Plant and Soil

, Volume 375, Issue 1–2, pp 303–315 | Cite as

N- and P-mediated seminal root elongation response in rice seedlings

  • Satoshi Ogawa
  • Michael Gomez Selvaraj
  • Angela Joseph Fernando
  • Mathias Lorieux
  • Manabu Ishitani
  • Susan McCouch
  • Juan David Arbelaez
Regular Article



In rice, seminal root elongation plays an important role in acquisition of nutrients such as N and P, but the extent to which different N forms and P concentrations affect root growth is poorly understood. This study aimed to examine N- and P-mediated seminal root elongation response and to identify putative QTLs associated with seminal root elongation.


Seminal root elongation was evaluated in 15 diverse wild and cultivated accessions of rice, along with 48 chromosome segment substitution lines (CSSLs) derived from a cross between the rice variety ‘Curinga’ and Oryza rufipogon (IRGC 105491). Root elongation in response to different forms of N (NH4 +, NO3 and NH4NO3) and concentrations of P was evaluated under hydroponic conditions, and associated putative QTL regions were identified.


The CSSL parents had contrasting root responses to N and P. Root elongation in O. rufipogon was insensitive to N source and concentration, whereas Curinga was responsive. In contrast to N, seminal root elongation and P concentration was positively correlated. Three putative QTLs for seminal root elongation in response to N were detected on chromosome 1, and one QTL on chromosome 3 was associated with low P concentration.


Genetic variation in seminal root elongation and plasticity of nutrient response may be appropriate targets for marker-assisted selection to improve rice nutrient acquisition efficiency.


Chromosome segment substitution lines NH4+ response N acquisition Seminal root elongation 



Chromosome segment substitution line




Nitrogen acquisition efficiency




Partial nitrate nutrition


Phosphorus acquisition efficiency


Quantitative trait locus


Single nucleotide polymorphism


Simple sequence repeat



We thank Dr. Edgar Torres (CIAT, Colombia) and Dr. Uga Y (National Institute of Agrobiological Sciences, Japan) for providing the seed materials used this study, and Dr. Joe Tohme, CIAT Agrobiodiversity Research Area Director, for his continuous support. We also thank Dr. T. Ramasubramanian (Sugarcane Breeding Institute, Indian Council of Agricultural Research, Tamil Nadu, India) for his critical evaluation of the manuscript, and are grateful for the assistance of Lucia Chavez and Milton Valencia.

This work was supported by Ministry of foreign Affairs of Japan.

Supplementary material

11104_2013_1955_MOESM1_ESM.pdf (376 kb)
ESM 1 (PDF 375 kb)


  1. Abdul Rahman Z, Musa MH (2009) Upland rice root characteristics and their relationship to nitrogen uptake. Pertanika J Trop Agric Sci 32:261–266Google Scholar
  2. Balkos KD, Britto DT, Kronzucker HJ (2010) Optimization of ammonium acquisition and metabolism by potassium in rice (Oryza sativa L. cv. IR-72). Plant Cell Environ 33:23–34PubMedGoogle Scholar
  3. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538CrossRefGoogle Scholar
  4. Bloom AJ, Frensch J, Taylor AR (2006) Influence of inorganic nitrogen and pH on the elongation of maize seminal roots. Ann Bot 97:867–873PubMedCrossRefGoogle Scholar
  5. Brar DS, Khush GS (1997) Alien introgression in rice. Plant Mol Biol 35:35–47PubMedCrossRefGoogle Scholar
  6. Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–584CrossRefGoogle Scholar
  7. Champoux MC, Wang G, Sarkarung S, Mackill DJ, O’Toole JC, Huang N, McCouch SR (1995) Locating genes associated with root morphology and drought avoidance in rice via linkage to molecular markers. Theor Appl Genet 90:969–981PubMedCrossRefGoogle Scholar
  8. Chen G, Guo S, Kronzucker HJ, Shi W (2013) Nitrogen use efficiency (NUE) in rice links to NH4 + toxicity and futile NH4 + cycling in roots. Plant Soil 369:351–363CrossRefGoogle Scholar
  9. Chin JH, Lu X, Haefele SM, Gamuyao R, Ismail A, Wissuwa M, Heuer S (2010) Development and application of gene-based markers for the major rice QTL Phosphorus uptake 1. Theor Appl Genet 120:1073–1086PubMedCrossRefGoogle Scholar
  10. Da Silva AA, Delatorre CA (2009) Alterações na arquitetura de raiz em resposta à disponibilidade de fósforo e nitrogênio. Rev Ciênc Agrov 8:152–163Google Scholar
  11. De la Torre F, De Santis L, Suárez MF, Crespillo R, Canovás FM (2006) Identification and functional analysis of a prokaryotic-type aspartate aminotransferase: implications for plant amino acid metabolism. Plant J 46:414–425PubMedCrossRefGoogle Scholar
  12. Duan YH, Zhang YL, Shen QR, Wang SW (2006) Nitrate effect on rice growth and nitrogen absorption and assimilation at different growth stages. Pedosphere 16:707–717CrossRefGoogle Scholar
  13. Falkengren-Grerup U (1995) Interspecies differences in the preference of ammonium and nitrate in vascular plants. Oecologia 102:305–311CrossRefGoogle Scholar
  14. Famoso AN, Clark RT, Shaff JE, Craft E, McCouch SR, Kochian LV (2010) Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal aluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol 153:1678–1691PubMedCentralPubMedCrossRefGoogle Scholar
  15. Fu Q, Zhang P, Tan L, Zhu Z, Ma D, Fu Y, Zhan X, Cai H, Sun C (2010) Analysis of QTLs for yield-related traits in Yuanjiang common wild rice (Oryza rufipogon Griff.). J Genet Genome 37:147–157CrossRefGoogle Scholar
  16. Gastal F, Lemaire G (2002) N uptake and distribution in crops: an agronomical and ecophysiological perspective. J Exp Bot 53:789–799PubMedCrossRefGoogle Scholar
  17. Gerendas J, Zhu Z, Bendixen R, Ratcliffe RG, Sattelmacher B (1997) Physiological and biochemical processes related to ammonium toxicity in higher plants. J Plant Nutr Soil Sci 160:239–251Google Scholar
  18. Hamada A, Nitta M, Nasuda S, Kato K, Fujita M, Matsunaka H, Okumoto Y (2011) Novel QTLs for growth angle of seminal roots in wheat (Triticum aestivum L.). Plant Soil 354:395–405CrossRefGoogle Scholar
  19. Imai I, Kimball JA, Conway B, Yeater KM, McCouch S, McClung A (2013) Validation of yield-enhancing QTLs from a low-yielding wild ancestor of rice. Mol Breed 32:101120CrossRefGoogle Scholar
  20. Jones MP, Dingkuhn M, Aluko GK, Semon M (1997) Interspecific Oryza sativa L. × O. glaberrima Steud. progenies in upland rice improvement. Euphytica 92:237–246CrossRefGoogle Scholar
  21. Kirk GJD, Du LV (1997) Changes in rice root architecture, porosity, and oxygen and proton release under phosphorus deficiency. New Phytol 135:191–200CrossRefGoogle Scholar
  22. Kronzucker HJ, Siddiqi MY, Glass ADM, Kirk GJD (1999) Nitrate–ammonium synergism in rice: a subcellular flux analysis. Plant Physiol 119:1041–1045PubMedCentralPubMedCrossRefGoogle Scholar
  23. Lian X, Xing Y, Yan H, Xu C, Li X, Zhang Q (2005) QTLs for low nitrogen tolerance at seedling stage identified using a recombinant inbred line population derived from an elite rice hybrid. Theor Appl Genet 112:85–96PubMedCrossRefGoogle Scholar
  24. Linkohr BI, Williamson LC, Fitter AH, Leyser HMO (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760PubMedCrossRefGoogle Scholar
  25. Lorieux M (2005) CSSL finder: a free program for managing introgression lines.
  26. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, LondonGoogle Scholar
  27. Nguyen TV, Pham LN, Nguyen HT (2002) Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, Oryza rufipogon Griff., into indica rice (Oryza sativa L.). Theor Appl Genet 106:583–593PubMedGoogle Scholar
  28. Obara M, Tamura W, Ebitani T, Yano M, Sato T, Yamaya T (2010) Fine-mapping of qRL6.1, a major QTL for root length of rice seedlings grown under a wide range of NH4 + concentrations in hydroponic conditions. Theor Appl Genet 121:535–547PubMedCentralPubMedCrossRefGoogle Scholar
  29. Obara M, Takeda T, Hayakawa T, Yamaya T (2011) Mapping quantitative trait loci controlling root length in rice seedlings grown with low or sufficient supply using backcross recombinant lines derived from a cross between Oryza sativa L. and Oryza glaberrima Steud. Soil Sci Plant Nutr 57:80–92CrossRefGoogle Scholar
  30. Price AH, Tomos AD (1997) Genetic dissection of root growth in rice (Oryza sativa L.) II: mapping quantitative trait loci using molecular markers. Theor Appl Genet 95:143–152CrossRefGoogle Scholar
  31. Price AH, Tomos AD, Virk DS (1997) Genetic dissection of root growth in rice (Oryza sativa L.) I: a hydrophonic screen. Theor Appl Genet 95:132–142CrossRefGoogle Scholar
  32. Rauh BL, Basten C, Buckler ES IV (2002) Quantitative trait loci analysis of growth response to varying nitrogen sources in Arabidopsis thaliana. Theor Appl Genet 104:743–750PubMedCrossRefGoogle Scholar
  33. Redoña ED, Mackill DJ (1996) Mapping quantitative trait loci for seedling vigor in rice using RFLPs. Theor Appl Genet 92:395–402PubMedCrossRefGoogle Scholar
  34. Roosta HR, Schjoerring JK (2008) Root carbon enrichment alleviates ammonium toxicity in cucumber plants. J Plant Nutr 31:941–958CrossRefGoogle Scholar
  35. Rorison IH (1985) Nitrogen source and the tolerance of Deschampsia flexuosa, Holcus lanatus and Bromus erectus to aluminium during seedling growth. J Ecol 73:83–90CrossRefGoogle Scholar
  36. Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and unicellular algae. Genes Dev 15:2122–2133PubMedCrossRefGoogle Scholar
  37. Sakai T, Duque MC, Cabrera FA, Martínez PC, Ishitani M (2010) Establishment of drought screening protocols for rice under field conditions. Acta Agron 59:338–346Google Scholar
  38. Shimizu A, Yanagihara S, Kawasaki S, Ikehashi H (2004) Phosphorus deficiency-induced root elongation and its QTL in rice (Oryza sativa L.). Theor Appl Genet 109:1361–1368PubMedCrossRefGoogle Scholar
  39. Song J, Yamamoto K, Shomura A, Yano M, Minobe Y, Sasaki T (1996) Characterization and mapping of cDNA encoding aspartate aminotransferase in rice, Oryza sativa L. DNA Res 3:303–310PubMedCrossRefGoogle Scholar
  40. Song W, Makeen K, Wang D, Zhang C, Xu Y, Zhao H, Tu E, Zhang Y, Shen Q, Xu G (2011) Nitrate supply affects root growth differentially in two rice cultivars differing in nitrogen use efficiency. Plant Soil 343:357–368CrossRefGoogle Scholar
  41. Subbarao GV, Ishikawa T, Ito OA, Nakahara K, Wang HY, Berry WL (2006) A bioluminescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola. Plant Soil 288:101–112CrossRefGoogle Scholar
  42. Suenaga A, Moriya K, Sonoda Y, Ikeda A, Von Wiren N, Hayakawa T, Yamaguchi J, Yamaya T (2003) Constitutive expression of a novel-type ammonium transporter OsAMT2 in rice plants. Plant Cell Physiol 44:206–211PubMedCrossRefGoogle Scholar
  43. Tanaka S, Yamauchi A, Kono Y (1993) Response of the seminal root elongation to NH4 + nitrogen in several rice (Oryza sativa) cultivars. Jpn J Crop Sci 62:288–293CrossRefGoogle Scholar
  44. Thomson MJ, Tai TH, McClung AM, Lai XH, Hinga ME, Lobos KB, Xu Y, Martinez CP, McCouch SR (2003) Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theor Appl Genet 107:479–493PubMedCrossRefGoogle Scholar
  45. Thomson MJ, Zhao K, Wright M, McNally KL, Rey J, Tung CW, Reynolds A, Scheffler B, Eizeng G, McClung A, Kim H, Ismail AM, Ocampo M, Mojica C, Reveche MY, Dilla-Ermita JC, Mauleon R, Leung H, Bustamante C, McCouch S (2012) High-throughput single nucleotide polymorphism genotyping for breeding applications in rice using the BeadXpress platform. Mol Breed 29:875–886CrossRefGoogle Scholar
  46. Tuberosa R, Sanguineti MC, Landi P, Giuliani MM, Salvi S, Conti S (2002) Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Mol Biol 48:697–712PubMedCrossRefGoogle Scholar
  47. Vinod KK, Heuer S (2012) Approaches towards nitrogen- and phosphorus-efficient rice. AoB Plants. doi: 10.1093/aobpla/pls028 Google Scholar
  48. Wang MY, Siddeqi MY, Ruth TJ, Glass ADM (1993) Ammonium uptake by rice roots. I. Kinetics of 13NH4 + influx across the plasmalemma. Plant Physiol 103:1259–1267PubMedCentralPubMedCrossRefGoogle Scholar
  49. Williamson LC, Ribrioux SP, Fitter AH, Leyser HM (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882PubMedCentralPubMedCrossRefGoogle Scholar
  50. Wissuwa M, Yano M, Ae N (1998) Mapping of QTLs for phosphorus-deficiency tolerance in rice (Oryza sativa L.). Theor Appl Genet 97:777–783CrossRefGoogle Scholar
  51. Wojciechowski T, Gooding MJ, Ramsay L, Gregory PJ (2009) The effects of dwarfing genes on seedling root growth of wheat. J Exp Bot 60:2565–2573PubMedCrossRefGoogle Scholar
  52. Wu P, Liao CY, Hu B, Yi KK, Jin WZ, Ni JJ, He C (2000) QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor Appl Genet 100:1295–1303CrossRefGoogle Scholar
  53. Xu CG, Li XQ, Xue Y, Huang YW, Gao J, Xing YZ (2004) Comparison of quantitative trait loci controlling seedling characteristics at two seedling stages using rice recombinant inbred lines. Theor Appl Genet 109:640–647PubMedGoogle Scholar
  54. Yadav R, Courtois B, Huang N, McLaren G (1997) Mapping genes controlling root morphology and root distribution in a doubled-haploid population of rice. Theor Appl Genet 94:619–632CrossRefGoogle Scholar
  55. Yeo ME, Yeo AR, Flowers TJ (1994) Photosynthesis and photorespiration in the genus Oryza. J Exp Bot 45:553–560CrossRefGoogle Scholar
  56. Zhang H, Rong H, Pilbeam D (2007) Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. J Exp Bot 58:2329–2338PubMedCrossRefGoogle Scholar
  57. Zhao XQ, Guo SW, Shinmachi F, Sunairi M, Noguchi A, Hasegawa I, Shen RF (2012) Aluminium tolerance in rice is antagonistic with nitrate preference and synergistic with ammonium preference. Ann Bot 111:69–77PubMedCrossRefGoogle Scholar
  58. Zhu J, Mickelson SM, Kaeppler SM, Lynch JP (2006) Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels. Theor Appl Genet 113:1–10PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Satoshi Ogawa
    • 1
    • 2
  • Michael Gomez Selvaraj
    • 1
  • Angela Joseph Fernando
    • 1
  • Mathias Lorieux
    • 1
    • 3
  • Manabu Ishitani
    • 1
  • Susan McCouch
    • 4
  • Juan David Arbelaez
    • 4
  1. 1.International Center for Tropical Agriculture (CIAT)CaliColombia
  2. 2.Department of Global Agriculture Science, Graduate School of Agriculture and Life ScienceThe University of TokyoTokyoJapan
  3. 3.Institut de Recherche pour le Développement (IRD), DIADE Research UnitMontpellierFrance
  4. 4.Department of Plant Breeding and GeneticsCornell UniversityIthacaUSA

Personalised recommendations