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Advances in genetic basis of nitrogen use efficiency of rice

Abstract

Nitrogen is one of the fundamental key element required for crop growth and development. Excessive use of N in crop production has become a major global concern as it is causing environmental degradation through soil–water and also atmosphere. Increasing N use efficiency (NUE) and a balance of crop yields to achieve food security is the need of current situation. It is also important that, judicious application of N along with developing N efficiency crops are to be targeted for reducing the global climate change impacts. Ample opportunities existing in the form of germplasm resources which are yet to be utilized, advancement of genetic tools such as QTLs, genes associated with N metabolism, proteomics, association mapping, microarray, miRNA, genetic transformation and transcriptomic strategies are yet to be fully implemented to decipher the secrets of natural efficiency of N in crop plants. Progress of N use efficient developed using some of the above tools in a multidisciplinary mode and the first set of improved N efficient rice lines are field tested so as to understand genetic basis of NUE.

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References

  1. Agrawal, G. K., Rakwal, R., & Iwahashi, H. (2002). Isolation of novel rice (Oryza sativa L.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues. Biochemical and Biophysical Research Communications, 294, 1009–1016.

    CAS  Article  PubMed  Google Scholar 

  2. Cai, H., Lu, Y., Xie, W., Zhu, T., & Lian, X. (2012). Transcriptome response to nitrogen starvation in rice. Journal of Biosciences, 37, 731–747. doi:10.1007/s12038-012-9242-2.

    CAS  Article  PubMed  Google Scholar 

  3. Cai, C., Wang, J. Y., Zhu, Y. G., Shen, Q. R., Li, B., Tong, Y. P., et al. (2008). Gene structure and expression of the high-affinity nitrate transport system in rice roots. Journal of Integrative Plant Biology, 50, 443–451.

    CAS  Article  PubMed  Google Scholar 

  4. Cho, Y. I., Jiang, W. Z., Chin, J. H., Piao, Z. Z., Cho, Y. G., McCouch, S. R., et al. (2007). Identification of QTLs associated with physiological nitrogen use efficiency in rice. Molecules and Cells, 23, 72–79.

    CAS  PubMed  Google Scholar 

  5. Deng, R. L., Gu, J. T., Lu, W. J., Xu, H. R., Cao, Y. F., & Xiao, K. (2007). Characterization, function and expression analysis of ammonium transporter gene OsAMT1.4 and OsAMT5 in rice (Oryza sativa). Scientia Agricultura Sinica, 40, 2395–2402.

    CAS  Google Scholar 

  6. Ding, C., You, J., & Liu, Z. (2011). Proteomic analysis of low nitrogen stress-responsive proteins in roots of rice. Plant Molecular Biology Reporter, 2011, 618–625.

    Article  Google Scholar 

  7. Fang, P., Tao, Q. N., & Wu, P. (2001). QTLs underlying rice root to uptake NH4–N and NO3–N and rice N use efficiency at seedling stage. Plant Nutrition and Fertilizer, Science, 7(2), 159–165.

    Google Scholar 

  8. Fang, P., & Wu, P. (2001). QTL × N-level interaction for plant height in rice (Oryza sativa L.). Plant and Soil, 236, 237–242.

    CAS  Article  Google Scholar 

  9. Feng, C., Liu, G., & Gong, Y. (2011). Rice DUR3 mediates high-affinity urea transport and plays an effective role in improvement of urea acquisition and utilization when expressed in arabidopsis. New Phytologist, 193, 254–265.

    Google Scholar 

  10. Forde, B. G., & Clarkson, D. T. (1999). Nitrate and ammonium nutrition of plants: Physiological and molecular perspectives. Advances in Botanical Research, 30, 1–90.

    CAS  Article  Google Scholar 

  11. Frink, C. R., Waggoner, P. E., & Ausubel, S. H. (1999). Nitrogen fertilizer: Retrospect and prospect. Proceedings of the National Academy of Sciences of the United States of America, 96, 1175–1180.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Funayama, K., Kojima, S., Tabuchi-Kobayashi, M., Sawa, Y., Nakayama, Y., & Hayakawa, T. (2013). Cytosolic glutamine synthetase1;2 is responsible for the primary assimilation of ammonium in rice roots. Plant and cell physiology, 54, 934–943.

    CAS  Article  PubMed  Google Scholar 

  13. Garnett, T., Conn, V., & Kaiser, B. K. (2009). Root based approaches to improving nitrogen use efficiency in plants. Plant, Cell and Environment, 32, 1272–1283.

    CAS  Article  PubMed  Google Scholar 

  14. Glass, A., Brito, D., Kaiser, B., Kronzucker, H., Okamoto, M., Rawat, S., et al. (2001). Nitro-gen transport in plants, with an emphasis on the regulation of fluxes to match plant demand. Journal of Plant Nutrition and Soil Sciences, 164, 199–207.

    CAS  Article  Google Scholar 

  15. Goto, S., Akagawa, T., Kojima, S., Hayakawa, T., & Yamaya, T. (1998). Organization and structure of NADH-dependent glutamate synthase gene from rice plants. Biochimica et Biophysica Acta, 1387, 298–308.

    CAS  Article  PubMed  Google Scholar 

  16. Hakeem, K. R., Mir, B. A., Qureshi, M. I., Ahmad, A., & Iqbal, M. (2013). Physiological studies and proteomic analysis for differentially expressed proteins and their possible role in the root of N-efficient rice (Oryza sativa L.). Molecular Breeding, 32, 785–798.

    CAS  Article  Google Scholar 

  17. Hayashi, H., & Chino, M. (1990). Chemical composition of phloem sap from the upper most internode of the rice plant. Plant and Cell Physiology, 31, 247–251.

    CAS  Google Scholar 

  18. Hirel, B., & Gadal, P. (1980). Glutamine synthetase in rice. Plant Physiology, 66, 619–623.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 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.

    CAS  Article  PubMed  Google Scholar 

  20. Hirel, B., Chardon, F., & Durand, J. (2009). The contribution of molecular physiology to the improvement of nitrogen use efficiency in crops. Journal of Crop Science and Biotechnolgy, 10, 123–132.

    Google Scholar 

  21. Ireland, R. J., & Lea, P. J. (1999). The enzymes of glutamine, glutamate, asparagine and aspartate metabolisms. In B. K. Singh (Ed.), Plant amino acids. Biochemistry and biotechnology (pp. 49–109). New York: Marcel Dekker.

    Google Scholar 

  22. Ishimaru, K., Kobayashi, N., Ono, K., Yano, M., & Ohsugi, R. (2001). Are contents of rubisco, soluble protein and nitrogen in flag leaves of rice controlled by the same genetics? Journal of Experimental Botany, 52, 1827–1833.

    CAS  Article  PubMed  Google Scholar 

  23. Kamachi, K., Yamaya, T., Mae, T., & Ojima, K. (1991). A role for glutamine synthetase in the remobilization of leaf nitrogen during natural senescence in rice leaves. Plant Physiology, 96, 411–417.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Kamada-Nobusada, T., Makita, N., Kojima, M., & Sakakibara, H. (2013). Nitrogen-dependent regulation of de novo cytokinin biosynthesis in rice: The role of glutamine metabolism as an additional signal. Plant Cell Physiology, 54, 1181–1893.

    Article  Google Scholar 

  25. Kim, S. G., Wang, Y., Wu, J., Kang, K. Y., & Kim, S. T. (2011). Physiological and proteomic analysis of young rice leaves grown under nitrogen-starvation conditions. Plant Biotechnology Reports, 5, 309–314.

    Article  Google Scholar 

  26. Kojima, S., Kimura, M., Nozaki, Y., & Yamaya, T. (2000). Analysis of a promoter for NADH-glutamate synthase gene in rice (Oryza sativa): Cell-type specific expression in developing organs of transgenic rice plants. Australian Journal of Plant Physiology, 27, 787–793.

    CAS  Google Scholar 

  27. Kronzucker, H. J., Glass, A. D. M., Siddiqi, M. Y., & Kirk, G. J. D. (2000). Comparative kinetic analysis of ammonium and nitrate acquisition by tropical lowland rice: Implications for rice cultivation and yield potential. New Phytologist, 145, 471–476.

    CAS  Article  Google Scholar 

  28. Lam, H.-M., Koschigano, K. T., Oliveira, I. C., Melo-Oliveira, R., & Coruzzi, G. M. (1996). The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annual Review Plant Physiology and Plant Molecular Biology, 47, 569–593.

    CAS  Article  Google Scholar 

  29. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., et al. (2007). Clustal W and clustal X version 2.0. Bioinformatics, 23, 2947–2948.

    CAS  Article  PubMed  Google Scholar 

  30. Lea, P. J., Robinson, S. A., & Stewart, G. R. (1990). The enzymology and metabolism of glutamine, glutamate and aspergine. In B. J. Mifflin & P. J. Lea (Eds.), The biochemistry of plants, vol 16. Intermediary nitrogen metabolism (pp. 121–157). San Diego: Academic Press.

    Chapter  Google Scholar 

  31. Li, B. Z., Merrick, M., Li, S. M., Li, H. Y., Zhu, S. W., Shi, W. M., et al. (2009). Molecular basis and regulation of ammonium transporter in rice. Rice Science, 16, 314–322.

    Article  Google Scholar 

  32. Lin, C. M., Koh, S., Stacey, G., Yu, S. M., Lin, T. Y., & Tsay, Y. F. (2000). Cloning and functional characterization of a constitutively expressed nitrate transporter gene, OsNRT1, from rice. Plant Physiology, 122, 379–388.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Lian, X., Wang, S., Zhang, J., Feng, Q., Zhang, L., Fan, D., et al. (2006). Expression profiles of 10, 422 genes at early stage of low nitrogen stress in rice assayed using a cDNA microarray. Plant Molecular Biology, 60, 617–631. doi:10.1007/s11103-005-5441-7.

    CAS  Article  PubMed  Google Scholar 

  34. Lian, X., Xing, Y., & Yan, H. (2005). QTLs for low nitrogen tolerance at seedling stage identified using a recombinant inbred line population derived from an elite rice hybrid. Theoretical and Applied Genetics, 112, 85–96.

    CAS  Article  PubMed  Google Scholar 

  35. Ma, X., Cheng, Z., Qin, R., Qiu, Y., Heng, Y., Yang, H., et al. (2013). OsARG encodes an arginase that plays critical roles in panicle development and grain production in rice. The Plant Journal, 73, 190–200.

    CAS  Article  PubMed  Google Scholar 

  36. Masclaux-Daubresse, C., Daniel-Vedele, F., & Dechorgnat, J. (2010). Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany, 2010, 1141–1157.

    Article  Google Scholar 

  37. Obara, M., Kajiura, M., Fukuta, Y., Yano, M., Hayashi, M., Yamaya, T., 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.

    CAS  Article  PubMed  Google Scholar 

  38. Obara, M., Sato, T., Sasaki, S., Kashiba, K., Nagano, A., & Nakamura, I. (2004). Identification and characterization of a QTL on chromosome 2 for cytosolic glutamine synthetase content and panicle number in rice. Theoretical Applied Genetics, 110, 1–11.

    CAS  Article  PubMed  Google Scholar 

  39. Obara, M., Sato, T., & Yamaya, T. (2000). High content of cytosolic glutamine synthetase does not accompany with a high activity of the enzyme in rice (Oryza sativa L.) leaves of indica cultivars during the life span. Physiologia Plantrum, 108, 11–18.

    CAS  Article  Google Scholar 

  40. Piao, Z., Li, M., & Li, P. (2009). Bayesian dissection for genetic architecture of traits associated with nitrogen utilization efficiency in rice. Journal of Biotechnology, 8, 6834–6839.

    CAS  Google Scholar 

  41. Rao, P. R., Neeraja, C. N., Vishnukiran, T., Srikanth, B., Vijayalakshmi, P., Rao, I. S., Swamy, K. N., Kondamudi, R., Sailaja, N., Subrahmanyam, D., Surekha, K., Prasadbabu, M. B. B., Subbarao, L. V., & Voleti, S. R. (2014). Nitrogen use efficiency in irrigated rice for climate change—A case study. Technical Bulletin no.82/2014, ISBN 978-81-928249-6-3. p. 57. Directorate of Rice Research, Rajendranagar, Hyderabad 500030, AP, India.

  42. Sakurai, N., Hayakawa, T., Nakamura, T., & Yamaya, T. (1996). Changes in the cellular localization of cytosolic glutamine synthetase protein in vascular bundles of rice leaves at various stages of development. Planta, 200, 306–311.

    CAS  Article  Google Scholar 

  43. Sechley, K. A., Yamaya, T., & Oaks, A. (1992). Compartmentation of nitrogen assimilation in higher plants. International Review of Cytology, 134, 85–163.

    CAS  Article  Google Scholar 

  44. Senthilvel, S., Vinod, K. K., Malarvizhi, P., & Maheswaran, M. (2008). QTL and QTL × environment effects on agronomic and nitrogen acquisition traits in rice. Journal of Integrative Plant Biology, 50, 1108–1117.

    CAS  Article  PubMed  Google Scholar 

  45. Sonoda, Y., Ikeda, A., Saiki, S., von Wiren, N., Yamaya, T., & Yamaguchi, J. (2003). Distinct expression and function of three ammonium transporter genes (OsAMT1;1–1;3) in rice. Plant and Cell Physiology, 44, 726–734.

    CAS  Article  PubMed  Google Scholar 

  46. Srikanth, B., Rao, I. S., Moiz, S. Z., Swamy, K. N., Surekha, K., Subrahmanyam, D., et al. (2016). Physiological and molecular characterization of three rice genotypes with differential nitrogen use efficiency. Asian Journal of BioScience, 11, 162–171.

    Google Scholar 

  47. Srikanth, B., Rao, I. S., Swamy, K. N., Vijayalakshmi, P., Surekha, K., Moiz, S. Z., et al. (2015a). Physiological and molecular analysis of GQ-25, a promising genotype for Nitrogen use efficiency. Progressive Research-An International Journal, 10, 651–656.

    Google Scholar 

  48. Srikanth, B., Subhakara Rao, I., Surekha, K., Subrahmanyam, D., Voleti, S. R., & Neeraja, C. N. (2015b). Enhanced expression of OsSPL14 gene and its association with yield components in rice (Oryza sativa) under low nitrogen conditions. Gene, 576, 441–450.

    Article  PubMed  Google Scholar 

  49. Suenaga, A., Moriya, K., Sonoda, Y., Ikeda, A., von Wiren, N., & Hayakawa, T. (2003). Constitutive expression of a novel-type ammonium trans-porter OsAMT2 in rice plants. Plant and Cell Physiology, 44, 206–211.

    CAS  Article  PubMed  Google Scholar 

  50. Swamy, K. N., Kondamudi, R., Kiran, T. V., Vijayalakshmi, P., Rao, P. R., Subrahmanyam, D., et al. (2015a). Screening for nitrogen use efficiency with their root characteristics in rice (Oryza spp.) genotypes. Annals of Biological Science, 3, 8–11.

    Google Scholar 

  51. Swamy, K. N., Kondamudi, R., Vijayalakshmi, P., Jaldhani, V., Munnam, S. B., Kiran, T. V., et al. (2015b). A comparative study on nitrogen response among upland, IRHTN, DRR and other released rice groups. African Journal of Agricultural Research, 10, 4364–4369. doi:10.5897/AJAR2015.10323.

    Article  Google Scholar 

  52. Tabuchi, M., Abiko, T., & Yamaya, T. (2007). Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.). Journal of Experimental Botany, 58, 2319–2327. doi:10.1093/jxb/erm016.

    CAS  Article  PubMed  Google Scholar 

  53. Tabuchi, M., Sugiyama, T., Ishiyama, K., Inoue, E., Sato, T., Takahashi, H., et al. (2005). Severe reduction in growth and grain filling of rice mutants lacking OsGS1;1, a cytosolic gluta-mine synthetase 1;1. The Plant Journal, 42, 641–655.

    CAS  Article  PubMed  Google Scholar 

  54. Tong, H. H., Mei, H. W., Yu, X. Q., Xu, X. Y., Li, M. S., Zhang, S. Q., et al. (2006). Identification of related QTLs at late developmental stage in rice (Oryza sativa L.) under two nitrogen levels. Acta Genetica Sinica, 33, 458–467.

    Article  PubMed  Google Scholar 

  55. Tong, H., Chen, L., Li, W., Mei, H., Xing, Y., Yu, X., et al. (2011). Identification and characterization of quantitative trait loci for grain yield and its components under different nitrogen fertilization levels in rice (Oryza sativa L.). Molecular Breeding, 28, 495–509.

    CAS  Article  Google Scholar 

  56. Vijayakshmi, P., VishnuKiran, T., Rao, Y. V., Srikanth, B., Rao, I. S., Sailaja, B., et al. (2013). Physiological approaches for increasing nitrogen use efficiency in rice. Indian Journal of Plant Physiology, 18, 208–222.

    Article  Google Scholar 

  57. Vijayalakshmi, P., Rao, Y. V., Vishnukiran, T., Yugandhar, P., Swamy, K. N., Surekha, K., et al. (2015a). Germination behavior and chlorophyll content of aromatic rice (Oryza sativa L.) genotypes under varied nitrogen concentrations. Journal of Global Biosciences., 7, 2911–2920.

    Google Scholar 

  58. Vijayalakshmi, P., Vishnukiran, T., Kumari, B. R., Srikanth, B., Rao, I. S., Swamy, K. N., et al. (2015b). Biochemical and physiological characterization for nitrogen use efficiency in aromatic rice genotypes. Field Crops Research, 179, 132–143.

    Article  Google Scholar 

  59. Von Wiren, N., Gazzarrini, S., Gojon, A., & Frommer, W. B. (2000). The molecular physiology of ammonium uptake and retrieval. Current Opinion in Plant Biology, 3, 254–261. doi:10.1016/S1369-5266(00)00073-X.

    Article  Google Scholar 

  60. Wang, M. Y., Siddiqi, M. Y., Ruth, T. J., & Glass, A. D. M. (1993). Ammonium uptake by rice roots. I. Fluxes and subcellular distribution of 13NH4+. Plant Physiology, 103, 1249–1258.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. Wang, X., Wang, Y., Tian, J., Lim, B. L., Yan, X., & Liao, H. (2009). Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiology, 151, 233–240.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  62. Wang, W. H., Kohler, B., Cao, F. Q., Liu, G. W., Gong, Y. Y., Sheng, S., et al. (2012). Rice DUR3 mediates high-affinity urea transport and plays an effective role in improvement of urea acquisition and utilization when expressed in arabidopsis. New Phytologist, 193, 432–444.

    CAS  Article  PubMed  Google Scholar 

  63. Wei, D., Cui, K., Pan, J., Wang, Q., Wang, K., Zhang, X., et al. (2012a). Identification of quantitative trait loci for grain yield and its components in response to low nitrogen application in rice. AJCS., 6(6), 986–994.

    CAS  Google Scholar 

  64. Wei, D., Cui, K., Ye, G., Pan, J., Xiang, J., Huang, J., et al. (2012b). QTL mapping for nitrogen-use efficiency and nitrogen-deficiency tolerance traits in rice. Plant and Soil, 359, 281–295.

    CAS  Article  Google Scholar 

  65. Williams, L., & Miller, A. (2001). Transporters responsible for the uptake and partitioning of nitrogenous solutes. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 659–688.

    CAS  Article  PubMed  Google Scholar 

  66. Xu, G., Fan, X., & Miller, A. J. (2012). Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology, 64, 153–82.

    Article  Google Scholar 

  67. Yamaya, T., Obara, M., Nakajima, H., Sasaki, 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.

    CAS  Article  PubMed  Google Scholar 

  68. Yan, M., Fan, X., Feng, H., Miller, A. J., Shen, Q., & Xu, G. (2011). RiceOsNAR2.1 interacts with OsNRT2.1, OsNRT2.2 and OsNRT2.3a nitrate transporters to provide uptake over high and low concentration ranges. Plant, Cell and Environment, 34, 1360–1372.

    CAS  Article  PubMed  Google Scholar 

  69. Yuan, L., Loqué, D., Ye, F., Frommer, W. B., & von Wirén, N. (2007). Nitrogen-dependence posttranscriptional regulation of the ammonium transporter AtAMT1;1. Plant Physiology, 143, 732–744.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Innovations in Climate Resilient Agriculture (NICRA), Indian Council of Agricultural Research (ICAR), Ministry of Agriculture, Govt. of India [F. No. Phy/NICRA/2011–2012].

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Correspondence to C. N. Neeraja.

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Neeraja, C.N., Subramanyam, D., Surekha, K. et al. Advances in genetic basis of nitrogen use efficiency of rice. Ind J Plant Physiol. 21, 504–513 (2016). https://doi.org/10.1007/s40502-016-0254-z

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Keywords

  • NUE-QTLs
  • Genes
  • Association mapping
  • Field evaluation