Plant and Soil

, Volume 404, Issue 1–2, pp 321–344 | Cite as

Nitrogen-utilization efficiency in rice: an analysis at leaf, shoot, and whole-plant level

Regular Article



If rice has a higher nitrogen use efficiency for dry matter production (NUE) and grain yield (NUEGY) than wild annuals, we may question whether the higher NUE is due to a higher productivity per plant N (NP) or a longer retention time of plant N (MRT) or both, and whether the higher NUEGY results also from a higher harvest index (HI).


Stands of rice were established at three N levels. Censuses were done for birth and death of every shoot and leaf from germination to full maturity. Nitrogen uptake, dry matter production, grain yield, HI, NUE, and NUEGY were determined at shoot and whole-plant levels.


Rice had a higher NUE, NUEGY and NP, but hardly higher plant-N MRT and HI than wild annuals. Leaf-N MRT was higher than leaf longevity in fertile shoots, while the opposite was true in sterile tillers. Shoot NUEGY was higher in late tillers due to higher HI.


High NUE of rice results from its high NP, not from high MRT at both whole-plant and leaf levels. Revenues gained from enhancing MRT would have been lower than the opportunity costs of reducing NP. N recycles between shoots. Sterile tillers function as an N storage for grain yield in fertile shoots.


Grain yield Leaf longevity Mean residence time Nitrogen use efficiency Rice Tiller 



We thank Kouki Hikosaka, Tadahiko Mae, and Amane Makino for discussion and comments on an earlier draft; Toshihiro Hasegawa and Hidemitsu Sakai of the National Institute of Agro-Environmental Sciences for supply of rice seeds and advice on rice cultivation; and Hitomi Yoshida for chemical analysis. We appreciate Niels Anten and an anonymous referee whose comments were useful for improving the manuscript. We are also grateful for the support of the staff members and students of the Laboratory for Agricultural Environmental Studies, Tokyo University of Agriculture. This work was funded by KAKENHI (no. 21114009, 23770027, 25440230) from the Japan Society for the Promotion of Science.

Supplementary material

11104_2016_2832_MOESM1_ESM.pptx (118 kb)
ESM 1 Table S1: Changes in nitrogen concentration of rice plants. Table S2: Number of leaves produced per shoot, and fraction of nitrogen taken up by the shoot that was allocated to leaf in the main stem and tillers. Fig. S1: Grain yield as a function of leaf area duration and leaf N duration in shoots. (PPTX 118 kb)


  1. Abeledo LG, Calderini DF, Slafer GA (2008) Nitrogen economy in old and modern malting barleys. Field Crop Res 106:171–178CrossRefGoogle Scholar
  2. Aerts R, Chapin FS III (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67CrossRefGoogle Scholar
  3. Ao H, Peng S, Zou Y, Tang Q, Visperas RM (2010) Reduction of unproductive tillers did not increase the grain yield of irrigated rice. Field Crop Res 116:108–115CrossRefGoogle Scholar
  4. Barraclough PB, Howarth JR, Jones J, Lopez-Bellido R, Parmar S, Shepherd CE, Hawkesford MJ (2010) Nitrogen efficiency of wheat: genotypic and environmental variation and prospects for improvement. Eur J Agron 33:1–11CrossRefGoogle Scholar
  5. Berendse F, Aerts R (1987) Nitrogen-use-efficiency: a biologically meaningful definition? Funct Ecol 1:293–296Google Scholar
  6. Bingham IJ, Karley AJ, White PJ, Thomas WTB, Russell JR (2012) Analysis of improvements in nitrogen use efficiency associated with 75 years of spring barley breeding. Eur J Agron 42:49–58CrossRefGoogle Scholar
  7. Brancourt-Hulmel M, Doussinault G, Lecomte C, Berard P, Le Buanec B, Trottet M (2003) Genetic improvement of agronomic traits of winter wheat cultivars released in France from 1946 to 1992. Crop Sci 43:37–45CrossRefGoogle Scholar
  8. Cassman KG (1994) Breaking the yield barrier. IRRI, Los BañosGoogle Scholar
  9. Cassman KG, Gines GC, Dizon MA, Samson MI, Alcantara JM (1996) Nitrogen-use efficiency in tropical lowland rice systems: contributions from indigenous and applied nitrogen. Field Crop Res 47:1–12CrossRefGoogle Scholar
  10. Cassman KG, Dobermann A, Walters DT, Yang H (2003) Meeting cereal demand while protecting natural resources and improving environmental quality. Annu Rev Environ Resour 28:315–358CrossRefGoogle Scholar
  11. Chafai-Elalaoui A, Simmons SR, Crookston RK (1988) Effects of tiller removal on spring barley. Crop Sci 28:305–307CrossRefGoogle Scholar
  12. Chafai-Elalaoui A, Simmons SR, Crookston RK (1992) Allocation of photoassimilate by main shoots and nonsurviving tillers in barley. Crop Sci 32:1233–1237CrossRefGoogle Scholar
  13. Chapin FS III, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447CrossRefGoogle Scholar
  14. Cohen D (1971) Maximizing final yield when growth is limited by time or by limiting resources. J Theor Biol 33:299–307CrossRefPubMedGoogle Scholar
  15. Counce PA, Siebenmorgen TJ, Poag MA, Holloway GE, Kocher MF, Lu R (1996) Panicle emergence of tiller types and grain yield of tiller order for direct-seeded rice cultivars. Field Crop Res 47:235–242CrossRefGoogle Scholar
  16. Crawley MJ (2005) Statistics: an introduction using R. Wiley, ChichesterCrossRefGoogle Scholar
  17. de Kroon H, van Groenendael J (1997) The ecology and evolution of clonal plants. Backhuys, LeidenGoogle Scholar
  18. Donald CM (1968) The breeding of crop ideotypes. Euphytica 17:385–403CrossRefGoogle Scholar
  19. Evans GC (1972) The quantitative analysis of plant growth. Blackwell, OxfordGoogle Scholar
  20. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19CrossRefGoogle Scholar
  21. Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. J Exp Bot 60:2235–2248CrossRefPubMedGoogle Scholar
  22. Evans LT (1993) Crop evolution, adaptation and yield. Cambridge Univ Press, CambridgeGoogle Scholar
  23. Evans LT, Fischer RA (1999) Yield potential: its definition, measurement, and significance. Crop Sci 39:1544–1551CrossRefGoogle Scholar
  24. FAO (1998) Fifth external progamme and management review of international rice research institute.
  25. FAO (2015) FAO-STAT Database – agricultural production.
  26. Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge Univ Press, Cambridge, pp 25–55Google Scholar
  27. Hanada K (1993) Tillers. In: Matsuo T, Hoshikawa K (eds) Science of the rice plant. 1. Food and Agriculture Policy Research Center, Tokyo, pp 222–258Google Scholar
  28. Harper JL (1977) Population biology of plants. Academic, LondonGoogle Scholar
  29. Hikosaka K (2004) Interspecific differences in the photosynthesis-nitrogen relationships: patterns, physiological causes and ecological importance. J Plant Res 117:481–494CrossRefPubMedGoogle Scholar
  30. Hirose T (1971) Nitrogen turnover and dry-matter production of a Solidago altissima population. Jpn J Ecol 21:18–32Google Scholar
  31. Hirose T (1975) Relations between turnover rate, resource utility and structure of some plant population: a study in the matter budgets. J Fac Sci Univ Tokyo III 11:355–407Google Scholar
  32. Hirose T (1978) Dry matter production and nitrogen uptake relationships in buckwheat plants. Jpn J Ecol 28:25–34Google Scholar
  33. Hirose T (2011) Nitrogen use efficiency revisited. Oecologia 166:863–867CrossRefPubMedGoogle Scholar
  34. Hirose T (2012) Leaf-level nitrogen use efficiency: definition and importance. Oecologia 169:591–597CrossRefPubMedGoogle Scholar
  35. Hirose T, Monsi M (1975) On a meaning of life form of plants in relation to their nitrogen utilization. In: Takahashi H (ed) Nitrogen fixation and nitrogen cycle (JIBP Synthesis 12). Univ Tokyo Press, Tokyo, pp 87–94Google Scholar
  36. Hirose T, Oikawa S (2012) Mean residence time of leaf number, area, mass, and nitrogen in canopy photosynthesis. Oecologia 169:927–937CrossRefPubMedGoogle Scholar
  37. Hoshikawa K (1989) The growing rice plant: an anatomical monograph. Nobunkyo, Tokyo. ISBN 3540881132Google Scholar
  38. Huang M, Yang C, Ji Q, Jiang L, Tan J, Li Y (2013) Tillering responses of rice to plant density and nitrogen rate in a subtropical environment of southern China. Field Crop Res 149:187–192CrossRefGoogle Scholar
  39. Imaizumi N, Usuda H, Nakamoto H, Ishihara K (1990) Changes in the rate of photosynthesis during grain filling and the enzymatic activities associated with the photosynthetic carbon metabolism in rice panicles. Plant Cell Physiol 31:835–843Google Scholar
  40. Ingestad T (1979) Nitrogen stress in birch seedlings II. N, K, P, Ca, and Mg nutrition. Physiol Plant 45:149–157CrossRefGoogle Scholar
  41. Ishizuka Y, Tanaka A (1963) Studies on the nutrio-physiology of the rice plant. Yokendo, Tokyo. (cited in Murata and Matsushima 1975)Google Scholar
  42. Jaffuel S, Dauzat J (2005) Synchlonism of leaf and tiller emergence relative to position and to main stem development stage in a rice cultivar. Ann Bot 95:401–412CrossRefPubMedGoogle Scholar
  43. Ju C, Buresh RJ, Wang Z, Zhang H, Liu L, Yang J, Zhang J (2015) Root and shoot traits for rice varieties with higher grain yield and higher nitrogen use efficiency at lower nitrogen rates application. Field Crop Res 175:47–55CrossRefGoogle Scholar
  44. King D, Roughgarden J (1983) Energy allocation patterns of the California grassland annuals Plantago erecta and Clarkia rubicunda. Ecology 64:16–27CrossRefGoogle Scholar
  45. Koutroubas SD, Ntanos DA (2003) Genotypic differences for grain yield and nitrogen utilization in Indica and Japonica rice under Mediterranean conditions. Field Crop Res 83:251–260CrossRefGoogle Scholar
  46. Ladha JK, Kirk GJD, Bennett J, Peng S, Reddy CK, Reddy PM, Sing U (1998) Opportunities for increased nitrogen-use efficiency from improved lowland rice germplasm. Field Crop Res 56:41–71CrossRefGoogle Scholar
  47. Ladha JK, Pathak H, Krupnik TJ, Six J, van Kessel C (2005) Efficiency of fertilizer nitrogen in cereal production: retrospects and prospects. Adv Agron 87:85–156CrossRefGoogle Scholar
  48. Li M, Zhang H, Yang X, Ge M, Ma Q, Wei H, Dai Q, Huo Z, Xu K, Luo D (2014) Accumulation and utilization of nitrogen, phosphorus and potassium of irrigated rice cultivars with high productivities and high N use efficiencies. Field Crop Res 161:55–63CrossRefGoogle Scholar
  49. Mae T (1997) Physiological nitrogen efficiency in rice: nitrogen utilization, photosynthesis, and yield potential. Plant Soil 196:201–210CrossRefGoogle Scholar
  50. Mae T (2011) Nitrogen acquisition and its relation to growth and yield in recent high-yielding cultivars of rice (Oryza sativa L.) in Japan. Soil Sci Plant Nutr 57:625–635CrossRefGoogle Scholar
  51. Mae T, Ohira K (1981) The mobilization of nitrogen related to leaf growth and senescence in rice plants (Oryza sativa L.). Plant Cell Physiol 22:1067–1074Google Scholar
  52. Mae T, Inaba A, Kaneta Y, Masaki S, Sasaki M, Aizawa M, Okawa S, Hasegawa S, Makino A (2006) A large-grain rice cultivar, Akita 63, exhibits high yield with high physiological N-use efficiency. Field Crop Res 97:227–237CrossRefGoogle Scholar
  53. Makino A (2011) Photosynthesis, grain yield, and nitrogen utilization in rice and wheat. Plant Physiol 155:125–129CrossRefPubMedGoogle Scholar
  54. Makino A, Mae T, Ohira K (1988) Differences between wheat and rice in the enzymatic properties of ribulose-1,5-bisphosphate carboxylase/oxygenase and the relationship to photosynthetic gas exchange. Planta 174:30–38CrossRefPubMedGoogle Scholar
  55. Makino A, Sakuma H, Sudo E, Mae T (2003) Differences between maize and rice in N-use efficiency for photosynthesis and protein allocation. Plant Cell Physiol 44:952–956CrossRefPubMedGoogle Scholar
  56. Mann CC (1999) Crop scientists seek a new revolution. Science 283:310–314CrossRefGoogle Scholar
  57. Matson PA, Naylor RL, Ortiz-Monasterio I (1998) Integration of environmental, agronomic, and economic aspects of fertilizer management. Science 280:112–115CrossRefPubMedGoogle Scholar
  58. Miller BC, Hill JE, Roberts SR (1991) Plant population effects on growth and yield in water-seeded rice. Agron J 83:291–297CrossRefGoogle Scholar
  59. Moll RH, Kamprath EL, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agron J 74:562–564CrossRefGoogle Scholar
  60. Morishima H (1984) Wild plant and domestication. In: Tsuoda S, Takahashi N (eds) Biology of rice. Jpn Sci Soc Press, Tokyo/Elsevier, pp 3–30CrossRefGoogle Scholar
  61. Murata Y, Matsushima S (1975) Rice. In: Evans LT (ed) Crop physiology: some case histories. Cambridge Univ Press, Cambridge, pp 73–99Google Scholar
  62. Nishimura E, Suzaki E, Irie M, Nagashima H, Hirose T (2010) Architecture and growth of an annual plant Chenopodium album in different light climates. Ecol Res 25:383–393CrossRefGoogle Scholar
  63. Novoa R, Loomis RS (1981) Nitrogen and plant production. Plant Soil 58:177–204CrossRefGoogle Scholar
  64. Ogawa T, Oikawa S, Hirose T (2015) Leaf dynamics in growth and reproduction of Xanthium canadense as influenced by stand density. Ann Bot 116:807–819CrossRefPubMedPubMedCentralGoogle Scholar
  65. Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreased photosynthetic nitrogen use efficiency. Funct Ecol 18:419–425CrossRefGoogle Scholar
  66. Onoda Y, Westoby M, Adler PB, Choong AMF, Colissold FJ, Cornelissen JHC et al (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312CrossRefPubMedGoogle Scholar
  67. Ortiz-Monasterio JI, Sayre KD, Rajaram S, McMahon M (1997) Genetic progress in wheat yield and nitrogen use efficiency under four nitrogen rates. Crop Sci 37:898–904CrossRefGoogle Scholar
  68. Peng S, Buresh RJ, Huang J, Yang J, Zou Y, Zhong X, Wang G, Zhang F (2006) Strategies for overcoming low agronomic nitrogen use efficiency in irrigated rice systems in China. Field Crop Res 96:37–47CrossRefGoogle Scholar
  69. Poorter H (1994) Construction costs and payback time of biomass: a whole plant perspective. In: Roy J, Garnier E (eds) A whole plant perspective on carbon-nitrogen interactions. SPB Acad Pub, The Hague, pp 111–127Google Scholar
  70. R Development Core Team (2010) R: a language and environment for statistical computing. Version 2.11.1. R Foundation for Statistical Computing, Vienna.
  71. Raun WR, Johnson GV (1999) Improving nitrogen use efficiency for cereal production. Agron J 91:357–363CrossRefGoogle Scholar
  72. Samonte SOPB, Wilson LT, Medley JC, Pinson SRM, McClung AM, Lales JS (2006) Nitrogen utilization efficiency: relationships with grain yield, grain protein, and yield-related traits in rice. Agron J 98:168–176CrossRefGoogle Scholar
  73. Shitaka Y, Hirose T (1993) Timing of seed germination and the reproductive effort in Xanthium canadense. Oecologia 95:334–339CrossRefGoogle Scholar
  74. Sinclair TR (1998) Historical changes in harvest index and crop nitrogen accumulation. Crop Sci 38:638–643CrossRefGoogle Scholar
  75. Singh U, Ladha JK, Castillo EG, Punzalan G, Tirol-Padre A, Duqueza M (1998) Genotypic variation in nitrogen use efficiency in medium- and long-duration rice. Field Crop Res 58:35–53CrossRefGoogle Scholar
  76. Skinner RH, Moore KJ (2007) Growth and development of forage plants. Forages, Sci Grassl Agric 2:13–66Google Scholar
  77. Sparkes DL, Holme SJ, Gaju O (2006) Does light quality initiate tiller death in wheat? Eur J Agron 24:212–217CrossRefGoogle Scholar
  78. Spiertz JHJ (2010) Nitrogen, sustainable agriculture and food security: a review. Agron Sustain Dev 30:43–55CrossRefGoogle Scholar
  79. Sprugel DG, Hinckley TM, Schaap W (1991) The theory and practice of branch autonomy. Annu Rev Ecol Syst 22:309–334CrossRefGoogle Scholar
  80. Sugiyama H, Hirose T (1991) Growth schedule of Xanthium canadense: does it optimize the timing of reproduction? Oecologia 88:55–60CrossRefGoogle Scholar
  81. Sui B, Feng X, Tian G, Hu X, Shen Q, Guo S (2013) Optimizing nitrogen supply increases rice yield and nitrogen use efficiency by regulating yield formation factors. Field Crop Res 150:99–107CrossRefGoogle Scholar
  82. Takai T, Matsuura S, Nishio T, Ohsumi A, Shiraiwa T, Horie T (2006) Rice yield potential is closely related to crop growth rate during late reproductive period. Field Crop Res 96:328–335CrossRefGoogle Scholar
  83. Thorne GN (1965) Physiological aspects of grain yield in cereals. In: Milthorpe FL, Ivins JD (eds) The growth of cereals and grasses. Butterworths, London, pp 88–105Google Scholar
  84. Thorne GN, Wood DW (1987) The fate of carbon in dying tillers of winter wheat. J Agric Sci 108:515–522CrossRefGoogle Scholar
  85. Vitousek PM (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119:553–572CrossRefGoogle Scholar
  86. Wang YC, Hanada K (1982) Translocation of 14C-assimilate among main stem and tillers in rice plants. Jpn J Crop Sci 51:483–491 (in Japanese with English abstract)CrossRefGoogle Scholar
  87. Watari R, Nagashima H, Hirose T (2012) Growth and nitrogen use in Xanthium canadense grown in an open or in a dense stand. Physiol Plant 144:335–345CrossRefPubMedGoogle Scholar
  88. Wright IJ, Reich PB, Cornelissen HC, Falster DS, Garnier E, Hikosaka K, Lamont BB et al (2005) Assessing the generality of global leaf trait relationships. New Phytol 166:485–496CrossRefPubMedGoogle Scholar
  89. Wu G, Wilson LT, McClung AM (1998) Contribution of rice tillers to dry matter accumulation and yield. Agron J 90:317–323CrossRefGoogle Scholar
  90. Yagi H (2010) All about agriculture (in Japanese). Natsume Co, TokyoGoogle Scholar
  91. Yan J, Yu J, Tao GC, Vos J, Bouman BAM, Xie GH, Meinke H (2010) Yield formation and tillering dynamics of direct-seeded rice in flooded and nonflooded soils in the Huai River Basin of China. Field Crop Res 116:252–259CrossRefGoogle Scholar
  92. Ying J, Peng S, He Q, Yang H, Yang C, Visperas RM, Cassman KG (1998a) Comparison of high-yield rice in tropical and subtropical environments. I. Determination of grain and dry matter yields. Field Crop Res 57:71–84CrossRefGoogle Scholar
  93. Ying J, Peng S, Yang G, Zhou N, Visperas RM, Cassman KG (1998b) Comparison of high-yield rice in tropical and subtropical environments. I. Nitrogen accumulation and utilization efficiency. Field Crop Res 57:85–93CrossRefGoogle Scholar
  94. Yoshida S (1972) Physiological aspects of grain yield. Annu Rev Plant Physiol 23:437–464CrossRefGoogle Scholar
  95. Yoshida S (1981) Fundamentals of rice crop science. IRRI, Los BañosGoogle Scholar
  96. Zhong X, Peng S, Sanico AL, Liu H (2003) Quantifying the interactive effect of leaf nitrogen and leaf area on tillering of rice. J Plant Nutr 26:1203–1222CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Takahiro Ogawa
    • 1
  • Shimpei Oikawa
    • 1
    • 2
  • Tadaki Hirose
    • 1
    • 3
  1. 1.Department of International Agricultural DevelopmentTokyo University of AgricultureTokyoJapan
  2. 2.Department of BiologyIbaraki UniversityMitoJapan
  3. 3.Graduate School of Life SciencesTohoku UniversitySendaiJapan

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