Abstract
Nitrogen is one of the most critical nutrients in rice production and increased rice productivity is attributed mostly to the nitrogen fertilizer responsive rice varieties. With its relevance to environment, breeding for nitrogen use efficiency is now a research priority in rice. Based on the physiological, biochemical and genetic studies, several genes have been identified for nitrogen uptake, transport, remobilization and assimilation. Many of the genes and gene families associated with tissues like root, shoot, leaf and panicle have been characterized under differential nitrogen conditions. Functional validation of the identified genes in nitrogen use efficiency, yield and other agro-morphological traits demonstrated their potential for deployment in rice breeding programs. In the present review, the information on possible genes associated with nitrogen use efficiency has been presented. The epigenetic regulation of genes including the non-coding RNA and new breeding technologies like genome editing have also been discussed for identification and validation of genes for NUE. We propose a combinatorial approach of deploying the information available for genes reported to be associated with NUE of rice by haplotyping, allele mining, spatial and temporal expression analyses, gene networking and validation through genome editing towards development of high yielding rice varieties under optimum nitrogen.
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References
Alfatih, A., Wu, J., Zhang, Z. S., Xia, J. Q., Jan, S. U., Yu, L. H., & Xiang, C. B. (2020). Rice NIN-LIKE PROTEIN 1 rapidly responds to nitrogen deficiency and improves yield and nitrogen use efficiency. Journal of Experimental Botany, 71(19), 6032–6042. https://doi.org/10.1093/jxb/eraa292
Bao, A., Liang, Z., Zhao, Z., & Cai, H. (2015a). Overexpressing of OsAMT1-3, a high affinity ammonium transporter gene, modifies rice growth and carbon-nitrogen metabolic status. International Journal of Molecular Sciences, 16(5), 9037–9063. https://doi.org/10.3390/ijms16059037
Bao, A., Zhao, Z., Ding, G., Shi, L., Xu, F., & Cai, H. (2015b). The stable level of Glutamine synthetase 2 plays an important role in rice growth and in carbon-nitrogen metabolic balance. International Journal of Molecular Sciences., 16(6), 12713–12736. https://doi.org/10.3390/ijms160612713
Bao, A., Zhao, Z., Ding, G., Shi, L., Xu, F., et al. (2014). Accumulated expression level of Cytosolic Glutamine Synthetase 1 gene (OsGS1;1 or OsGS1;2) alter plant development and the carbon-nitrogen metabolic status in rice. PLoS ONE, 9(4), e95581. https://doi.org/10.1371/journal.pone.0095581
Barbadikar, K. M., Aglawe, S. B., Mangrauthia, S. K., Madhav, M. S., & Kumar, S. P. J. (2019). Genome editing: New breeding technologies in plants. OMICS-Based Approaches in Plant Biotechnology, 2019, 245–285.
Beier, M. P., Fujita, T., Sasaki, K., Kanno, K., Ohashi, M., Tamura, W., Konishi, N., Saito, M., Imagawa, F., Ishiyama, K., Miyao, A., Yamaya, T., & Kojima, S. (2019). The urea transporter DUR3 contributes to rice production under nitrogen-deficient and field conditions. Physiologia Plantarum, 167(1), 75–89.
Beier, M. P., Obara, M., Taniai, A., Sawa, Y., Ishizawa, J., & Yoshida, H. (2018). Lack of ACTPK1, an STY kinase, enhances ammonium uptake and use, and promotes growth of rice seedlings under sufficient external ammonium. Plant Journal, 93(6), 992–1006. https://doi.org/10.1111/tpj.13824
Bernard, S. M., & Habash, D. Z. (2009). The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytologist, 182(3), 608–620. https://doi.org/10.1111/J.1469-8137.2009.02823.X
Bhogireddy, S., Mangrauthia, S. K., Kumar, R., Pandey, A. K., Singh, S., Jain, A., Budak, H., Varshney, R. K., & Kudapa, H. (2021). Regulatory non-coding RNAs: a new frontier in regulation of plant biology. Functional and Integrative Genomics, 21(3–4), 313–330. https://doi.org/10.1007/s10142-021-00787-8
Biswal, A. K., Mangrauthia, S. K., Reddy, M. R., & Yugandhar, P. (2019). CRISPR mediated genome engineering to develop climate smart rice: Challenges and opportunities. Seminars in Cell and Developmental Biology, 96, 100–106. https://doi.org/10.1016/j.semcdb.2019.04.005
Budak, H., Kaya, S. B., & Cagirici, H. B. (2020). Long non-coding RNA in plants in the era of reference sequences. Frontiers in Plant Science, 11, 276. https://doi.org/10.3389/fpls.2020.00276
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 Reports, 28, 527–537. https://doi.org/10.1007/s00299-008-0665-z
Chen, G., Guo, S., Kronzucker, H. J., & Shi, W. (2013). Nitrogen use efficiency (NUE) in rice links to NH4+ toxicity and futile NH4+ cycling in roots. Plant and Soil, 369(1–2), 351–363. https://doi.org/10.1007/s11104-012-1575-y
Chen, J., Fan, X., Qian, K., Zhang, Y., Song, M., Liu, Y., Xu, G., & Fan, X. (2017). pOsNAR2.1:OsNAR2.1 expression enhances nitrogen uptake efficiency and grain yield in transgenic rice plants. Plant Biotechnology Journal, 15(10), 1273–1283. https://doi.org/10.1111/pbi.12714
Chen, Z., Jiang, Q., Jiang, P., Zhang, W., Huang, J., Liu, C., Halford, N. G., & Lu, R. (2020). Novel low-nitrogen stress-responsive long non-coding RNAs (lncRNA) in barley landrace B968 (Liuzhutouzidamai) at seedling stage. BMC Plant Biology. https://doi.org/10.1186/s12870-020-02350-2
Coruzzi, G. M., & Zhou, L. (2001). Carbon and nitrogen sensing and signaling in plants: Emerging matrix effects. Current Opinion in Plant Biology, 4, 247–253. https://doi.org/10.1016/S1369-5266(00)00168-0
De Datta, S. K., & Buresh, R. J. (1989). Integrated nitrogen management in irrigated rice. Advances in Soil Science, 10, 143–169. https://doi.org/10.1007/978-1-4613-8847-0_4
Du, C. Q., Lin, J. Z., Dong, L. A., Liu, C., Tang, D. Y., Yan, L., Chen, M. D., Liu, S., & Liu, X. M. (2019). Overexpression of an NADP(H)-dependent glutamate dehydrogenase gene, TrGDH, from Trichurus improves nitrogen assimilation, growth status and grain weight per plant in rice. Breeding Science, 69(3), 429–438. https://doi.org/10.1270/jsbbs.19014
Fan, T., Yang, W., Zeng, X., Xu, X., Xu, Y., Fan, X., et al. (2020). A rice autophagy gene OsATG8b is involved in nitrogen remobilization and control of grain quality. Frontiers in Plant Science. https://doi.org/10.3389/FPLS.2020.00588
Fan, X., Feng, H., Tan, Y., Xu, Y., Miao, Q., & Xu, G. (2016a). A putative 6-transmembrane nitrate transporter OsNRT1.1b plays a key role in rice under low nitrogen. Journal of Integrative Plant Biology, 58, 590–599. https://doi.org/10.1111/jipb.12382
Fan, X., Liu, L., Qian, K., Chen, J., Zhang, Y., Xie, P., Xu, M., Hu, Z., Yan, W., Wu, Y., & Xu, G. (2021). Plant DNA methylation is sensitive to parent seed N content and influences the growth of rice. BMC Plant Biology, 21(1), 1–18. https://doi.org/10.1186/s12870-021-02953-3
Fan, X., Shen, Q., Ma, Z., Zhu, H., Yin, X., & Miller, A. J. (2005). A comparison of nitrate transport in four different rice (Oryza sativa L.) cultivars. Science in China Series C Life Sciences, 48(2), 897–911. https://doi.org/10.1007/BF03187128
Fan, X., Tang, Z., Tan, Y., Zhang, Y., Luo, B., Yang, M., Lian, X., Shen, Q., Miller, A. J., & Xu, G. (2016b). Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. Proceedings of the National Academy of Sciences of the United States of America, 113(26), 7118–7123. https://doi.org/10.1073/pnas.1525184113
Fang, J., Zhang, F., Wang, H., Wang, W., Zhao, F., Li, Z., Sun, C., Chen, F., Xu, F., Chang, S., Wu, L., Bu, Q., Wang, P., Xie, J., Chen, F., Huang, X., Zhang, Y., Zhu, X., Han, B., & Chu, C. (2019). Ef-cd locus shortens rice maturity duration without yield penalty. Proceedings of the National Academy of Sciences of the United States of America, 116(37), 18717–18722. https://doi.org/10.1073/pnas.1815030116
Fang, Z., Bai, G., Huang, W., Wang, Z., Wang, X., & Zhang, M. (2017). The rice peptide transporter OsNPF7.3 is induced by organic nitrogen, and contributes to nitrogen allocation and grain yield. Frontiers in Plant Science, 8, 1338. https://doi.org/10.3389/fpls.2017.01338
Fang, Z., Wu, B., & Ji, Y. (2021). The amino acid transporter osaap4 contributes to rice tillering and grain yield by regulating neutral amino acid allocation through two splicing variants. Rice. https://doi.org/10.1186/s12284-020-00446-9
Fang, Z., Xia, K., Yang, X., Grotemeyer, M. S., Meier, S., Rentsch, D., Xu, X., & Zhang, M. (2013). Altered expression of the PTR/NRT1 homologue OsPTR9 affects nitrogen utilization efficiency, growth and grain yield in rice. Plant Biotechnology Journal, 11(4), 446–458. https://doi.org/10.1111/pbi.12031
Feng, H., Li, B., Zhi, Y., Chen, J., Li, R., Xia, X., Xu, G., & Fan, X. (2017). Overexpression of the nitrate transporter, OsNRT2.3b, improves rice phosphorus uptake and translocation. Plant Cell Reports, 36(8), 1287–1296. https://doi.org/10.1007/s00299-017-2153-9
Ferreira, L. M., de Souza, V. M., Tavares, O. C. H., Zonta, E., Santa-Catarina, C., de Souza, S. R., et al. (2015). OsAMT1.3 expression alters rice ammonium uptake kinetics and root morphology. Plant Biotechnology Reports, 9(4), 221–229. https://doi.org/10.1007/S11816-015-0359-2
Funayama, K., Kojima, S., Tabuchi-Kobayashi, M., Sawa, Y., Nakayama, Y., Hayakawa, T., & Yamaya, T. (2013). Cytosolic glutamine synthetase1;2 is responsible for the primary assimilation of ammonium in rice roots. Plant and Cell Physiology, 54(6), 934–943. https://doi.org/10.1093/pcp/pct046
Gao, Y., Xu, Z., Zhang, L., Li, S., Wang, S., Yang, H., Liu, X., Zeng, D., Liu, Q., Qian, Q., Zhang, B., & Zhou, Y. (2020). MYB61 is regulated by GRF4 and promotes nitrogen utilization and biomass production in rice. Nature Communications. https://doi.org/10.1038/s41467-020-19019-x
Gao, Z., Wang, Y., Chen, G., Zhang, A., Yang, S., Shang, L., Wang, D., Ruan, B., Liu, C., Jiang, H., et al. (2019). The indica nitrate reductase gene OsNR2 allele enhances rice yield potential and nitrogen use efficiency. Nature Communications, 10, 5207. https://doi.org/10.1038/s41467-019-13110-8
Gho, Y. S., Song, M. Y., Bae, D. Y., Choi, H., & Jung, K. H. (2021). Rice pin auxin efflux carriers modulate the nitrogen response in a changing nitrogen growth environment. International Journal of Molecular Sciences. https://doi.org/10.3390/ijms22063243
Guo, N., Gu, M., Hu, J., Qu, H., & Xu, G. (2020a). Rice OsLHT1 functions in leaf-to-panicle nitrogen allocation for grain yield and quality. Frontiers in Plant Science, 11, 1150. https://doi.org/10.3389/fpls.2020.01150
Guo, N., Hu, J., Yan, M., Qu, H., Luo, L., Tegeder, M., & Xu, G. (2020b). Oryza sativa Lysine-Histidine-type Transporter 1 functions in root uptake and root-to-shoot allocation of amino acids in rice. Plant Journal, 103(1), 395–411. https://doi.org/10.1111/tpj.14742
Hu, B., Wang, W., Ou, S., Tang, J., Li, H., Che, R., Zhang, Z., Chai, X., Wang, H., Wang, Y., Liang, C., Liu, L., Piao, Z., Deng, Q., Deng, K., Xu, C., Liang, Y., Zhang, L., Li, L., & Chu, C. (2015). Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nature Genetics, 47(7), 834–838. https://doi.org/10.1038/ng.3337
Hu, R., Qiu, D., Chen, Y., Miller, A. J., Fan, X., Pan, X., & Zhang, M. (2016). Knock-Down of a tonoplast localized low-affinity nitrate transporter OsNPF7.2 affects rice Growth under high nitrate supply. Frontiers in Plant Science, 7, 1529. https://doi.org/10.3389/fpls.2016.01529
Hua, Y. P., Zhou, T., Huang, J. Y., Yue, C. P., Song, H. X., Guan, C. Y., & Zhang, Z. H. (2020). Genome-wide differential DNA methylation and miRNA expression profiling reveals epigenetic regulatory mechanisms underlying nitrogen-limitation-triggered adaptation and use efficiency enhancement in allotetraploid rapeseed. International Journal of Molecular Science, 21(22), 8453. https://doi.org/10.3390/ijms21228453
Huang, A., Sang, Y., Sun, W., Fu, Y., & Yang, Z. (2016). Transcriptomic analysis of responses to imbalanced carbon: Nitrogen availabilities in rice seedlings. PLoS ONE, 11(11), e0165732. https://doi.org/10.1371/JOURNAL.PONE.0165732
Huang, W., Bai, G., Wang, J., Zhu, W., Zeng, Q., Lu, K., Sun, S., & Fang, Z. (2018). Two splicing variants of OsNPF7.7 regulate shoot branching and nitrogen utilization efficiency in rice. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2018.00300
Ji, Y., Huang, W., Wu, B., Fang, Z., & Wang, X. (2020). The amino acid transporter AAP1 mediates growth and grain yield by regulating neutral amino acid uptake and reallocation in Oryza sativa. Journal of Experimental Botany, 71(16), 4763–4777. https://doi.org/10.1093/jxb/eraa256
Kolbert, Z., & Erdei, L. (2008). Involvement of nitrate reductase in auxin-induced NO synthesis. Plant Signaling and Behavior, 3(11), 972–973. https://doi.org/10.4161/psb.6170
Kou, H. P., Li, Y., Song, X. X., Ou, X. F., Xing, S. C., Ma, J., Von Wettstein, D., & Liu, B. (2011). Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice (Oryza sativa L.). Journal of Plant Physiology, 168(14), 1685–1693. https://doi.org/10.1016/j.jplph.2011.03.017
Kumagai, E., Araki, T., Hamaoka, N., & Ueno, O. (2011). Ammonia emission from rice leaves in relation to photorespiration and genotypic differences in glutamine synthetase activity. Annals of Botany, 108(7), 1381–1386. https://doi.org/10.1093/aob/mcr245
Kumari, S., Sharma, N., & Raghuram, N. (2021). Meta-Analysis of yield-related and N-responsive genes reveals chromosomal hotspots, key processes and candidate genes for nitrogen-use efficiency in rice. Frontiers in Plant Science, 12, 627955. https://doi.org/10.3389/fpls.2021.627955
Kurai, T., Wakayama, M., Abiko, T., Yanagisawa, S., Aoki, N., & Ohsugi, R. (2011). Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low-nitrogen conditions. Plant Biotechnology Journal, 9(8), 826–837. https://doi.org/10.1111/J.1467-7652.2011.00592.X
Kusano, M., Fukushima, A., Tabuchi-Kobayashi, M., Funayama, K., Kojima, S., Maruyama, K., Yamamoto, Y. Y., Nishizawa, T., Kobayashi, M., Wakazaki, M., Sato, M., Toyooka, K., Osanai-Kondo, K., Utsumi, Y., Seki, M., Fukai, C., Saito, K., & Yamaya, T. (2020). Cytosolic glutamine synthetase1;1 modulates metabolism and chloroplast development in ROOTs1[open]. Plant Physiology, 182(4), 1894–1909. https://doi.org/10.1104/PP.19.01118
Ladha, J. K., Jat, M. L., Stirling, C. M., Chakraborty, D., Pradhan, P., Krupnik, T. J., Sapkota, T. B., Pathak, H., Rana, D. S., Tesfaye, K., & Gerard, B. (2020). Achieving the sustainable development goals in agriculture: The crucial role of nitrogen in cereal-based systems. Advances in Agronomy, 163, 39–116.
Lee, S. (2021). Recent advances on nitrogen use efficiency in rice. Agronomy, 11(4), 753. https://doi.org/10.3390/agronomy11040753
Lee, S., Marmagne, A., Park, J., Fabien, C., Yim, Y., Kim, S. J., Kim, T. H., Lim, P. O., Masclaux-Daubresse, C., & Nam, H. G. (2020a). Concurrent activation of OsAMT1; 2 and OsGOGAT1 in rice leads to enhanced nitrogen use efficiency under nitrogen limitation. The Plant Journal, 103(1), 7–20. https://doi.org/10.1111/tpj.14794
Lee, S., Park, J., Lee, J., Shin, D., Marmagne, A., Lim, P. O., et al. (2020b). OsASN1 overexpression in rice increases grain protein content and yield under nitrogen-limiting conditions. Plant and Cell Physiology, 61(7), 1309–1320. https://doi.org/10.1093/PCP/PCAA060
Leran, S., Varala, K., Boyer, J. C., Chiurazzi, M., Crawford, N., Daniel-Vedele, F., David, L., Dickstein, R., Fernandez, E., Forde, B., Gassmann, W., Geiger, D., Gojon, A., Gong, J. M., Halkier, B. A., Harris, J. M., Hedrich, R., Limami, A. M., Rentsch, D., … Lacombe, B. (2014). A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends in Plant Science, 19(1), 5–9. https://doi.org/10.1016/j.tplants.2013.08.008
Li, B., Byrt, C., Qiu, J., Baumann, U., Hrmova, M., Evrard, A., Johnson, A. A. T., Birnbaum, K. D., Mayo, G. M., Jha, D., Henderson, S. W., Tester, M., Gilliham, M., & Roy, S. J. (2016a). Identification of a stelar-localized transport protein that facilitates root-to-shoot transfer of chloride in arabidopsis. Plant Physiology, 170(2), 1014–1029. https://doi.org/10.1104/pp.15.01163
Li, C., Tang, Z., Wei, J., Qu, H., Xie, Y., & Xu, G. (2016b). The OsAMT1.1 gene functions in ammonium uptake and ammonium-potassium homeostasis over low and high ammonium concentration ranges. Journal of Genetics and Genomics, 43, 639–649. https://doi.org/10.1016/j.jgg.2016.11.001
Li, H., Hu, B., Wang, W., Zhang, Z., Liang, Y., Gao, X., Li, P., Liu, Y., Zhang, L., & Chu, C. (2016c). Identification of microRNAs in rice root in response to nitrate and ammonium. Journal of Genetics and Genomics, 43(11), 651–661. https://doi.org/10.1016/j.jgg.2015.12.002
Li, H., Hu, B., Wang, W., Zhang, Z., Liang, Y., Gao, X., Li, P., Liu, Y., Zhang, L., & Chu, C. (2016d). Identification of microRNAs in rice root in response to nitrate and ammonium. Journal of Genetics and Genomics, 43(11), 651–661. https://doi.org/10.1016/j.jgg.2015.12.002
Li, S., Qian, Q., Fu, Z., Zeng, D., Meng, X., Kyozuka, J., Maekawa, M., Zhu, X., Zhang, J., Li, J., & Wang, Y. (2009). Short panicle1 encodes a putative PTR family transporter and determines rice panicle size. Plant Journal, 58, 592–605. https://doi.org/10.1111/j.1365-313X.2009.03799.x
Li, S., Tian, Y., Wu, K., Ye, Y., Yu, J., Zhang, J., et al. (2018). Modulating plant growth–metabolism coordination for sustainable agriculture. Nature, 560(7720), 595–600. https://doi.org/10.1038/s41586-018-0415-5
Li, Y., Ouyang, J., Wang, Y. Y., Hu, R., Xia, K., Duan, J., Wang, Y., Tsay, Y. F., & Zhang, M. (2015a). Disruption of the rice nitrate transporter OsNPF2.2 hinders root-to-shoot nitrate transport and vascular development. Scientific Reports, 5, 9635. https://doi.org/10.1038/srep09635
Li, Y., Ouyang, J., Wang, Y. Y., Hu, R., Xia, K., Duan, J., Wang, Y., Tsay, Y. F., & Zhang, M. (2015b). Disruption of the rice nitrate transporter OsNPF2.2 hinders root-to-shoot nitrate transport and vascular development. Scentific Reports, 5, 9635. https://doi.org/10.1038/srep09635
Liang, Y., Wang, J., Zeng, F., Wang, Q., Zhu, L., Li, H., Guo, N., & Chen, H. (2020). Photorespiration regulates carbon-nitrogen metabolism by magnesium chelatase D subunit in rice. Journal of Agricultural and Food Chemistry, 69(1), 112–125. https://doi.org/10.1021/acs.jafc.0c05809
Lu, K., Wu, B., Wang, J., Zhu, W., Nie, H., Qian, J., et al. (2018). Blocking amino acid transporter OsAAP3 improves grain yield by promoting outgrowth buds and increasing tiller number in rice. Plant Biotechnology Journal, 16(10), 1710–1722. https://doi.org/10.1111/PBI.12907
Lu, Y., & Zhu, J. K. (2017). Precise Editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Molecular Plant, 10(3), 523–525. https://doi.org/10.1016/j.molp.2016.11.013
Mandal, V. K., Sharma, N., & Raghuram, N. (2018). Molecular targets for improvement of crop nitrogen use efficiency: Current and emerging options. Engineering Nitrogen Utilization in Crop Plants. https://doi.org/10.1007/978-3-319-92958-3_5
Masclaux-Daubresse, C., & Chardon, F. (2011). Exploring nitrogen remobilization for seed filling using natural variation in Arabidopsis thaliana. Journal of Experimental Botany, 62(6), 2131–2142. https://doi.org/10.1093/JXB/ERQ405
Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L., & Suzuki, A. (2010). Nitrogen uptake, assimilation and remobilization in plants: Challenges for sustainable and productive agriculture. Annals of Botany, 105(7), 1141–1157. https://doi.org/10.1093/aob/mcq028
Meng, X., Yu, X., Wu, Y., Kim, D. H., Nan, N., Cong, W., Wang, S., Liu, B., & Xu, Z. Y. (2020). Chromatin remodeling protein ZmCHB101 regulates nitrate-responsive gene expression in maize. Frontiers in Plant Science, 11, 52. https://doi.org/10.3389/fpls.2020.00052
Miao, C., Wang, D., He, R., Liu, S., & Zhu, J. K. (2020). Mutations in MIR396e and MIR396f increase grain size and modulate shoot architecture in rice. Plant Biotechnology Journal, 18(2), 491–501. https://doi.org/10.1111/pbi.13214
Moll, R. H., Kamprath, E. J., & Jackson, W. A. (1982). Analysis and interpretation of factors which contribute to efficiency to nitrogen utilization. Agronomy Journal, 74, 562–564.
Nazish, T., Arshad, M., Jan, S. U., Javaid, A., Khan, M. H., Naeem, M. A., et al. (2021). Transporters and transcription factors gene families involved in improving nitrogen use efficiency (NUE) and assimilation in rice (Oryza sativa L.). Transgenic Research, 2021, 1–20. https://doi.org/10.1007/S11248-021-00284-5
Neeraja, C. N., Voleti, S. R., Subrahmanyam, D., Surekha, K., Desiraju, B. S., Krishnakanth, T., & Raghuveer, R. P. (2021). Molecular breeding for improving nitrogen use efficiency in rice: Progress and perspectives. Molecular Breeding for Rice Abiotic Stress Tolerance and Nutritional Quality. https://doi.org/10.1002/9781119633174.ch12
Niu, Y. F., Chai, R. S., Jin, G. L., Wang, H., Tang, C. X., & Zhang, Y. S. (2013). Responses of root architecture development to low phosphorus availability: A review. Annals of Botany, 112(2), 391–408. https://doi.org/10.1093/aob/mcs285
Ohashi, M., Ishiyama, K., Kojima, S., Konishi, N., Nakano, K., Kanno, K., et al. (2015). Asparagine synthetase1, but not asparagine synthetase2, is responsible for the biosynthesis of asparagine following the supply of ammonium to rice roots. Plant and Cell Physiology, 56(4), 769–778. https://doi.org/10.1093/PCP/PCV005
Ohashi, M., Ishiyama, K., Kojima, S., Konishi, N., Sasaki, K., Miyao, M., Hayakawa, T., & Yamaya, T. (2018). Outgrowth of rice tillers requires availability of glutamine in the basal portions of shoots. Rice. https://doi.org/10.1186/s12284-018-0225-2
Qiu, X., Xie, W., Lian, X., & Zhang, Q. (2009). Molecular analyses of the rice glutamate dehydrogenase gene family and their response to nitrogen and phosphorous deprivation. Plant Cell Reports, 28(7), 1115–1126. https://doi.org/10.1007/s00299-009-0709-z
Raghuram, N., Sutton, M. A., Jeffery, R., Ramachandran, R., & Adhya, T. K. (2021). From South Asia to the world: Embracing the challenge of global sustainable nitrogen management. One Earth, 4(1), 22–27. https://doi.org/10.1016/j.oneear.2020.12.017
Ranathunge, K., El-Kereamy, A., Gidda, S., Bi, Y. M., & Rothstein, S. J. (2014). AMT1;1 transgenic rice plants with enhanced NH4+ permeability show superior growth and higher yield under optimal and suboptimal NH4+ conditions. Journal of Experimental Botany, 65(4), 965–979. https://doi.org/10.1093/jxb/ert458
Sevanthi, A. M., Sinha, S. K., Sureshkumar, V., Rani, M., Saini, M. R., Kumari, S., Kaushik, M., Prakash, C., Venkatesh, K., Singh, G. P., & Mohapatra, T. (2021). Integration of dual stress transcriptomes and major qtls from a pair of genotypes contrasting for drought and chronic nitrogen starvation identifies key stress responsive genes in rice. Rice, 14, 49. https://doi.org/10.1186/s12284-021-00487-8
Shin, S. Y., Jeong, J. S., Lim, J. Y., Kim, T., Park, J. H., Kim, J. K., & Shin, C. (2018). Transcriptomic analyses of rice (Oryza sativa) genes and non-coding RNAs under nitrogen starvation using multiple omics technologies. BMC Genomics, 19(1), 1–20. https://doi.org/10.1186/s12864-018-4897-1
Sinha, S. K., Sevanthi, V. A. M., Chaudhary, S., Tyagi, P., Venkadesan, S., Rani, M., & Mandal, P. K. (2018). Transcriptome analysis of two rice varieties contrasting for nitrogen use efficiency under chronic N starvation reveals differences in chloroplast and starch metabolism-related genes. Genes, 9(4), 206. https://doi.org/10.3390/genes9040206
Sonoda, Y., Ikeda, A., Saiki, S., von Wirén, N., Yamaya, T., & Yamaguchi, J. (2003). Distinct expression and function of three ammonium transporter genes (OsAMT1;1–1;3) in rice. Plant Cell Physiology, 44(7), 726–734.
Suenaga, A., Moriya, K., Sonoda, Y., Ikeda, A., von Wirén, N., Hayakawa, T., Yamaguchi, J., & Yamaya, T. (2003). Constitutive expression of a novel-type ammonium transporter OsAMT2 in rice plants. Plant Cell Physiology, 44(2), 206–211.
Sun, H., Tao, J., Bi, Y., Hou, M., Lou, J., Chen, X., Zhang, X., Luo, L., Xie, X., Yoneyama, K., Zhao, Q., Xu, G., & Zhang, Y. (2018). OsPIN1b is involved in rice seminal root elongation by regulating root apical meristem activity in response to low nitrogen and phosphate. Scientific Reports, 8(13014), 10–20. https://doi.org/10.1038/s41598-018-29784-x
Surekha, K., Kumar, R. M., Subhramanyam, D., Neeraja, C. N., Rajesh, K., & Voleti, S. R. (2019). All India co-ordinated rice improvement programme aprroaches in improving nitrogen use efficiency in rice. Indian Journal of Fertilisers, 15(4), 64–75.
Sutton, M. A., Howard, C. M., Kanter, D. R., Lassaletta, L., Móring, A., Raghuram, N., & Read, N. (2021). The nitrogen decade: Mobilizing global action on nitrogen to 2030 and beyond. One Earth, 4(1), 10–14. https://doi.org/10.1016/j.oneear.2020.12.016
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. https://doi.org/10.1093/jxb/erm016
Tabuchi, M., Sugiyama, K., Ishiyama, K., Inoue, E., Sato, T., Takahashi, H., & Yamaya, T. (2005). Severe reduction in growth rate and grain filling of rice mutants lacking OsGS1;1, a cytosolic glutamine synthetase1;1. Plant Journal, 42(5), 641–651. https://doi.org/10.1111/j.1365-313X.2005.02406.x
Tamura, W., Hidaka, Y., Tabuchi, M., Kojima, S., Hayakawa, T., Sato, T., Obara, M., Kojima, M., Sakakibara, H., & Yamaya, T. (2010). Reverse genetics approach to characterize a function of NADH-glutamate synthase1 in rice plants. Amino Acids, 39(4), 1003–1012. https://doi.org/10.1007/s00726-010-0531-5
Tamura, W., Kojima, S., Toyokawa, A., Watanabe, H., Tabuchi-Kobayashi, M., Hayakawa, T., & Yamaya, T. (2011). Disruption of a novel NADH-glutamate synthase2 gene caused marked reduction in spikelet number of rice. Frontiers in Plant Science, 2, 57. https://doi.org/10.3389/fpls.2011.00057
Tang, W., Ye, J., Yao, X., Zhao, P., Xuan, W., Tian, Y., Zhang, Y., Xu, S., An, H., Chen, G., Yu, J., Wu, W., Ge, Y., Liu, X., Li, J., Zhang, H., Zhao, Y., Yang, B., Jiang, X., & Wan, J. (2019). Genome-wide associated study identifies NAC42-activated nitrate transporter conferring high nitrogen use efficiency in rice. Nature Communications. https://doi.org/10.1038/s41467-019-13187-1
Tang, Z., Fan, X., Li, Q., Feng, H., Miller, A. J., Shen, Q., & Xu, G. (2012). Knockdown of a rice stelar nitrate transporter alters long-distance translocation but not root influx. Plant Physiology., 160, 2052–2063. https://doi.org/10.1104/pp.112.204461
Taylor, M. R., Reinders, A., & Ward, J. M. (2015). Transport function of rice amino acid permeases (AAPs). Plant and Cell Physiology, 56(7), 1355–1363. https://doi.org/10.1093/pcp/pcv053
Tegeder, M., & Rentsch, D. (2010). Uptake and partitioning of amino acids and peptides. Molecular Plant, 3(6), 997–1011. https://doi.org/10.1093/mp/ssq047
The, S. V., Snyder, R., & Tegeder, M. (2021). Targeting nitrogen metabolism and transport processes to improve plant nitrogen use efficiency. Frontiers in Plant Science, 11, 628366. https://doi.org/10.3389/fpls.2020.628366
Tiong, J., Sharma, N., Sampath, R., MacKenzie, N., Watanabe, S., Metot, C., Lu, Z., Skinner, W., Lu, Y., Kridl, J., Baumann, U., Heuer, S., Kaiser, B., & Okamoto, M. (2021). Improving nitrogen use efficiency through overexpression of alanine aminotransferase in rice, wheat, and barley. Frontiers in Plant Science, 12, 628521. https://doi.org/10.3389/fpls.2021.628521
Udvardi, M., Below, F. E., Castellano, M. J., Eagle, A. J., Giller, K. E., Ladha, J. K., Liu, X., Maaz, T. M. C., Nova-Franco, B., Raghuram, N., Robertson, G. P., Roy, S., Saha, M., Schmidt, S., Tegeder, M., York, L. M., & Peters, J. W. (2021). A research road map for responsible use of agricultural nitrogen. Frontiers in Sustainable Food Systems. https://doi.org/10.3389/fsufs.2021.660155
Vinod, K. K., & Heuer, S. (2012). Approaches towards nitrogen- and phosphorus-efficient rice. Annals of Botany Plants. https://doi.org/10.1093/aobpla/pls028
Wang, D., Xu, T., Yin, Z., Wu, W., Geng, H., Li, L., et al. (2020a). Overexpression of OsMYB305 in rice enhances the nitrogen uptake under low-nitrogen condition. Frontiers in Plant Science. https://doi.org/10.3389/FPLS.2020.00369
Wang, J., Lu, K., Nie, H., Zeng, Q., Wu, B., Qian, J., & Fang, Z. (2018a). Rice nitrate transporter OsNPF72 positively regulates tiller number and grain yield. Rice, 11(1), 1–13. https://doi.org/10.1186/S12284-018-0205-6
Wang, J., Wu, B., Lu, K., Wei, Q., Qian, J., Chen, Y., & Fang, Z. (2019). The Amino Acid Permease 5 (OsAAP5) regulates tiller number and grain yield in rice. Plant Physiology, 180, 1031–1045. https://doi.org/10.1104/pp.19.00034
Wang, Q., Su, Q., Nian, J., Zhang, J., Guo, M., Dong, G., et al. (2021a). The Ghd7 transcription factor represses ARE1 expression to enhance nitrogen utilization and grain yield in rice. Molecular Plant, 14(6), 1012–1023. https://doi.org/10.1016/J.MOLP.2021.04.012
Wang, Q., Su, Q., Nian, J., Zhang, J., Guo, M., Dong, G., Hu, J., Wang, R., Wei, C., Li, G., Wang, W., Guo, H. S., Lin, S., Qian, W., Xie, X., Qian, Q., Chen, F., & Zuo, J. (2021b). The Ghd7 transcription factor represses ARE1 expression to enhance nitrogen utilization and grain yield in rice. Molecular Plant., 14, 1012–1023.
Wang, S., Chen, A., Xie, K., Yang, X., Luo, Z., Chen, J., Zeng, D., Ren, Y., Yang, C., Wang, L., Feng, H., Lizbeth López-Arredondo, D., Rafael Herrera-Estrella, L., Xu, G., Gojon, A., Harrison, M. J., & Wang, E. (2020b). Functional analysis of the OsNPF4.5 nitrate transporter reveals a conserved mycorrhizal pathway of nitrogen acquisition in plants. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.2000926117
Wang, W. H., Köhler, B., Cao, F. Q., Liu, G. W., Gong, Y. Y., Sheng, S., Song, Q. C., Cheng, X. Y., Garnett, T., Okamoto, M., Qin, R., Mueller-Roeber, B., Tester, M., & Liu, L. H. (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(2), 432–444. https://doi.org/10.1111/j.1469-8137.2011.03929.x
Wang, W., Hu, B., Yuan, D., Liu, Y., Che, R., Hu, Y., et al. (2018b). Expression of the nitrate transporter gene OsNRT1.1A/OsNPF6.3 confers high yield and early maturation in rice. The Plant Cell, 30(3), 638–651. https://doi.org/10.1105/TPC.17.00809
Wang, W., Hu, B., Yuan, D., Liu, Y., Che, R., Hu, Y., Ou, S., Liu, Y., Zhang, Z., Wang, H., & Li, H. (2018c). Expression of the nitrate transporter gene OsNRT1.1A/OsNPF6.3 confers high yield and early maturation in rice. The Plant Cell, 30(3), 638–651. https://doi.org/10.1105/tpc.17.00809
Wei, J., Zheng, Y., Feng, H., Qu, H., Fan, X., Yamaji, N., Ma, J. F., & Xu, G. (2018). OsNRT2.4 encodes a dual-affinity nitrate transporter and functions in nitrate-regulated root growth and nitrate distribution in rice. Journal of Experimental Botany, 69(5), 1095–1107. https://doi.org/10.1093/jxb/erx486
Wu, J., Zhang, Z. S., Xia, J. Q., Alfatih, A., Song, Y., Huang, Y. J., Wan, G. Y., Sun, L. Q., Tang, H., Liu, Y., Wang, S. M., Zhu, Q. S., Qin, P., Wang, Y. P., Li, S. G., Mao, C. Z., Zhang, G. Q., Chu, C., Yu, L. H., & Xiang, C. B. (2021). Rice NIN-LIKE PROTEIN 4 plays a pivotal role in nitrogen use efficiency. Plant Biotechnology Journal, 19(3), 448–461. https://doi.org/10.1111/pbi.13475
Wu, Y., Yang, W., Wei, J., Yoon, H., & An, G. (2017). Transcription Factor OsDOF18 controls ammonium uptake by inducing ammonium transporters in rice roots. Molecules and Cells, 40(3), 178–185. https://doi.org/10.14348/molcells.2017.2261
Xia, X., Fan, X., Wei, J., Feng, H., Qu, H., Xie, D., Miller, A. J., & Xu, G. (2015a). Rice nitrate transporter OsNPF2.4 functions in low-affinity acquisition and long-distance transport. Journal of Experimental Botany, 66(1), 317–331. https://doi.org/10.1093/jxb/eru425
Xia, Y., DeBolt, S., Dreyer, J., Scott, D., & Williams, M. A. (2015b). Characterization of culturable bacterial endophytes and their capacity to promote plant growth from plants grown using organic or conventional practices. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2015.00490
Xu, G., Fan, X., & Miller, A. J. (2012). Plant nitrogen assimilation and use efficiency. Annual Review in Plant Biology., 63, 153–182. https://doi.org/10.1146/annurev-arplant-042811-105532
Yamaya, T., & Kusano, M. (2014). Evidence supporting distinct functions of three cytosolic glutamine synthetases and two NADH-glutamate synthases in rice. Journal of Experimental Botany, 65(19), 5519–5525. https://doi.org/10.1093/jxb/eru103
Yan, M., Fan, X., Feng, H., Miller, A. J., Shen, Q., & Xu, G. (2011). Rice OsNAR2.1 interacts with OsNRT2.1, OsNRT2.2 and OsNRT2.3 a nitrate transporters to provide uptake over high and low concentration ranges. Plant Cell Environment, 34, 1360–1372. https://doi.org/10.1111/j.1365-3040.2011.02335.x
Yang, X., Nian, J., Xie, Q., Feng, J., Zhang, F., Jing, H., Zhang, J., Dong, G., Liang, Y., Peng, J., Wang, G., Qian, Q., & Zuo, J. (2016). Rice ferredoxin-dependent glutamate synthase regulates nitrogen-carbon metabolomes and is genetically differentiated between japonica and indica subspecies. Molecular Plant, 9(11), 1520–1534. https://doi.org/10.1016/j.molp.2016.09.004
Yu, J., Xuan, W., Tian, Y., Fan, L., Sun, J., Tang, W., Chen, G., Wang, B., Liu, Y., Wu, W., Liu, X., Jiang, X., Zhou, C., Dai, Z., Xu, D., Wang, C., & Wan, J. (2021a). Enhanced OsNLP4-OsNiR cascade confers nitrogen use efficiency by promoting tiller number in rice. Plant Biotechnology Journal, 19(1), 167–176. https://doi.org/10.1111/pbi.13450
Yu, J., Xuan, W., Tian, Y., Fan, L., Sun, J., Tang, W., Chen, G., Wang, B., Liu, Y., Wu, W., & Liu, X. (2021b). Enhanced OsNLP4-OsNiR cascade confers nitrogen use efficiency by promoting tiller number in rice. Plant Biotechnology Journal, 19(1), 167–176. https://doi.org/10.1111/pbi.13450
Yu, J., Zhen, X., Li, X., Li, N., & Xu, F. (2019). Increased autophagy of rice can increase yield and nitrogen use efficiency (NUE). Frontiers in Plant Science. https://doi.org/10.3389/FPLS.2019.00584
Zamani-Nour, S., Lin, H. C., Walker, B. J., Mettler-Altmann, T., Khoshravesh, R., Karki, S., Bagunu, E., Sage, T. L., Quick, W. P., & Weber, A. P. (2021). Overexpression of the chloroplastic 2-oxoglutarate/malate transporter disturbs carbon and nitrogen homeostasis in rice. Journal of Experimental Botany, 72(1), 137–152. https://doi.org/10.1093/jxb/eraa343
Zeng, D. D., Qin, R., Li, M., Alamin, M., Jin, X. L., Liu, Y., & Shi, C. H. (2017). The ferredoxin-dependent glutamate synthase (OsFd-GOGAT) participates in leaf senescence and the nitrogen remobilization in rice. Molecular Genetics and Genomics, 292(2), 385–395. https://doi.org/10.1007/s00438-016-1275-z
Zhang, J., Zhou, Z., Bai, J., Tao, X., Wang, L., Zhang, H., & Zhu, J. K. (2020). Disruption of MIR396e and MIR396f improves rice yield under nitrogen-deficient conditions. National Science Review, 7(1), 102–112. https://doi.org/10.1093/nsr/nwz142
Zhang, M., Wang, Y., Chen, X., Xu, F., Ding, M., Ye, W., Kawai, Y., Toda, Y., Hayashi, Y., Suzuki, T., Zeng, H., Xiao, L., Xiao, X., Xu, J., Guo, S., Yan, F., Shen, Q., Xu, G., Kinoshita, T., & Zhu, Y. (2021). Plasma membrane H+-ATPase overexpression increases rice yield via simultaneous enhancement of nutrient uptake and photosynthesis. Nature Communications. https://doi.org/10.1038/s41467-021-20964-4
Zhen, X., Li, X., Yu, J., & Xu, F. (2019a). OsATG8c-mediated increased autophagy regulates the yield and nitrogen use efficiency in rice. International Journal of Molecular Sciences, 20(19), 4956. https://doi.org/10.3390/IJMS20194956
Zhen, X., Xu, F., Zhang, W., Li, N., & Li, X. (2019b). Overexpression of rice gene OsATG8b confers tolerance to nitrogen starvation and increases yield and nitrogen use efficiency (NUE) in Arabidopsis. PLoS ONE. https://doi.org/10.1371/journal.pone.0223011
Zhen, X., Zheng, N., Yu, J., Bi, C., & Xu, F. (2021). Autophagy mediates grain yield and nitrogen stress resistance by modulating nitrogen remobilization in rice. PLoS ONE, 16(1), e0244996. https://doi.org/10.1371/JOURNAL.PONE.0244996
Zheng, Z. L. (2009). Carbon and nitrogen nutrient balance signaling in plants. Plant Signaling and Behavior, 4(7), 584–591. https://doi.org/10.4161/psb.4.7.8540
Zhou, Y., Cai, H., Xiao, J., Li, X., Zhang, Q., & Lian, X. (2009). Over-expression of aspartate aminotransferase genes in rice resulted in altered nitrogen metabolism and increased amino acid content in seeds. Theoretical and Applied Genetics, 118(7), 1381–1390. https://doi.org/10.1007/s00122-009-0988-3
Zhou, Y., Zhang, C., Lin, J., Yang, Y., Peng, Y., Tang, D., Zhao, X., Zhu, Y., & Liu, X. (2015). Over-expression of a glutamate dehydrogenase gene, MgGDH, from Magnaporthe grisea confers tolerance to dehydration stress in transgenic rice. Planta, 241(3), 727–740. https://doi.org/10.1007/s00425-014-2214-z
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The authors acknowledge the funding agencies viz., NICRA, NEWS and SANH for providing grants and to the Director for providing research facilities.
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National Initiative on Climate Resilient Agriculture (NICRA), Indian Council of Agricultural Research (ICAR), Ministry of Agriculture, Govt. of India, 2. Indo-UK Virtual Centre on Nitrogen Efficiency of Whole cropping Systems (NEWS) BT/IN/UK-VNC/44/NR/2015-16 and 3. UKRI GCRF South Asian Nitrogen Hub (SANH) (NE/S009019/1).
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Neeraja, C.N., Barbadikar, K.M., Mangrauthia, S.K. et al. Genes for NUE in rice: a way forward for molecular breeding and genome editing. Plant Physiol. Rep. 26, 587–599 (2021). https://doi.org/10.1007/s40502-021-00632-x
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DOI: https://doi.org/10.1007/s40502-021-00632-x