Skip to main content
Log in

Association analysis of genes involved in maize (Zea mays L.) root development with seedling and agronomic traits under contrasting nitrogen levels

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

A better understanding of the genetic control of root development might allow one to develop lines with root systems with the potential to adapt to soils with limited nutrient availability. For this purpose, an association study (AS) panel consisting of 74 diverse set of inbred maize lines were screened for seedling root traits and adult plant root traits under two contrasting nitrogen (N) levels (low and high N). Allele re-sequencing of RTCL, RTH3, RUM1, and RUL1 genes related to root development was carried out for AS panel lines. Association analysis was carried out between individual polymorphisms, and both seedling and adult plant traits, while controlling for spurious associations due to population structure and kinship relations. Based on the SNPs identified in RTCL, RTH3, RUM1, and RUL1, lines within the AS panel were grouped into 16, 9, 22, and 7 haplotypes, respectively. Association analysis revealed several polymorphisms within root genes putatively associated with the variability in seedling root and adult plant traits development under contrasting N levels. The highest number of significantly associated SNPs with seedling root traits were found in RTCL (19 SNPs) followed by RUM1 (4 SNPs) and in case of RTH3 and RUL1, two and three SNPs, respectively, were significantly associated with root traits. RTCL and RTH3 were also found to be associated with grain yield. Thus considerable allelic diversity is present within the candidate genes studied and can be utilized to develop functional markers that allow identification of maize lines with improved root architecture and yield under N stress conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abbe EC, Stein OL (1954) The growth of the shoot apex in maize: embryogeny. Am J Bot 41:285–293

    Article  Google Scholar 

  • Abdel-Ghani AH, Kumar B, Reyes-Matamoros J, Gonzalez-Portilla PJ, Jansen C, San Martin JP, Lee M, Lübberstedt T (2013) Genotypic variation and relationships between seedling and adult plant traits in maize (Zea mays L.) inbred lines grown under contrasting nitrogen levels. Euphytica 189:123–133

    Article  CAS  Google Scholar 

  • Agrama HS, Zakaria AG, Said FB, Tuinstra M (1999) Identification of quantitative trait loci for nitrogen use efficiency in maize. Mol Breed 5:187–195

    Article  Google Scholar 

  • Alpert KB, Tanksley SD (1996) High-resolution mapping and isolation of a yeast artificial chromosome contig containing fw2.2: a major fruit weight quantitative trait locus in tomato. Proc Natl Acad Sci USA 93:15503–15507

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Andersen JR, Lübberstedt T (2003) Functional markers in plants. Trends Plant Sci 8:554–560

    Article  CAS  PubMed  Google Scholar 

  • Andersen JR, Zein I, Wenzel G, Darnhofer B, Eder J, Ouzunova M, Lübberstedt T (2008) Characterization of phenylpropanoid pathway genes within European maize (Zea mays L.) inbreds. BMC Plant Biol 8:2

    Article  PubMed Central  PubMed  Google Scholar 

  • Anuradha M, Narayanan A (1991) Promotion of root elongation by phosphorus deficiency. Plant Soil 136:273–275

    Article  CAS  Google Scholar 

  • Arbuckle JL (2006) Amos computer program (version 7.0). SPSS, Chicago

    Google Scholar 

  • Arregui LM, Quemada M (2008) Strategies to improve nitrogen use efficiency in winter cereal crops under rain fed conditions. Agron J 100:277–284

    Article  CAS  Google Scholar 

  • Bailigar VC, Fageria NK, He ZL (2001) Nutrient use efficiency in plants. Commun Soil Sci Plant Anal 4:921–950

    Article  Google Scholar 

  • Bänziger M, Lafitte HR (1997) Efficiency of secondary traits for improving maize for low-nitrogen target environments. Crop Sci 37:1110–1117

    Article  Google Scholar 

  • Barber SA, MacKay AD (1986) Root growth and phosphorus and potassium uptake by two corn genotypes in the field. Fertil Res 10:217–230

    Article  Google Scholar 

  • Beló 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 279:1–10

    Article  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300

    Google Scholar 

  • Bolaños J, Edmeades GO (1996) The importance of the anthesis-silking interval in breeding for drought tolerance in tropical maize. Field Crop Res 48:65–80

    Article  Google Scholar 

  • Bonifas KD, Walters DT, Cassman KG (2005) Nitrogen supply affects root: shoot ratio in corn and velvetleaf (Abutilon theophrasti). Weed Sci 53:670–675

    Article  CAS  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Brady SM, Song S, Dhugga KS, Rafalski JA, Benfey PN (2007) Combining expression and comparative evolutionary analysis. The COBRA gene family. Plant Physiol 143:172–187

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brenner A, Zein I, Chen Y, Andersen JR, Wenzel G, Ouzunova M, Eder J, Darnhofer B, Frei U, Barrière Y, Lübberstedt T (2010) Polymorphisms in O-methyltransferase genes are associated with stover cell wall digestibility in European maize (Zea mays L.). BMC Plant Biol 10:27

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Chen Y, Zein I, Brenner EA, Andersen JR, Landbeck M, Ouzunova M, Lübberstedt T (2010) Polymorphisms in monolignol biosynthetic genes are associated with biomass yield and agronomic traits in European maize (Zea mays L.). BMC Plant Biol 10:12

    Article  PubMed Central  PubMed  Google Scholar 

  • Chun L, Chen F, Zhang F, Mi GH (2005) Root growth, nitrogen uptake and yield formation of hybrid maize with different N efficiency. Plant Nutr Fert Sci 11:615–619

    Google Scholar 

  • Eghball B, Maranville JW (1993) Root development and nitrogen influx of corn genotypes grown under combined drought and N stress. Agron J 85:147–152

    Article  CAS  Google Scholar 

  • Ersoz ES, Yu J, Buckler ES (2009) Applications of linkage disequilibrium and association mapping in maize. In: Kriz A, Larkins B (eds) Molecular genetic approaches to maize improvement. Springer, Berlin

    Google Scholar 

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

    Article  Google Scholar 

  • FAO (2006) Fertilizer use by crop (FAO Fertilizer and Plant Nutrition Bulletin No. 17). Food and Agriculture Organization of the United Nations

  • FAO (2010) Current world fertilizer trends and outlook to 2014. Food and Agriculture Organization of the United Nations, Palazzo

    Google Scholar 

  • Feldman L (1994) The maize root. In: Freeling M, Walbot V (eds) The maize handbook. Springer, New York, pp 29–37

    Chapter  Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    Article  CAS  PubMed  Google Scholar 

  • Garcés-Claver A, Fellman SM, Gil-Ortega R, Jahn M, Arnedo-Andrés MS (2007) Identification, validation and survey of a single nucleotide polymorphism (SNP) associated with pungency in Capsicum spp. Theor Appl Genet 115:907–916

    Article  PubMed  Google Scholar 

  • Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461–485

    Article  CAS  PubMed  Google Scholar 

  • Hershey DR (1994) Solution culture hydroponic: history and inexpensive equipment. Solution culture hydroponics. Am Biol Teach 56:111–118

    Article  Google Scholar 

  • Hertz W, Hochholdinger F, Schwall F, Feix G (1996) Isolation and characterization of rtcs, a mutant deficient in the formation of nodal roots. Plant J 10:845–857

    Article  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58:2369–2387

    Article  CAS  PubMed  Google Scholar 

  • Hochholdinger F (2009) The maize root system: morphology, anatomy and genetics. In: Bennetzen J, Hake S (eds) The Handbook of Maize. Springer, New York Inc, pp 145–160

    Chapter  Google Scholar 

  • Hochholdinger F, Feix G (1998) Early post-embryonic root formation is specifically affected in the maize mutant lrt1. Plant J 16:247–255

    Article  CAS  PubMed  Google Scholar 

  • Hochholdinger F, Park WJ, Feix G (2001) Cooperative action of SLR1 and SLR2 is required for lateral root specific cell-elongation in maize. Plant Physiol 125:1529–1539

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hochholdinger F, Wen TJ, Zimmermann R, Chimot-Marolle P, da Costa e Silva O O, Bruce W, Lamkey KR, Wienand U, Schnable PS (2008) The maize (Zea mays L.) roothairless3 gene encodes a putative GPI-anchored, monocot-specific, COBRA-like protein that significantly affects grain yield. Plant J 54:888–898

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Horst WJ, Kamh M, Jibrin JM, Chude VO (2001) Agronomic measures for increasing P availability to crops. Plant Soil 237:211–223

    Article  CAS  Google Scholar 

  • Hund A, Ruta N, Liedgens M (2009) Rooting depth and water use efficiency of tropical maize inbred lines, differing in drought tolerance. Plant Soil 318:311–325

    Article  CAS  Google Scholar 

  • Hund A, Reimer R, Messmer R (2011) A consensus map of QTLs controlling the root length of maize. Plant Soil 344:143–158

    Article  CAS  Google Scholar 

  • Huttley GA, Smith MW, Carrington M, O’Brien SJ (1999) Genetics 152:1711–1722

    PubMed Central  CAS  PubMed  Google Scholar 

  • Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura L, Hasegawa Y, Ashikari M, Kitano H, Matsuokaa M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17:1387–1396

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C, Machida Y (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43:467–478

    Article  CAS  PubMed  Google Scholar 

  • Jannink JL, Bink MCAM, Jansen RC (2001) Using complex plant pedigrees to map valuable genes. Trends Plant Sci 6:337–342

    Article  CAS  PubMed  Google Scholar 

  • Jeong Y, Mun J, Lee I, Woo JC, Hong CB, Kim S (2006) Distinct roles of the first introns on the expression of Arabidopsis Profilin gene family members. Plant Physiol 140:196–209

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Khan MH, Dar AN (2009) Correlation and path coefficient analysis of some quantitative traits in wheat. Africa Crop Sci J 18(1):9–14

    Google Scholar 

  • Kim S (2007) Recombination and linkage disequilibrium in Arabidopsis thaliana. Nat Genet 39:1151–1155

    Article  CAS  PubMed  Google Scholar 

  • Kim Y, Nielsen R (2004) Linkage disequilibrium as a signature of selective sweeps. Genetics 167:1513–1524

    Article  PubMed Central  PubMed  Google Scholar 

  • Krill AM, Kirst M, Kochian LV, Buckler ES, Hoekenga OA (2010) Association and linkage analysis of aluminum tolerance genes in maize. PLoS ONE 5(4):e9958

    Article  PubMed Central  PubMed  Google Scholar 

  • Kumar B, Abdel-Ghani AH, Pace J, Reyes-Matamoros J, Hochholdinger F, Lübberstedt T (2014) Association analysis of single nucleotide polymorphisms in candidate genes with root traits in maize (Zea mays L.) seedlings. Plant Sci 224:9–19

    Article  CAS  PubMed  Google Scholar 

  • Laffitte HR, Edmeades GO (1994) Improvements of tolerance to low soil nitrogen in tropical maize I. Selection criteria. Field Crops Res 39:1–14

    Article  Google Scholar 

  • Li J, Shi-Qing L, Yi L, Xiao-Li C (2009) Effects of increased ammonia on root/shoot ratio, grain yield and nitrogen use efficiency of two wheat varieties with various N supply. Plant Soil Environ 55:273–280

    CAS  Google Scholar 

  • Liu H, Wang S, Yu X, Yu J, He X, Zhang S, Shou H, Wu P (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J 43:47–56

    Article  PubMed  Google Scholar 

  • Liu J, Li J, Chen F, Zhang F, Ren T, Zhuang Z, Mi G (2008) Mapping QTLs for root traits under different nitrate levels at the seedling stage in maize (Zea mays L.). Plant Soil 305:253–265

    Article  CAS  Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. COPB 6:280–287

    CAS  Google Scholar 

  • Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56

    Article  CAS  Google Scholar 

  • Maizlisch NA, Fritton DD, Kendall WA (1980) Root morphology and early development of maize at varying levels of nitrogen. Agron J 72:5–31

    Article  Google Scholar 

  • Majer C, Xu C, Berendzen KW, Hochholdigner F (2012) Molecular interaction of ROOTLESS CONCERNING CROWN AND SEMINAL ROOTS, a LOB domain protein regulating shoot-borne root initiation in maize (Zea mays L.). Philos Trans R Soc 367:1542–1551

    Article  CAS  Google Scholar 

  • Marschner H (1998) Role of root growth, arbuscular mycorrhiza, and root exudates for the efficiency in nutrient acquisition. Field Crops Res 56:203–207

    Article  Google Scholar 

  • McMaster G, Wilhelm WW (1997) Growing degree-days: one equation, two interpretations. Agr For Meteorol 87:291–300

    Article  Google Scholar 

  • Moll RH, Kamprath EJ, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agron J 74:562–564

    Article  Google Scholar 

  • Monaco TA, Mackown CT, Johnson DA, Jones TA, Norton JM, Norton JB, Redinbaugh MG (2003) Nitrogen effects on seed germination and seedling growth. J Range Manag 56:646–653

    Article  Google Scholar 

  • Muurinen S, Kleemola J, Peltonen-Sainio P (2007) Accumulation and translocation of nitrogen in spring cereal cultivars differing in nitrogen use efficiency. Agron J 99:441–449

    Article  CAS  Google Scholar 

  • Narayanan A, Reddy BK (1982) Effect of phosphorus deficiency on the form of plant root system. In: Scaife A (ed) Plant nutrition, vol 2. Commonwealth Agricultural Bureau, Slough, pp 412–417

    Google Scholar 

  • Neuffer MG, Coe EH, Wessler SR (1997) Mutants of maize. Cold Spring Harbor Laboratory Press, Plainview

    Google Scholar 

  • Ortiz-Monasterio RJI, Sayre KD, Rajaram S, McMahon M (1997) Genetic progress in wheat yield and nitrogen use efficiency under four nitrogen rates. Crop Sci 37:898–904

    Article  Google Scholar 

  • Pace J, Lee N, Naik HS, Ganapathysubramanian B, Lubberstedt T (2014) Analysis of Maize (Zea mays L.) seedling roots with the high-throughput image analysis tool ARIA (automatic root image analysis). PLoS ONE 9(9):e108255

    Article  PubMed Central  PubMed  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 15:1795–1806

    Article  PubMed Central  CAS  PubMed  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 101:9885–9890

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Piepho HP, Möhring J, Melchinger AE, Büchse A (2008) BLUP for phenotypic selection in plant breeding and variety testing. Euphytica 161:209–228

    Article  Google Scholar 

  • Pollmer WG, Eberhard D, Klein D, Dhillon BS (1979) Genetic control of nitrogen uptake and translocation in maize. Crop Sci 19:82–86

    Article  CAS  Google Scholar 

  • Presterl T, Seitz G, Schmidt W, Geiger HH (2002) Improving nitrogen-use efficiency in European maize- comparison between line per se and testcross performance under high and low soil nitrogen. Maydica 47:83–91

    Google Scholar 

  • Presterl T, Seitz G, Landbeck M, Thiemt EM, Schmidt W, Geiger HH (2003) Improving nitrogen-use efficiency in European maize: estimation of quantitative genetic parameters. Crop Sci 43:1259–1265

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multi locus genotype data. Genetics 155:945–959

    PubMed Central  CAS  PubMed  Google Scholar 

  • Raun WR, Johnson GV (1999) Improving nitrogen use efficiency for cereal production. Agron J 91:357–363

    Article  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 98:11479–11484

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ribaut JM, Frachebond Y, Monneveux P, Banziger M, Vargas M, Jiang CJ (2007) Quantitative trait loci for yield and correlated traits under high and low soil nitrogen conditions in tropical maize. Mol Breed 20:15–29

    Article  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Ruta N, Liedgens M, Fracheboud Y, Stamp P, Hund A (2009) QTLs for the elongation of axile and lateral roots of maize in response to low water potential. Theor Appl Genet 120:621–631

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Storey JD, Taylor JE, Siegmund D (2004) Strong control, conservative point estimation, and simultaneous conservative consistency of false discovery rates: a unified approach. J R Stat Soc B 66:187–205

    Article  Google Scholar 

  • Stuber CW, Polacco M, Senior ML (1999) Synergy of empirical breeding, marker-assisted selection, and genomics to increase crop yield potential. Crop Sci 39:1571–1583

    Article  Google Scholar 

  • Taramino G, Sauer M, Stauffer J, Multani D, Niu X, Sakai H, Hochholdinger F (2007) The RTCS gene in maize (Zea mays L.) encodes a lob domain protein that is required for postembryonic shoot-borne and embryonic seminal root initiation. Plant J 50:649–659

    Article  CAS  PubMed  Google Scholar 

  • Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289

    Article  CAS  PubMed  Google Scholar 

  • Tian Q, Chen F, Zhang F, Mi G (2005) Possible involvement of cytokinin in nitrate-mediated root growth in maize. Plant Soil 277:185–196

    Article  CAS  Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677

    Article  CAS  PubMed  Google Scholar 

  • Tuberosa R, Salvi S (2007) From QTLs to genes controlling root traits in maize. In: Spiertz JHJ, Struik PC, Van Laar HH (eds) Scale and complexity in plant systems research: gene–plant–crop relations. Springer, Berlin, pp 13–22

    Google Scholar 

  • Tuberosa R, Salvi S, Sanguineti MC, Maccaferri M, Giuliani S, Maccaferri M, Sanguineti MC, Landi P (2003) Searching for quantitative trait loci controlling root traits in maize: a critical appraisal. Plant Soil 255:35–54

    Article  CAS  Google Scholar 

  • von Behrens I, Komatsu M, Zhang Y, Berendzen KW, Niu X, Sakai H, Taramino G, Hochholdinger F (2011) Rootless with undetectable meristem1 encodes a monocot-specific AUX/IAA protein that controls embryonic seminal and postembryonic lateral root initiation in maize. Plant J 66:341–353

    Article  Google Scholar 

  • Wang Y, Mi G, Chen F, Zhang J, Zhang F (2004) Response of root morphology to nitrate supply and its contribution to nitrogen accumulation in maize. J Plant Nutr 27:2189–2202

    Article  CAS  Google Scholar 

  • Wen TJ, Schnable PS (1994) Analyses of mutants of three genes that influence root hair development in Zea mays (Gramineae) suggest that root hairs are dispensable. Am J Bot 81:833–842

    Article  Google Scholar 

  • Wen TJ, Hochholdinger F, Sauer M, Bruce W, Schnable PS (2005) The roothairless1 gene of maize (Zea mays) encodes a homolog of sec3, which is involved in polar exocytosis. Plant Physiol 138:1637–1643

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Woll K, Borsuk L, Stransky H, Nettleton D, Schnable PS, Hochholdinger F (2005) Isolation, characterization and pericycle specific transcriptome analyses of the novel maize (Zea mays L.) lateral and seminal root initiation mutant rum1. Plant Physiol 139:1255–1267

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Worku M, Bänziger M, Erley GSA, Friesen D, Diallo AO, Horst WJ (2007) Nitrogen uptake and utilization in contrasting nitrogen efficient tropical maize hybrids. Crop Sci 47:519

    Article  CAS  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    Article  CAS  PubMed  Google Scholar 

  • Zhang N, Gur A, Gibon Y, Sulpice R, Flint-Garcia S, McMullen MD, Stitt M, Buckler ES (2010) Genetic analysis of central carbon metabolism unveils an amino acid substitution that alters maize NAD-dependent isocitrate dehydrogenase activity. PLoS ONE 5(4):e9991

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhu JM, Kaeppler SM, Lynch JP (2005) Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply. Theor Appl Genet 111:688–695

    Article  CAS  PubMed  Google Scholar 

  • Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was carried out while Dr. Adel Abdel-Ghani was a visiting Fulbright Postdoctoral Fellow and during the sabbatical leave granted from Mu’tah University, Jordon during the academic year 2011–2012 at Iowa State University (ISU), Ames, USA. Dr. Jenaro Reyes-Matamoros contributed in this study while he was on a sabbatical leave at ISU. Authors are very thankful to Guan Yi and Leigh Lihs for their technical assistance. Authors would also like to thank USDA’s National Institute of Food and Agriculture (Project Number: IOW05180) and RF Baker Center for Plant Breeding for funding this work. The authors also thank Ryan Pape, Jeff Schussler, Kanwarpal S. Dhugga and Mark Cooper from DuPont Pioneer for their assistance in carrying this study. Financial assistance from RF Baker Center for Plant Breeding is highly appreciated.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jordon Pace.

Additional information

Adel H. Abdel-Ghani and Bharath Kumar have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 212 kb)

Supplementary material 2 (DOCX 33 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdel-Ghani, A.H., Kumar, B., Pace, J. et al. Association analysis of genes involved in maize (Zea mays L.) root development with seedling and agronomic traits under contrasting nitrogen levels. Plant Mol Biol 88, 133–147 (2015). https://doi.org/10.1007/s11103-015-0314-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-015-0314-1

Keywords

Navigation