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Nitrogen use efficiency (NUE): elucidated mechanisms, mapped genes and gene networks in maize (Zea mays L.)

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Abstract

Nitrogen, the vital primary plant growth nutrient at deficit soil conditions, drastically affects the growth and yield of a crop. Over the years, excess use of inorganic nitrogenous fertilizers resulted in pollution, eutrophication and thereby demanding the reduction in the use of chemical fertilizers. Being a C4 plant with fibrous root system and high NUE, maize can be deployed to be the best candidate for better N uptake and utilization in nitrogen deficient soils. The maize germplasm sources has enormous genetic variation for better nitrogen uptake contributing traits. Adoption of single cross maize hybrids as well as inherent property of high NUE has helped maize cultivars to achieve the highest growth rate among the cereals during last decade. Further, considering the high cost of nitrogenous fertilizers, adverse effects on soil health and environmental impact, maize improvement demands better utilization of existing genetic variation for NUE via introgression of novel allelic combinations in existing cultivars. Marker assisted breeding efforts need to be supplemented with introgression of genes/QTLs related to NUE in ruling varieties and thereby enhancing the overall productivity of maize in a sustainable manner. To achieve this, we need mapped genes and network of interacting genes and proteins to be elucidated. Identified genes may be used in screening ideal maize genotypes in terms of better physiological functionality exhibiting high NUE. Future genome editing may help in developing lines with increased productivity under low N conditions in an environment of optimum agronomic practices.

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References

  • Agrama HAS, Zakaria AG, Said FB, Tuinstra M (1999) Identification of quantitative trait loci for nitrogen use efficiency in maize. Mol Breeding 5:187–195

    Google Scholar 

  • Alexandratos N, Jelle B (2012) World agriculture towards 2030/2050: The 2012 revision

  • Amiour N, Imbaud S, Clement G, Agier N, Zivy M, Valot B, Balliau T, Armengaud P, Quillere I, Canas T et al (2012) The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. J Exp Bot 63:5017–5033

    CAS  PubMed  Google Scholar 

  • Ansari MA, Prakash N, Ashok Kumar, Jat SL, Baishya LK, Sharma SK, Bungbungcha CH, Sanatombi KH, Sanjay Singh S. (2015). Maize production technology highlighted in North East India. Training Manual RCM (TM)—05. ICAR Research Complex for NEH Region, Manipur Centre, Lamphelpat, Imphal795004

  • Aseel DG, Mostafa Y, Riad SA, Hafez EE (2019) Improvement of nitrogen use efficiency in maize using molecular and physiological approaches. Symbiosis 78(3):263–274

    CAS  Google Scholar 

  • Balyan HS, Gahlaut V, Kumar A, Jaiswal V, Dhariwal R, Tyagi S, Agarwal P, Kumari S, Gupta PK (2016) Nitrogen and phosphorus use efficiencies in wheat: physiology, phenotyping, genetics, and breeding. Plant Breed Rev 40:167–214

    Google Scholar 

  • Bertin P, Gallais A (2000a) Genetic variation for nitrogen use efficiency in a set of recombinant maize inbred lines. I. Agrophysiological results. Maydica 45:53–66

    Google Scholar 

  • Bertin P, Gallais A (2000b) Physiological and genetic basis of nitrogen use efficiency in maize. I. Agrophysiological Results. Maydica 45:53–66

    Google Scholar 

  • Bertin P, Gallais A (2001) Physiological and genetic basis of nitrogen use efficiency in maize. II. QTL Detection and Coincidences. Maydica 46:53–68

    Google Scholar 

  • Bloch SE, Ryu M, Ozaydin B, Broglie R (2020) Harnessing atmospheric nitrogen for cereal crop production. Curr Opin Biotech 62:181–188

    CAS  PubMed  Google Scholar 

  • Cai H, Chen F, Mi G, Zhang F, Maurer HP, Liu W et al (2012) Mapping QTLs for root system architecture of maize (Zea mays L.) in the field at different developmental stages. Theor Appl Genet 125:1313–1324. https://doi.org/10.1007/s00122-012-1915-6

    Article  PubMed  Google Scholar 

  • Chun L, Mi GH, Li JS, Chen FJ, Zhang FS (2005) Genetic analysis of maize root characteristics in response to low nitrogen stress. Plant Soil 276:369–382. https://doi.org/10.1007/s11104-005-5876-2

    Article  CAS  Google Scholar 

  • Clay DE, Ki-In Kim J, Chang SAC, Dalsted K (2006) Characterizing Water and Nitrogen Stress in Corn Using Remote Sensing. Agron J 98:579–587

    Google Scholar 

  • Contreras-Cubas C, Palomar M, Arteaga-V A, Zquez M, Reyes JEL, Covarrubias AA (2012) Non-coding RNAs in the plant response to abiotic stress. Planta 236:943–958. https://doi.org/10.1007/s00425-012-1693-z

    Article  CAS  PubMed  Google Scholar 

  • Coque M, Bertin P, Hirel B, Gallais A (2006) Genetic variation and QTLs for 15N natural abundance in a set of maize recombinant inbred lines. Field Crop Res 97(2–3):310–321

    Google Scholar 

  • Coque M, Martin A, Veyrieras JB, Hirel B, Gallais A (2008) Genetic variation for N-remobilization and postsilking N-uptake in a set of maize recombinant inbred lines. 3. QTL detection and coincidences. Theor Appl Genet 117(5):729–747

    CAS  PubMed  Google Scholar 

  • Costa C, Dwyer LM, Zhou X, Dutilleul P, Hamel C, Reid LM, Smith DL (2002) Root morphology of contrasting maize genotypes. Agron J 94:96–105

    Google Scholar 

  • Dechorgnat J, Francis KL, Dhugga KS, Rafalski JA, Tyerman SD, Kaiser BN (2019) Tissue and nitrogen-linked expression profiles of ammonium and nitrate transporters in maize. BMC Plant Biol 19:206

    PubMed  PubMed Central  Google Scholar 

  • deDorlodot S, Forster B, Pages L, Price A, Tuberosa R, Draye X (2007) Root system architecture: opportunities and constraints for genetic improvement of crops. Trends Plant Sci 12:474–481. https://doi.org/10.1016/j.tplants.2007.08.012

    Article  CAS  Google Scholar 

  • Di C, Yuan J, Wu Y, Li J, Lin H, Hu L, Zhang T, Qi Y, Gerstein MB, Guo Y et al (2014) Characterization of stress-responsive lncRNAs in Arabidopsis thaliana by integrating expression, epigenetic and structural features. Plant J 80:848–861. https://doi.org/10.1111/tpj.12679

    Article  CAS  PubMed  Google Scholar 

  • Ding L, Wang KJ, Jiang GM, Biswas DK, Xu H, Li LF, Li YH (2005) Effects of nitrogen deficiency on photosynthetic traits of maize hybrids released in different years. Ann Bot 96:925–930

    CAS  PubMed  PubMed Central  Google Scholar 

  • Downs GS, Bi YM, Colasanti J, Wu WQ, Chen X, Zhu T, Rothstein SJ, Lukens LN (2013) A developmental transcriptional network for maize defines coexpression modules. Plant Physiol 161:1830–1843

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eck HV (1984) Irrigation corn yield responses to nitrogen and water. Agron J 76:421–428

    Google Scholar 

  • Elings A, White J, Edmeades GO (1996) Modelling tropical maize under drought and low N. Annual Abstracts. Agronomy Meeting. American Society of Agronomy. Indianapolis, Indiana. November 3–8. p 109

  • Fageria NK (2014) Nitrogen harvest index and its association with crop yields. J Plant Nutr 37:795–810

    CAS  Google Scholar 

  • FAO (Food and Agricultural Organization) (2017). http://www.fao.org/faost at/en/#data/RFN. Accessed 25 April 2020

  • FAO (2020). FAOSTAT data. Food and Agricultural Organization, Italy, Rome. http://faostat.fao.org/

  • Fang XZ, Fang SQ, Ye ZQ, Liu D, Zhao KL, Jin CW (2021) NRT1.1 Dual-affinity nitrate transport/signalling and its roles in plant abiotic stress resistance. Front Plant Sci 12:715694

    PubMed  PubMed Central  Google Scholar 

  • Fatica A, Bozzoni I (2014) Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 15:7–21. https://doi.org/10.1038/nrg3606

    Article  CAS  PubMed  Google Scholar 

  • Fernandez JA, DeBruin J, Messina CD, Ciampitti IA (2020) Late-season nitrogen fertilization on maize yield: a meta-analysis. Field Crops Res 247:107586

    Google Scholar 

  • FICCI (2021) Boosting Growth of India's Maize Ecosystem-Key Imperatives. pp. 9

  • Gallais A, Hirel B (2004) An approach to the nitrogen use efficiency in maize. J Exp Bot 55(396):295–306

    CAS  PubMed  Google Scholar 

  • Gallais A, Coque M (2005) Genetic variation and selection for nitrogen use efficiency in maize: a synthesis. Maydica 50:531–537

    Google Scholar 

  • Garnett T, Conn V, Plett D, Conn S, Zanghellini J, Mackenzie N, Enju A, Francis K, Holtham L, Roessner U, Boughton B, Bacic A, Shirley N, Rafalski A, Dhugga K, Tester M, Kaiser BN (2013) The response of the maize nitrate transport system to nitrogen demand and supply across the lifecycle. N Phytol 198:82–94. https://doi.org/10.1111/nph.12166

    Article  CAS  Google Scholar 

  • Ge M, Wang Y, Liu Y, Jiang LU, He B, Ning L, Du H, Lv Y, Zhou L, Lin F, Zhang T (2020) The NIN-like protein 5 (ZmNLP5) transcription factor is involved in modulating the nitrogen response in maize. Plant J 102(2):353–368

    CAS  PubMed  PubMed Central  Google Scholar 

  • Giller KE, Chalk P, Dobermann A, Hammond L, Heffer P, Ladha JK, Nyamudeza P, Maene L, Ssali H, Freney J (2004) Emerging technologies to increase the efficiency of use of fertilizer nitrogen. In: Mosier AR, Syers KJ, Freney JR (eds) Agriculture and the nitrogen cycle: assessing the impacts of fertilizer use on food production and the environment. Island Press, Washington, pp 35–51

    Google Scholar 

  • Giuliani S, Sanguineti MC, Tuberosa R, Bellotti M, Salvi S, Landi P (2005) Root-ABA1, a major constitutive QTL, affects maize root architecture and leaf ABA concentration at different water regimes. J Exp Bot 56(422):3061–3070

    CAS  PubMed  Google Scholar 

  • Gong X, Liu X, Pan Q, Mi G, Chen F, Yuan L (2020) Combined physiological, transcriptome, and genetic analysis reveals a molecular network of nitrogen remobilization in maize. J Exp Bot 71(16):5061–5073

    CAS  PubMed  Google Scholar 

  • Guil SON, Esteller M (2012) Cis-acting noncoding RNAs: friends and foes. Nat StructMol Biol 19:1068–1075. https://doi.org/10.1038/nsmb.2428

    Article  CAS  Google Scholar 

  • Guan M, Chen M, Cao Z (2021) NRT2.1, a major contributor to cadmium uptake controlled by high-affinity nitrate transporters. Ecotoxicol Environ Saf 218:11226

    Google Scholar 

  • Gutiérrez RA, Lejay LV, Dean A, Chiaromonte F, Shasha DE, Coruzzi GM (2007) Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol 8:R7

    PubMed  PubMed Central  Google Scholar 

  • Hailegnaw NS, Mercl F, Kulhánek M, Száková J, Tlustoš P (2021) Co-application of high temperature biochar with 3, 4-dimethylpyrazole-phosphate treated ammonium sulphate improves nitrogen use efficiency in maize. Sci Rep 11(1):1–13

    Google Scholar 

  • Hammad HM, Farhad W, Abbas F, Fahad S, Saeed S, Nasim W, Bakhat HF (2017) Maize plant nitrogen uptake dynamics at limited irrigation water and nitrogen. Environ Sci Pollut Res 24(3):2549–2557

    CAS  Google Scholar 

  • Han M, Wong J, Su T, Beatty PH, Good AG (2016) Identification of nitrogen use efficiency genes in barley: searching for QTLs controlling complex physiological traits. Front Plant Sci 7:1587. https://doi.org/10.3389/fpls.2016.01587

    Article  PubMed  PubMed Central  Google Scholar 

  • He K, Xu S, Zhang X, Li Y, Chang L, Wang Y, Shi Y, Cui T, Dong Y, Lan T, Liu X (2020) Mining of candidate genes for nitrogen use efficiency in maize based on genome-wide association study. Mol Breeding 40(9):1–7

    Google Scholar 

  • Hirel B, Bertin P, Quilleré I, Bourdoncle W, Attagnant C, Dellay C, Gallais A (2001) Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol 125(3):1258–1270

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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. J Exp Bot 58:2369–2387

    CAS  PubMed  Google Scholar 

  • Hochholdinger F, Zimmermann R (2008) Conserved and diverse mechanisms in root development. Curr Opin Plant Biol 11:70–74. https://doi.org/10.1016/j.pbi.2007.10.002

    Article  CAS  PubMed  Google Scholar 

  • Hopf N, Plesofsky-Vig N, Brambl R (1992) The heat shock response of pollen and other tissues of maize. Plant Mol Biol 19:623–630. https://doi.org/10.1007/BF00026788

    Article  CAS  PubMed  Google Scholar 

  • Huang YZ, Feng Z, Fuzhu Z (2000) Study on loss of nitrogen fertilizer from agricultural felds and countermeasure. J Grad Sch Academia Sinica 17(2):49–58

    Google Scholar 

  • Humbert S, Subedi S, Cohn J, Zeng B, Bi YM, Chen X, Zhu T, McNicholas PD, Rothstein SJ (2013) Genome-wide expression profiling of maize in response to individual and combined water and nitrogen stresses. BMC Genom 14:3

    CAS  Google Scholar 

  • Humtsoe BM, Dawson J, Rajana P (2018) Effect of nitrogen, boron and zinc as basal and foliar application on growth and yield of maize (Zea mays L.). J Pharmacogn Phytochem 7(6):01–04

    CAS  Google Scholar 

  • Hund A, Reimer R, Messmer R (2011) A consensus map of QTLs controlling the root length of maize. Plant Soil 344:143–158. https://doi.org/10.1007/s11104-011-0735-9

    Article  CAS  Google Scholar 

  • Ibrahim A, Jin XL, Zhang YB, Cruz J, Vichyavichien P, Esiobu N, Zhang XH (2017) Tobacco plants expressing the maize nitrate transporter ZmNrt2.1 exhibit altered responses of growth and gene expression to nitrate and calcium. Bot Stud 58:51

    PubMed  PubMed Central  Google Scholar 

  • Islam, S., Zhang, J., Zhao, Y., She, M., and Ma, W. (2021). Genetic regulation of the traits contributing to wheat nitrogen use efficiency. Plant Sci. 303:110759.

  • Jenison JR, Shank DB, Penny LH (1981) Root characteristics of 44 maize inbreds evaluated in 4 environments. Crop Sci 21:233–237

    Google Scholar 

  • John GW, Schmitt MA (2007) Advisability of fall-applying nitrogen. In: Proceedings of the 2008 Wisconsin Fertilizer, Aglime and Pest Management Conference, held on the 15–17th January, 2008 at University of Wisconsin, Madison, WI. pp. 90–96

  • Kant S, Bi YM, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62(4):1499–1509

    CAS  PubMed  Google Scholar 

  • Khan A, Jan A, Bashir S, Noor M (2005) Effect of nitrogen and seed size on maize crop. I: Stand and plant height. J Agric Soc Sci 1(4):380–381

    Google Scholar 

  • Knyazikhin Y, Schull MA, Stenberg P, Mottus M, Rautiainen M, Yang Y, Marshak A, Carmona PL, Kaufmann RK, Lewis P et al (2013) Hyperspectral remote sensing of foliar nitrogen content. Proc Nat Acad Sci USA 110:E185–E192

    CAS  PubMed  Google Scholar 

  • Kumar B, Abdel-Ghani AH, Reyes-Matamoros J, Hochholdinger F, Luebberstedt T (2012) Genotypic variation for root architecture traits in seedlings of maize (Zea mays L.) inbred lines. Plant Breed 131:465–478. https://doi.org/10.1111/j.1439-0523.2012.01980.x

    Article  Google Scholar 

  • Kumar V, Singh AK, Jat SL, Parihar CM, Pooniya V, Singh B, Sharma S (2015) Precision nutrient and conservation agriculture practices for enhancing productivity, profitability, nutrient-use efficiencies and soil nutrient status of maize (Zea mays) hybrids. Indian J Agric Sci 85(7):926–930

    CAS  Google Scholar 

  • 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. Front Plant Sci. https://doi.org/10.3389/fpls.2021.627955

    Article  PubMed  PubMed Central  Google Scholar 

  • Lal R (2007) Anthropogenic influences on world soils and implications to global food security. Adv Agron 93:69–93

    CAS  Google Scholar 

  • Landi P, Albrecht B, Giuliani MM, Sanguineti MC (1998) Seedling characteristics in hydroponic culture and field performance of maize genotypes with different resistance to root lodging. Maydica 43:111–116

    Google Scholar 

  • Landi P, Sanguineti MC, Salvi S, Giuliani S, Bellotti M, Maccaferri M, Conti S, Tuberosa R (2005) Validation and characterization of a major QTL affecting leaf ABA concentration in maize. Mol Breeding 15(3):291–303

    CAS  Google Scholar 

  • Langridge P, Fleury D (2011) Making the most of ‘omics’ for crop breeding. Trends Biotechnol 29:33–40

    CAS  PubMed  Google Scholar 

  • Lassaletta L, Billen G, Garnier J, Bouwman L, Velazquez E, Mueller ND, Gerber JS (2016) Nitrogen use in the global food system: past trends and future trajectories of agronomic performance, pollution, trade, and dietary demand. Environ Res Lett 11:095007

    Google Scholar 

  • Lebreton C, Lazicjancic V, Steed A, Pekic S, Quarrie SA (1995) Identification of QTL for drought responses in maize and their use in testing causal relationships between traits. J Exp Bot 46:853–865. https://doi.org/10.1093/jxb/46.7.853

    Article  CAS  Google Scholar 

  • Lee S (2021) Recent Advances on Nitrogen Use Efficiency in Rice. Agronomy 11(4):753

    CAS  Google Scholar 

  • Li MG, Villemur R, Hussey PJ, Silflow CD, Gantt JS, Snustad DP (1993) Differential expression of six glutamine synthetase genes in Zea mays. Plant Mol Biol 23:401–407

    CAS  PubMed  Google Scholar 

  • Li M, Xu J, Gao Z, Tian H, Gao Y, Kariman K (2020) Genetically modified crops are superior in their nitrogen use efficiency-A meta-analysis of three major cereals. Sci Rep 10(1):1–9

    Google Scholar 

  • Li P, Chen F, Cai H, Liu J, Pan Q, Liu Z, Gu R, Mi G, Zhang F, Yuan L (2015) A genetic relationship between nitrogen use efficiency and seedling root traits in maize as revealed by QTL analysis. J Exp Bot 66(11):3175–3188

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Li Z, Cui S, Chang SX, Jia C, Zhang Q (2019) A global synthesis of the effect of water and nitrogen input on maize (Zea mays) yield, water productivity and nitrogen use efficiency. Agric for Meteorol 268:136–145

    Google Scholar 

  • Liu J, Jung C, Xu J, Wang H, Deng S, Bernad L, Arenas-Huertero C, Chua NH (2012a) Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24:4333–4345. https://doi.org/10.1105/tpc.112.102855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu R, Zhang H, Zhao P, Zhang Z, Liang W, Tian Z, Zheng Y (2012b) Mining of candidate maize genes for nitrogen use efficiency by integrating gene expression and QTL data. Plant Mol Biol Rep 30(2):297–308

    CAS  Google Scholar 

  • Liu Z, Gao K, Shan S, Gu R, Wang Z, Craft EJ, Mi G, Yuan L, Chen F (2017) Comparative Analysis of Root Traits and the Associated QTLs for Maize Seedlings Grown in Paper Roll, Hydroponics and Vermiculite Culture System. Front Plant Sci 8:436. https://doi.org/10.3389/fpls.2017.00436

    Article  PubMed  PubMed Central  Google Scholar 

  • Lv Y, Liang Z, Ge M, Qi W, Zhang T, Lin F, Peng Z, Zhao H (2016) Genome-wide identification and functional prediction of nitrogen-responsive intergenic and intronic long non-coding RNAs in maize (Zea mays L.). BMC Genomics 17:350. https://doi.org/10.1186/s12864-016-2650-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049. https://doi.org/10.1104/pp.111.175414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot 112:347–357. https://doi.org/10.1093/aob/mcs293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mandolino CI, D’Andrea KE, Olmos SE, Otegui ME, Eyhérabide GH (2018) Maize nitrogen use efficiency: QTL mapping in a US Dent x Argentine-Caribbean flint RILs population. Maydica 63(1):17

    Google Scholar 

  • Martin A, Lee J, Kichey T, Gerentes D et al (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18:3252–3274

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matsui A, Nguyen AH, Nakaminami K, Seki M (2013) Arabidopsis non-coding RNA regulation in abiotic stress responses. Int J Mol Sci 14:22642–22654. https://doi.org/10.3390/ijms141122642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumura T, Sakakibara H, Nakano R, Kimata Y, Sugiyama T, Hase T (1997) A nitrate-inducible ferredoxin in maize roots. Genomic organization and differential expression of two nonphotosynthetic ferredoxin isoproteins. Plant Physiol 114:653–660

    CAS  PubMed  PubMed Central  Google Scholar 

  • McCullough DE, Girardin P, Mihajlovic M, Aguilera A, Tollenaar M (1994) Influence of N supply on development and dry matter accumulation of an old and a new maize hybrid. Can J Plant Sci 74:471–477

    Google Scholar 

  • Mercer TR, Mattick JS (2013) Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 20:300–307. https://doi.org/10.1038/nsmb.2480

    Article  CAS  PubMed  Google Scholar 

  • Mi G, Chen F, Wu Q, Lai N, Yuan L, Zhang F (2010) Ideotype root architecture for efficient nitrogen acquisition by maize in intensive cropping systems. Sci China-Life Sci 53:1369–1373. https://doi.org/10.1007/s11427-010-4097-y

    Article  PubMed  Google Scholar 

  • Moll RH, Kamprath EJ, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency to nitrogen utilization. Agron J 74:562–564

    Google Scholar 

  • Moose S, Below FE (2009) Biotechnology approaches to improving maize nitrogen use efficiency. In: Kriz AL, Larkins BA (eds). Molecular genetic approaches to maize improvement. Springer, Berlin. Volume 63. Part II

  • Muers M (2011) RNA: Genome-wide views of long non-coding RNAs. Nat Rev Genet 12(11):742–743. https://doi.org/10.1038/nrg3088

    Article  CAS  PubMed  Google Scholar 

  • Naeem MA, Khalid M, Aon M, Abbas G, Amjad M, Murtaza B, Khan WUD, Ahmad N (2018) Combined application of biochar with compost and fertilizer improves soil properties and grain yield of maize. J Plant Nutr 41(1):112–122

    CAS  Google Scholar 

  • Pan X, Abdulaha-Al Baquy M, Guan P, Yan J, Wang R, Xu R, Xie L (2020) Effect of soil acidification on the growth and nitrogen use efficiency of maize in Ultisols. J Soils Sediments 20(3):1435–1445

    CAS  Google Scholar 

  • Parnell JJ, Berka R, Young HA, Sturino JM, Kang Y, Barnhart DM, DiLeo MV (2016) From the lab to the farm: an industrial perspective of plant beneficial microorganisms. Front Plant Sci 7:1110

    PubMed  PubMed Central  Google Scholar 

  • Peña PA, Quach T, Sato S, Ge Z, Nersesian N, Changa T, Dweikat I, Soundararajan M, Clemente TE (2017) Expression of the maize Dof1 transcription factor in wheat and sorghum. Front Plant Sci 8:434

    PubMed  PubMed Central  Google Scholar 

  • Pestsova E, Lichtblau D, Wever C, Presterl T, Bolduan T, Ouzunova M, Westhoff P (2016) QTL mapping of seedling root traits associated with nitrogen and water use efficiency in maize. Euphytica 209(3):585–602

    CAS  Google Scholar 

  • Pingali PL, Pandey S (2001) Meeting world maize needs: technological opportunities and priorities for the public sector. In: Pingali PL (ed) 1999/2000 world maize facts and trends. CIMMYT, Mexico. pp 1–24

  • Pii Y, Alessandrini M, Dall’Osto L, Guardini K, Prinsi B, Espen L, Zamboni A, Varanini Z (2016) Time-resolved investigation of molecular components involved in the induction of NO–3NO3– high affinity transport system in maize roots. Front Plant Sci 7:1657. https://doi.org/10.3389/fpls.2016.01657

    Article  PubMed  PubMed Central  Google Scholar 

  • Prinsi B, Espen (2015) Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize. BMC Plant Biol 15:96

    PubMed  PubMed Central  Google Scholar 

  • Qi X, Xie S, Liu Y, Yi F, Yu J (2013) Genome-wide annotation of genes and noncoding RNAs of foxtail millet in response to simulated drought stress by deep sequencing. Plant Mol Biol 83:459–473. https://doi.org/10.1007/s11103-013-0104-6

    Article  CAS  PubMed  Google Scholar 

  • Qi D, Hu T, Song X, Zhang M (2019) Effect of nitrogen supply method on root growth and grain yield of maize under alternate partial root-zone irrigation. Sci Rep 9(1):1–10

    Google Scholar 

  • Raun WR, Johnson GV (1999) Improving nitrogen use efficiency for cereal production. Agron J 91:357–363

    Google Scholar 

  • Ribaut JM, Fracheboud Y, Monneveux P, Banzinger M, Vargas M, Jiang C (2007) Quantitative trait loci for yield and correlated traits under high and low soil nitrogen conditions in tropical maize. Mol Breeding 20:15–29

    CAS  Google Scholar 

  • Rostami M, Koocheki AR, Mahallati MN, Kafi M (2008) Evaluation of chlorophyll meter (SPAD) for prediction of nitrogen status in corn (Zea mays L.). American-Eurasian J Agricu Environ Sci 3(1):79–85

    Google Scholar 

  • Saengwilai P, Tian X, Lynch JP (2014) Low crown root number enhances nitrogen acquisition from low-nitrogen soils in maize. Plant Physiol 166:581–589. https://doi.org/10.1104/pp.113.232603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 11:440–448

    CAS  PubMed  Google Scholar 

  • Sandhu N, Sethi M, Kumar A, Dang D, Singh J, Chhuneja P (2021) Biochemical and Genetic Approaches Improving Nitrogen Use Efficiency in Cereal Crops: A Review. Front Plant Sci 12:757

    Google Scholar 

  • Santi S, Locci G, Monte R, Pinton R, Varanini Z (2003) Induction of nitrate uptake in maize roots: expression of a putative high-affinity nitrate transporter and plasma membrane H+-ATPase isoforms. J.EXP. Bot 54:1851–1864

    CAS  Google Scholar 

  • Santos AD, Amaral Júnior ATD, Fritsche-Neto R, Kamphorst SH, Ferreira FRA, Amaral JFTD, Vivas JMS, Santos PHAD, Lima VJD, Khan S, Schmitt KFM (2019) Relative importance of gene effects for nitrogen-use efficiency in popcorn. PLoS ONE 14(9):e0222726

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schlüter U, Mascher M, Colmsee C, Scholz U, Bräutigam A, Fahnenstich H, Sonnewald U (2012) Maize source leaf adaptation to nitrogen deficiency affects not only nitrogen and carbon metabolism but also control of phosphate homeostasis. Plant Physiol 160:1384–1406

    PubMed  PubMed Central  Google Scholar 

  • Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR, Leon ND, Kaeppler SM (2011) Genome-wide atlas of transcription during maize development. Plant J 66:553–563

    CAS  PubMed  Google Scholar 

  • Shaner DL, Boyer JS (1976) Nitrate reductase activity in maize (Zea mays L.) leaves: II. regulation by nitrate flux at low leaf water potential. Plant Physiol 58:505–559

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sheoran S, Kumar S, Kumar P, Meena RS, Rakshit S (2021). Nitrogen fixation in maize: breeding opportunities. Theor Appl Genet pp1–18

  • Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ (2019) STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47(D1):607–613. https://doi.org/10.1093/nar/gky1131

    Article  CAS  Google Scholar 

  • Tadesse Ertiro B, Olsen M, Das B, Gowda M, Labuschagne M (2020) Genetic dissection of grain yield and agronomic traits in maize under optimum and low-nitrogen stressed environments. Int J Mol Sci 21(2):543

    PubMed Central  Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677

    CAS  PubMed  Google Scholar 

  • Torbert HA, Potter KN, Morrison JE Jr (2011) Tillage system, fertilizer nitrogen rate, and timing effect on corn yields in the Texas Blackland Prairie. Agron J 93:1119–1124

    Google Scholar 

  • Toubiana D, Fernie AR, Nikoloski Z, Fait A (2013) Network analysis: tackling complex data to study plant metabolism. Trends Biotechnol 31:29–36

    CAS  PubMed  Google Scholar 

  • Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2013) Maize root growth angles become steeper under low N conditions. Field Crops Res 140:18–31. https://doi.org/10.1016/j.fcr.2012.09.010

    Article  Google Scholar 

  • Trevisan S, Borsa P, Botton A, Varotto S, Malagoli M, Ruperti B, Quaggiotti S (2008) Expression of two maize putative nitrate transporters in response to nitrate and sugar availability. Plant Biol (stuttg) 10:462–475

    CAS  Google Scholar 

  • Tuberosa R, Salvi S, Sanguineti MC, Maccaferri M, Giuliani S, Landi P (2003) Searching for quantitative trait loci controlling root traits in maize: a critical appraisal. Plant Soil 255:35–54. https://doi.org/10.1023/a:1026146

    Article  CAS  Google Scholar 

  • U.S. Bureau of the Census. 2009. Current Population Projections. www.census.gov/.

  • Uhart SA, Andrade FH (1995) Nitrogen and carbon accumulation and remobilization during grain filling in maize under different source/sink ratios. Crop Sci 35:183–190

    Google Scholar 

  • Van Oosten MJ, Dell’Aversana E, Ruggiero A, Cirillo V, Gibon Y, Woodrow P, Maggio A, Carillo P (2019) Omeprazole treatment enhances nitrogen use efficiency through increased nitrogen uptake and assimilation in corn. Front Plant Sci 10:1507

    PubMed  PubMed Central  Google Scholar 

  • Virlet N, Sabermanesh K, Sadeghi-Tehran P, Hawkesford MJ (2017) Field Scanalyzer: an automated robotic field phenotyping platform for detailed crop monitoring. Funct Plant Biol 44(1):143–153

    Google Scholar 

  • Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13:87–115

    Google Scholar 

  • Wan TENG, Xue HE, Tong YP (2017) Transgenic approaches for improving use efficiency of nitrogen, phosphorus and potassium in crops. J Integr Agric 16(12):2657–2673

    Google Scholar 

  • Wang H, Chung PJ, Liu J, Jang I, Kean MJ, Xu J, Chua N (2014) Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res 24:444–453. https://doi.org/10.1101/gr.165555.113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang RC, Okamoto M, Xing XJ, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol 132:556–567

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang RC, Guegler K, LaBrie ST, Crawford NM (2000) Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell 12:1491–1509

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Janz B, Engedal T, de Neergaard A (2017) Efect of irrigation regimes and nitrogen rates on water use efciency and nitrogen uptake in maize. Agric Water Manag 179:271–276

    Google Scholar 

  • Wang Z, Ma BL, Yu X, Gao J, Sun J, Su Z, Yu S (2019) Physiological Basis of Heterosis for Nitrogen Use Efficiency of Maize. Sci Rep 9(1):1–11

    Google Scholar 

  • Wen ZY, Tyerman SD, Dechorgnat J, Ovchinnikova E, Dhugga KS, Kaiser BN (2017) Maize NPF6 proteins are homologs of Arabidopsis CHL1 that are selective for both nitrate and chloride. Plant Cell. https://doi.org/10.1105/tpc.16.00724

    Article  PubMed  PubMed Central  Google Scholar 

  • Wen Z, Kaiser BN (2018) Unraveling the functional role of NPF6 transporters. Front Plant Sci 9:973

    PubMed  PubMed Central  Google Scholar 

  • White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Ann Bot 105:1073–1080. https://doi.org/10.1093/aob/mcq085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu P, Liu F, Li H, Cai T, Zhang P, Jia Z (2021) Suitable fertilizer application depth can increase nitrogen use efficiency and maize yield by reducing gaseous nitrogen losses. Sci Total Environ 27:146787

    Google Scholar 

  • Yan P, Pan J, Zhang W, Shi J, Chen X, Cui Z (2017) A high plant density reduces the ability of maize to use soil nitrogen. PLoS ONE 12(2):e0172717

    PubMed  PubMed Central  Google Scholar 

  • Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004) Metabolic engineering with Dof1 transcription factor in plants: Improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl AcadSci USA 101:7833–7838

    CAS  Google Scholar 

  • Yang XS, Wu JR, Ziegler TE, Yang X, Zayed A, Rajani MS, Zhou DF, Basra AS, Schachtman DP, Peng MS et al (2010) Gene expression biomarkers provide sensitive indicators of in planta nitrogen status in maize. Plant Physiol 157:1841–1852

    Google Scholar 

  • Yang JT, Schneider HM, Brown KM, Lynch JP (2019) Genotypic variation and nitrogen stress effects on root anatomy in maize are node-specic. J Exp Bot 70(19):5311–5325

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zamboni A, Astolfi S, Zuchi S, Pii Y, Guardini K, Tononi P, Varanini Z (2014) Nitrate induction triggers different transcriptional changes in a high and a low nitrogen use efficiency maize inbred line. J Integr Plant Biol 56:1080–1094

    CAS  PubMed  Google Scholar 

  • Zanin L, Tomasi N, Zamboni A, Varanini Z, Pinton R (2015) The urease inhibitor NBPT negatively affects DUR3-mediated uptake and assimilation of urea in maize roots. Front Plant Sci 6:1007. https://doi.org/10.3389/fpls.2015.01007

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Barber SA (1993) Corn root distribution between ammonium fertilized and unfertilized soil. Soil Science and Plant Anal. 24: 411–419. Frontiers in Plant Science12Agronomy11

  • Zheng ZP, Liu XH (2013) QTL identification of ear leaf morphometric traits under different nitrogen regimes in maize. Genet Mol Res 12(4):4342–4351

    CAS  PubMed  Google Scholar 

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Acknowledgements

Authors are grateful to their respective institutions.

Funding

This work was partially supported by the Indian Council of Agricultural Research –National Bureau of Plant Genetic Resources [PGR/DFP-BUR-DEL-01.01]. AZ is thankful to Aligarh Muslim University and UGC-New Delhi India for financial assistance.

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SHW conceived the idea, SHW, RV, MK, AK, AZ, VS, PK and JKY wrote the MS.

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Wani, S.H., Vijayan, R., Choudhary, M. et al. Nitrogen use efficiency (NUE): elucidated mechanisms, mapped genes and gene networks in maize (Zea mays L.). Physiol Mol Biol Plants 27, 2875–2891 (2021). https://doi.org/10.1007/s12298-021-01113-z

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