E, Corneti S, Salvi S, Sonnante G, Desiderio F, Marè C, Crosatti C, Mica E, Özkan H, Kilian B, De Vita P, Marone D, Joukhadar R, Mazzucotelli E, Nigro D, Gadaleta A, Chao S, Faris JD, Melo ATO, Pumphrey M, Pecchioni N, Milanesi L, Wiebe K, Ens J, MacLachlan RP, Clarke JM, Sharpe AG, Koh CS, Liang KYH, Taylor GJ, Knox R, Budak H, Mastrangelo AM, Xu SS, Stein N, Hale I, Distelfeld A, Hayden MJ, Tuberosa R, Walkowiak S, Mayer KFX, Ceriotti A, Pozniak CJ, Cattivelli L (2019) Durum wheat genome highlights past domestication signatures and future improvement targets. Nat Genet 51:885–895. https://doi.org/10.1038/s41588-019-0381-3
Mago R, Simkova H, Brown-Guedira G, Dreisigacker S, Breen J, Jin Y, Singh R, Appels R, Lagudah ES, Ellis J, Dolezel J, Spielmeyer W (2011a) An accurate DNA marker assay for stem rust resistance gene Sr2 in wheat. Theor Appl Genet 122:735–744. https://doi.org/10.1007/s00122-010-1482-7
Mago R, Tabe L, McIntosh RA, Pretorius Z, Kota R, Paux E, Wicker T, Breen J, Lagudah ES, Ellis JG, Spielmeyer W (2011b) A multiple resistance locus on chromosome arm 3BS in wheat confers resistance to stem rust (Sr2), leaf rust (Lr27) and powdery mildew. Theor Appl Genet 123:615–623. https://doi.org/10.1007/s00122-011-1611-y
McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Appels R, Xia XC (2014) Catalogue of gene symbols for wheat: 2013–2014 (Supplement). https://shigen.nig.ac.jp/wheat/komugi/genes/macgene/supplement2013.pdf. Accessed 6 Dec 201923
McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Appels R, Xia XC (2016) Catalogue of gene symbols for wheat: 2015–2016 (Supplement). https://shigen.nig.ac.jp/wheat/komugi/genes/macgene/supplement 2015.pdf. Accessed 6 Dec 201924
McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Xia XC (2017) Catalogue of gene symbols for wheat: 2017 (Supplement). https://shigen.nig.ac.jp/wheat/komugi/genes/macgene/supplement2017.pdf. Accessed 6 Dec 2019
Moore JW, Herrera-Foessel S, Lan C, Schnippenkoetter W, Aylife M, Huerta-Espino J, Lillemo M, Viccars L, Milne R, Periyannan S, Kong X, Spielmeyer W, Talbot M, Bariana H, Patrick JW, Dodds P, Singh R, Lagudah E (2015) Recent evolution of a hexose transporter variant confers resistance to multiple pathogens in wheat. Nat Genet 47:1494–1498. https://doi.org/10.1038/ng.3439
Negruk V, Yang P, Subramanian M, McNevin JP, Lemieux B (1996) Molecular cloning and characterization of the CER2 gene of Arabidopsis thaliana. Plant J 9:137–145. https://doi.org/10.1046/j.1365-313x.1996.09020137.x
Omasits U, Ahrens CH, Müller S, Wollscheid B (2014) Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30:884–886. https://doi.org/10.1093/bioinformatics/btt607
Peterson RF, Campbell AB, Hannah AE (1948) A diagrammatic scale for estimating rust intensity on leaves and stems of cereals. Can J Res 26:496–500. https://doi.org/10.1139/cjr48c-033
Qi LL, Echalier B, Chao S, Lazo GR, Butler GE, Anderson OD, Akhunov ED, Dvorák J, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Bermudez-Kandianis CE, Greene RA, Kantety R, La Rota CM, Munkvold JD, Sorrells SF, Sorrells ME, Dilbirligi M, Sidhu D, Erayman M, Randhawa HS, Sandhu D, Bondareva SN, Gill KS, Mahmoud AA, Ma XF, Miftahudin GJP, Conley EJ, Nduati V, Gonzalez-Hernandez JL, Anderson JA, Peng JH, Lapitan NL, Hossain KG, Kalavacharla V, Kianian SF, Pathan MS, Zhang DS, Nguyen HT, Choi DW, Fenton RD, Close TJ, McGuire PE, Qualset CO, Gill BS (2004) A chromosome bin map of 16,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712. https://doi.org/10.1534/genetics.104.034868
Ramirez-Gonzalez RH, Uauy C, Caccamo M (2015) PolyMarker: a fast polyploid primer design pipeline. Bioinformatics 31:2038–2039. https://doi.org/10.1093/bioinformatics/btv069
Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, Davey M, Jacobs J, van Ex F, Pasha A, Khedikar Y, Robinson SJ, Cory AT, Florio T, Concia L, Juery C, Schoonbeek H, Steuernagel B, Xiang D, Ridout CJ, Chalhoub B, Mayer KFX, Benhamed M, Latrasse D, Bendahmane A; International Wheat Genome Sequencing Consortium, Wulff BBH, Appels R, Tiwari V, Datla R, Choulet F, Pozniak CJ, Provart NJ, Sharpe AG, Paux E, Spannagl M, Bräutigam A, Uauy C (2018) The transcriptional landscape of polyploid wheat. Science 361:eaar6089. https://doi.org/10.1126/science.aar6089
Reynolds M, Foulkes J, Furbank R, Griffiths S, King J, Murchie E, Parry M, Slafer M (2012) Achieving yield gains in wheat. Plant Cell Environ 35:1799–1823. https://doi.org/10.1111/j.1365-3040.2012.02588.x
Risk JM, Selter LL, Krattinger SG, Viccars LA, Richardson TM, Buesing G, Herren G, Lagudah ES, Keller B (2012) Functional variability of the Lr34 durable resistance gene in transgenic wheat. Plant Biotechnol J 10:477–487. https://doi.org/10.1111/j.1467-7652.2012.00683.x
Risk JM, Selter LL, Chauhan H, Krattinger SG, Kumlehn J, Hensel G, Viccars LA, Richardon TM, Buesing G, Troller A, Lagudah ES, Keller B (2013) The wheat Lr34 gene provides resistance against multiple fungal pathogens in barley. Plant Biotechnol J 11:847–854. https://doi.org/10.1111/pbi.12077
Sánchez-Martín J, 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. https://doi.org/10.1016/j.pbi.2021.102053
Sánchez-Martín J, Steuernagel B, Ghosh S, Herren G, Hurni S, Adamski N, Vrana J, Kubalakova M, Krattinger SG, Wicker T, Doležel J, Keller B (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
Sato K, Abe F, Mascher M, Haberer G, Gundlach H, Spannagl M, Shirasawa K, Isobe S (2021) Chromosome-scale genome assembly of the transformation-amenable common wheat cultivar ‘Fielder.’ DNA Res 28:dsab008. https://doi.org/10.1093/dnares/dsab008
Schmalenbach I, March TJ, Bringezu T, Waugh R, Pillen K (2011) High-resolution genotyping of wild barley introgression lines and fine-mapping of the thresh ability locus thresh-1 using the Illumina Golden Gate Assay. G3 Genes/genomes/genetics 1:187–196. https://doi.org/10.1534/g3.111.000182
Schnippenkoetter W, Lo C, Liu G, Dibley K, Chan WL, White J, Milne R, Zwart A, Kwong E, Keller B, Godwin I, Krattinger SG, Lagudah ES (2017) The wheat Lr34 multipathogen resistance gene confers resistance to anthracnose and rust in sorghum. Plant Biotechnol J 15:1387–1396. https://doi.org/10.1111/pbi.12723
Singh RP, Mujeeb-Kazi A, Huerta-Espino J (1998) Lr46: a gene conferring slow-rusting resistance to leaf rust in wheat. Phytopathology 88:890–894. https://doi.org/10.1094/PHYTO.1998.88.9.890
Singh RP, Huerta-Espino J, Rajaram S (2000a) Achieving near-immunity to leaf and stripe rusts in wheat by combining slow rusting resistance genes. Acta Phytopathologica Et Entomologica Hungarica 35:133–139
Singh RP, Nelson JC, Sorrells ME (2000b) Mapping Yr28 and other genes for resistance to stripe rust in wheat. Crop Sci 40:1148–1155. https://doi.org/10.1094/PHYTO-03-15-0060-R
Singh RP, Huerta-Espino J, William HM (2005) Genetics and breeding for durable resistance to leaf and stripe rusts in wheat. Turk J Agric for 29:121–127
Singh RP, Singh PK, Rutkoski J, Hodson DP, He XY, 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. https://doi.org/10.1146/annurev-phyto-080615-095835/
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
Spielmeyer W, Sharp PJ, Lagudah ES (2003) Identification and validation of markers linked to broad-spectrum stem rust resistance gene Sr2 in wheat (Triticum aestivum L.). Crop Sci 43:333–336. https://doi.org/10.2135/cropsci2003.3330
Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: join map. Plant J 5:739–744. https://doi.org/10.1111/j.1365-313X.1993.00739.x
Sucher J, Boni R, Yang P, Rogowsky P, Büchner H, Kastner C, Kumlehn J, Krattinger SG, Keller B (2017) The durable wheat disease resistance gene Lr34 confers common rust and northern corn leaf blight resistance in maize. Plant Biotechnol J 15:489–496. https://doi.org/10.1111/pbi.12647
Tacke E, Korfhage C, Michel D, Maddaloni M, Motto M, Lanzini S, Salamini F, Doring HP (1995) Transposon tagging of the maize Glossy2 locus with the transposable element En/Spm. Plant J 8:907–917. https://doi.org/10.1046/j.1365-313x.1995.8060907.x
Walkowiak S, Gao L, Monat C, Haberer G, Kassa MT, Brinton J, Ramirez-Gonzalez RH, Kolodziej MC, Delorean E, Thambugala D, Klymiuk V, Byrns B, Gundlach H, Bandi V, Siri JN, Nilsen K, Aquino C, Himmelbach A, Copetti D, Ban T, Venturini L, Bevan M, Clavijo B, Koo DH, Ens J, Wiebe K, N’Diaye A, Fritz AK, Gutwin C, Fiebig A, Fosker C, Fu BX, Accinelli GG, Gardner KA, Fradgley N, Gutierrez-Gonzalez J, Halstead-Nussloch G, Hatakeyama M, Koh CS, Deek J, Costamagna AC, Fobert P, Heavens D, Kanamori H, Kawaura K, Kobayashi F, Krasileva K, Kuo T, McKenzie N, Murata K, Nabeka Y, Paape T, Padmarasu S, Percival-Alwyn L, Kagale S, Scholz U, Sese J, Juliana P, Singh R, Shimizu-Inatsugi R, Swarbreck D, Cockram J, Budak H, Tameshige T, Tanaka T, Tsuji H, Wright J, Wu J, Steuernagel B, Small I, Cloutier S, Keeble-Gagnère G, Muehlbauer G, Tibbets J, Nasuda S, Melonek J, Hucl PJ, Sharpe AG, Clark M, Legg E, Bharti A, Langridge P, Hall A, Uauy C, Mascher M, Krattinger SG, Handa H, Shimizu KK, Distelfeld A, Chalmers K, Keller B, Mayer KFX, Poland J, Stein N, McCartney CA, Spannagl M, Wicker T, Pozniak CJ (2020) Multiple wheat genomes reveal global variation in modern breeding. Nature 588:277–283. https://doi.org/10.1038/s41586-020-2961-x
Wang K, Li MY, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38:e164. https://doi.org/10.1093/nar/gkq603
Wissuwa M, Wegner J, Ae N, Yano M (2002) Substitution mapping of Pup1: a major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. Theor Appl Genet 105:890–897. https://doi.org/10.1007/s00122-002-1051-9
Wu YY, Li M, He ZH, Dreisigacker S, Wen WE, Jin H, Zhai SN, Li FJ, Gao FM, Liu JD, Wang RG, Zhang PZ, Wan YX, Cao SH, Xia XC (2020) Development and validation of high-throughput and low-cost STARP assays for genes underpinning economically important traits in wheat. Theor Appl Genet 133:2431–2450. https://doi.org/10.1007/s00122-020-03609-w
Xia Y, Nikolau BJ, Schnable PS (1996) Cloning and characterization of CER2, an Arabidopsis gene that affects cuticular wax accumulation. Plant Cell 8:1291–1304. https://doi.org/10.1105/tpc.8.8.1291
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, Karafiatova M, Vrana J, Baros J, Dolezel 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
Xu XT, Zhu ZW, Jia AL, Wang FJ, Wang JP, Zhang YL, Fu C, Fu LP, Bai GH, Xia XC, Hao YF (2020) Mapping of QTL for partial resistance to powdery mildew in two Chinese common wheat cultivars. Euphytica. https://doi.org/10.1007/s10681-019-2537-8
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
Yan XC, Li MM, Zhang PP, Yin GH, Zhang HZ, Gebrewahid TW, Zhang JP, Dong LL, Liu DQ, Liu ZY, Li ZF (2021) High-temperature wheat leaf rust resistance gene Lr13 exhibits pleiotropic effects on hybrid necrosis. Mol Plant 14:1029–1032. https://doi.org/10.1016/j.molp.2021.05.009
Yang Q, Zhang DF, Xu ML (2012) A sequential quantitative trait locus fine-mapping strategy using recombinant-derived progeny. J Integr Plant Biol 54:228–237. https://doi.org/10.1111/j.1744-7909.2012.01108.x
Zeng FS, Yang LJ, Gong SJ, Shi WQ, Zhang XJ, Wang H, Xiang LB, Xue MF, Yu DZ (2014) Virulence and diversity of Blumeria graminis f. sp. tritici populations in China. J Integr Agric 13:2424–2437. https://doi.org/10.1016/S2095-3119(13)60669-3
Zhang PP, Yin GH, Zhou Y, Qi AY, Gao FM, Xia XC, He ZH, Li ZF, Liu DQ (2017) QTL mapping of adult-plant resistance to leaf rust in the wheat cross Zhou8425B/Chinese spring using high-density SNP markers. Front Plant Sci 8:793. https://doi.org/10.3389/fpls.2017.00793
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 (Triticum turgdium var. dicoccoides) is tightly linked in repulsion with stripe rust resistance gene Yr5. Crop J 7:761–770. https://doi.org/10.1016/j.cj.2019.03.003
Zhang PP, Yan XC, Gebrewahid TW, Zhou Y, Yang EN, Xia XC, He ZH, Li ZF, Liu DQ (2021) Genome-wide association mapping of leaf rust and stripe rust resistance in wheat accessions using the 90K SNP array. Theor Appl Genet 134:1233–1251. https://doi.org/10.1007/s00122-021-03769-3
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
The authors are grateful to Prof. R. A. McIntosh, Plant Breeding Institute, University of Sydney, for critical review of this manuscript. This study was supported by the National Natural Science Foundation of China (31961143007, U1904109), Henan Science and Technology Foundation (202102110016) and CAAS Science and Technology Innovation Program.
Funding
This study was supported by the National Natural Science Foundation of China (31961143007, U1904109), Henan Science and Technology Foundation (202102110016) and CAAS Science and Technology Innovation Program.
Author information
Authors and Affiliations
Contributions
Y. Dong performed the experiments and data analyses and wrote the paper. D. A. Xu analyzed the RNA-Seq data. F. M. Gao analyzed the re-sequenced data of Zhou8425B. X. W. Xu, Y. Ren, J. Song, A. L. Jia and Y. F. Hao participated in the field trials. Z. H. He and X. C. Xia designed the experiment and assisted in writing the paper. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval
We declare that these experiments complied with the ethical standards in China.
Additional information
Communicated by Beat Keller.
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
About this article
Cite this article
Dong, Y., Xu, D., Xu, X. et al. Fine mapping of QPm.caas-3BS, a stable QTL for adult-plant resistance to powdery mildew in wheat (Triticum aestivum L.). Theor Appl Genet 135, 1083–1099 (2022). https://doi.org/10.1007/s00122-021-04019-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-021-04019-2