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Genetic modification of rice for efficient nitrogen utilization

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Abstract

Rice is a major crop worldwide, providing staple nourishment to half the global population. Improvements in rice productivity are essential to meet the needs of the growing global population. Rice productivity relies heavily on nitrogen (N) fertilization as N is crucial for rice growth and development and is the major limiting factor in most agricultural practices. However, excessive reliance on N fertilizer has adverse environmental impacts and increases production costs. Enhancing nitrogen use efficiency (NUE) is an urgent challenge in sustainable agriculture. This review summarizes the current understanding of N metabolism in rice and outlines the genetic modification of genes associated with N uptake and transport, assimilation, remobilization, and regulation to improve NUE. Recent research into NUE efficiency will facilitate the practical development of novel rice lines with increased productivity alongside low inputs of N fertilization.

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References

  • Alfatih A, Wu J, Zhang ZS, Xia JQ, Jan SU, Yu LH, Xiang CB (2020) Rice NIN-LIKE PROTEIN 1 rapidly responds to nitrogen deficiency and improves yield and nitrogen use efficiency. J Exp Bot 71:6032–6042

    Article  CAS  PubMed  Google Scholar 

  • Anas M, Liao F, Verma KK, Sarwar MA, Mahmood A, Chen ZL, Li Q, Zeng XP, Liu Y, Li YR (2020) Fate of nitrogen in agriculture and environment: agronomic, eco-physiological and molecular approaches to improve nitrogen use efficiency. Biol Res 53:47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bao A, Liang Z, Zhao Z, Cai H (2015) Overexpressing of OsAMT1-3, a High Affinity Ammonium Transporter Gene, Modifies Rice Growth and Carbon-Nitrogen Metabolic Status. Int J Mol Sci 16:9037–9063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bao A, Zhao Z, Ding G, Shi L, Xu F, Cai H (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:e95581

  • Bhattacharya A (2019) Chapter 4 - Nitrogen-Use Efficiency Under Changing Climatic Conditions. In: Bhattacharya A (ed) Changing Climate and Resource Use Efficiency in Plants. Academic Press, London, pp 181–240

    Chapter  Google Scholar 

  • Bu Y, Takano T, Nemoto K, Liu S (2011) Research progress of ammonium transporter in rice plants. Genomics Appl Biol 2:19–23

    Google Scholar 

  • Chen L, Liao H (2017) Engineering crop nutrient efficiency for sustainable agriculture. J Integr Plant Biol 59:710–735

    Article  PubMed  Google Scholar 

  • Chen J, Zhang Y, Tan Y, Zhang M, Zhu L, Xu G, Fan X (2016) Agronomic nitrogen-use efficiency of rice can be increased by driving OsNRT2.1 expression with the OsNAR2.1 promoter. Plant Biotechnol J 14:1705–1715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Biotechnol J 15:1273–1283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen KE, Chen HY, Tseng CS, Tsay YF (2020) Improving nitrogen use efficiency by manipulating nitrate remobilization in plants. Nat Plants 6:1126–1135

    Article  CAS  PubMed  Google Scholar 

  • Dawar K, Zaman M, Rowarthc JS, Blennerhassett J, Turnbull MH (2011) Urease inhibitor reduces N losses and improves plant-bioavailability of urea applied in fine particle and granular forms under field conditions. Agric Ecosyst Environ 144:41–50

    Article  CAS  Google Scholar 

  • Dellero Y (2020) Manipulating Amino Acid Metabolism to Improve Crop Nitrogen Use Efficiency for a Sustainable Agriculture. Front Plant Sci 11:602548.

  • Fan X, Tang Z, Tan Y, Zhang Y, Luo B, Yang M, Lian X, Shen Q, Miller AJ, Xu G (2016) Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. Proc Natl Acad Sci USA 113:7118–7123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan T, Yang W, Zeng X, Xu X, Xu Y, Fan X, Luo M, Tian C, Xia K, Zhang M (2020) A Rice Autophagy gene OsATG8b is involved in nitrogen remobilization and control of grain quality. Front Plant Sci 11:588

    Article  PubMed  PubMed Central  Google Scholar 

  • Fang Z, Xia K, Yang X, Grotemeyer MS, 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 Biotechnol J 11:446–458

    Article  CAS  PubMed  Google Scholar 

  • 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 14:2

    Article  PubMed  PubMed Central  Google Scholar 

  • 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. Front Plant Sci 8:1338

  • FAO (2021) Food and Agriculture Organization of the United Nations, Rome. http://www.fao.org/faostat/en/#data/OA

  • 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 Cell Physiol 54:934–943

    Article  CAS  PubMed  Google Scholar 

  • Gao Z, Wang Y, Chen G, Zhang A, Yang S, Shang L, Wang D, Ruan B, Liu C, Jiang H, Dong G, Zhu L, Hu J, Zhang G, Zeng D, Guo L, Xu G, Teng S, Harberd NP, Qian Q (2019) The indica nitrate reductase gene OsNR2 allele enhances rice yield potential and nitrogen use efficiency. Nat Commun 10:5207

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Giovannini L, Palla M, Agnolucci M, Avio L, Sbrana C, Turrini A, Giovannetti M (2020) Arbuscular Mycorrhizal Fungi and Associated Microbiota as Plant Biostimulants: Research Strategies for the Selection of the Best Performing Inocula. Agronomy 10:106

    Article  Google Scholar 

  • Gooding MJ, Addisu M, Uppal RK, Snape JW, Jones HE (2012) Effect of wheat dwarfing genes on nitrogen-use efficiency. J Agric Sci 150:3–22

    Article  CAS  Google Scholar 

  • 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. Front Plant Sci 11:1150

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 J 103:395–411

    Article  CAS  PubMed  Google Scholar 

  • Han M, Okamoto M, Beatty PH, Rothstein SJ, Good AG (2015) The Genetics of Nitrogen Use Efficiency in Crop Plants. Annu Rev Genet 49:269–289

    Article  CAS  PubMed  Google Scholar 

  • Hawkesford MJ, Griffiths S (2019) Exploiting genetic variation in nitrogen use efficiency for cereal crop improvement. Curr Opin Plant Biol 49:35–42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi H, Chino M (1990) Chemical composition of phloem sap from the upper most internode of the rice plant. Plant Cell Physiol 31:247–251

    CAS  Google Scholar 

  • Hirel B, Le Gouis J, Ney B (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. J Exp Bot 58:2369–2387

    Article  CAS  PubMed  Google Scholar 

  • Hirel B, Tétu T, Lea PJ, Dubois F (2011) Improving Nitrogen Use Efficiency in Crops for Sustainable Agriculture. Sustainability 3:1452–1485

    Article  CAS  Google Scholar 

  • 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. Nat Genet 47:834–838

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Zhao C, Zhang Y, Wang C (2017) Nitrogen use efficiency in rice. In: Fahad S (ed) Amanullah. Nitrogen in Agriculture-Updates. IntechOpen, London, pp 188–208

    Google Scholar 

  • 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. Front Plant Sci 9:300

  • IFA (2021) International Fertilizer Association, Paris. https://www.ifastat.org/databases/graph/1_1

  • Iwamoto M, Tagiri A (2016) MicroRNA-targeted transcription factor gene RDD1 promotes nutrient ion uptake and accumulation in rice. Plant J 85:466–477

    Article  CAS  PubMed  Google Scholar 

  • Jagadhesan B, Sathee L, Meena HS, Jha SK, Chinnusamy V, Kumar A, Kumar S (2020) Genome wide analysis of NLP transcription factors reveals their role in nitrogen stress tolerance of rice. Sci Rep 10:9368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. J Exp Bot 71:4763–4777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim HS, Kwak SS (2020) Crop biotechnology for sustainable agriculture in the face of climate crisis. Plant Biotechnol Rep 14:139–141

    Article  Google Scholar 

  • Kim SG, Wang Y, Wu J, Kang KY, Kim ST (2011) Physiological and proteomic analysis of young rice leaves grown under nitrogen-starvation conditions. Plant Biotechnol Rep 5:309–315

    Article  Google Scholar 

  • Ladha JK, Tirol-Padre A, Reddy CK, Cassman KG, Verma S, Powlson DS, van Kessel C, de B Richter D, Chakraborty D, Pathak H, (2016) Global nitrogen budgets in cereals: A 50-year assessment for maize, rice and wheat production systems. Sci Rep 6:19355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lammerts van Bueren ET, Struik PC (2017) Diverse concepts of breeding for nitrogen use efficiency. A Review Agron Sustain Dev 37:50

    Article  CAS  Google Scholar 

  • Lee S, Marmagne A, Park J, Fabien C, Yim Y, Kim SJ, Kim TH, Lim PO, Masclaux-Daubresse C, Nam HG (2020a) Concurrent activation of OsAMT1;2 and OsGOGAT1 in rice leads to enhanced nitrogen use efficiency under nitrogen limitation. Plant J 103:7–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S, Park J, Lee J, Shin D, Marmagne A, Lim PO, Masclaux-Daubresse C, An G, Nam HG (2020b) OsASN1 Overexpression in Rice Increases Grain Protein Content and Yield under Nitrogen-Limiting Conditions. Plant Cell Physiol 61:1309–1320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Kronzucker HJ, Shi W (2016) Microprofiling of nitrogen patches in paddy soil: Analysis of spatiotemporal nutrient heterogeneity at the microscale. Sci Rep 6:27064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Hu B, Chu C (2017) Nitrogen use efficiency in crops: lessons from Arabidopsis and rice. J Exp Bot 68:2477–2488

    Article  CAS  PubMed  Google Scholar 

  • Li S, Tian Y, Wu K, Ye Y, Yu J, Zhang J, Liu Q, Hu M, Li H, Tong Y, Harberd NP, Fu X (2018) Modulating plant growth-metabolism coordination for sustainable agriculture. Nature 560:595–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Wang T, Gong J (2020a) Alternative Strategies Toward Sustainable Ammonia Synthesis. Trans Tianjin Univ 26:67–91

    Article  CAS  Google Scholar 

  • Li M, Xu J, Gao Z, Tian H, Gao Y, Kariman K (2020b) Genetically modified crops are superior in their nitrogen use efficiency-A meta-analysis of three major cereals. Sci Rep 10:8568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Ouyang J, Wang YY, Hu R, Xia K, Duan J, Wang Y, Tsay YF, Zhang M (2015) Disruption of the rice nitrate transporter OsNPF2.2 hinders root-to-shoot nitrate transport and vascular development. Sci Rep 5:9635

  • Liu Y, Wang H, Jiang Z, Wang W, Xu R, Wang Q, Zhang Z, Li A, Liang Y, Ou S, Liu X, Cao S, Tong H, Wang Y, Zhou F, Liao H, Hu B, Chu C (2021) Genomic basis of geographical adaptation to soil nitrogen in rice. Nature 590:600–605

    Article  CAS  PubMed  Google Scholar 

  • Loss Sperandio MV, Santos LA, Huertas Tavares OC, Fernandes MS, de Freitas Lima M, de Souza SR (2020) Silencing the Oryza sativa plasma membrane H+-ATPase isoform OsA2 affects grain yield and shoot growth and decreases nitrogen concentration. J Plant Physiol 251:153220

  • Lu K, Wu B, Wang J, Zhu W, Nie H, Qian J, Huang W, Fang Z (2018) Blocking amino acid transporter OsAAP3 improves grain yield by promoting outgrowth buds and increasing tiller number in rice. Plant Biotechnol J 16:1710–1722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masclaux-Daubresse C, Chen Q, Havé M (2017) Regulation of nutrient recycling via autophagy. Curr Opin Plant Biol 39:8–17

    Article  CAS  PubMed  Google Scholar 

  • McAllister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: the current status. Plant Biotechnol J 10:1011–1125

    Article  CAS  PubMed  Google Scholar 

  • Ohashi M, Ishiyama K, Kojima S, Konishi N, Nakano K, Kanno K, Hayakawa T, Yamaya T (2015) Asparagine synthetase1, but not asparagine synthetase2, is responsible for the biosynthesis of asparagine following the supply of ammonium to rice roots. Plant Cell Physiol 56:769–778

    Article  CAS  PubMed  Google Scholar 

  • Okumoto S, Pilot G (2011) Amino acid export in plants: a missing link in nitrogen cycling. Mol Plant 4:453–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perchlik M, Tegeder M (2017) Improving Plant Nitrogen Use Efficiency through Alteration of Amino Acid Transport Processes. Plant Physiol 175:235–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ranathunge K, El-Kereamy A, Gidda S, Bi YM, Rothstein SJ (2014) AMT1;1 transgenic rice plants with enhanced NH4+ permeability show superior growth and higher yield under optimal and suboptimal NH4+ conditions. J Exp Bot 65:965–979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selvaraj MG, Valencia MO, Ogawa S, Lu Y, Wu L, Downs C, Skinner W, Lu Z, Kridl JC, Ishitani M, van Boxtel J (2017) Development and field performance of nitrogen use efficient rice lines for Africa. Plant Biotechnol J 15:775–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma V, Gupta P, Priscilla K, SharanKumar HB, Veershetty A, Ramrao DP, Suresh S, Narasanna R, Naik GR, Kumar A, Guo B, Zhuang W, Varshney RK, Pandey MK, Kumar R (2021) Metabolomics Intervention Towards Better Understanding of Plant Traits. Cells 10:346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG (2008) Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol J 6:722–732

    Article  CAS  PubMed  Google Scholar 

  • Sun H, Qian Q, Wu K, Luo J, Wang S, Zhang C, Ma Y, Liu Q, Huang X, Yuan Q, Han R, Zhao M, Dong G, Guo L, Zhu X, Gou Z, Wang W, Wu Y, Lin H, Fu X (2014) Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet 46:652–656

    Article  CAS  PubMed  Google Scholar 

  • 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 J 42:641–651

    Article  CAS  PubMed  Google Scholar 

  • 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 39:1003–1012

    Article  CAS  PubMed  Google Scholar 

  • 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. Front Plant Sci 2:57

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, Peng C, Zhou C, Terzaghi W, Wang C, Wan J (2019) Genome-wide associated study identifies NAC42-activated nitrate transporter conferring high nitrogen use efficiency in rice. Nat Commun 10:5279

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tegeder M (2012) Transporters for amino acids in plant cells: some functions and many unknowns. Curr Opin Plant Biol 15:315–321

    Article  CAS  PubMed  Google Scholar 

  • Tegeder M, Masclaux-Daubresse C (2018) Source and sink mechanisms of nitrogen transport and use. New Phytol 217:35–53

    Article  PubMed  Google Scholar 

  • Tegeder M, Ruan YL, Patrick JW (2013) Roles of membrane transporters in phloem functions. In: Thompson G, Van Bel A (eds) Biochemistry of Phloem. Wiley-Blackwell, Oxford, pp 63–101

    Google Scholar 

  • The SV, Snyder R, Tegeder M (2021) Targeting Nitrogen Metabolism and Transport Processes to Improve Plant Nitrogen Use Efficiency. Front Plant Sci 11:628366

  • Thomsen HC, Eriksson D, Møller IS, Schjoerring JK (2014) Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency? Trends Plant Sci 19:656–663

    Article  CAS  PubMed  Google Scholar 

  • 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. Front Plant Sci 12: 628521

  • Ueda Y, Konishi M, Yanagisawa S (2017) Molecular basis of the nitrogen response in plants. Soil Sci Plant Nutr 63:329–341

    Article  CAS  Google Scholar 

  • Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17:458–467

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Nian J, Xie X, Yu H, Zhang J, Bai J, Dong G, Hu J, Bai B, Chen L, Xie Q, Feng J, Yang X, Peng J, Chen F, Qian Q, Li J, Zuo J (2018b) Genetic variations in ARE1 mediate grain yield by modulating nitrogen utilization in rice. Nat Commun 9:735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang W, Hu B, Yuan D, Liu Y, Che R, Hu Y, Ou S, Liu Y, Zhang Z, Wang H, Li H, Jiang Z, Zhang Z, Gao X, Qiu Y, Meng X, Liu Y, Bai Y, Liang Y, Wang Y, Zhang L, Li L, Sodmergen JH, Li J, Chu C (2018c) Expression of the nitrate transporter gene OsNRT1.1A/OsNPF6.3 confers high yield and early maturation in rice. Plant Cell 30:638–651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Physiol 180:1031–1045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Chen A, Xie K, Yang X, Luo Z, Chen J, Zeng D, Ren Y, Yang C, Wang L, Feng H, López-Arredondo DL, Herrera-Estrella LR, Xu G (2020) Functional analysis of the OsNPF4.5 nitrate transporter reveals a conserved mycorrhizal pathway of nitrogen acquisition in plants. Proc Natl Acad Sci U S A 117:16649–16659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Su Q, Nian J, Zhang J, Guo M, Dong G, Hu J, Wang R, Wei C, Li G, Wang W, Guo HS, Lin S, Qian W, Xie X, Qian Q, Chen F, Zuo J (2021) The Ghd7 transcription factor represses ARE1 expression to enhance nitrogen utilization and grain yield in rice. Mol Plant 14:1012–1023

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Lu K, Nie H, Zeng Q, Wu B, Qian J, Fang Z (2018a) Rice nitrate transporter OsNPF7.2 positively regulates tiller number and grain yield. Rice 11:12

  • Witte CP (2011) Urea metabolism in plants. Plant Sci 180:431–438

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Zhang ZS, Xia JQ, Alfatih A, Song Y, Huang YJ, Wan GY, Sun LQ, Tang H, Liu Y, Wang SM, Zhu QS, Qin P, Wang YP, Li SG, Mao CZ, Zhang GQ, Chu C, Yu LH, Xiang CB (2021) Rice NIN-LIKE PROTEIN 4 plays a pivotal role in nitrogen use efficiency. Plant Biotechnol J 19:448–461

    Article  CAS  PubMed  Google Scholar 

  • Wu K, Wang S, Song W, Zhang J, Wang Y, Liu Q, Yu J, Ye Y, Li S, Chen J, Zhao Y, Wang J, Wu X, Wang M, Zhang Y, Liu B, Wu Y, Harberd NP, Fu X (2020) Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice. Science 367:eaaz2046

  • Xia X, Fan X, Wei J, Feng H, Qu H, Xie D, Miller AJ, Xu G (2015) Rice nitrate transporter OsNPF2.4 functions in low-affinity acquisition and long-distance transport. J Exp Bot 66:317–331

    Article  CAS  PubMed  Google Scholar 

  • Xiaochuang C, Meiyan W, Chunquan Z, Chu Z, Junhua Z, Lianfeng Z, Lianghuan W, Qianyu J (2020) Glutamate dehydrogenase mediated amino acid metabolism after ammonium uptake enhances rice growth under aeration condition. Plant Cell Rep 39:363–379

    Article  PubMed  CAS  Google Scholar 

  • Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182

    Article  CAS  PubMed  Google Scholar 

  • Xu C, Chen L, Chen S, Chu G, Wang DY, Zhang XF (2020) Rhizosphere aeration improves nitrogen transformation in soil, and nitrogen absorption and accumulation in rice plants. Rice Sci 27:162–174

    Article  Google Scholar 

  • Yadav MR, Kumar R, Parihar CM, Yadav RK, Jat SL, Ram H, Meena RK, Singh M, Birbal VAP, Kumar U, Ghosh A, Jat ML (2017) Strategies for improving nitrogen use efficiency: A review. Agric Rev 38:29–40

    Google Scholar 

  • Yamaya T, Kusano M (2014) Evidence supporting distinct functions of three cytosolic glutamine synthetases and two NADH-glutamate synthases in rice. J Exp Bot 65:5519–5525

    Article  CAS  PubMed  Google Scholar 

  • Yang HC, Kan CC, Hung TH, Hsieh PH, Wang SY, Hsieh WY, Hsieh MH (2017) Identification of early ammonium nitrate-responsive genes in rice roots. Sci Rep 7:16885

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang G, Wei Q, Huang H, Xia J (2020) Amino Acid Transporters in Plant Cells: A Brief Review. Plants 9:967

    Article  CAS  PubMed Central  Google Scholar 

  • 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. Rice Ferredoxin-Dependent Glutamate Synthase Regulates Nitrogen-Carbon Metabolomes and Is Genetically Differentiated between japonica and indica Subspecies. Mol Plant 29:1520–1534

  • Yu J, Zhen X, Li X, Li N, Xu F (2019) Increased Autophagy of Rice Can Increase Yield and Nitrogen Use Efficiency (NUE). Front Plant Sci 10:584

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng DD, Qin R, Li M, Alamin M, Jin XL, Liu Y, Shi CH (2017) The ferredoxin-dependent glutamate synthase (OsFd-GOGAT) participates in leaf senescence and the nitrogen remobilization in rice. Mol Genet Genomics 292:385–395

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Davidson EA, Mauzerall DL, Searchinger TD, Dumas P, Shen Y (2015) Managing nitrogen for sustainable development. Nature 528:51–59

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Zhang Y, Li K, Yan M, Zhang J, Yu M, Tang S, Wang L, Qu H, Luo L, Xuan W, Xu G (2021a) Nitrogen Mediates Flowering Time and Nitrogen Use Efficiency via Floral Regulators in Rice. Curr Biol 31:671-683.e5

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZS, Xia JQ, Alfatih A, Song Y, Huang YJ, Sun LQ, Wan GY, Wang SM, Wang YP, Hu BH, Zhang GH, Qin P, Li, SG, Yu LH, Wu J, Xiang CB (2021b) Rice NIN-LIKE PROTEIN 3 plays a significant role in nitrogen use efficiency and grain yield under nitrate-sufficient conditions. bioRxiv. https://doi.org/10.1101/2021.02.19.432039

  • Zhen X, Li X, Yu J, Xu F (2019) OsATG8c-mediated increased autophagy regulates the yield and nitrogen use efficiency in rice. Int J Mol Sci 20:4956

    Article  CAS  PubMed Central  Google Scholar 

  • 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:e0244996

  • 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. Theor Appl Genet 118:1381–1390

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was funded by the Institute for Basic Science (IBS-R013-D1) from the Ministry of Science, ICT & Future Planning.

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SL wrote the manuscript with JP and YY. All authors reviewed and approved the final manuscript.

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Correspondence to Sichul Lee.

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Lee, S., Park, J. & Yim, Y. Genetic modification of rice for efficient nitrogen utilization. Plant Biotechnol Rep 15, 573–583 (2021). https://doi.org/10.1007/s11816-021-00705-1

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