Identification of powdery mildew resistance loci in wheat by integrating genome-wide association study(GWAS) and linkage mapping
|
摘要
Wheat powdery mildew(Blumeria graminis f.sp.tritici, Bgt) is a disease of increasing importance globally due to the adoption of high yielding varieties and modern sustainable farming technologies.Growing resistant cultivars is a preferred approach to managing this disease, and novel powdery mildew resistance genes are urgently needed for new cultivar development.A genome-wide association study was performed on a panel of 1292 wheat landraces and historical cultivars using 5011 single nucleotide polymorphism(SNP)markers.The association panel was evaluated for reactions to three Bgt inoculants, OKS(14)-B-3-1, OKS(14)-C-2-1, and Bgt15.Linkage disequilibrum(LD) analysis indicated that genome-wide LD decayed to 0.1 at 23 Mb, and population structure analysis revealed seven subgroups in the panel.Association analysis using a mixed linear model(MLM) identified three loci for powdery mildew resistance on chromosome 2 B, designated QPm.stars-2BL1,QPm.stars-2BL2, and QPm.stars-2BL3.To evaluate the efficacy of GWAS in gene discovery,QPm.stars-2BL2 was validated using F_2 and F_(2:3) populations derived from PI420646 × OK1059060-126135-3.Linkage analysis delimited the powdery mildew resistance gene in PI 420646 to an interval where QPm.stars-2BL2 was located, lending credence to the GWAS results.QPm.stars-2BL1 and QPm.stars-2BL3, which were associated with four SNPs located at 457.7–461.7 Mb and two SNPs located at 696.6–715.9 Mb in the Chinese Spring reference IWGSC RefSeq v1.0, respectively, are likely novel loci for powdery mildew resistance and can be used in wheat breeding to improve powdery mildew resistance.
Wheat powdery mildew(Blumeria graminis f.sp.tritici, Bgt) is a disease of increasing importance globally due to the adoption of high yielding varieties and modern sustainable farming technologies.Growing resistant cultivars is a preferred approach to managing this disease, and novel powdery mildew resistance genes are urgently needed for new cultivar development.A genome-wide association study was performed on a panel of 1292 wheat landraces and historical cultivars using 5011 single nucleotide polymorphism(SNP)markers.The association panel was evaluated for reactions to three Bgt inoculants, OKS(14)-B-3-1, OKS(14)-C-2-1, and Bgt15.Linkage disequilibrum(LD) analysis indicated that genome-wide LD decayed to 0.1 at 23 Mb, and population structure analysis revealed seven subgroups in the panel.Association analysis using a mixed linear model(MLM) identified three loci for powdery mildew resistance on chromosome 2 B, designated QPm.stars-2BL1,QPm.stars-2BL2, and QPm.stars-2BL3.To evaluate the efficacy of GWAS in gene discovery,QPm.stars-2BL2 was validated using F_2 and F_(2:3) populations derived from PI420646 × OK1059060-126135-3.Linkage analysis delimited the powdery mildew resistance gene in PI 420646 to an interval where QPm.stars-2BL2 was located, lending credence to the GWAS results.QPm.stars-2BL1 and QPm.stars-2BL3, which were associated with four SNPs located at 457.7–461.7 Mb and two SNPs located at 696.6–715.9 Mb in the Chinese Spring reference IWGSC RefSeq v1.0, respectively, are likely novel loci for powdery mildew resistance and can be used in wheat breeding to improve powdery mildew resistance.
Wheat powdery mildew(Blumeria graminis f.sp.tritici, Bgt) is a disease of increasing importance globally due to the adoption of high yielding varieties and modern sustainable farming technologies.Growing resistant cultivars is a preferred approach to managing this disease, and novel powdery mildew resistance genes are urgently needed for new cultivar development.A genome-wide association study was performed on a panel of 1292 wheat landraces and historical cultivars using 5011 single nucleotide polymorphism(SNP)markers.The association panel was evaluated for reactions to three Bgt inoculants, OKS(14)-B-3-1, OKS(14)-C-2-1, and Bgt15.Linkage disequilibrum(LD) analysis indicated that genome-wide LD decayed to 0.1 at 23 Mb, and population structure analysis revealed seven subgroups in the panel.Association analysis using a mixed linear model(MLM) identified three loci for powdery mildew resistance on chromosome 2 B, designated QPm.stars-2BL1,QPm.stars-2BL2, and QPm.stars-2BL3.To evaluate the efficacy of GWAS in gene discovery,QPm.stars-2BL2 was validated using F_2 and F_(2:3) populations derived from PI420646 × OK1059060-126135-3.Linkage analysis delimited the powdery mildew resistance gene in PI 420646 to an interval where QPm.stars-2BL2 was located, lending credence to the GWAS results.QPm.stars-2BL1 and QPm.stars-2BL3, which were associated with four SNPs located at 457.7–461.7 Mb and two SNPs located at 696.6–715.9 Mb in the Chinese Spring reference IWGSC RefSeq v1.0, respectively, are likely novel loci for powdery mildew resistance and can be used in wheat breeding to improve powdery mildew resistance.
引文
[1]J.Dixon,H.J.Braun,P.Kosina,J.Crouch,Wheat Facts and Futures 2009,CIMMYT,Mexico,2009.
[2]Morgounov,H.A.Tufan,R.Sharma,B.Akin,A.Bagci,H.J.Braun,Y.Kaya,M.Keser,T.S.Payne,K.Sonder,R.McIntosh,Global incidence of wheat rusts and powdery mildew during1969-2010 and durability of resistance of winter wheat variety Bezostaya 1,Eur.J.Plant Pathol.132(2012)323-340.
[3]R.A.McIntosh,J.Dubcovsky,J.W.Rogers,C.F.Morris,R.Appels,X.Xia,Catalogue of gene symbols for wheat,in:Y.Ogihara(Ed.),Proceeding of the 12th International Wheat Genetics Symposium,Yokohama,Japan,2013.
[4]R.A.McIntosh,J.Dubcovsky,J.W.Rogers,C.F.Morris,R.Appels,X.Xia,Catalogue of gene symbols for wheat:2013-2014 Supplement,Morphological and Physiological Traits(https://wheat.pw.usda.gov/GG2/Triticum/wgc/2013/2013-2014_Supplement.pdf).
[5]H.Xu,Y.Yi,P.Ma,Y.Qie,X.Fu,Y.Xu,X.Zhang,D.An,Molecular tagging of a new broad-spectrum powdery mildew resistance allele Pm2c in Chinese wheat landrace Niaomai,Theor.Appl.Genet.128(2015)2077-2084.
[6]Y.Hao,R.Parks,C.Cowger,Z.Chen,Y.Wang,D.Bland,J.P.Murphy,M.Guedira,G.Brown-Guedira,J.Johnson,Molecular characterization of a new powdery mildew resistance gene Pm54 in soft red winter wheat,Theor.Appl.Genet.128(2015)465-476.
[7]R.Zhang,B.Sun,J.Chen,A.Cao,L.Xing,Y.Feng,C.Lan,P.Chen,Pm55,a developmental-stage and tissue-specific powdery mildew resistance gene introgressed from Dasypyrum villosum into common wheat,Theor.Appl.Genet.129(2016)1975-1984.
[8]L.Tommasini,N.Yahiaoui,P.Srichumpa,B.Keller,Development of functional markers specific for seven Pm3 resistance alleles and their validation in the bread wheat gene pool,Theor.Appl.Genet.114(2006)165-175.
[9]C.Cowger,L.K.Mehra,C.Arellano,Virulence differences in Blumeria graminis f.sp.tritici from the central and eastern United States,Phytopathology 108(2018)402-411.
[10]T.Cao,Y.Chen,D.Li,Y.Zhang,X.Wang,H.Zhao,Z.Liu,Identification and molecular detection of powdery mildew resistance of new bred wheat varieties(lines)in Henan Province,China,Acta Agron.Sin.41(2015)1172-1182(in Chinese with English abstract).
[11]G.Li,X.Xu,G.Bai,B.F.Carver,R.Hunger,J.M.Bonman,Identification of novel powdery mildew resistance sources in wheat,Crop Sci.56(2016)1817-1830.
[12]W.Chen,Y.Gao,W.Xie,L.Gong,K.Lu,W.Wang,Y.Li,X.Liu,H.Zhang,H.Dong,W.Zhang,Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism,Nat.Genet.46(2014)714-721.
[13]J.M.Chia,C.Song,P.J.Bradbury,D.Costich,N.De Leon,J.Doebley,R.J.Elshire,B.Gaut,L.Geller,J.C.Glaubitz,M.Gore,Maize HapMap2 identifies extant variation from a genome in flux,Nat.Genet.44(2012)803-807.
[14]J.Cockram,J.White,D.J.Zuluaga,D.Smith,J.Comadran,M.Macaulay,Z.Luo,M.J.Kearsey,P.Werner,D.Harrap,C.Tapsell,Genome-wide association mapping to candidate polymorphism resolution in the unsequenced barley genome,Proc.Natl.Acad.Sci.U.S.A.107(2010)21611-21616.
[15]X.Huang,Q.Feng,Q.Qian,Q.Zhao,L.Wang,A.Wang,J.Guan,D.Fan,Q.Weng,T.Huang,G.Dong,High-throughput genotyping by whole-genome resequencing,Genome Res.19(2009)1068-1076.
[16]X.Huang,T.Sang,Q.Zhao,Q.Feng,Y.Zhao,C.Li,C.Zhu,T.Lu,Z.Zhang,M.Li,D.Fan,Genome-wide association studies of 14 agronomic traits in rice landraces,Nat.Genet.42(2010)961-967.
[17]X.Huang,Y.Zhao,C.Li,A.Wang,Q.Zhao,W.Li,Y.Guo,L.Deng,C.Zhu,D.Fan,Y.Lu,Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm,Nat.Genet.44(2012)32-39.
[18]S.Sukumaran,S.Dreisigacker,M.Lopes,P.Chavez,M.P.Reynolds,Genome-wide association study for grain yield and related traits in an elite spring wheat population grown in temperate irrigated environments,Theor.Appl.Genet.128(2015)353-363.
[19]F.Breseghello,M.E.Sorrells,Association mapping of kernel size and milling quality in wheat(Triticum aestivum L.)cultivars,Genetics 172(2006)1165-1177.
[20]G.Li,G.Bai,B.F.Carver,N.C.Elliott,R.S.Bennett,Y.Wu,R.Hunger,J.M.Bonman,X.Xu,Genome-wide association study reveals genetic architecture of coleoptile length in wheat,Theor.Appl.Genet.130(2017)391-401.
[21]P.Juliana,J.E.Rutkoski,J.A.Poland,R.P.Singh,S.Murugasamy,S.Natesan,H.Barbier,M.Sorrells,Genomewide association mapping for leaf tip necrosis and pseudoblack chaff in relation to durable rust resistance in wheat,Plant Genome 8(2015)https://doi.org/10.3835/plantgenome2015.01.0002.
[22]a M.Maccaferri,M.C.Sanguineti,P.Mantovani,A.Demontis,A.Massi,K.Ammar,J.A.Kolmer,J.H.Czembor,S.Ezrati,R.Tuberosa,Association mapping of leaf rust response in durum wheat,Mol.Breed.26(2010)189-228;b A.Kertho,S.Mamidi,J.M.Bonman,P.E.McClean,M.Acevedo,Genome-wide association mapping for resistance to leaf and stripe rust in winter-habit hexaploid wheat landraces,PLoS One 10(2015),e0129580.
[24]G.Li,X.Xu,G.Bai,B.F.Carver,R.Hunger,J.M.Bonman,J.Kolmer,H.Dong,Genome-wide association mapping reveals novel QTL for seedling leaf rust resistance in a worldwide collection of winter wheat,Plant Genome 9(2016)https://doi.org/10.3835/plantgenome2016.06.0051.
[25]M.Maccaferri,J.Zhang,P.Bulli,Z.Abate,S.Chao,D.Cantu,E.Bossolini,X.Chen,M.Pumphrey,J.Dubcovsky,A genomewide association study of resistance to stripe rust(Puccinia striiformis f.sp.tritici)in a worldwide collection of hexaploid spring wheat(Triticum aestivum L.),G3:Genes Genomes Genet.5(2015)449-465.
[26]L.X.Yu,A.Morgounov,R.Wanyera,M.Keser,S.K.Singh,M.Sorrells,Identification of Ug99 stem rust resistance loci in winter wheat germplasm using genome-wide association analysis,Theor.Appl.Genet.125(2012)749-758.
[27]D.Zhang,G.Bai,R.M.Hunger,W.W.Bockus,J.Yu,B.F.Carver,G.Brown-Guedira,Association study of resistance to Soilborne wheat mosaic virus in U.S.winter wheat,Phytopathology 10(2011)1322-1329.
[28]J.M.Bonman,E.M.Babiker,A.Cuesta-Marcos,K.Esvelt-Klos,G.Brown-Guedira,S.Chao,D.See,J.Chen,E.Akhunov,J.Zhang,H.E.Bockelman,Genetic diversity among wheat accessions from the USDA National Small Grains Collection,Crop Sci.55(2015)1243-1253.
[29]Z.L.Wang,L.H.Li,Z.H.He,X.Y.Duan,Y.L.Zhou,X.M.Chen,M.Lillemo,R.V.Singh,H.Wang,X.C.Xia,Seedling and adult plant resistance to powdery mildew in Chinese bread wheat cultivars and lines,Plant Dis.89(2005)457-463.
[30]S.Wang,D.Wong,K.Forrest,A.Allen,S.Chao,B.E.Huang,M.Maccaferri,S.Salvi,S.G.Milner,L.Cattivelli,A.M.Mastrangelo,Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array,Plant Biotechnol.J.12(2014)787-796.
[31]T.Jombart,An Introduction to Adegenet 2.0.0,Imperial College,London,2015.
[32]J.K.Pritchard,M.Stephens,P.Donnelly,Inference of population structure using multilocus genotype data,Genetics 155(2000)945-959.
[33]J.Yu,G.Pressoir,W.H.Briggs,I.V.Bi,M.Yamasaki,J.F.Doebley,M.D.McMullen,B.S.Gaut,D.M.Nielsen,J.B.Holland,S.Kresovich,A unified mixed-model method for association mapping that accounts for multiple levels of relatedness,Nat.Genet.38(2006)203-208.
[34]P.J.Bradbury,Z.Zhang,D.E.Kroon,T.M.Casstevens,Y.Ramdoss,E.S.Buckler,TASSEL:software for association mapping of complex traits in diverse samples,Bioinformatics23(2007)2633-2635.
[35]J.B.Endelman,J.L.Jannink,Shrinkage estimation of the realized relationship matrix,G3:Genes Genomes Genet.2(2012)1405-1413.
[36]Y.Benjamini,Y.Hochberg,Controlling the false discovery rate:a practical and powerful approach to multiple testing,J.Roy.Stat.Soc.B.57(1995)289-300.
[37]J.Dubcovsky,A.F.Galvez,J.Dvo?ák,Comparison of the genetic organization of the early salt-stress-response gene system in salt tolerant Lophopyrum elongatum and saltsensitive wheat,Theor.Appl.Genet.87(1994)957-964.
[38]R.W.Michelmore,I.Paran,R.V.Kesseli,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(1991)9828-9832.
[39]X.Y.Xu,G.H.Bai,B.F.Carver,G.E.Shaner,R.M.Hunger,Mapping of QTLs prolonging the latent period of Puccinia triticina infection in wheat,Theor.Appl.Genet.110(2005)244-251.
[40]X.Wang,L.Wang,GMATA:an integrated software package for genome-scale SSR mining,marker development and viewing,Front.Plant Sci.7(2016)1350.
[41]S.E.Lincoln,M.J.Daly,E.S.Lander,Constructing genetic linkage maps with MAPMAKER/EXP version 3.0:A tutorial and reference manual,A Whitehead Institute for Biomedical Research Technical Report,Whitehead Institute,Cambridge,USA 1993,p.3.
[42]D.D.Kosambi,The estimation of map distances from recombination values,Ann.Eugenics 12(1844)172-175.
[43]J.H.Jorgensen,C.J.Jensen,Genes for resistance to wheat powdery mildew in derivatives of Triticum timopheevi and T.carthlicum,Euphytica 21(1972)121-128.
[44]J.H.Jorgensen,C.J.Jensen,Gene Pm6 for resistance to powdery mildew in wheat,Euphytica 22(1973)423.
[45]W.Tao,D.Liu,J.Liu,Y.Feng,P.D.Chen,Genetic mapping of the powdery mildew resistance gene Pm6 in wheat by RFLPanalysis,Theor.Appl.Genet.100(2000)564-568.
[46]J.Ji,B.Qin,H.Wang,A.Cao,S.Wang,P.Chen,L.Zhuang,Y.Du,D.Liu,X.Wang,STS markers for powdery mildew resistance gene Pm6 in wheat,Euphytica 163(2008)159-165.
[47]X.K.Shen,L.X.Ma,S.F.Zhong,N.Liu,M.Zhang,W.Q.Chen,Y.L.Zhou,H.J.Li,Z.J.Chang,X.Li,G.H.Bai,H.Y.Zhang,F.Q.Tan,Z.L.Ren,P.G.Luo,Identification and genetic mapping of the putative Thinopyrum intermedium-derived dominant powdery mildew resistance gene PmL962 on wheat chromosome arm2BS,Theor.Appl.Genet.128(2015)517-528.
[48]Z.Liu,J.Zhu,Y.Cui,Y.Liang,H.Wu,W.Song,Q.Liu,T.Yang,Q.Sun,Z.Liu,Identification and comparative mapping of a powdery mildew resistance gene derived from wild emmer(Triticum turgidum var.dicoccoides)on chromosome 2BS,Theor.Appl.Genet.124(2012)1041-1049.
[49]L.Piarulli,A.Gadaleta,G.Mangini,M.A.Signorile,M.Pasquini,A.Blanco,R.Simeone,Molecular identification of a new powdery mildew resistance gene on chromosome 2BSfrom Triticum turgidum ssp.dicoccum,Plant Sci.196(2012)101-106.
[50]J.K.Rong,E.Millet,J.Manisterski,M.Feldman,A new powdery mildew resistance gene:introgression from wild emmer into common wheat and RFLP-based mapping,Euphytica 115(2000)121-126.
[51]W.Hua,Z.Liu,J.Zhu,C.Xie,T.Yang,Y.Zhou,X.Duan,Q.Sun,Z.Liu,Identification and genetic mapping of pm42,a new recessive wheat powdery mildew resistance gene derived from wild emmer(Triticum turgidum var.dicoccoides),Theor.Appl.Genet.119(2009)223-230.
[52]E.B?rner,A.Schumann,H.Fürste,B.C?ster,M.Leithold,W.Weber R?der,Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat(Triticum aestivum L.),Theor.Appl.Genet.105(2002)921-936.
[53]Z.Zhu,R.Zhou,X.Kong,Y.Dong,J.Jia,Microsatellite markers linked to two powdery mildew resistance genes introgressed from Triticum carthlicum accession PS5 into common wheat,Genome 48(2005)585-590.
[54]H.Zhan,G.Li,X.Zhang,X.Li,H.Guo,W.Gong,J.Jia,L.Qiao,Y.Ren,Z.Yang,Z.Chang,Chromosomal location and comparative genomics analysis of powdery mildew resistance gene Pm51 in a putative wheat-Thinopyrum ponticum introgression line,PLoS One 9(2014),e113455.
[55]Z.Zhao,H.Sun,W.Song,M.Lu,J.Huang,L.Wu,X.Wang,H.Li,Genetic analysis and detection of the gene Ml LX99 on chromosome 2BL conferring resistance to powdery mildew in the wheat cultivar Liangxing 99,Theor.Appl.Genet.126(2013)3081-3089.
[56]R.Zhang,Y.Fan,L.Kong,L,Pm62,an adult-plant powdery mildew resistance gene introgressed from Dasypyrum villosum chromosome arm 2VL into wheat,Theor.Appl.Genet.131(2018)2613-2620.
[57]G.Yin,G.Y.Li,Z.He,J.Liu,H.Wang,X.Xia,Molecular mapping of powdery mildew resistance gene in wheat cultivar Jimai 22,Acta Agron.Sin.35(2009)1425-1431(in Chinese with English abstract).
[58]J.J.Maxwell,J.H.Lyerly,G.Srnic,R.Parks,C.Cowger,D.Marshall,G.Brown-Guedira,J.P.Murphy,MlAB10:a Triticum turgidum subsp.dicoccoides derived powdery mildew resistance gene identified in common wheat,Crop Sci.50(2010)2261-2267.
[59]V.Mohler,F.J.Zeller,G.Wenzel,S.L.K.Hsam,Chromosomal location of genes for resistance to powdery mildew in common wheat(Triticum aestivum L.em Thell.):gene MlZec1from the Triticum dicoccoides-derived wheat line Zecoi-1,Euphytica 142(2005)161-167.
[60]L.L.Qi,P.D.Chen,D.Liu,Development of translocation lines of Triticum aestivum with powdery mildew resistance introduced from Haynaldia villosa,Proceedings of the 8th International Wheat Genetics Symposium,China Agricultural Scientech Press,Beijing 1993,pp.333-337.
[61]X.Huang,L.Wang,M.Xu,M.R?der,Microsatellite mapping of the powdery mildew resistance gene Pm5e in common wheat(Triticum aestivum L.),Theor.Appl.Genet.106(2003)858-865.
[62]F.Xue,W.W.Zhai,X.Y.Duan,Y.L.Zhou,W.Q.Ji,Microsatellite mapping of a powdery mildew resistance gene in wheat landrace Xiaobaidong,Acta Agron.Sin.35(2009)1806-1811(in Chinese with English abstract).
[63]M.Xiao,F.Song,J.Jiao,X.Wang,H.Xu,H.Li,Identification of the gene Pm47 on chromosome 7BS conferring resistance to powdery mildew in the Chinese wheat landrace Hongyanglazi,Theor.Appl.Genet.126(2013)1397-1403.
[64]Z.Wang,H.Li,D.Zhang,L.Guo,J.Chen,Y.Chen,Q.Wu,J.Xie,Y.Zhang,Q.Sun,J.Dvorak,M.C.Luo,Z.Y.Liu,Genetic and physical mapping of powdery mildew resistance gene MlHLTin Chinese wheat landrace Hulutou,Theor.Appl.Genet.128(2015)365-373.
[65]H.Sun,J.Hu,W.Song,D.Qiu,L.Cui,P.Wu,H.Zhang,H.Liu,L.Yang,Y.Qu,Y.Li,Pm61:a recessive gene for resistance to powdery mildew in wheat landrace Xuxusanyuehuang identified by comparative genomics analysis,Theor.Appl.Genet.131(2018)2085-2097.
[2]Morgounov,H.A.Tufan,R.Sharma,B.Akin,A.Bagci,H.J.Braun,Y.Kaya,M.Keser,T.S.Payne,K.Sonder,R.McIntosh,Global incidence of wheat rusts and powdery mildew during1969-2010 and durability of resistance of winter wheat variety Bezostaya 1,Eur.J.Plant Pathol.132(2012)323-340.
[3]R.A.McIntosh,J.Dubcovsky,J.W.Rogers,C.F.Morris,R.Appels,X.Xia,Catalogue of gene symbols for wheat,in:Y.Ogihara(Ed.),Proceeding of the 12th International Wheat Genetics Symposium,Yokohama,Japan,2013.
[4]R.A.McIntosh,J.Dubcovsky,J.W.Rogers,C.F.Morris,R.Appels,X.Xia,Catalogue of gene symbols for wheat:2013-2014 Supplement,Morphological and Physiological Traits(https://wheat.pw.usda.gov/GG2/Triticum/wgc/2013/2013-2014_Supplement.pdf).
[5]H.Xu,Y.Yi,P.Ma,Y.Qie,X.Fu,Y.Xu,X.Zhang,D.An,Molecular tagging of a new broad-spectrum powdery mildew resistance allele Pm2c in Chinese wheat landrace Niaomai,Theor.Appl.Genet.128(2015)2077-2084.
[6]Y.Hao,R.Parks,C.Cowger,Z.Chen,Y.Wang,D.Bland,J.P.Murphy,M.Guedira,G.Brown-Guedira,J.Johnson,Molecular characterization of a new powdery mildew resistance gene Pm54 in soft red winter wheat,Theor.Appl.Genet.128(2015)465-476.
[7]R.Zhang,B.Sun,J.Chen,A.Cao,L.Xing,Y.Feng,C.Lan,P.Chen,Pm55,a developmental-stage and tissue-specific powdery mildew resistance gene introgressed from Dasypyrum villosum into common wheat,Theor.Appl.Genet.129(2016)1975-1984.
[8]L.Tommasini,N.Yahiaoui,P.Srichumpa,B.Keller,Development of functional markers specific for seven Pm3 resistance alleles and their validation in the bread wheat gene pool,Theor.Appl.Genet.114(2006)165-175.
[9]C.Cowger,L.K.Mehra,C.Arellano,Virulence differences in Blumeria graminis f.sp.tritici from the central and eastern United States,Phytopathology 108(2018)402-411.
[10]T.Cao,Y.Chen,D.Li,Y.Zhang,X.Wang,H.Zhao,Z.Liu,Identification and molecular detection of powdery mildew resistance of new bred wheat varieties(lines)in Henan Province,China,Acta Agron.Sin.41(2015)1172-1182(in Chinese with English abstract).
[11]G.Li,X.Xu,G.Bai,B.F.Carver,R.Hunger,J.M.Bonman,Identification of novel powdery mildew resistance sources in wheat,Crop Sci.56(2016)1817-1830.
[12]W.Chen,Y.Gao,W.Xie,L.Gong,K.Lu,W.Wang,Y.Li,X.Liu,H.Zhang,H.Dong,W.Zhang,Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism,Nat.Genet.46(2014)714-721.
[13]J.M.Chia,C.Song,P.J.Bradbury,D.Costich,N.De Leon,J.Doebley,R.J.Elshire,B.Gaut,L.Geller,J.C.Glaubitz,M.Gore,Maize HapMap2 identifies extant variation from a genome in flux,Nat.Genet.44(2012)803-807.
[14]J.Cockram,J.White,D.J.Zuluaga,D.Smith,J.Comadran,M.Macaulay,Z.Luo,M.J.Kearsey,P.Werner,D.Harrap,C.Tapsell,Genome-wide association mapping to candidate polymorphism resolution in the unsequenced barley genome,Proc.Natl.Acad.Sci.U.S.A.107(2010)21611-21616.
[15]X.Huang,Q.Feng,Q.Qian,Q.Zhao,L.Wang,A.Wang,J.Guan,D.Fan,Q.Weng,T.Huang,G.Dong,High-throughput genotyping by whole-genome resequencing,Genome Res.19(2009)1068-1076.
[16]X.Huang,T.Sang,Q.Zhao,Q.Feng,Y.Zhao,C.Li,C.Zhu,T.Lu,Z.Zhang,M.Li,D.Fan,Genome-wide association studies of 14 agronomic traits in rice landraces,Nat.Genet.42(2010)961-967.
[17]X.Huang,Y.Zhao,C.Li,A.Wang,Q.Zhao,W.Li,Y.Guo,L.Deng,C.Zhu,D.Fan,Y.Lu,Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm,Nat.Genet.44(2012)32-39.
[18]S.Sukumaran,S.Dreisigacker,M.Lopes,P.Chavez,M.P.Reynolds,Genome-wide association study for grain yield and related traits in an elite spring wheat population grown in temperate irrigated environments,Theor.Appl.Genet.128(2015)353-363.
[19]F.Breseghello,M.E.Sorrells,Association mapping of kernel size and milling quality in wheat(Triticum aestivum L.)cultivars,Genetics 172(2006)1165-1177.
[20]G.Li,G.Bai,B.F.Carver,N.C.Elliott,R.S.Bennett,Y.Wu,R.Hunger,J.M.Bonman,X.Xu,Genome-wide association study reveals genetic architecture of coleoptile length in wheat,Theor.Appl.Genet.130(2017)391-401.
[21]P.Juliana,J.E.Rutkoski,J.A.Poland,R.P.Singh,S.Murugasamy,S.Natesan,H.Barbier,M.Sorrells,Genomewide association mapping for leaf tip necrosis and pseudoblack chaff in relation to durable rust resistance in wheat,Plant Genome 8(2015)https://doi.org/10.3835/plantgenome2015.01.0002.
[22]a M.Maccaferri,M.C.Sanguineti,P.Mantovani,A.Demontis,A.Massi,K.Ammar,J.A.Kolmer,J.H.Czembor,S.Ezrati,R.Tuberosa,Association mapping of leaf rust response in durum wheat,Mol.Breed.26(2010)189-228;b A.Kertho,S.Mamidi,J.M.Bonman,P.E.McClean,M.Acevedo,Genome-wide association mapping for resistance to leaf and stripe rust in winter-habit hexaploid wheat landraces,PLoS One 10(2015),e0129580.
[24]G.Li,X.Xu,G.Bai,B.F.Carver,R.Hunger,J.M.Bonman,J.Kolmer,H.Dong,Genome-wide association mapping reveals novel QTL for seedling leaf rust resistance in a worldwide collection of winter wheat,Plant Genome 9(2016)https://doi.org/10.3835/plantgenome2016.06.0051.
[25]M.Maccaferri,J.Zhang,P.Bulli,Z.Abate,S.Chao,D.Cantu,E.Bossolini,X.Chen,M.Pumphrey,J.Dubcovsky,A genomewide association study of resistance to stripe rust(Puccinia striiformis f.sp.tritici)in a worldwide collection of hexaploid spring wheat(Triticum aestivum L.),G3:Genes Genomes Genet.5(2015)449-465.
[26]L.X.Yu,A.Morgounov,R.Wanyera,M.Keser,S.K.Singh,M.Sorrells,Identification of Ug99 stem rust resistance loci in winter wheat germplasm using genome-wide association analysis,Theor.Appl.Genet.125(2012)749-758.
[27]D.Zhang,G.Bai,R.M.Hunger,W.W.Bockus,J.Yu,B.F.Carver,G.Brown-Guedira,Association study of resistance to Soilborne wheat mosaic virus in U.S.winter wheat,Phytopathology 10(2011)1322-1329.
[28]J.M.Bonman,E.M.Babiker,A.Cuesta-Marcos,K.Esvelt-Klos,G.Brown-Guedira,S.Chao,D.See,J.Chen,E.Akhunov,J.Zhang,H.E.Bockelman,Genetic diversity among wheat accessions from the USDA National Small Grains Collection,Crop Sci.55(2015)1243-1253.
[29]Z.L.Wang,L.H.Li,Z.H.He,X.Y.Duan,Y.L.Zhou,X.M.Chen,M.Lillemo,R.V.Singh,H.Wang,X.C.Xia,Seedling and adult plant resistance to powdery mildew in Chinese bread wheat cultivars and lines,Plant Dis.89(2005)457-463.
[30]S.Wang,D.Wong,K.Forrest,A.Allen,S.Chao,B.E.Huang,M.Maccaferri,S.Salvi,S.G.Milner,L.Cattivelli,A.M.Mastrangelo,Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array,Plant Biotechnol.J.12(2014)787-796.
[31]T.Jombart,An Introduction to Adegenet 2.0.0,Imperial College,London,2015.
[32]J.K.Pritchard,M.Stephens,P.Donnelly,Inference of population structure using multilocus genotype data,Genetics 155(2000)945-959.
[33]J.Yu,G.Pressoir,W.H.Briggs,I.V.Bi,M.Yamasaki,J.F.Doebley,M.D.McMullen,B.S.Gaut,D.M.Nielsen,J.B.Holland,S.Kresovich,A unified mixed-model method for association mapping that accounts for multiple levels of relatedness,Nat.Genet.38(2006)203-208.
[34]P.J.Bradbury,Z.Zhang,D.E.Kroon,T.M.Casstevens,Y.Ramdoss,E.S.Buckler,TASSEL:software for association mapping of complex traits in diverse samples,Bioinformatics23(2007)2633-2635.
[35]J.B.Endelman,J.L.Jannink,Shrinkage estimation of the realized relationship matrix,G3:Genes Genomes Genet.2(2012)1405-1413.
[36]Y.Benjamini,Y.Hochberg,Controlling the false discovery rate:a practical and powerful approach to multiple testing,J.Roy.Stat.Soc.B.57(1995)289-300.
[37]J.Dubcovsky,A.F.Galvez,J.Dvo?ák,Comparison of the genetic organization of the early salt-stress-response gene system in salt tolerant Lophopyrum elongatum and saltsensitive wheat,Theor.Appl.Genet.87(1994)957-964.
[38]R.W.Michelmore,I.Paran,R.V.Kesseli,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(1991)9828-9832.
[39]X.Y.Xu,G.H.Bai,B.F.Carver,G.E.Shaner,R.M.Hunger,Mapping of QTLs prolonging the latent period of Puccinia triticina infection in wheat,Theor.Appl.Genet.110(2005)244-251.
[40]X.Wang,L.Wang,GMATA:an integrated software package for genome-scale SSR mining,marker development and viewing,Front.Plant Sci.7(2016)1350.
[41]S.E.Lincoln,M.J.Daly,E.S.Lander,Constructing genetic linkage maps with MAPMAKER/EXP version 3.0:A tutorial and reference manual,A Whitehead Institute for Biomedical Research Technical Report,Whitehead Institute,Cambridge,USA 1993,p.3.
[42]D.D.Kosambi,The estimation of map distances from recombination values,Ann.Eugenics 12(1844)172-175.
[43]J.H.Jorgensen,C.J.Jensen,Genes for resistance to wheat powdery mildew in derivatives of Triticum timopheevi and T.carthlicum,Euphytica 21(1972)121-128.
[44]J.H.Jorgensen,C.J.Jensen,Gene Pm6 for resistance to powdery mildew in wheat,Euphytica 22(1973)423.
[45]W.Tao,D.Liu,J.Liu,Y.Feng,P.D.Chen,Genetic mapping of the powdery mildew resistance gene Pm6 in wheat by RFLPanalysis,Theor.Appl.Genet.100(2000)564-568.
[46]J.Ji,B.Qin,H.Wang,A.Cao,S.Wang,P.Chen,L.Zhuang,Y.Du,D.Liu,X.Wang,STS markers for powdery mildew resistance gene Pm6 in wheat,Euphytica 163(2008)159-165.
[47]X.K.Shen,L.X.Ma,S.F.Zhong,N.Liu,M.Zhang,W.Q.Chen,Y.L.Zhou,H.J.Li,Z.J.Chang,X.Li,G.H.Bai,H.Y.Zhang,F.Q.Tan,Z.L.Ren,P.G.Luo,Identification and genetic mapping of the putative Thinopyrum intermedium-derived dominant powdery mildew resistance gene PmL962 on wheat chromosome arm2BS,Theor.Appl.Genet.128(2015)517-528.
[48]Z.Liu,J.Zhu,Y.Cui,Y.Liang,H.Wu,W.Song,Q.Liu,T.Yang,Q.Sun,Z.Liu,Identification and comparative mapping of a powdery mildew resistance gene derived from wild emmer(Triticum turgidum var.dicoccoides)on chromosome 2BS,Theor.Appl.Genet.124(2012)1041-1049.
[49]L.Piarulli,A.Gadaleta,G.Mangini,M.A.Signorile,M.Pasquini,A.Blanco,R.Simeone,Molecular identification of a new powdery mildew resistance gene on chromosome 2BSfrom Triticum turgidum ssp.dicoccum,Plant Sci.196(2012)101-106.
[50]J.K.Rong,E.Millet,J.Manisterski,M.Feldman,A new powdery mildew resistance gene:introgression from wild emmer into common wheat and RFLP-based mapping,Euphytica 115(2000)121-126.
[51]W.Hua,Z.Liu,J.Zhu,C.Xie,T.Yang,Y.Zhou,X.Duan,Q.Sun,Z.Liu,Identification and genetic mapping of pm42,a new recessive wheat powdery mildew resistance gene derived from wild emmer(Triticum turgidum var.dicoccoides),Theor.Appl.Genet.119(2009)223-230.
[52]E.B?rner,A.Schumann,H.Fürste,B.C?ster,M.Leithold,W.Weber R?der,Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat(Triticum aestivum L.),Theor.Appl.Genet.105(2002)921-936.
[53]Z.Zhu,R.Zhou,X.Kong,Y.Dong,J.Jia,Microsatellite markers linked to two powdery mildew resistance genes introgressed from Triticum carthlicum accession PS5 into common wheat,Genome 48(2005)585-590.
[54]H.Zhan,G.Li,X.Zhang,X.Li,H.Guo,W.Gong,J.Jia,L.Qiao,Y.Ren,Z.Yang,Z.Chang,Chromosomal location and comparative genomics analysis of powdery mildew resistance gene Pm51 in a putative wheat-Thinopyrum ponticum introgression line,PLoS One 9(2014),e113455.
[55]Z.Zhao,H.Sun,W.Song,M.Lu,J.Huang,L.Wu,X.Wang,H.Li,Genetic analysis and detection of the gene Ml LX99 on chromosome 2BL conferring resistance to powdery mildew in the wheat cultivar Liangxing 99,Theor.Appl.Genet.126(2013)3081-3089.
[56]R.Zhang,Y.Fan,L.Kong,L,Pm62,an adult-plant powdery mildew resistance gene introgressed from Dasypyrum villosum chromosome arm 2VL into wheat,Theor.Appl.Genet.131(2018)2613-2620.
[57]G.Yin,G.Y.Li,Z.He,J.Liu,H.Wang,X.Xia,Molecular mapping of powdery mildew resistance gene in wheat cultivar Jimai 22,Acta Agron.Sin.35(2009)1425-1431(in Chinese with English abstract).
[58]J.J.Maxwell,J.H.Lyerly,G.Srnic,R.Parks,C.Cowger,D.Marshall,G.Brown-Guedira,J.P.Murphy,MlAB10:a Triticum turgidum subsp.dicoccoides derived powdery mildew resistance gene identified in common wheat,Crop Sci.50(2010)2261-2267.
[59]V.Mohler,F.J.Zeller,G.Wenzel,S.L.K.Hsam,Chromosomal location of genes for resistance to powdery mildew in common wheat(Triticum aestivum L.em Thell.):gene MlZec1from the Triticum dicoccoides-derived wheat line Zecoi-1,Euphytica 142(2005)161-167.
[60]L.L.Qi,P.D.Chen,D.Liu,Development of translocation lines of Triticum aestivum with powdery mildew resistance introduced from Haynaldia villosa,Proceedings of the 8th International Wheat Genetics Symposium,China Agricultural Scientech Press,Beijing 1993,pp.333-337.
[61]X.Huang,L.Wang,M.Xu,M.R?der,Microsatellite mapping of the powdery mildew resistance gene Pm5e in common wheat(Triticum aestivum L.),Theor.Appl.Genet.106(2003)858-865.
[62]F.Xue,W.W.Zhai,X.Y.Duan,Y.L.Zhou,W.Q.Ji,Microsatellite mapping of a powdery mildew resistance gene in wheat landrace Xiaobaidong,Acta Agron.Sin.35(2009)1806-1811(in Chinese with English abstract).
[63]M.Xiao,F.Song,J.Jiao,X.Wang,H.Xu,H.Li,Identification of the gene Pm47 on chromosome 7BS conferring resistance to powdery mildew in the Chinese wheat landrace Hongyanglazi,Theor.Appl.Genet.126(2013)1397-1403.
[64]Z.Wang,H.Li,D.Zhang,L.Guo,J.Chen,Y.Chen,Q.Wu,J.Xie,Y.Zhang,Q.Sun,J.Dvorak,M.C.Luo,Z.Y.Liu,Genetic and physical mapping of powdery mildew resistance gene MlHLTin Chinese wheat landrace Hulutou,Theor.Appl.Genet.128(2015)365-373.
[65]H.Sun,J.Hu,W.Song,D.Qiu,L.Cui,P.Wu,H.Zhang,H.Liu,L.Yang,Y.Qu,Y.Li,Pm61:a recessive gene for resistance to powdery mildew in wheat landrace Xuxusanyuehuang identified by comparative genomics analysis,Theor.Appl.Genet.131(2018)2085-2097.