Responses of cereals to nitrogen deficiency: Adaptations on  morphological, physiological, biochemical, hormonal and genetic basis

D Shanmugapriya; A Senthil; M Raveendran; M Djanaguiraman; K Anitha; V Ravichandran; R Pushpam; S Marimuthu

doi:10.14719/pst.6367

Authors

D Shanmugapriya Department of Crop Physiology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0009-0004-8608-1872
A Senthil Department of Crop Physiology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0002-6438-8935
M Raveendran Department of Biotechnology, Tamil Nadu Agricultural University, Coimbatore 641 003, India
M Djanaguiraman Department of Crop Physiology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0002-8803-7662
K Anitha Department of Crop Physiology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0001-6589-105X
V Ravichandran Department of Crop Physiology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0002-6447-6417
R Pushpam Department of Forage crops, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0001-6991-6090
S Marimuthu Department of Agricultural Nanotechnology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0002-5534-1246

DOI:

https://doi.org/10.14719/pst.6367

Keywords:

adaptations, food security, low nitrogen, nitrogen use efficiency, productivity, sustainable agriculture

Abstract

Nitrogen (N) is a primary macronutrient essential for plant growth and development. Global nitrogen fertilizer consumption is approximately 120 million tons, with nitrogen use efficiency (NUE) ranging between 25 % and 50 %. Excessive use of nitrogen fertilizer poses significant risks to the envi ronment and living organisms, highlighting the need to reduce fertilizer ap plication, improve NUE, and sustain crop productivity. Sustainable agricul tural practices emphasize minimizing fertilizer usage. Therefore, developing high-NUE crop varieties capable of maintaining yields under reduced nitro gen input is critical for ensuring food security and protecting ecosystem. A promising strategy involves investigating plant responses to varying nitro gen levels, particularly under low-nitrogen conditions. This review explores the morphological, physiological, biochemical, hormonal, and genetic changes in cereals subjected to low-nitrogen conditions. Morphological adaptations include alterations in root and shoot architecture, while physi ological responses involve enhanced chlorophyll content, leaf nitrogen lev els, and photosynthetic efficiency. Biochemical changes are characterized by increased activity of nitrogen uptake and assimilation enzymes, accom panied by hormonal shifts such as elevated auxin levels in roots. These traits provide a foundation for developing nitrogen-efficient crop varieties. Future research should prioritize breeding crops with enhanced tolerance to low-nitrogen conditions to improve NUE, grain quality, and yield potential.

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References

Zahoor Z, Waqar AWA, Hira K, Ullah B, Khan A, Shah Z, et al. Role of nitrogen fertilizer in crop productivity and environmental pollution. Int J Agri Forestry. 2014;4(3):201–06. https://doi.org/10.5923/j.ijaf.20140403.09

Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S. Agricultural sustainability and intensive production practices. Nature. 2002;418(6898):671–77. https://doi.org/10.1038/nature01014

Ladha JK, Pathak H, Krupnik TJ, Six J, van Kessel C. Efficiency of fertilizer nitrogen in cereal production: retrospects and prospects. Advances in Agronomy. 2005;87:85–156. https://doi.org/10.1016/S0065-2113(05)87003-8

Statista. Paddy rice production worldwide in 2022, by country; 2023. Available at: https://www.statista.com/statistics/paddy-rice-production (Accessed: 14 December 2024).

Indiastat. Area, production and productivity of rice during 2022-2023; 2023. https://www.indiastat.com/table/agriculture/selected-state-season-wise-area production -product/63808

Anonymous. World agricultural production. United States Department of Agriculture (USDA). 2023;22:3. Available: https://www.usda.gov

Fageria NK, Barbosa FMP. Nitrogen use efficiency in lowland rice genotypes. Communications in Soil Science and Plant Analysis. 2001;32(13-14):2079–89. https://doi.org/10.1081/CSS-120000270

Raun WR, Johnson GV. Improving nitrogen use efficiency for cereal production. Agronomy Journal. 1999;91(3):357–63.

Ward MH. Too much of a good thing? Nitrate from nitrogen fertilizers and cancer. Reviews on Environmental Health. 2009;24(4):357–63. https://doi.org/10.1515/REVEH.2009.24.4.357.

Ahmed M, Rauf M, Mukhtar Z, Saeed NA. Excessive use of nitrogenous fertilizers: an unawareness causing serious threats to environment and human health. Environmental Science and Pollution Research. 2017;24:26983–87. https://doi.org/10.1007/s11356-017-0589-7.

FAO. FAOSTAT. Food and Agriculture Organization of the United Nations, Rome, Italy;2009.

Chivenge P, Sharma S, Bunquin MA, Hellin J. Improving nitrogen use efficiency—a key for sustainable rice production systems. Frontiers in Sustainable Food Systems. 2021;5:737412. https://doi.org/10.3389/fsufs.2021.737412

Vijayalakshmi P, Kiran TV, Rao YV, Srikanth B, Rao IS, Sailaja B, et al. Physiological approaches for increasing nitrogen use efficiency in rice. Indian Journal of Plant Physiology. 2013;18:208–22. https://doi.org/10.1007/s40502-013-0042-y.

Ladha JK, Kirk GJ, Bennett J, Peng S, Reddy CK, Reddy PM, Singh U. Opportunities for increased nitrogen-use efficiency from improved lowland rice germplasm. Field Crops Research. 1998;56(1-2):41–71. https://doi.org/10.1016/S0378-4290(97)00123-8.

Vijayalakshmi P, Vishnukiran T, Kumari BR, Srikanth B, Rao IS, Swamy KN, et al. Biochemical and physiological characterization for nitrogen use efficiency in aromatic rice genotypes. Field Crops Research. 2015;179:132–43. https://doi.org/10.1016/j.fcr.2015.04.012.

Grindlay DJ. Review towards an explanation of crop nitrogen demand based on the optimization of leaf nitrogen per unit leaf area. The J Agri Sci. 1997;128(4):377–96.

Lemaire G, van Oosterom E, Jeuffroy MH, Gastal F, Massignam A. Crop species present different qualitative types of response to N deficiency during their vegetative growth. Field Crops Research. 2008;105(3):253–65. https://doi.org/10.1016/j.fcr.2007.10.009.

Kumar N, Mathpal B, Sharma A, Shukla A, Shankhdhar D, Shankhdhar SC. Physiological evaluation of nitrogen use efficiency and yield attributes in rice (Oryza sativa L.) genotypes under different nitrogen levels. Cereal Research Communications. 2015;43(1):166–77. https://doi.org/10.1556/crc.2014.0032.

Forde B, Lorenzo H. The nutritional control of root development. Plant and Soil. 2001;232:51–68. https://doi.org/10.1023/A:1010329902165.

Gholizadeh A, Amin MS, Anuar AR, Aimrun W. Evaluation of SPAD chlorophyll meter in two different rice growth stages and its temporal variability. European Journal of Scientific Research. 2009;37(4):591–98.

Sinclair TR. Nitrogen influence on the physiology of crop yield. In: Rabbinge R, Goudriaan J, van Keulen H, Penning de Vries FWT, van Laar HH, editors. Theoretical Production Ecology: Reflections and Prospects. Pudoc, Wageningen; 1990. p. 41–45

Zhao D, Reddy KR, Kakani VG, Reddy VR. Nitrogen deficiency effects on plant growth, leaf photosynthesis and hyperspectral reflectance properties of sorghum. European Journal of Agronomy. 2005;22(4):391–403. https://doi.org/10.1016/j.eja.2004.06.005

Abubakar AW, Manga AA, Kamara AY, Tofa AI. Physiological evaluations of maize hybrids under low nitrogen. Advances in Agriculture. 2019. https://doi.org/10.1155/2019/2624707.

Wang J, Song K, Sun L, Qin Q, Sun Y, Pan J, Xue Y. Morphological and transcriptome analysis of wheat seedlings response to low nitrogen stress. Plants. 2019;8:98. 10.3390/plants8040098.

Liu X, Yin C, Xiang L, Jiang W, Xu S, Mao Z. Transcription strategies related to photosynthesis and nitrogen metabolism of wheat in response to nitrogen deficiency. BMC Plant Biology. 2020;20:1–3. https://doi.org/10.1186/s12870-020-02662-3.

Qi Z, Ling F, Jia D, Cui J, Zhang Z, Xu C, et al. Effects of low nitrogen on seedling growth, photosynthetic characteristics and antioxidant system of rice varieties with different nitrogen efficiencies. Scientific Reports. 2023;13(1):19780. https://doi.org/10.1038/s41598-023-47260-z.

Wang Y, Wang D, Tao Z, Yang Y, Gao Z, Zhao G, Chang X. Impacts of nitrogen deficiency on wheat (Triticum aestivum L.) grain during the medium filling stage: transcriptomic and metabolomic comparisons. Frontiers in Plant Science. 2021;12:674433. https://doi.org/10.3389/fpls.2021.674433

Moller AL, Pedas PA, Andersen B, Svensson B, Schjoerring JK, Finnie C. Responses of barley root and shoot proteomes to long?term nitrogen deficiency, short?term nitrogen starvation and ammonium. Plant Cell Environment. 2011;34(12):2024–37. https://doi.org/10.1111/j.1365-3040.2011.02396.x.

Bondada BR, Syvertsen JP. Concurrent changes in net Co2 assimilation and chloroplast ultrastructure in nitrogen deficient citrus leaves. Environmental and Experimental Botany. 2005;54:41–48. 10.1016/j.envexpbot.2004.05.005.

Diaz C, Saliba-Colombani V, Loudet O, Belluomo P, Moreau L, Daniel-Vedele F, et al. Leaf yellowing and anthocyanin accumulation are two genetically independent strategies in response to nitrogen limitation in Arabidopsis thaliana. Plant and Cell Physiology. 2006;47(1):74–83. 10.1093/pcp/ pci225.

Wei S, Wang X, Shi D, Li Y, Zhang J, Liu P, et al. The mechanisms of low nitrogen induced weakened photosynthesis in summer maize (Zea mays L.) under field conditions. Plant Physiol Biochem. 2016;105:118–28. 10.1016/j.plaphy.2016.04.007.

Xin W, Zhang L, Zhang W, Gao J, Yi J, Zhen X, et al. An integrated analysis of the rice transcriptome and metabolome reveals differential regulation of carbon and nitrogen metabolism in response to nitrogen availability. Int J Mol Sci. 2019;20(9):2349. https://doi.org/10.3390/ijms20092349.

Wu YW, Qiang LI, Rong JI, Wei CH, Liu XL, Kong FL, et al. Effect of low-nitrogen stress on photosynthesis and chlorophyll fluorescence characteristics of maize cultivars with different low-nitrogen tolerances. Journal of Integrative Agriculture. 2019;18(6):1246–56. https://doi.org/10.1016/S2095-3119(18)62030-1.

Sagwal V, Kumar U, Sihag P, Singh Y, Balyan P, Singh KP. Physiological traits and expression profile of genes associated with nitrogen and phosphorous use efficiency in wheat. Molecular Biology Reports. 2023;50(6):5091–103. https://doi.org/10.1007/s11033-023-08413-5.

Zhao D, Reddy RK, Kakani VG, Read JJ, Carter GA. Corn (Zea mays L.) growth, leaf pigment concentration, photosynthesis and leaf hyperspectral reflectance properties as affected by nitrogen supply. Plant and Soil. 2003;257:205–18. https://doi.org/10.1023/A:1026233732507

Li P, Weng J, Zhang Q, Yu L, Yao Q, Chang L, Niu Q. Physiological and biochemical responses of Cucumis melo L. chloroplasts to low-phosphate stress. Frontiers in Plant Science. 2018;9:1525. https://doi.org/10.3389/fpls.2018.01525.

Zhou X, Sun C, Zhu P, Liu F. Effects of antimony stress on photosynthesis and growth of Acorus calamus. Frontiers in Plant Science. 2018;9:579. https://doi.org/10.3389/fpls.2018.00579.

Ding L, Wang KJ, Jiang GM, Biswas DK, Xu H, Li LF, Li YH. Effects of nitrogen deficiency on photosynthetic traits of maize hybrids released in different years. Annals of Botany. 2005;96(5):925–30. https://doi.org/10.1093/aob/mci244

Tantray AY, Bashir SS, Ahmad A. Low nitrogen stress regulates chlorophyll fluorescence in coordination with photosynthesis and Rubisco efficiency of rice. Physiology and Molecular Biology of Plants. 2020;26:83–94. https://doi.org/10.1007/s12298-019-00721-0.

Kovacik J, Klejdus B, Backor M. Nitric oxide signals ROS scavenger-mediated enhancement of PAL activity in nitrogen-deficient Matricaria chamomilla roots: side effects of scavengers. Free Radical Biology and Medicine. 2009;46(12):1686–93. https://doi.org/10.1016/j.freeradbiomed.2009.03.020.

Makino Y, Ueno O. Structural and physiological responses of the C4 grass Sorghum bicolor to nitrogen limitation. Plant Production Science. 2018;21(1):39–50. https://doi.org/10.1080/1343943X.2018.1432290.

Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, et al. Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature. 2006;440(7086):922–25. https://doi.org/10.1038/nature04486.

Nunes-Nesi A, Fernie AR, Stitt M. Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Molecular Plant. 2010;3(6):973–96.

Wang W, Xin W, Chen N, Yang F, Li J, Qu G, et al. Transcriptome and co-expression network analysis reveals the molecular mechanism of rice root systems in response to low-nitrogen conditions. Int J Mol Sci. 2023;24(6):5290. https://doi.org/10.3390/ijms24065290.

Kovacik J, Klejdus B, Babula P, Jarošová M. Variation of antioxidants and secondary metabolites in nitrogen-deficient barley plants. Journal of Plant Physiology. 2014;171(3–4):260-68. https://doi.org/10.1016/j.jplph.2013.08.004.

Zhang M, Ma D, Wang C, Zhao H, Zhu Y, Guo T. Responses of amino acid composition to nitrogen application in high?and low?protein wheat cultivars at two planting environments. Crop Science. 2016;56(3):1277–87. https://doi.org/10.2135/cropsci2015.08.0504.

Ahmad N, Jiang Z, Zhang L, Hussain I, Yang X. Insights on phytohormonal crosstalk in plant

response to nitrogen stress: a focus on plant root growth and development. Int J Mol Sci. 2023;24(4): 3631. https://doi.org/10.3390/ijms24043631.

Sun X, Chen F, Yuan L, Mi G. The physiological mechanism underlying root elongation in response to nitrogen deficiency in crop plants. Planta. 2020;251:1–4. https://doi.org/10.1007/s00425-020-03376–4.

Yue K, Li L, Xie J, Liu Y, Xie J, Anwar S, Fudjoe SK. Nitrogen supply affects yield and grain filling of maize by regulating starch metabolizing enzyme activities and endogenous hormone contents. Frontiers in Plant Science. 2022;12:798119. https://doi.org/10.3389/fpls.2021.798119.

Hirel B, Tetu T, Lea PJ, Dubois F. Improving nitrogen use efficiency in crops for sustainable agriculture. Sustainability. 2011;3(9):1452–85. https://doi.org/10.3390/su3091452.

Ullah I, Ali N, Durrani S, Shabaz MA, Hafeez A, Ameer H, et al. Effect of different nitrogen levels on growth, yield and yield contributing attributes of wheat. Int J Sci Eng. 2018;9(9):595–602.

Curci PL, Aiese CR, Zuluaga DL, Janni M, Sanseverino W, Sonnante G. Transcriptomic response of durum wheat to nitrogen starvation. Scientific Reports. 2017;7(1):1176. https://doi.org/10.1038/s41598-017-01377-0.

Hammad HM, Ahmad A, Wajid A, Akhter JA. Maize response to time and rate of nitrogen application. Pakistan Journal of Botany. 2011;43(4):1935–42.

Garnett T, Conn V, Kaiser BN. Root based approaches to improving nitrogen use efficiency in

plants. Plant Cell Environment. 2009;32(9):1272–83. https://doi.org/10.1111/j.1365-3040.2009.02011.x

Xue YF, Zhang W, Liu DY, Yue SC, Cui ZL, Chen XP, et al. Effects of nitrogen management on root morphology and zinc translocation from root to shoot of winter wheat in the field. Field Crops Research. 2014;161:38–45. 10.1016/j.fcr.2014.01.009.

Lv X, Zhang Y, Hu L, Zhang Y, Zhang B, Xia H, et al. Low-nitrogen stress stimulates lateral root initiation and nitrogen assimilation in wheat: roles of phytohormone signaling. Journal of Plant Growth Regulation. 2021;40:436-50. https://doi.org/10.1007/s00344-020-10112-5.

Chu G, Chen S, Xu C, Wang D, Zhang X. Agronomic and physiological performance of indica/japonica hybrid rice cultivar under low nitrogen conditions. Field Crops Research. 2019;243:107625. https://doi.org/10.1016/j.fcr.2019.107625.

Gao R, Zhou L, Guo G, Li Y, Chen Z, Lu R, et al. Comparative analysis of root transcriptome of high-NUE mutant and wild-type barley under low-nitrogen conditions. Agronomy. 2023;13(3):806. https://doi.org/10.3390/agronomy13030806.

Lynch JP. Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Annals of Botany. 2013;112(2):347–57. https://doi.org/10.1093/aob/mcs293.

Lynch JP. Harnessing root architecture to address global challenges. The Plant Journal. 2022;109(2):415-31. https://doi.org/10.1111/tpj.15560.

Chun L, Mi G, Li J, Chen F, Zhang F. Genetic analysis of maize root characteristics in response to low nitrogen stress. Plant and Soil. 2005;276:369–82. https://doi.org/10.1007/s11104-005-5876-2.

Saengwilai P, Tian X, Lynch JP. Low crown root number enhances nitrogen acquisition from low-nitrogen soils in maize. Plant Physiology. 2014;166(2):581–89. https://doi.org/10.1104/pp.113.232603

Trachsel S, Kaeppler SM, Brown KM, Lynch JP. Maize root growth angles become steeper under low N conditions. Field Crops Research. 2013;140:18–31.

https://doi.org/10.1016/j.fcr.2012.09.010

Saengwilai P, Nord EA, Chimungu JG, Brown KM, Lynch JP. Root cortical aerenchyma enhances nitrogen acquisition from low-nitrogen soils in maize. Plant Physiology. 2014;166(2):726–35. https://doi.org/10.1104/pp.114.241711.

Xin W, Zhang L, Gao J, Zhang W, Yi J, Zhen X, et al. Adaptation mechanism of roots to low and high nitrogen revealed by proteomic analysis. Rice. 2021;14:1–4. https://doi.org/10.1186/s12284-020-00443-y.

Sandhu N, Sethi M, Kumar A, Dang D, Singh J, Chhuneja P. Biochemical and genetic approaches improving nitrogen use efficiency in cereal crops: a review. Frontiers in Plant Science. 2021;12:657629.

Ryu MH, Zhang J, Toth T, Khokhani D, Geddes BA, Mus F, et al. Control of nitrogen fixation in bacteria that associate with cereals. Nature Microbiology. 2020;(2):314–30.

Ju C, Buresh RJ, Wang Z, Zhang H, Liu L, Yang J, Zhang J. Root and shoot traits for rice varieties with higher grain yield and higher nitrogen use efficiency at lower nitrogen rates application. Field Crops Research. 2015;175:47–55. https://doi.org/10.1016/j.fcr.2015.02.007.

Quan X, Zeng J, Han Z, Zhang G. Ionomic and physiological responses to low nitrogen stress in Tibetan wild and cultivated barley. Plant Physiology and Biochemistry. 2017;111:257-65. https://doi.org/10.1016/j.plaphy.2016.12.008.

Gaju O, Allard V, Martre P, Snape JW, Heumez E, LeGouis J, et al. Identification of traits to improve the nitrogen-use efficiency of wheat genotypes. Field Crops Research. 2011;123(2):139–52. https://doi.org/10.1016/j.fcr.2011.05.010.

Li D, Tian M, Cai J, Jiang D, Cao W, Dai T. Effects of low nitrogen supply on relationships between photosynthesis and nitrogen status at different leaf position in wheat seedlings. Plant Growth Regulation. 2013;70:257–63. https://doi.org/10.1007/s10725-013-9797-4.

Lian X, Wang S, Zhang J, Feng Q, Zhang L, Fan D, et alExpression profiles of 10,422 genes at early stage of low nitrogen stress in rice assayed using a cDNA microarray. Plant Molecular Biology. 2006;60:617–31. https://doi.org/10.1007/s11103-005-5441-7.

Kovacik J, Backor M. Changes of phenolic metabolism and oxidative status in nitrogen-deficient Matricaria chamomilla plants. Plant Soil. 2007;297:255–65.

Hajibarat Z, Saidi A, Ghazvini H, Hajibarat Z. Comparative analysis of physiological traits and gene expression patterns in nitrogen deficiency among barley cultivars. J Genet Eng Biotechnol. 2023;21(1):110. https://doi.org/10.1186/s43141-023-00567-w.

Nazir M, Pandey R, Siddiqi TO, Ibrahim MM, Qureshi MI, Abraham G, et al. Nitrogen-deficiency stress induces protein expression differentially in low-N tolerant and low-N sensitive maize genotypes. Frontiers in Plant Science. 2016;7:298. https://doi.org/10.3389/fpls.2016.00298.

Guo T, Xuan H, Yang Y, Wang L, Wei L, Wang Y, Kang G. Transcription analysis of genes encoding the wheat root transporter NRT1 and NRT2 families during nitrogen starvation. Journal of Plant Growth Regulation. 2014;33:837–48. https://doi.org/10.1007/s00344-014-9435-z.

Sun H, Guo X, Zhu X, Gu P, Zhang W, Tao W, et al.e Strigolactone and gibberellin signaling coordinately regulate metabolic adaptations to changes in nitrogen availability in rice. Molecular Plant. 2023;16(3):588–98. 10.1016/j.molp.2023.01.009.

Quan X, Zeng J, Ye L, Chen G, Han Z, Shah JM, Zhang G. Transcriptome profiling analysis for two Tibetan wild barley genotypes in responses to low nitrogen. BMC Plant Biology. 2016;16:1–6. https://doi.org/10.1186/s12870-016-0721-8

Li J, Xin W, Wang W, Zhao S, Xu L, Jiang X, et al. Mapping of candidate genes in response to low nitrogen in rice seedlings. Rice. 2022;15(1):51. https://doi.org/10.1186/s12284-022-00597-x.

Singh P, Kumar K, Jha AK, Yadava P, Pal M, Rakshit S, Singh I. Global gene expression profiling under nitrogen stress identifies key genes involved in nitrogen stress adaptation in maize (Zea mays L.). Scientific Reports. 2022;12(1):4211. https://doi.org/10.1038/s41598-022-07709-z.

Chen R, Tian M, Wu X, Huang Y. Differential global gene expression changes in response to low nitrogen stress in two maize inbred lines with contrasting low nitrogen tolerance. Genes and Genomics. 2011;33:491–97. https://doi.org/10.1007/s13258-010-0163-x.

Du QG, Juan YA, Sadiq SS, Yang RX, Yu JJ, Li WX. Comparative transcriptome analysis of different nitrogen responses in low-nitrogen sensitive and tolerant maize genotypes. Journal of Integrative Agriculture. 2021;20(8):2043–55. https://doi.org/10.1016/S2095-3119(20)63220-8.

Yadav MR, Kumar S, Lal MK, Kumar D, Kumar R, Yadav RK, et al. Mechanistic understanding of leakage and consequences and recent technological advances in improving nitrogen use efficiency in cereals. Agronomy. 2023 Feb 11;13(2):527.

Gao Y, Xu Z, Zhang L, Li S, Wang S, Yang H, et al. MYB61 is regulated by GRF4 and promotes nitrogen utilization and biomass production in rice. Nature Communications. 2020 Oct 15;11(1):5219.

Zhang J, Zhang H, Li S, Li J, Yan L, Xia L. Increasing yield potential through manipulating of an ARE1 ortholog related to nitrogen use efficiency in wheat by CRISPR/Cas9. Journal of Integrative Plant Biology. 2021 Sep;63(9):1649–63.

Zuluaga DL, Liuzzi V, Curci PL, Sonnante G. MicroRNAs in durum wheat seedlings under chronic and short-term nitrogen stress. Functional and Integrative Genomics. 2018;18:645–57. https://doi.org/10.1007/s10142-018-0619-7.

Zhao Y, Xu Z, Mo Q, Zou C, Li W, Xu Y, Xie C. Combined small RNA and degradome sequencing reveals novel miRNAs and their targets in response to low nitrate availability in maize. Annals of Botany. 2013;112(3):633–42. https://doi.org/10.1093/aob/mct133.

Zhao YZY, Guo LGL, Lu WLW, Li XLX, Chen H CH, Guo CGC, Xiao KXK. Expression pattern analysis of microRNAs in root tissue of wheat (Triticum aestivum L.) under normal nitrogen and low nitrogen conditions. 2015;143–53.

Shriram V, Kumar V, Devarumath RM, Khare TS, Wani SH. MicroRNAs as potential targets for abiotic stress tolerance in plants. Frontiers in Plant Science. 2016 Jun 14;7:817.

Wang W, Hu B, Yuan D, Liu Y, Che R, Hu Y, et al. Expression of the nitrate transporter gene OsNRT1. 1A/OsNPF6. 3 confers high yield and early maturation in rice. The Plant Cell. 2018;30(3):638–51. https://doi.org/10.1105/tpc.17.00809.

Tang Z, Fan X, Li Q, Feng H, Miller AJ, Shen Q, Xu G. Knockdown of a rice stelar nitrate transporter alters long-distance translocation but not root influx. Plant Physiology. 2012;160(4):2052-63. https://doi.org/10.1104/pp.112.204461.

Lee S, Marmagne A, Park J, Fabien C, Yim Y, Kim SJ, et al. Concurrent activation of OsAMT1; 2 and OsGOGAT1 in rice leads to enhanced nitrogen use efficiency under nitrogen limitation. The Plant Journal. 2020 ;103(1):7–20. https://doi.org/10.1111/tpj.14794

Cai H, Zhou Y, Xiao J, Li X, Zhang Q, Lian X. Overexpressed glutamine synthetase gene modifies nitrogen metabolism and abiotic stress responses in rice. Plant cell reports. 2009;28:527–37. https://doi.org/10.1007/s00299-008-0665-z.

Hou M, Luo F, Wu D, Zhang X, Lou M, Shen D, et al. OsPIN9, an auxin efflux carrier, is required for the regulation of rice tiller bud outgrowth by ammonium. New Phytologist. 2021;229(2):935–49. https://doi.org/10.1111/nph.16901.

Garnett T, Plett D, Heuer S, Okamoto M. Genetic approaches to enhancing nitrogen-use efficiency (NUE) in cereals: challenges and future directions. Functional Plant Biology. 2015;42(10):921–41. https://doi.org/10.1071/FP15025

Tian H, Fu J, Drijber RA, Gao Y. Expression patterns of five genes involved in nitrogen metabolism in two winter wheat (Triticum aestivum L.) genotypes with high and low nitrogen utilization efficiencies. Journal of Cereal Science. 2015;61:48–54. https://doi.org/10.1016/j.jcs.2014.09.007

Hasnain A, Irfan M, Bashir A, Maqbool A, Malik KA. Transcription factor TaDof1 improves nitrogen and carbon assimilation under low-nitrogen conditions in wheat. Plant Molecular Biology Reporter. 2020;38:441–51. https://doi.org/10.1007/s11105-020-01208-z.

Jiang L, Ball G, Hodgman C, Coules A, Zhao H, Lu C. Analysis of gene regulatory networks of maize in response to nitrogen. Genes. 2018;9(3):151. https://doi.org/10.3390/genes9030151.