Meta-analysis of soybean amino acid QTLs and candidate gene mining
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摘要
The composition and quantity of amino acids influence the protein content and nutritional value of soybeans and also have an important impact upon soybean quality. After integrating and proofreading 140 original QTLs associated with amino acid contentfrom soybase(http://www.soybase.org/), 138 QTLs were further analyzed to determine high-confidence QTL regions. Meta-analysis was first carried out using the Bio Mercator ver. 2.1 software, yielding 33 consensus QTLs. The consensus QTL confidence intervals(CIs) ranged from 0.07 to 19.85 Mb. Next, the overview method was used to optimize the CIs, and 57 "real" QTLs were mapped. Candidate genes in the consensus QTL regions were obtained from Phytozome and were annotated using the Gene Ontology(GO), Kyoto Encyclopedia of Genes and Genomes(KEGG), Swissprot, and gene annotation databases. Finally, 16 unpublished candidate genes controlling the content of five types of amino acids were identified with Blast. These results laid the foundation for fine mapping of soybean amino acid-related QTLs and marker-assisted selection.
The composition and quantity of amino acids influence the protein content and nutritional value of soybeans and also have an important impact upon soybean quality. After integrating and proofreading 140 original QTLs associated with amino acid contentfrom soybase(http://www.soybase.org/), 138 QTLs were further analyzed to determine high-confidence QTL regions. Meta-analysis was first carried out using the Bio Mercator ver. 2.1 software, yielding 33 consensus QTLs. The consensus QTL confidence intervals(CIs) ranged from 0.07 to 19.85 Mb. Next, the overview method was used to optimize the CIs, and 57 "real" QTLs were mapped. Candidate genes in the consensus QTL regions were obtained from Phytozome and were annotated using the Gene Ontology(GO), Kyoto Encyclopedia of Genes and Genomes(KEGG), Swissprot, and gene annotation databases. Finally, 16 unpublished candidate genes controlling the content of five types of amino acids were identified with Blast. These results laid the foundation for fine mapping of soybean amino acid-related QTLs and marker-assisted selection.
The composition and quantity of amino acids influence the protein content and nutritional value of soybeans and also have an important impact upon soybean quality. After integrating and proofreading 140 original QTLs associated with amino acid contentfrom soybase(http://www.soybase.org/), 138 QTLs were further analyzed to determine high-confidence QTL regions. Meta-analysis was first carried out using the Bio Mercator ver. 2.1 software, yielding 33 consensus QTLs. The consensus QTL confidence intervals(CIs) ranged from 0.07 to 19.85 Mb. Next, the overview method was used to optimize the CIs, and 57 "real" QTLs were mapped. Candidate genes in the consensus QTL regions were obtained from Phytozome and were annotated using the Gene Ontology(GO), Kyoto Encyclopedia of Genes and Genomes(KEGG), Swissprot, and gene annotation databases. Finally, 16 unpublished candidate genes controlling the content of five types of amino acids were identified with Blast. These results laid the foundation for fine mapping of soybean amino acid-related QTLs and marker-assisted selection.
引文
Arcade A,Labourdette A,Falque M,Mangin B,Chardon F,Charcosset A,Joets J.2004.Bio Mercator:Integrating genetic maps and QTL towards discovery of candidate genes.Bioinformatics,20,2324-2326.
Bolger M E,Weisshaar B,Scholz U,Stein N,Usadel B,Mayer K F.2014.Plant genome sequencing-applications for crop improvement.Current Opinion in Biotechnology,26,31-37.
Catoni E,Desimone M,Hilpert M,Wipf D,Kunze R,Schneider A,Flügge U,Schumacher K,Frommer W B.2003.Expression pattern of a nuclear encoded mitochondrial arginineornithine translocator gene from Arabidopsis.BMC Plant Biology,3,1.
Chardon F,Virlon B,Moreau L,Falque M,Joets J,Decousset L,Murigneux A,Charcosset A.2004.Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome.Genetics,168,2169-2185.
Chen N W,Sévignac M,Thareau V,Magdelenat G,David P,Ashfield T,Innes R W,Geffroy V.2010.Specific resistances against Pseudomonas syringae effectors Avr B and Avr Rpm1 have evolved differently in common bean(Phaseolus vulgaris),soybean(Glycine max),and Arabidopsis thaliana.New Phytologist,187,941-956.
Danan S,Veyrieras J B,Lefebvre V.2011a.Construction of a potato consensus map and QTL meta-analysis offer new insights into the genetic architecture of late blight resistance and plant maturity traits.BMC Plant Biology,11,16.
Danan S,Veyrieras J B,Lefebvre V.2011b.Genomic selection in tree breeding:Testing accuracy of prediction models including dominance effect.BMC Proceedings,5,1753-6561.
Gao L F,Guo Y,Hao Z B,Qiu L J.2013.Integration and“Overview”analysis of QTLs related to plant height in soybean.Hereditas,35,215-224.
Glass G V.1976.Primary,secondary,and meta-analysis of research 1.Educational Researcher,5,3-8.
Goffinet B,Gerber S.2000.Quantitative trait loci:A metaanalysis.Genetics,155,463-473.
von Groll U,Berger D,Altmann T.2002.The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development.The Plant Cell,14,1527-1539.
Guo B,Sleper D A,Lu P,Shannon J G,Nguyen H T,Arelli PR.2006.QTLs associated with resistance to soybean cyst nematode in soybean:Meta-analysis of QTL locations.Crop Science,46,595-602.
Gutierrez-Gonzalez J J,Vuong T D,Zhong R,Yu O,Lee JD,Shannon G,Ellersieck M,Nguyen H T,Sleper D A.2011.Major locus and other novel additive and epistatic loci involved in modulation of isoflavone concentration in soybean seeds.Theoretical and Applied Genetics,123,1375-1385.
Gutierrez-Gonzalez J J,Wu X,Gillman J D,Lee J D,Zhong R,Yu O,Shannon G,Ellersieck M,Nguyen H T,Sleper D A.2010.Intricate environment-modulated genetic networks control isoflavone accumulation in soybean seeds.BMCPlant Biology,10,105.
Gutierrez-Gonzalez J J,Wu X,Zhang J,Lee J D,Ellersieck M,Shannon J G,Yu O,Nguyen H T,Sleper D A.2009.Genetic control of soybean seed isoflavone content:Importance of statistical model and epistasis in complex traits.Theoretical and Applied Genetics,119,1069-1083.
Hao Z,Li X,Liu X,Xie C,Li M,Zhang D,Zhang S.2010.Meta-analysis of constitutive and adaptive QTL for drought tolerance in maize.Euphytica,174,165-177.
Hoover T A,Roof W D,Foltermann K F,O’Donovan G A,Bencini D A,Wild J R.1983.Nucleotide sequence of the structural gene(pyr B)that encodes the catalytic polypeptide of aspartate transcarbamoylase of Escherichia coli.Proceedings of the National Academy of Sciences of the United States of America,80,2462-2466.
Huang L L,Zhong K Z,Ma Q B,Nian H,Yang Y.2011.Integrated QTLs map of phosphorus efficiency in soybean by Meta-analysis.Chinese Journal of Oil Crop Sciences,33,25-32.(in Chinese)
Kassem M A,Meksem K,Iqbal M J,Njiti V N,Banz W J,Winters T A,Wood A,Lightfoot D A.2004.Definition of soybean genomic regions that control seed phytoestrogen amounts.Bio Med Research International,2004,52-60.
Kwanyuen P,Burton J W.2010.A modified amino acid analysis using PITC derivatization for soybeans with accurate determination of cysteine and half-cystine.Journal of the American Oil Chemists’Society,87,127-132.
Lewis M W,Leslie M E,Fulcher E H,Darnielle L,Healy PN,Youn J Y,Liljegren S J.2010.The SERK1 receptorlike kinase regulates organ separation in Arabidopsis flowers.The Plant Journal,62,817-828.
Li M W,Xin D,Gao Y,Li K P,Fan K,Mu?oz N B,Yung W S,Lam H M.2016.Using genomic information to improve soybean adaptability to climate change.Journal of Experimental Botany,68,1823-1834.
Liu S,Luo L,Liu Z X,Guan R X,Qiu L J.2011.Integration of QTLs related to soybean protein content and“qualification”of them by overview method.Soybean Science,30,1-7.(in Chinese)
Medic J,Atkinson C,Hurburgh Jr C R.2014.Current knowledge in soybean composition.Journal of the American Oil Chemists’Society,91,363-384.
Panthee D R,Kwanyuen P,Sams C E,West D R,Saxton A M,Pantalone V R.2004.Quantitative trait loci forβ-conglycinin(7S)and glycinin(11S)fractions of soybean storage protein.Journal of the American Oil Chemists’Society,81,1005-1012.
Panthee D R,Pantalone V R,Sams C E,Saxton A M,West D R,Orf J H,Killam A S.2006a.Quantitative trait loci controlling sulfur containing amino acids,methionine and cysteine,in soybean seeds.Theoretical and Applied Genetics,112,546-553.
Panthee D R,Pantalone V R,Saxton A M,West D R,Sams C E.2006b.Genomic regions associated with amino acid composition in soybean.Molecular Breeding,17,79-89.
Primomo V S,Poysa V,Ablett G R,Jackson C J,Gijzen M,Rajcan I.2005.Mapping QTL for individual and total isoflavone content in soybean seeds.Crop Science,45,2454-2464.
Qi Z M,Wu Q,Han X,Sun Y N,Du X Y,Liu C Y,Jiang H W,Hu G H,Chen Q S.2011.Soybean oil content QTL mapping and integrating with meta-analysis method for mining genes.Euphytica,179,499-514.
Qiu H M,Li Z,Yu Y,Ma X P,Zheng Y H,Meng F F,Hou Y L,Wang Y Q,Wang S M.2015.Mining and analysis of genes related to sulfur containing amino acids in soybean and bioinformatic analysis based on meta-QTL.Chinese Journal of Oil Crop Sciences,37,141-147.(in Chinese)
Qiu H M,Yang C M,Gao S Q,Hou Y L,Ma X P,Sun X M,Zheng H Y,Wang Y Q,Wang S M.2014.Phenotype identification and cluster analysis of soybean in upper latitudes regions based on protein content and amino acid composition.Journal of Plant Genetic Resources,15,1202-1208.(in Chinese)
Schmutz J I,Cannon S B,Schlueter J,Ma J,Mitros T,Nelson W,Hyten D L,Song Q,Thelen J J,Cheng J,Xu D,Hellsten U,May G D,Yu Y,Sakurai T,Umezawa T,Bhattacharyya M K,Sandhu D,Valliyodan B,Lindquist E,et al.2010.Genome sequence of the palaeopolyploid soybean.Nature,463,178-183.
Shah K,Vervoort J,de Vries S C.2001.Role of threonines in the Arabidopsis thaliana somatic embryogenesis receptor kinase 1 activation loop in phosphorylation.Journal of Biological Chemistry,276,41263-41269.
Smallwood C J.2012.Detection of quantitative trait loci for marker-assisted selection of soybean isoflavone genistein.MSc thesis,University of Tennessee,Knoxville.
Stock K F,J?nsson L,Ricard A,Mark T.2016.Genomic applications in horse breeding.Animal Frontiers,6,45-52.
Stombaugh S K,Orf J H,Jung H G,Chase K,Lark K G,Somers D A.2004.Quantitative trait loci associated with cell wall polysaccharides in soybean seed.Crop Science,44,2101-2106.
Sun Y N,Luan H H,Qi Z M,Shan D P,Liu C Y,Hu G H,Chen Q S.2012a.Mapping and meta-analysis of height QTLs in soybean.Legume Genomics and Genetics,3,1-7.
Sun Y N,Pan J B,Shi X L,Du X Y,Wu Q,Qi Z M,Jiang H W,Xin D W,Liu C Y,Hu G H,Chen Q S.2012b.Multi-environment mapping and meta-analysis of 100-seed weight in soybean.Molecular Biology Reports,39,9435-9443.
Thilakarathna M S,Raizada M N.2017.A meta-analysis of the effectiveness of diverse rhizobia inoculants on soybean traits under field conditions.Soil Biology and Biochemistry,105,177-196.
Thu N B A,Nguyen Q T,Hoang X L T,Thao N P,Tran L S P.2014.Evaluation of drought tolerance of the Vietnamese soybean cultivars provides potential resources for soybean production and genetic engineering.Bio Med Research International,2014,809736.
Trijatmiko K R,Prasetiyono J,Thomson M J,Cruz C MV,Moeljopawiro S,Pereira A.2014.Meta-analysis of quantitative trait loci for grain yield and component traits under reproductive-stage drought stress in an upland rice population.Molecular Breeding,34,283-295.
Verret V,Gardarin A,Pelzer E,Médiène S,Makowski D,Valantin-Morison M.2017.Can legume companion plants control weeds without decreasing crop yield?A metaanalysis.Field Crops Research,204,158-168.
Wang J,Song W K,Zhang W B,Liu C Y,Hu G H,Chen Q S.2009.Meta-analysis of insect-resistance QTLs in soybean.Hereditas,31,593-561.
Wang J L,Liu C Y,Wang J,Qi Z M,Hui L I,Hu G H,Chen Q S.2010.An integrated QTL Map of fungal disease resistance in soybean(Glycine max L.Merr):A method of meta-analysis for mining R genes.Agricultural Sciences in China,9,223-232.
Wang J Y,Xiong Y C,Li F M,Siddique K H,Turner N C.2017.Effects of drought stress on morphophysiological traits,biochemical characteristics,yield,and yield components in different ploidy wheat:A meta-analysis.Advances in Agronomy,143,139-173.
Wang X,Jiang G L,Song Q,Cregan P B,Scott R A,Zhang J,Yen Y,Brown M.2015.Quantitative trait locus analysis of seed sulfur-containing amino acids in two recombinant inbred line populations of soybean.Euphytica,201,293-305.
Warrington C V,Abdel-Haleem H,Hyten D L,Cregan P B,Orf JH,Killam A S,Bajjalieh N,Li Z,Boerma H R.2015.QTL for seed protein and amino acids in the Benning×Danbaekkong soybean population.Theoretical and Applied Genetics,128,839-850.
Wu Q,Qi Z M,Liu C Y,Hu G H,Chen Q S.2009.An integrated QTL map of growth stage in soybean[Glycine max(L.)Merr.]:Constructed through meta-analysis.Acta Agronomica Sinica,35,1418-1424.(in Chinese)
Yang K,Moon J K,Jeong N,Chun H K,Kang S T,Back K,Jeong S C.2011.Novel major quantitative trait loci regulating the content of isoflavone in soybean seeds.Genes&Genomics,33,685-692.
Yellareddygari S K R,Pasche J S,Taylor R J,Gudmestad NC.2016.Individual participant data meta-analysis of foliar fungicides applied for potato early blight management.Plant Disease,100,200-206.
Yoshikawa T,Okumoto Y,Ogata D,Sayama T,Teraishi M,Terai M,Toda T,Yamada K,Yagasaki K,Yamada N,Tsukiyama T.2010.Transgressive segregation of isoflavone contents under the control of four QTLs in a cross between distantly related soybean varieties.Breed Science,60,243-254.
Zeng G,Li D,Han Y,Teng W,Wang J,Qiu L,Li W.2009.Identification of QTL underlying isoflavone contents in soybean seeds among multiple environments.Theoretical and Applied Genetics,118,1455-1463.
Bolger M E,Weisshaar B,Scholz U,Stein N,Usadel B,Mayer K F.2014.Plant genome sequencing-applications for crop improvement.Current Opinion in Biotechnology,26,31-37.
Catoni E,Desimone M,Hilpert M,Wipf D,Kunze R,Schneider A,Flügge U,Schumacher K,Frommer W B.2003.Expression pattern of a nuclear encoded mitochondrial arginineornithine translocator gene from Arabidopsis.BMC Plant Biology,3,1.
Chardon F,Virlon B,Moreau L,Falque M,Joets J,Decousset L,Murigneux A,Charcosset A.2004.Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome.Genetics,168,2169-2185.
Chen N W,Sévignac M,Thareau V,Magdelenat G,David P,Ashfield T,Innes R W,Geffroy V.2010.Specific resistances against Pseudomonas syringae effectors Avr B and Avr Rpm1 have evolved differently in common bean(Phaseolus vulgaris),soybean(Glycine max),and Arabidopsis thaliana.New Phytologist,187,941-956.
Danan S,Veyrieras J B,Lefebvre V.2011a.Construction of a potato consensus map and QTL meta-analysis offer new insights into the genetic architecture of late blight resistance and plant maturity traits.BMC Plant Biology,11,16.
Danan S,Veyrieras J B,Lefebvre V.2011b.Genomic selection in tree breeding:Testing accuracy of prediction models including dominance effect.BMC Proceedings,5,1753-6561.
Gao L F,Guo Y,Hao Z B,Qiu L J.2013.Integration and“Overview”analysis of QTLs related to plant height in soybean.Hereditas,35,215-224.
Glass G V.1976.Primary,secondary,and meta-analysis of research 1.Educational Researcher,5,3-8.
Goffinet B,Gerber S.2000.Quantitative trait loci:A metaanalysis.Genetics,155,463-473.
von Groll U,Berger D,Altmann T.2002.The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development.The Plant Cell,14,1527-1539.
Guo B,Sleper D A,Lu P,Shannon J G,Nguyen H T,Arelli PR.2006.QTLs associated with resistance to soybean cyst nematode in soybean:Meta-analysis of QTL locations.Crop Science,46,595-602.
Gutierrez-Gonzalez J J,Vuong T D,Zhong R,Yu O,Lee JD,Shannon G,Ellersieck M,Nguyen H T,Sleper D A.2011.Major locus and other novel additive and epistatic loci involved in modulation of isoflavone concentration in soybean seeds.Theoretical and Applied Genetics,123,1375-1385.
Gutierrez-Gonzalez J J,Wu X,Gillman J D,Lee J D,Zhong R,Yu O,Shannon G,Ellersieck M,Nguyen H T,Sleper D A.2010.Intricate environment-modulated genetic networks control isoflavone accumulation in soybean seeds.BMCPlant Biology,10,105.
Gutierrez-Gonzalez J J,Wu X,Zhang J,Lee J D,Ellersieck M,Shannon J G,Yu O,Nguyen H T,Sleper D A.2009.Genetic control of soybean seed isoflavone content:Importance of statistical model and epistasis in complex traits.Theoretical and Applied Genetics,119,1069-1083.
Hao Z,Li X,Liu X,Xie C,Li M,Zhang D,Zhang S.2010.Meta-analysis of constitutive and adaptive QTL for drought tolerance in maize.Euphytica,174,165-177.
Hoover T A,Roof W D,Foltermann K F,O’Donovan G A,Bencini D A,Wild J R.1983.Nucleotide sequence of the structural gene(pyr B)that encodes the catalytic polypeptide of aspartate transcarbamoylase of Escherichia coli.Proceedings of the National Academy of Sciences of the United States of America,80,2462-2466.
Huang L L,Zhong K Z,Ma Q B,Nian H,Yang Y.2011.Integrated QTLs map of phosphorus efficiency in soybean by Meta-analysis.Chinese Journal of Oil Crop Sciences,33,25-32.(in Chinese)
Kassem M A,Meksem K,Iqbal M J,Njiti V N,Banz W J,Winters T A,Wood A,Lightfoot D A.2004.Definition of soybean genomic regions that control seed phytoestrogen amounts.Bio Med Research International,2004,52-60.
Kwanyuen P,Burton J W.2010.A modified amino acid analysis using PITC derivatization for soybeans with accurate determination of cysteine and half-cystine.Journal of the American Oil Chemists’Society,87,127-132.
Lewis M W,Leslie M E,Fulcher E H,Darnielle L,Healy PN,Youn J Y,Liljegren S J.2010.The SERK1 receptorlike kinase regulates organ separation in Arabidopsis flowers.The Plant Journal,62,817-828.
Li M W,Xin D,Gao Y,Li K P,Fan K,Mu?oz N B,Yung W S,Lam H M.2016.Using genomic information to improve soybean adaptability to climate change.Journal of Experimental Botany,68,1823-1834.
Liu S,Luo L,Liu Z X,Guan R X,Qiu L J.2011.Integration of QTLs related to soybean protein content and“qualification”of them by overview method.Soybean Science,30,1-7.(in Chinese)
Medic J,Atkinson C,Hurburgh Jr C R.2014.Current knowledge in soybean composition.Journal of the American Oil Chemists’Society,91,363-384.
Panthee D R,Kwanyuen P,Sams C E,West D R,Saxton A M,Pantalone V R.2004.Quantitative trait loci forβ-conglycinin(7S)and glycinin(11S)fractions of soybean storage protein.Journal of the American Oil Chemists’Society,81,1005-1012.
Panthee D R,Pantalone V R,Sams C E,Saxton A M,West D R,Orf J H,Killam A S.2006a.Quantitative trait loci controlling sulfur containing amino acids,methionine and cysteine,in soybean seeds.Theoretical and Applied Genetics,112,546-553.
Panthee D R,Pantalone V R,Saxton A M,West D R,Sams C E.2006b.Genomic regions associated with amino acid composition in soybean.Molecular Breeding,17,79-89.
Primomo V S,Poysa V,Ablett G R,Jackson C J,Gijzen M,Rajcan I.2005.Mapping QTL for individual and total isoflavone content in soybean seeds.Crop Science,45,2454-2464.
Qi Z M,Wu Q,Han X,Sun Y N,Du X Y,Liu C Y,Jiang H W,Hu G H,Chen Q S.2011.Soybean oil content QTL mapping and integrating with meta-analysis method for mining genes.Euphytica,179,499-514.
Qiu H M,Li Z,Yu Y,Ma X P,Zheng Y H,Meng F F,Hou Y L,Wang Y Q,Wang S M.2015.Mining and analysis of genes related to sulfur containing amino acids in soybean and bioinformatic analysis based on meta-QTL.Chinese Journal of Oil Crop Sciences,37,141-147.(in Chinese)
Qiu H M,Yang C M,Gao S Q,Hou Y L,Ma X P,Sun X M,Zheng H Y,Wang Y Q,Wang S M.2014.Phenotype identification and cluster analysis of soybean in upper latitudes regions based on protein content and amino acid composition.Journal of Plant Genetic Resources,15,1202-1208.(in Chinese)
Schmutz J I,Cannon S B,Schlueter J,Ma J,Mitros T,Nelson W,Hyten D L,Song Q,Thelen J J,Cheng J,Xu D,Hellsten U,May G D,Yu Y,Sakurai T,Umezawa T,Bhattacharyya M K,Sandhu D,Valliyodan B,Lindquist E,et al.2010.Genome sequence of the palaeopolyploid soybean.Nature,463,178-183.
Shah K,Vervoort J,de Vries S C.2001.Role of threonines in the Arabidopsis thaliana somatic embryogenesis receptor kinase 1 activation loop in phosphorylation.Journal of Biological Chemistry,276,41263-41269.
Smallwood C J.2012.Detection of quantitative trait loci for marker-assisted selection of soybean isoflavone genistein.MSc thesis,University of Tennessee,Knoxville.
Stock K F,J?nsson L,Ricard A,Mark T.2016.Genomic applications in horse breeding.Animal Frontiers,6,45-52.
Stombaugh S K,Orf J H,Jung H G,Chase K,Lark K G,Somers D A.2004.Quantitative trait loci associated with cell wall polysaccharides in soybean seed.Crop Science,44,2101-2106.
Sun Y N,Luan H H,Qi Z M,Shan D P,Liu C Y,Hu G H,Chen Q S.2012a.Mapping and meta-analysis of height QTLs in soybean.Legume Genomics and Genetics,3,1-7.
Sun Y N,Pan J B,Shi X L,Du X Y,Wu Q,Qi Z M,Jiang H W,Xin D W,Liu C Y,Hu G H,Chen Q S.2012b.Multi-environment mapping and meta-analysis of 100-seed weight in soybean.Molecular Biology Reports,39,9435-9443.
Thilakarathna M S,Raizada M N.2017.A meta-analysis of the effectiveness of diverse rhizobia inoculants on soybean traits under field conditions.Soil Biology and Biochemistry,105,177-196.
Thu N B A,Nguyen Q T,Hoang X L T,Thao N P,Tran L S P.2014.Evaluation of drought tolerance of the Vietnamese soybean cultivars provides potential resources for soybean production and genetic engineering.Bio Med Research International,2014,809736.
Trijatmiko K R,Prasetiyono J,Thomson M J,Cruz C MV,Moeljopawiro S,Pereira A.2014.Meta-analysis of quantitative trait loci for grain yield and component traits under reproductive-stage drought stress in an upland rice population.Molecular Breeding,34,283-295.
Verret V,Gardarin A,Pelzer E,Médiène S,Makowski D,Valantin-Morison M.2017.Can legume companion plants control weeds without decreasing crop yield?A metaanalysis.Field Crops Research,204,158-168.
Wang J,Song W K,Zhang W B,Liu C Y,Hu G H,Chen Q S.2009.Meta-analysis of insect-resistance QTLs in soybean.Hereditas,31,593-561.
Wang J L,Liu C Y,Wang J,Qi Z M,Hui L I,Hu G H,Chen Q S.2010.An integrated QTL Map of fungal disease resistance in soybean(Glycine max L.Merr):A method of meta-analysis for mining R genes.Agricultural Sciences in China,9,223-232.
Wang J Y,Xiong Y C,Li F M,Siddique K H,Turner N C.2017.Effects of drought stress on morphophysiological traits,biochemical characteristics,yield,and yield components in different ploidy wheat:A meta-analysis.Advances in Agronomy,143,139-173.
Wang X,Jiang G L,Song Q,Cregan P B,Scott R A,Zhang J,Yen Y,Brown M.2015.Quantitative trait locus analysis of seed sulfur-containing amino acids in two recombinant inbred line populations of soybean.Euphytica,201,293-305.
Warrington C V,Abdel-Haleem H,Hyten D L,Cregan P B,Orf JH,Killam A S,Bajjalieh N,Li Z,Boerma H R.2015.QTL for seed protein and amino acids in the Benning×Danbaekkong soybean population.Theoretical and Applied Genetics,128,839-850.
Wu Q,Qi Z M,Liu C Y,Hu G H,Chen Q S.2009.An integrated QTL map of growth stage in soybean[Glycine max(L.)Merr.]:Constructed through meta-analysis.Acta Agronomica Sinica,35,1418-1424.(in Chinese)
Yang K,Moon J K,Jeong N,Chun H K,Kang S T,Back K,Jeong S C.2011.Novel major quantitative trait loci regulating the content of isoflavone in soybean seeds.Genes&Genomics,33,685-692.
Yellareddygari S K R,Pasche J S,Taylor R J,Gudmestad NC.2016.Individual participant data meta-analysis of foliar fungicides applied for potato early blight management.Plant Disease,100,200-206.
Yoshikawa T,Okumoto Y,Ogata D,Sayama T,Teraishi M,Terai M,Toda T,Yamada K,Yagasaki K,Yamada N,Tsukiyama T.2010.Transgressive segregation of isoflavone contents under the control of four QTLs in a cross between distantly related soybean varieties.Breed Science,60,243-254.
Zeng G,Li D,Han Y,Teng W,Wang J,Qiu L,Li W.2009.Identification of QTL underlying isoflavone contents in soybean seeds among multiple environments.Theoretical and Applied Genetics,118,1455-1463.