Korean Journal of Breeding Science (한국육종학회지)

The Korean Society of Breeding Science (한국육종학회)
권호 표지

Improvement of Nitrogen Use Efficiency for Sustainable and Productive Agriculture

지속 가능한 농업생산성 증대를 위한 질소 이용 효율 향상

  • Chang, Ancheol (Department of Agricultural Biotechnology, National Academy of Agricultural Science & Technology, Rural Development Administration) ;
  • Choi, Ji-Young (Technology Cooperation Bureau, Rural Development Administration) ;
  • Park, Soon-Ki (Division of Plant Biosciences, Kyungpook National University) ;
  • Kim, Dong-Hern (Department of Agricultural Biotechnology, National Academy of Agricultural Science & Technology, Rural Development Administration) ;
  • Bae, Shin-Chul (Department of Agricultural Biotechnology, National Academy of Agricultural Science & Technology, Rural Development Administration)
  • 장안철 (농촌진흥청 국립농업과학원 농업생명자원부) ;
  • 최지영 (농촌진흥청 기술협력국) ;
  • 박순기 (경북대학교 농생대 응용생명과학부) ;
  • 김동헌 (농촌진흥청 국립농업과학원 농업생명자원부) ;
  • 배신철 (농촌진흥청 국립농업과학원 농업생명자원부)
  • Received : 2011.12.15
  • Accepted : 2011.12.20
  • Published : 2011.12.30
⟨ Previous Next ⟩

Abstract

Agriculture plays a vital role in the sustenance of human society and is the fundamental of developing economies. Nitrogen is one of the most critical inputs that define crop productivity. To ensure better value for investment as well as to minimize the adverse impacts of the accumulative nitrogen species in environment, improving nitrogen use efficiency of crop plants is of key importance. Efforts have been made to study the genetic and molecular biological basis as well as the biochemical mechanisms involved in nitrogen uptake, assimilation, translocation and remobilization in crops and model plants. This review gives an overview of metabolic, enzymatic, genetic and biotechnological aspects of nitrogen uptake, assimilation, remobilization and regulation. This review presents the complexity of nitrogen use efficiency and the need for an integrated approach combining physiology, quantitative trait genetics, system biology, soil science, ecophysiology and biotechnological interventions to improve nitrogen use efficiency.

Keywords

Acknowledgement

Supported by : 국립농업과학원

References

  1. Almagro A, Lin S, Tsay Y. 2008. Characterization of the Arabidopsis nitrate transporter NRT1.6 reveals a role of nitrate in early embryo development. The Plant Cell. 20:3289-3299. https://doi.org/10.1105/tpc.107.056788
  2. Ameziane R, Bernhard K, Lightfoot D. 2000. Expression of the bacterial gdhA gene encoding a NADPH glutamate dehydrogenase in tobacco affects plant growth and development. Plant Soil. 221:47-57. https://doi.org/10.1023/A:1004794000267
  3. Asano T, Wakayama M, Aoki N, Komatsu S, Ichikawa H, Hirochika H, Ohsugi R. 2010. Overexpression of a calcium-dependent protein kinase gene enhances growth of rice under low-nitrogen conditions. Plant Biotechnology. 27:369-373. https://doi.org/10.5511/plantbiotechnology.27.369
  4. Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J. 2007. A central integrator of transcription networks in plant stress and energy signalling. Nature. 448:938-942. https://doi.org/10.1038/nature06069
  5. Bernard SM, Habash DZ. 2009. The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytologist. 182:608-620. https://doi.org/10.1111/j.1469-8137.2009.02823.x
  6. Bi YM, Kant S, Clarke J, Gidda S, Ming F, Xu J, Rochon A, Shelp BJ, Hao L, Zhao R, Mullen RT, Zhu T, Rothstein SJ. 2009. Increased nitrogen-use efficiency in transgenic rice plants over-sxpressing anitrogen-responsive early nodulin gene identified from rice expression profiling. Plant, Cell & Environment. 32:1749-60. https://doi.org/10.1111/j.1365-3040.2009.02032.x
  7. Brears T, Liu C, Knight TJ, Coruzzi GM. 1993. Ectopic overexpression of asparagine synthetase in transgenic tobacco. Plant Physiol. 103:1285-1290.
  8. Buchanan-Wollaston V, Earl S, Harrison E, et al. 2003. The molecular analysis of leaf senescence a genomics approach. Plant Biotechnology Journal. 1:3-22.
  9. Cai H, Zhou Y, Xiao J, Li X, Zhang Q, Lian X. 2009. Overexpressed glutamine synthetase gene modifies nitrogen metabolism and abiotic stress responses in rice. Plant Cell Rep. 28:527-537. https://doi.org/10.1007/s00299-008-0665-z
  10. Castaings L, Camargo A, Pocholle D, et al. 2009. The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. The Plant Journal. 57: 426-435. https://doi.org/10.1111/j.1365-313X.2008.03695.x
  11. Chiu CC, Lin CS, Hsia AP, Su RC, Lin HL, Tsay YF. 2004. Mutation of a nitrate transporter, AtNRT1:4, results in a reduced petiole nitrate content and altered leaf development. Plant and Cell Physiology. 45:1139-1148. https://doi.org/10.1093/pcp/pch143
  12. Chopin F, Orsel M, Dorbe MF, et al. 2007. The Arabidopsis ATNRT2.7 nitrate transporter controls nitrate content in seeds. The Plant Cell. 19:1590-1602. https://doi.org/10.1105/tpc.107.050542
  13. Crete P, Caboche M, Meyer C. 1997. Nitrite reductase expression is regulated at the post-transcriptional level by the nitrogen source in Nicotiana plumbaginifolia and Arabidopsis thaliana, Plant J. 11:625-634. https://doi.org/10.1046/j.1365-313X.1997.11040625.x
  14. Curtis IS, Power JB, de Llat AAM. 1999. Expression of chimeric nitrate reductase gene in transgenic lettuce reduces nitrate in leaves. Plant Cell Rep. 18:889-896. https://doi.org/10.1007/s002990050680
  15. Das SK, Pathak RR, Choudhury D, Raghuram N. 2007. Genomewide computational analysis of nitrate response elements in rice and Arabidopis. Molecular Genetics and Genomics. 278:519-525. https://doi.org/10.1007/s00438-007-0268-3
  16. Diaz C, Lemaismlrnre smlrtre T, Christ C, et al. 2008. Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiology. 147:1437-1449. https://doi.org/10.1104/pp.108.119040
  17. Djannane S, Chauvin JE, Meyer, C. 2002. Glasshouse behaviour of eight transgenic potato clones with a modified nitrate reductase expression under two fertilization regimes. J. Exp. Bot. 53:1037-1045. https://doi.org/10.1093/jexbot/53.371.1037
  18. Ferrario-Mery S, Valadier MH, Foyer C. 1998. Overexpression of nitrate reductase in tobacco delays droughtinduced decreases in nitrate reductase activity and mRNA. Plant Physiol. 117:293-302. https://doi.org/10.1104/pp.117.1.293
  19. Ferrario-Mery S, Valadier MH, Godefroy N, Miallier D, Hirel B, Foyer CH, Suzuki A. 2002. Diurnal changes in ammonia assimilation in transformed tobacco plants expressing ferredoxin-dependent glutamate synthase mRNA in the antisense orientation. Plant Sci. 163:59-67. https://doi.org/10.1016/S0168-9452(02)00058-4
  20. Filleur S, Dorbe M, Cerezo M, et al. 2001. An arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake. FEBS Letters. 489:220-224. https://doi.org/10.1016/S0014-5793(01)02096-8
  21. Fraisier V, Gojon A, Tillard P, Daniel-Vedele F. 2000. Constitutive expression of a putative high affinity nitrate transporter in Nicotiana plumbaginifolia: evidence for a post transcriptional regulation by a reduced nitrogen source. The Plant Journal. 23:489-496. https://doi.org/10.1046/j.1365-313x.2000.00813.x
  22. Fuentes SI, Allen DJ, Ortiz-Lopez A, Hernandez G. 2001. Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. J. Exp. Bot. 52:1071-1081. https://doi.org/10.1093/jexbot/52.358.1071
  23. Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wiren N. 1999. Three functional transporters for constitutive, diurnally regulated, and starvation induced uptake of ammonium into Arabidopsis roots. The Plant Cell. 11:937-947.
  24. Good AG, Johnson SJ, De Pauw M. 2007. Engineering nitrogen use efficiency with alanine aminotransferase. Canadian Journal of Botany. 85:252-262. https://doi.org/10.1139/B07-019
  25. Good AG, Shrawat AK, Muench DG. 2004. Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends in Plant Science. 9:597-605. https://doi.org/10.1016/j.tplants.2004.10.008
  26. Guo Y, Cai Z, Gan S. 2004. Transcriptome of Arabidopsis leaf senescence. Plant Cell and Environment. 27:521-549. https://doi.org/10.1111/j.1365-3040.2003.01158.x
  27. Habash DZ, Massiah AJ, Rong HL, Wallsgrove RM, Leigh RA. 2001. The role of cytosolic glutamine synthetase in wheat. Ann. Appl. Biol. 138:83-89. https://doi.org/10.1111/j.1744-7348.2001.tb00087.x
  28. Herrera-Rodriguez MB, Maldonado JM, Perez-Vicente R. 2006. Role of asparagine and asparagine synthetase genes in sunflower (Helianthus annuus) germination and natural senescence. Journal of Plant Physiology. 163:1061-1070. https://doi.org/10.1016/j.jplph.2005.10.012
  29. 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. Journal of Experimental Botany. 58:2369-2387. https://doi.org/10.1093/jxb/erm097
  30. Hirner A, Ladwig F, Stransky H, et al. 2006. Arabidopsis LHT1 is a highaffinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. The Plant Cell. 18:1931-1946. https://doi.org/10.1105/tpc.106.041012
  31. Ho C, Lin S, Hu H, Tsay Y. 2009. CHL1 functions as a nitrate sensor in plants. Cell. 18:1184-1194.
  32. Hoshida H, Tanaka Y, Hibino T, et al. 2000. Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Molecular Biology. 43:103-111. https://doi.org/10.1023/A:1006408712416
  33. Hoque MS, Masle J, Udvardi MK, Ryan PR, Upadhyaya NM. 2006. Over-expression of the rice OsAMT1-1 gene increases ammonium uptake and content, but impairs growth and development of plants under high ammoniun nutrition. Functional Plant Biology. 33:153-163. https://doi.org/10.1071/FP05165
  34. Hu HC, Wang YY, Tsay YF. 2009. AtCIPK8, a CBLinteracting protein kinase, regulates the low-affinity phase of the primary nitrate response. The Plant Journal. 57: 264-278. https://doi.org/10.1111/j.1365-313X.2008.03685.x
  35. Huang NC, Liu KH, Lo HJ, Tsay YF. 1999. Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. The Plant Cell. 11:1381-1392.
  36. Ishiyama K, Inoue E, Watanabe-Takahashi A, Obara M, Yamaya T, Takahashi H. 2004. Kinetic properties and ammonium-dependent regulation of cytosolic isoenzymes of glutamine synthetase in Arabidopsis. The Journal of Biological Chemistry. 279:16598-16605. https://doi.org/10.1074/jbc.M313710200
  37. Kichey T, Hirel B, Heumez E, Dubois F, Le Gouis J. 2007. In winter wheat (Triticum aestivum L.), post-anthesis nitrogen uptake and remobilization to the grain correlates with agronomic traits and nitrogen physiological markers. Field Crop Research. 102:22-32. https://doi.org/10.1016/j.fcr.2007.01.002
  38. Kisaka H, Kida T, Miwa T. 2007. Transgenic tomato plants that overexpress a gene for NADH-dependent glutamate dehydrogenase (legdh1). Breed. Sci. 57:101-106. https://doi.org/10.1270/jsbbs.57.101
  39. Kozaki A, Takeba G. 1996. Photorespiration protects C3 plants from photooxidation. Nature. 384:557-560. https://doi.org/10.1038/384557a0
  40. Lam HM, Wong P, Chan HK, et al. 2003. Overexpression of the ASN1 gene enhances nitrogen status in seeds of Arabidopsis. Plant Physiology. 132:926-935. https://doi.org/10.1104/pp.103.020123
  41. Lea PJ, Forde BG. 1994. The use of mutants and transgenic plants to study amino acid metabolism Plant, Cell & Environment. 17:541-556. https://doi.org/10.1111/j.1365-3040.1994.tb00148.x
  42. Lightfoot DA. 2009. Genes for improving nitrate use efficiency in crops. p.167-184. In Jenks M.A. and Woods A.J. (ed.) Genes for Plant Abiotic Stress. Wiley-Blackwell , Ames, IA.
  43. Lillo C. 2008. Signalling cascades integrating light-enhanced nitrate metabolism. Biochemical Journal. 415:11-19. https://doi.org/10.1042/BJ20081115
  44. Lin SH, Kuo HF, Canivenc G, et al. 2008. Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. The Plant Cell. 20:2514-2528. https://doi.org/10.1105/tpc.108.060244
  45. Limami MA, et al. 1999. Does root glutamine synthetase control plant biomass production in Lotus japonicus L.? Planta. 209:495-502. https://doi.org/10.1007/s004250050753
  46. Liu KH, Huang CY, Tsay YF. 1999. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell. 11:865-874.
  47. Mae T, Makino A, Ohira K. 1983. Changes in the amounts of ribulose biphosphate carboxylase synthesized and degraded during the life span of rice leaf (Oryza sativa L.). Plant and Cell Physiology. 24:10791086.
  48. Martin A, Belastegui-Macadam X, QuillereI, et al. 2005. Nitrogen management and senescence in two maize hybrids differing in the persistence of leaf greenness: agronomic, physiological and molecular aspects. New Phytologist. 167:483-492. https://doi.org/10.1111/j.1469-8137.2005.01430.x
  49. Martin A, Lee J, Kichey T, et al. 2006. Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. The Plant Cell. 18:3252-3274. https://doi.org/10.1105/tpc.106.042689
  50. Masclaux C, Quillere' I, Gallais A, Hirel B. 2001. The challenge of remobilization in plant nitrogen economy. A survey of physio-agronomic and molecular approaches. Annals of Applied Biology. 138:68-81.
  51. Masclaux-Daubresse C, Carrayol E, Valadier M-H. 2005. The two nitrogen mobilisation- and senescence-associated GS1 and GDH genes are controlled by C and N metabolites. Planta. 221:580-588. https://doi.org/10.1007/s00425-004-1468-2
  52. Masclaux-Daubresse C, Reisdorf-Cren M, Orsel M. 2008. Leaf nitrogen remobilisation for plant development and grain filling. Plant Biology. 10:23-36.
  53. Meyer C, Stitt M. 2001. Nitrate reductase and signalling. p. 37-59. In Lea PJ, Morot-Gaudry J-F (ed.) Plant nitrogen. Springer, New York.
  54. Migge A, Carrayol E, Hirel B, Becker TW. 2000. Leaf specific overexpression of plastidic glutamine synthetase stimulates the growth of transgenic tobacco seedlings. Planta. 2:252-260.
  55. Mungur R, Glass ADM, Goodenow DB, Lightfoot DA. 2005. Metabolite fingerprinting in transgenic Nicotiana tabacum altered by the Escherichia coli glutamate dehydrogenase gene. J. Biomed. Biotechnol. 2:198-214.
  56. Na"sholm T, Kielland K, Ganeteg U. 2009. Uptake of organic nitrogen by plants. New Phytologist. 182:31-48. https://doi.org/10.1111/j.1469-8137.2008.02751.x
  57. Obara M, Kajiura M, Fukuta Y, et al. 2001. Mapping of QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.). Journal of Experimental Botany. 52:1209-1217. https://doi.org/10.1093/jexbot/52.359.1209
  58. ObaraM, Sato T, Sasaki S, et al. 2004. Identification and characterization of a QTL on chromosome 2 for cytosolic glutamine synthetase content and panicle number in rice. Theoretical and Applied Genetics. 110:1-11. https://doi.org/10.1007/s00122-004-1828-0
  59. Oliveira IC, Brears T, Knight TJ, Clark A, Coruzzi GM. 2002. Overexpression of cytosolic glutamate synthetase. Relation to nitrogen, light, and photorespiration. Plant Physiol. 129:1170-1180. https://doi.org/10.1104/pp.020013
  60. Pathak RR, Ahmad A, Lochab S, Raghuram N. 2008. Molecular physiology of plant N-use efficiency and biotechnological options for its enhancement. Current Science. 94:1394-1403.
  61. Rentsch D, Schmidt S, Tegeder M. 2007. Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Letters. 581:2281-2289. https://doi.org/10.1016/j.febslet.2007.04.013
  62. Scheible WR, MorcuendeR, Czechowski T, et al. 2004. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiology. 136:2483-2499. https://doi.org/10.1104/pp.104.047019
  63. Schoenbeck MA. et al. 2000. Decreased NADH-glutamate synthase activity in nodules and flowers of alfalfa (Medicago sativa L.) transformed with an antisense glutamate synthase transgene. J. Exp. Bot. 51:29-39. https://doi.org/10.1093/jexbot/51.342.29
  64. Sentoku N, Tanignchi M, Sugiyama T, Ishimaru K, Ohsugi R, Takaiwa F, Toki S. 2000. Analysis of the transgenic tobacco plants expressing Panicum miliaceum aspartate aminotransferase genes. Plant Cell Rep. 19:598- 603. https://doi.org/10.1007/s002990050779
  65. Shrawat AK, Carroll RT, DePauw M, et al. 2008. Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnology Journal. 6:722-732. https://doi.org/10.1111/j.1467-7652.2008.00351.x
  66. Sonoda Y, Ikeda A, Saiki S, Yamaya T, Yamaguchi J. 2003. Feedback regulation of the ammonium transporter gene family AMT1 by glutamine in rice. Plant Cell and Physiology. 44:1396-1402. https://doi.org/10.1093/pcp/pcg169
  67. Suarez R, Marquez J, Shishkova S, Hernandez G. 2003. Overexpression of alfalfa cytosolic glutamine synthetase in nodules and flowers of transgenic Lotus japonicus plants. Physiol Plant. 117:326-336. https://doi.org/10.1034/j.1399-3054.2003.00053.x
  68. Suzuki A, Knaff DB. 2005. Glutamate synthase: structural, mechanistic and regulatory properties, and role in the amino acid metabolism. Photosynthesis Research. 83:191- 217. https://doi.org/10.1007/s11120-004-3478-0
  69. Svennerstam H, Ganeteg U, Nasholm T. 2008. Root uptake of cationic amino acids by Arabidopsis depends on functional expression of amino acid permease 5. New Phytologist. 180:620-630. https://doi.org/10.1111/j.1469-8137.2008.02589.x
  70. Takahashi M, Sasaki Y, Ida S, Morikawa H. 2001. Nitrite reductase gene enrichment improves assimilation of NO2 in Arabidopsis. Plant Physiol. 126:731-741. https://doi.org/10.1104/pp.126.2.731
  71. Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK. 2007. Nitrate transporters and peptide transporters. FEBS Letters. 581:2290-2300. https://doi.org/10.1016/j.febslet.2007.04.047
  72. Vanlerberghe GC, Turpin DH. 1990. Anaerobic metabolism in the N-limited green algae selenastrum minutum. II. Assimilation of ammonium by anaerobic cells. Plant Physiol. 94:1124-1130. https://doi.org/10.1104/pp.94.3.1124
  73. Vincent R, et al. 1997. Over expression of a soyabean gene encoding cytosolic glutamine synthetase in shoots of transgenic Lotus cornicultus L. plants triggers changes in ammonium and plant development. Planta. 201:424-433. https://doi.org/10.1007/s004250050085
  74. Vincentz M, CabocheM. 1991. Constitutive expression of nitrate reductase allows normal growth and development of Nicotiana plumbaginifolia plants. EMBO J. 10:1027- 1035.
  75. Wang R, Tischner R, Gutie'rrez R, et al. 2004. Genomic analysis of the nitrate response using a nitrate reductasenull mutant of Arabidopsis. Plant Physiology. 136:2512- 2522. https://doi.org/10.1104/pp.104.044610
  76. Wirth J, Chopin F, Santoni V, et al. 2007. Regulation of root nitrate uptake at the NRT2.1 protein level in Arabidopsis thaliana. Journal of Biological Chemistry. 282: 23541-23552. https://doi.org/10.1074/jbc.M700901200
  77. Yamaya T, Obara M, Nakajima H, Saski S, Hayakawa T, Sato T. 2002. Genetic manipulation and quantitative trait loci mapping for nitrogen recycling in rice. Journal of Experimental Botany. 53:917-925. https://doi.org/10.1093/jexbot/53.370.917
  78. Yanagisawa S. 2000. Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J. 21:281-288. https://doi.org/10.1046/j.1365-313x.2000.00685.x
  79. Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T. 2004. Metabolic engineering with Dof1 transcriptiion factor in plants: Improved nitrogen assimilation and growth under low-nitrogen conditions. Proc. Natl. Acad. Sci. USA. 101:7833-7838. https://doi.org/10.1073/pnas.0402267101
  80. Yuan L, Loque D, Ye F, Frommer WB, von Wiren N. 2007. Nitrogen-dependent posttranscriptional regulation of the ammonium transporter AtAMT1;1. Plant Physiol. 143:732-744.
  81. Zhang H,Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science. 279:407-409. https://doi.org/10.1126/science.279.5349.407
  82. Zhang Y, Dickinson JR, Paul MJ, Halford NJ. 2003. Molecular cloning of an Arabidopsis homologue of GCN2, a protein kinase involved in co-ordinated response to amino acid starvation. Planta. 217:668-675. https://doi.org/10.1007/s00425-003-1025-4