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Identification of Major QTL for Waterlogging Tolerance Using Genome-Wide Association and Linkage Mapping of Maize Seedlings

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Abstract

To investigate the genetic basis of maize seedling response to waterlogging, we performed a genome-wide association study in 144 maize inbred lines, measuring length, fresh and dry weight of roots and shoots under normal and waterlogged conditions using 45,868 SNPs. This panel was divided into three subgroups based on the population structure results and the LD decay distance was 180 kb. A biparental advanced backcross (AB) population was also used to detect quantitative trait loci (QTL). In a comparison of 16 different models, principal components analysis (PCA/top PC3) + K was found to be best for reduction of false-positive associations for further analysis. A whole-genome scan detected four strong peak signals (P < 2.18 × 10−5) significantly associated with the waterlogging response on chromosomes 5, 6 and 9. SNP4784, SNP200, SNP298, and SNP6314 showed significant association with corresponding traits under waterlogging and explained 14.99–19.36 %, 15.75–17.64 %, 16.08 % and 15.44 % of the phenotypic variation, respectively. The identified SNPs were located in GRMZM2G012046, GRMZM2G009808, GRMZM2G137108 and GRMZM2G369629 (AGPV1). SNP4784 (GRMZM2G012046) was colocalized with the major QTL that was identified with the same traits in the AB population. Forty-seven SNPs significantly associated (P < 2.18 × 10−4) with six traits in association mapping were identified and, among these, 33 SNPs were already reported in literature as waterlogging-related traits. These results will help elucidate the genetic basis of differential responses and tolerance to waterlogging stress among maize inbred lines, and provide novel loci for improvement of waterlogging tolerance of maize inbred lines using marker-assisted selection.

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Fig. 1a,b
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Abbreviations

SNP:

Single nucleotide polymorphism

AB:

Advanced backcross

PCA:

Principal components analysis

LD:

Linkage disequilibrium

QTL:

Quantitative trait locus

GWAS:

Genome-wide association study

SH:

Seedling height

RL:

Root length

SFW:

Shoot fresh weight

RFW:

Root fresh weight

SDW:

Shoot dry weight

RDW:

Root dry weight

References

  • Abiko T, Kotula L, Shiono K, Malik AI, Colmer TD, Nakazono M (2012) Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays). Plant Cell Environ 35:1618–1630. doi:10.1111/j.1365-3040.2012.02513.x

    Google Scholar 

  • Aranzana MJ, Kim S, Zhao K, Bakker E, Horton M, Jakob K, Lister C, Molitor J, Shindo C, Tang C, Toomajian C, Traw B, Zheng H, Bergelson J, Dean C, Marjoram P, Nordborg M (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1(5):e60. doi:10.1371/journal.pgen.0010060

    Article  PubMed  Google Scholar 

  • Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT, Jiang R, Muliyati NW, Zhang X, Amer MA, Baxter I, Brachi B, Chory J, Dean C, Debieu M, de Meaux J, Ecker JR, Faure N, Kniskern JM, Jones JD, Michael T, Nemri A, Roux F, Salt DE, Tang C, Todesco M, Traw MB, Weigel D, Marjoram P, Borevitz JO, Bergelson J, Nordborg M (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465(7298):627–631

    Article  PubMed  CAS  Google Scholar 

  • Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21(2):263–265

    Article  PubMed  CAS  Google Scholar 

  • Belo A, Zheng P, Luck S, Shen B, Meyer DJ, Li B, Tingey S, Rafalski A (2008) Whole genome scan detects an allelic variant of fad2 associated with increased oleic acid levels in maize. Mol Genet Genomics 279(1):1–10

    Article  PubMed  CAS  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172(2):1165–1177

    Article  PubMed  Google Scholar 

  • Burgos M, Messmer M, Stamp P, Schmid J (2001) Flooding tolerance of spelt (Triticum spelta L.) compared to wheat (Triticum aestivum L.)—a physiological and genetic approach. Euphytica 122(2):287–295

    Article  Google Scholar 

  • Ching A, Caldwell KS, Jung M, Dolan M, Smith OS, Tingey S, Morgante M, Rafalski AJ (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet 3:19

    Article  PubMed  Google Scholar 

  • Cook JP, McMullen MD, Holland JB, Tian F, Bradbury P, Ross-Ibarra J, Buckler ES, Flint-Garcia SA (2012) Genetic architecture of maize kernel composition in the nested association mapping and inbred association panels. Plant Physiol 158(2):824–834

    Article  PubMed  CAS  Google Scholar 

  • Dennis ES, Dolferus R, Ellis M, Rahman M, Wu Y, Hoeren FU, Grover A, Ismond KP, Good AG, Peacock WJ (2000) Molecular strategies for improving waterlogging tolerance in plants. J Exp Bot 51(342):89–97

    Article  PubMed  CAS  Google Scholar 

  • Devlin B, Roeder K (1999) Genomic control for association studies. Biometrics 55(4):997–1004

    Article  PubMed  CAS  Google Scholar 

  • Ellis MH, Dennis ES, Peacock WJ (1999) Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. Plant Physiol 119(1):57–64

    Article  PubMed  CAS  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6(5)

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4):1567–1587

    PubMed  CAS  Google Scholar 

  • Good AG, Johnson SJ, DePauw M, Carroll RT, Savidov N (2007) Engineering nitrogen use efficiency with alanine aminotransferase. Can J Bot 85:252–262

    Article  CAS  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2(4):618–620

    Article  Google Scholar 

  • Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H, Matsuoka M, Mori H, Ashikari M (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460(7258):1026–1030

    Article  PubMed  CAS  Google Scholar 

  • Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Lin Z, Buckler ES, Qian Q, Zhang QF, Li J, Han B (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42(11):961–967

    Article  PubMed  CAS  Google Scholar 

  • Huang X, Zhao Y, Wei X, Li C, Wang A, Zhao Q, Li W, Guo Y, Deng L, Zhu C, Fan D, Lu Y, Weng Q, Liu K, Zhou T, Jing Y, Si L, Dong G, Huang T, Lu T, Feng Q, Qian Q, Li J, Han B (2012) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44(1):32–39

    Article  Google Scholar 

  • Ingvarsson PK, Street NR (2011) Association genetics of complex traits in plants. New Phytol 189(4):909–922

    Article  PubMed  Google Scholar 

  • Knapp SJ, Stroup WW, Ross WM (1985) Exact confidence intervals for heritability on a progeny mean basis. Crop Sci 25:192–195

    Article  Google Scholar 

  • Kump KL, Bradbury PJ, Wisser RJ, Buckler ES, Belcher AR, Oropeza-Rosas MA, Zwonitzer JC, Kresovich S, McMullen MD, Ware D, Balint-Kurti PJ, Holland JB (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat Genet 43(2):163–168

    Article  PubMed  CAS  Google Scholar 

  • Li HH, Ye GY, Wang JK (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175(1):361–374

    Article  PubMed  Google Scholar 

  • Li H, Vaillancourt R, Mendham N, Zhou M (2008) Comparative mapping of quantitative trait loci associated with waterlogging tolerance in barley (Hordeum vulgare L.). BMC Genomics 9:401

    Article  PubMed  Google Scholar 

  • Li HM, Liang H, Tang ZX, Zhang HQ, Yan BJ, Ren ZL (2012) QTL Analysis for grain pentosans and hardness index in a Chinese 1RS.1BL × non-1RS.1BL wheat cross. Plant Mol Biol Report. doi:10.1007/s11105-012-0517-4

  • Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21(9):2128–2129

    Article  PubMed  CAS  Google Scholar 

  • Liu YZ, Tang B, Zheng YL, Ma KJ, Xu SZ, Qiu FZ (2010) Screening methods for waterlogging tolerance at Maize (Zea mays L.) seedling stage. Agric Sci China 9(3):362–369

    Article  Google Scholar 

  • Lu Y, Zhang S, Shah T, Xie C, Hao Z, Li X, Farkhari M, Ribaut JM, Cao M, Rong T, Xu Y (2010) Joint linkage-linkage disequilibrium mapping is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize. Proc Natl Acad Sci USA 107(45):19585–19590

    Article  PubMed  CAS  Google Scholar 

  • Mackay TF (2009) Genetics. A-maize-ing diversity. Science 325(5941):688–689

    Article  PubMed  CAS  Google Scholar 

  • Mano Y, Omori F (2008) Verification of QTL controlling root aerenchyma formation in a maize × teosinte “Zea nicaraguensis” advanced backcross population. Breeding Sci 58:217–223

    Article  Google Scholar 

  • Mano Y, Omori F (2009) High-density linkage map around the root aerenchyma locus Qaer1.06 in the backcross populations of maize Mi29 × teosinte “Zea nicaraguesis”. Breeding Sci 59:427–733

    Article  CAS  Google Scholar 

  • Mano Y, Muraki M, Komatsu T, Fujimori M, Akiyama F, Takamizo T (2002) Varietal difference in pre-germination flooding tolerance and waterlogging tolerance at the seedling stage in maize inbred lines. Jpn J Crop Sci 71(3):361–367

    Article  Google Scholar 

  • Mano Y, Muraki M, Fujimori M, Takamizo T, Kindiger B (2005a) AFLP–SSR maps of maize × teosinte and maize × maize: comparison of map length and segregation distortion. Plant Breeding 124:432–439

    Article  CAS  Google Scholar 

  • Mano Y, Muraki M, Fujimori M, Takamizo T, Kindiger B (2005b) Identification of QTL controlling adventitious root formation during flooding conditions in teosinte (Zea mays ssp. huehuetenangensis) seedlings. Euphytica 142:33–42

    Article  Google Scholar 

  • Mano Y, Omori F, Muraki M, Takamizo T (2005c) QTL mapping of adventitious root formation under flooding conditions in tropical maize (Zea mays L.) seedlings. Breeding Sci 55(3):343–347

    Article  Google Scholar 

  • Mano Y, Muraki M, Takamizo T (2006) Identification of QTL controlling flooding tolerance in reducing soil conditions in maize (Zea mays L.) seedlings. Plant Prod Sci 9(2):176–181

    Article  CAS  Google Scholar 

  • Mano Y, Omori F, Takamizo T, Kindiger B, Bird RM, Loaisiga CH, Takahashi H (2007) QTL mapping of root aerenchyma formation in seedlings of a maize × rare teosinte “Zea nicaraguensis” cross. Plant Soil 295:103–113

    Article  CAS  Google Scholar 

  • Mano Y, Omori F, Kindiger B, Takahashi H (2008) A linkage map of maize × teosinte Zea luxurians and identification of QTLs controlling root aerenchyma formation. Mol Breeding 21:327–337

    Article  CAS  Google Scholar 

  • Mano Y, Omori F, Loaisiga CH, Bird RM (2009) QTL mapping of above-ground adventitious roots during flooding in maize × teosinte “Zea nicaraguensis” backcross population. Plant Root 3:3–9

    Article  CAS  Google Scholar 

  • Mano Y, Omori F, Takeda K (2012) Construction of intraspecific linkage maps, detection of a chromosome inversion, and mapping of QTL for constitutive root aerenchyma formation in the teosinte “Zea nicaraguensis”. Mol Breeding 29:137–146

    Article  Google Scholar 

  • Morita-Yamamuro C, Tsutsui T, Sato M, Yoshioka H, Tamaoki M, Ogawa D, Matsuura H, Yoshihara T, Ikeda A, Uyeda I, Yamaguchi J (2005) The Arabidopsis gene CAD1 controls programmed cell death in the plant immune system and encodes a protein containing a MACPF domain. Plant Cell Physiol 46(6):902–912

    Article  PubMed  CAS  Google Scholar 

  • Nielsen R (2004) Late season flooding of maize. Pioneer Technical Insights 342:1–5

    Google Scholar 

  • Noutoshi Y, Kuromori T, Wada T, Hirayama T, Kamiya A, Imura Y, Yasuda M, Nakashita H, Shirasu K, Shinozaki K (2006) Loss of Necrotic Spotted Lesions 1 associates with cell death and defense responses in Arabidopsis thaliana. Plant Mol Biol 62(1–2):29–42

    Article  PubMed  CAS  Google Scholar 

  • Palaisa KA, Morgante M, Williams M, Rafalski A (2003) Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15(8):1795–1806

    Article  PubMed  CAS  Google Scholar 

  • Palaisa K, Morgante M, Tingey S, Rafalski A (2004) Long-range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep. Proc Natl Acad Sci USA 101(26):9885–9890

    Article  PubMed  CAS  Google Scholar 

  • Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. Plos Genetics 2(12):e190

    Article  PubMed  Google Scholar 

  • Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38(8):904–909

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67(1):170–181

    Article  PubMed  CAS  Google Scholar 

  • Purcell S, Cherny SS, Sham PC (2003) Genetic power calculator: design of linkage and association genetic mapping studies of complex traits. Bioinformatics 19(1):149–150

    Article  PubMed  CAS  Google Scholar 

  • Qiu F, Zheng Y, Zhang Z, Xu S (2007) Mapping of QTL associated with waterlogging tolerance during the seedling stage in maize. Ann Bot 99(6):1067–1081

    Article  PubMed  Google Scholar 

  • Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5(2):94–100

    Article  PubMed  CAS  Google Scholar 

  • Rafalski JA (2010) Association genetics in crop improvement. Curr Opin Plant Biol 13(2):174–180

    Article  PubMed  CAS  Google Scholar 

  • Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98(20):11479–11484

    Article  PubMed  CAS  Google Scholar 

  • Rohlf FJ (2000) NTSYS-pc numerical taxonomy and multivariate analysis system. version 21 Exeter Software: New York

  • Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81(24):8014–8018

    Article  PubMed  CAS  Google Scholar 

  • Salavati A, Khatoon A, Nanjo Y, Komatsu S (2012) Analysis of proteomic changes in roots of soybean seedlings during recovery after flooding. J Proteomics 75(3):878–893

    Article  PubMed  CAS  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326(5956):1112–1115

    Article  PubMed  CAS  Google Scholar 

  • Setter TL, Yan J, Warburton M, Ribaut JM, Xu Y, Sawkins M, Buckler ES, Zhang Z, Gore MA (2011) Genetic association mapping identifies single nucleotide polymorphisms in genes that affect abscisic acid levels in maize floral tissues during drought. J Exp Bot 62(2):701–716

    Article  PubMed  CAS  Google Scholar 

  • Shapiro SS, Wilk MB (1965) Analysis of variance test for normality (complete samples). Biometrika 52:591–611

    Google Scholar 

  • Sharma A, Chauhan RS (2012) Identification and association analysis of castor bean orthologous candidate gene-based markers for high oil content in Jatropha curcas. Plant Mol Biol Rep 30(4):1025–1031. doi:10.1007/s11105-011-0408-0

    Article  CAS  Google Scholar 

  • Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG (2008) Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol J 6:722–732

    Article  PubMed  CAS  Google Scholar 

  • Su Z, Li X, Hao Z, Xie C, Li M, Weng J, Zhang D, Liang X, Wang Z, Gao J, Zhang S (2011) Association analysis of the nced and rab28 genes with phenotypic traits under water stress in maize. Plant Mol Biol Rep 29(3):714–722. doi:10.1007/s11105-010-0279-9

    Article  Google Scholar 

  • Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA 98(16):9161–9166

    Article  PubMed  CAS  Google Scholar 

  • Tian F, Bradbury PJ, Brown PJ, Hung H, Sun Q, Flint-Garcia S, Rocheford TR, McMullen MD, Holland JB, Buckler ES (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 43(2):159–162

    Article  PubMed  CAS  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0, software for the calculation of genetic linkage maps. Plant Research International Wageningen, The Netherlands

    Google Scholar 

  • VanToai T, St Martin S, Chase K, Boru G, Schnipke V, Schmitthenner A, Lark K (2001) Identification of a QTL associated with tolerance of soybean to soil waterlogging. Crop Sci 41(4):1247–1252

    Article  Google Scholar 

  • Visser EJW, Voesenek LACJ, Vartapetian BB, Jackson MB (2003) Flooding and plant growth. Ann Bot-London 91(2):107–109

    Article  CAS  Google Scholar 

  • Wang M, Zhang X, Zhao J, Song W, Zheng Y (2011) Evaluation of the genetic diversity and genome-wide linkage disequilibrium of Chinese maize inbred lines. Aust J Crop Sci 5:1790–1795

    CAS  Google Scholar 

  • Wisser RJ, Kolkman JM, Patzoldt ME, Holland JB, Yu JM, Krakowsky M, Nelson RJ, Balint-Kurti PJ (2011) Multivariate analysis of maize disease resistances suggests a pleiotropic genetic basis and implicates a GST gene. Proc Natl Acad Sci USA 108(18):7339–7344

    Article  PubMed  CAS  Google Scholar 

  • Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442(7103):705–708

    Article  PubMed  CAS  Google Scholar 

  • Yan J, Shah T, Warburton ML, Buckler ES, McMullen MD, Crouch J (2009) Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS One 4(12):e8451. doi:10.1371/journal.pone.0008451

    Article  PubMed  Google Scholar 

  • Yan J, Kandianis CB, Harjes CE, Bai L, Kim EH, Yang X, Skinner DJ, Fu Z, Mitchell S, Li Q, Fernandez MG, Zaharieva M, Babu R, Fu Y, Palacios N, Li J, Dellapenna D, Brutnell T, Buckler ES, Warburton ML, Rocheford T (2010a) Rare genetic variation at Zea mays crtRB1 increases beta-carotene in maize grain. Nat Genet 42(4):322–327

    Article  PubMed  CAS  Google Scholar 

  • Yan J, Yang X, Shah T, Sanchez-Villeda H, Li J, Warburton M, Zhou Y, Crouch JH, Xu Y (2010b) High-throughput SNP genotyping with the GoldenGate assay in maize. Mol Breeding 25:441–451

    Article  CAS  Google Scholar 

  • Yan J, Warburton M, Crouch J (2011) Association mapping for enhancing maize (Zea mays L.) genetic improvement. Crop Sci 51. doi:10.2135/cropsci2010.04.0233

  • Yang X, Yan J, Shah T, Warburton ML, Li Q, Li L, Gao Y, Chai Y, Fu Z, Zhou Y, Xu S, Bai G, Meng Y, Zheng Y, Li J (2010) Genetic analysis and characterization of a new maize association mapping panel for quantitative trait loci dissection. Theor Appl Genet 121(3):417–431

    Article  PubMed  Google Scholar 

  • Yang X, Gao S, Xu S, Zhang Z, Prasanna BM, Li L, Li J, Yan J (2011) Characterization of a global germplasm collection and its potential utilization for analysis of complex quantitative traits in maize. Mol Breeding 28(4):511–526. doi:10.1007/s11032-010-9500-7

    Article  Google Scholar 

  • Yu JM, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38(2):203–208

    Article  PubMed  CAS  Google Scholar 

  • Zaidi PH, Rafiquea S, Rai PK, Singha NN, Srinivasanb G (2004) Tolerance to excess moisture in maize (Zea mays L.): susceptible crop stages and identification of tolerant genotypes. Field Crop Res 90(2–3):189–202

    Article  Google Scholar 

  • Zhang N, Gibon Y, Gur A, Chen C, Lepak N, Hohne M, Zhang Z, Kroon D, Tschoep H, Stitt M, Buckler E (2010a) Fine quantitative trait loci mapping of carbon and nitrogen metabolism enzyme activities and seedling biomass in the maize IBM mapping population. Plant Physiol 154(4):1753–1765

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010b) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42(4):355–360

    Article  PubMed  CAS  Google Scholar 

  • Zhao KY, Aranzana MJ, Kim S, Lister C, Shindo C, Tang CL, Toomajian C, Zheng HG, Dean C, Marjoram P, Nordborg M (2007) An Arabidopsis example of association mapping in structured samples. Plos Genetics 3(1)

  • Zhu C, Yu J (2009) Nonmetric multidimensional scaling corrects for population structure in association mapping with different sample types. Genetics 182(3):875–888

    Article  PubMed  Google Scholar 

  • Zondervan KT, Cardon LR (2004) The complex interplay among factors that influence allelic association. Nat Rev Genet 5(2):89–100

    Article  PubMed  CAS  Google Scholar 

  • Zou X, Jiang Y, Liu L, Zhang Z, Zheng Y (2010) Identification of transcriptome induced in roots of maize seedlings at the late stage of waterlogging. BMC Plant Biol 10:189

    Article  PubMed  Google Scholar 

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Acknowledgments

This research was supported by the Fundamental Research Funds for the Central University (no. 2011PY132), the National Natural Science Foundation of China (31071428), and the National Basic Research Program of China (973 Program) (2009CB118402).

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Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China

    Xiaobo Zhang, Bin Tang, Feng Yu, Liu Li, Ming Wang, Yadong Xue, Zuxin Zhang, Jianbing Yan, Bing Yue, Yonglian Zheng & Fazhan Qiu

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  1. Xiaobo Zhang
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  2. Bin Tang
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Correspondence to Fazhan Qiu.

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Zhang, X., Tang, B., Yu, F. et al. Identification of Major QTL for Waterlogging Tolerance Using Genome-Wide Association and Linkage Mapping of Maize Seedlings. Plant Mol Biol Rep 31, 594–606 (2013). https://doi.org/10.1007/s11105-012-0526-3

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