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Mechanisms Involved in Nitrogen-Use Efficiency in Maize: Comparison
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Please note this is a comparison between Version 2 by Catherine Yang and Version 1 by Talles de Oliveira Santos.
Nitrogen is a nutrient that has great mobility in plants, so its metabolism involves several processes, including absorption, reduction, assimilation, translocation and remobilization. The genetic differences between nitrogen uptake or productivity per unit of nitrogen applied to the soil have been studied for several grasses, especially those of commercial importance, such as wheat, rice, oats and, mainly, corn. The latter, in general, is one of the most produced cereals worldwide and one that most requires nitrogen fertilizers to increase productivity.
  • abiotic stress
  • sustainable agriculture
  • nitrogen-use efficiency

1. Nitrogen Uptake and Transport

Nitrogen is a limiting macronutrient for plant growth and development [70,71][1][2]. Soil nitrogen availability is normally low and can be influenced by factors such as precipitation, temperature, pH and soil type. The form of nitrogen preferred by plants is intrinsically related to their adaptation and soil conditions [72][3]. Plants can use both nitrate (NO3−) and ammonium (NH4+) as sources of N [8,73,74][4][5][6]. NO3− is the main and most readily available source of nitrogen for most higher plants [75[7][8],76], however, NO3− concentrations in soils can be very varied, depending on environmental variations and, therefore, plants have developed several specific adaptations for the uptake of available NO3− [72,77][3][9].
Nitrate is actively transported into cells, mainly by the NO3− transcarriers of the NRT family, which depend on the energy supply and electrochemical gradient and are divided into two systems existing in the cell membranes of the roots [77,78,79,80][9][10][11][12]. One of them is the high affinity transport system (HATS), which is activated when there is a high concentration of nitrate available to the plant. The other, the low affinity transport system (LATS), is activated under conditions of low nitrate concentration [71,72,78,81][2][3][10][13].
NRT transporters belong to three main families: the first, NRT1—or NPF—contains many genes, which can be divided into 8 to 10 subfamilies in Arabidopsis, which are predominantly low-affinity transporters [71,78,80,82][2][10][12][14]. The other families—NRT2/NRT3 (NAR2)—play an important role in the high-affinity transport of NO3− [72,80][3][12]. As in Arabidopsis, NRTs have been identified in rice, sorghum and maize and show differences in gene numbers and family structure. Studies show that in the corn genome there are four copies of genes of the ZmNRT2 family, namely: ZmNRT2.1, ZmNRT2.2, ZmNRT2.3 and ZmNRT2.5, of which only two were studied: ZmNRT2.1 and ZmNRT2.2, that have about 98% homology in their amino acid sequence [81][13]. Both are inducible to NO3− in seedling roots, having been found transcripts of the former in the region of the root cortex while, for the latter, in the cortex, stele, and lateral primordia of the roots [83][15].
For the NRT3 family, two copies of the NRT3.1 gene were described in the maize genome: ZmNRT3.1A and ZmNRT3.1B, both never characterized in maize, but which are strong candidates in the NO3− transport complex [72,84,85][3][16][17] More recently, Wang et al. [86][18], after analyzing the proteome of two contrasting hybrids for the efficiency in the use of nitrogen, verified the function of the ZmTGA gene and the study found that the gene has an important role in maintaining the tolerance of plants in low conditions. N, giving greater length and area of the root system, greater shoot/root ratio, in addition to lower leaf senescence compared when comparing the mutant with the wild type. TGA transcription factors are a very important group of the bZIP (basic leucine zipper) family [87][19] and can bind to the -1 (as-1) activation sequence with TGACG as the core and activate or inhibit the translation of downstream target genes, having, therefore, an important role in the defense and response of plants to various biotic and abiotic stresses, such as low nitrogen availability. Furthermore, studies show that plants with overexpression of the TGA1 or TGA4 genes show a significant increase in the nitrate transporter genes NRT2.1 and NRT2.2 [88[20][21],89], whose functions we discussed earlier.
Ammonium is also a direct source of nitrogen taken up by plant roots, but, in general, the ammonium content in unfertilized soils is up to 1000 times lower than that of nitrate. [90][22]. However, efficient ammonium uptake is critical for optimal plant growth and development, as it confers several beneficial effects, such as root density and corn seedling length [91,92][23][24] or enhanced H+ proton extrusion, which subsequently acidifies the rhizosphere and leads to increased bioavailability of poorly soluble nutrients such as P or Fe [93][25]. Therefore, this NH4+ absorption process is expected to be highly regulated under adverse conditions of N availability in the soil.
Whenever the ammonium concentration in the soil solution is low, the contribution of high-affinity transport systems (HATSs) becomes more relevant to the overall ammonium uptake by roots [93][25]. In general, high-affinity ammonium transport is mediated by AMT1-type ammonium transporters: ZmAMT1; 1a and ZmAMT1; 3, which belong to the ammonium/methylammonium permease/rhesus transporters (AMT/MEP/Rh) [93,94][25][26].
The two ZmAMTs confer high-affinity ammonium transport activities and are localized in the plasma membrane of maize root epidermal cells. Furthermore, their gene expressions are induced by ammonium, and one study revealed high correlations with high-affinity ammonium and increased root influx rates [93][25]. Although ZmAMT1; 1a e ZmAMT1; 3 are likely to be the main components for ammonium uptake in the root, not much is known about their physiological contribution to N uptake and use efficiency [94][26].

2. Nitrogen Reduction and Assimilation

Once incorporated, nitrate is reduced to nitrite in plant cells in a reaction that takes place in the cytosol and is catalyzed by a nitrate reductase (NR) [95,96][27][28]. The nitrite is then translocated to plastids and chloroplasts, where it is reduced to ammonium by the enzyme nitrite reductase (NiR). Nitrate-derived ammonium, or that produced by photorespiration or amino acid recycling, is more assimilated in plastids by the GS/GOGAT cycle [97,98][29][30].
Ammonium is attached to glutamate to form glutamine by glutamine synthase (GS; family of Gln genes), of which there is a plastid isoform (GS2) and a cytosolic isoform (GS1). In maize, a single gene encodes GS2 (Gln2), while at least 5 genes encode GS1 (Gln1-1 to Gln1-5), which are differentially expressed during development [77,99,100,101][9][31][32][33].
Glutamate can serve as an amino acid donor to other amino acids and nitrogen-requiring compounds, or act as an amine acceptor in the GS-GOGAT cycle to regenerate glutamine. Plants have two types of GOGAT enzymes—NADH-GOGAT and Fd-GOGAT—which use NADH and ferredoxin as electron donors, respectively [102][34]. Different parallels of GOGAT show constitutive or tissue-specific activity in plants, including maize [99][31]. Ferridoxine-GOGAT is localized in leaf chloroplasts, while NADH-GOGAT is expressed in non-photosynthetic tissues, including root plastids [97][29]. After nitrogen assimilation, glutamine, glutamate and other amino acids, including asparagine and aspartate, are transported by vascular tissues to growing organs [97][29]. Nitrate and ammonium can also be stored in vacuoles before or after long-distance transport.

3. Translocation and Remobilization of Nitrogen

During senescence, leaf proteins and photosynthetic proteins are extensively degraded, becoming a huge source of nitrogen, which plants can exploit to supplement the nutrition of growing organs [97][29].
During the grain filling period, the absorption and assimilation of nitrogen are often insufficient for the high demand required at this stage, making re-mobilization in the different organs of the plant necessary to direct nitrogen to the seeds [98][30]. The contribution of this process to supplying N in cereals such as rice, wheat and corn varies according to the cultivar, at rates of 50 to 90% [97][29]. N remobilization also depends on the environment and is favored under conditions of nitrate limitation [103][35].
In this sense, glutamine (Gln) is the main amino acid translocated in cereals as a source of N. Therefore, in senescence, glutamine concentrations increase in the phloem sap, being remobilized to the reproductive organs. In this process, GS and GOGAT enzymes are important for the remobilization and reuse of N in senescent and developing organs, respectively [80,104][12][36]. Some studies have shown that GS1-1 is responsible for this process and that NADH-GOGAT1 plays a key role in the reuse of Gln transported in the developing organs of rice [104,105][36][37]. In maize, wheat, and barley, grain N content is correlated with senescence of flag leaves and appears to play a significant role in N availability for grain filling [72,100,105][3][32][37].

References

  1. Kang, J.; Turano, F.J. The Putative Glutamate Receptor 1.1 (AtGLR1.1) Functions as a Regulator of Carbon and Nitrogen Metabolism in Arabidopsis Thaliana. Proc. Natl. Acad. Sci. USA 2003, 100, 6872–6877.
  2. Raddatz, N.; Morales de los Ríos, L.; Lindahl, M.; Quintero, F.J.; Pardo, J.M. Coordinated Transport of Nitrate, Potassium, and Sodium. Front. Plant Sci. 2020, 11, 247.
  3. Zuluaga, D.L.; Sonnante, G. The Use of Nitrogen and Its Regulation in Cereals: Structural Genes, Transcription Factors, and the Role of MiRNAs. Plants 2019, 8, 294.
  4. Andrews, M.; Lea, P.J. Our Nitrogen ‘Footprint’: The Need for Increased Crop Nitrogen Use Efficiency. Ann. Appl. Biol. 2013, 163, 165–169.
  5. Simons, M.; Saha, R.; Guillard, L.; Clement, G.; Armengaud, P.; Canas, R.; Maranas, C.D.; Lea, P.J.; Hirel, B. Nitrogen-Use Efficiency in Maize (Zea mays L.): From “omics” Studies to Metabolic Modelling. J. Exp. Bot. 2014, 65, 5657–5671.
  6. Plett, D.C.; Holtham, L.R.; Okamoto, M.; Garnett, T.P. Nitrate Uptake and Its Regulation in Relation to Improving Nitrogen Use Efficiency in Cereals. Semin. Cell Dev. Biol. 2018, 74, 97–104.
  7. Engineer, C.B.; Kranz, R.G. Reciprocal Leaf and Root Expression of AtAmt1.1 and Root Architectural Changes in Response to Nitrogen Starvation. Plant Physiol. 2007, 143, 236–250.
  8. Ma, N.; Dong, L.; Lü, W.; Lü, J.; Meng, Q.; Liu, P. Transcriptome Analysis of Maize Seedling Roots in Response to Nitrogen-, Phosphorus-, and Potassium Deficiency. Plant Soil 2020, 447, 637–658.
  9. Vidal, E.A.; Moyano, T.C.; Krouk, G.; Katari, M.S.; Tanurdzic, M.; McCombie, W.R.; Coruzzi, G.M.; Gutiérrez, R.A. Integrated RNA-Seq and SRNA-Seq Analysis Identifies Novel Nitrate-Responsive Genes in Arabidopsis Thaliana Roots. BMC Genom. 2013, 14, 701.
  10. Fan, X.; Naz, M.; Fan, X.; Xuan, W.; Miller, A.J.; Xu, G. Plant Nitrate Transporters: From Gene Function to Application. J. Exp. Bot. 2017, 68, 2463–2475.
  11. Yang, Z.; Wang, Z.; Yang, C.; Yang, Z.; Li, H.; Wu, Y. Physiological Responses and Small RNAs Changes in Maize under Nitrogen Deficiency and Resupply. Genes Genom. 2019, 41, 1183–1194.
  12. Wang, Y.; Yao, Q.; Zhang, Y.; Zhang, Y.; Xing, J.; Yang, B.; Mi, G.; Li, Z.; Zhang, M. The Role of Gibberellins in Regulation of Nitrogen Uptake and Physiological Traits in Maize Responding to Nitrogen Availability. Int. J. Mol. Sci. 2020, 21, 1824.
  13. Dechorgnat, J.; Francis, K.L.; Dhugga, K.S.; Rafalski, J.A.; Tyerman, S.D.; Kaiser, B.N. Tissue and Nitrogen-Linked Expression Profiles of Ammonium and Nitrate Transporters in Maize. BMC Plant Biol. 2019, 19, 206.
  14. Ohkubo, Y.; Kuwata, K.; Matsubayashi, Y. A Type 2C Protein Phosphatase Activates High-Affinity Nitrate Uptake by Dephosphorylating NRT2.1. Nat. Plants 2021, 7, 310–316.
  15. Trevisan, S.; Borsa, P.; Botton, A.; Varotto, S.; Malagoli, M.; Ruperti, B.; Quaggiotti, S. Expression of Two Maize Putative Nitrate Transporters in Response to Nitrate and Sugar Availability. Plant Biol. 2008, 10, 462–475.
  16. Sinha, S.; Sevanthi, V.A.; Chaudhary, S.; Tyagi, P.; Venkadesan, S.; Rani, M.; Mandal, P. 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 2018, 9, 206.
  17. Goel, P.; Sharma, N.K.; Bhuria, M.; Sharma, V.; Chauhan, R.; Pathania, S.; Swarnkar, M.K.; Chawla, V.; Acharya, V.; Shankar, R.; et al. Transcriptome and Co-Expression Network Analyses Identify Key Genes Regulating Nitrogen Use Efficiency in Brassica juncea L. Sci. Rep. 2018, 8, 7451.
  18. Wang, Y.; Wang, N.; Liu, S.; Dong, A.; Zenda, T.; Liu, X.; Li, J.; Duan, H. Comparative Proteomic Analysis of Two Contrasting Maize Hybrids’ Responses to Low Nitrogen Stress at the Twelve Leaf Stage and Function Verification of ZmTGA Gene. Genes 2022, 13, 670.
  19. Jakoby, M.; Weisshaar, B.; Dröge-Laser, W.; Vicente-Carbajosa, J.; Tiedemann, J.; Kroj, T.; Parcy, F. BZIP Transcription Factors in Arabidopsis. Trends Plant Sci. 2002, 7, 106–111.
  20. Alvarez, J.M.; Riveras, E.; Vidal, E.A.; Gras, D.E.; Contreras-López, O.; Tamayo, K.P.; Aceituno, F.; Gómez, I.; Ruffel, S.; Lejay, L.; et al. Systems Approach Identifies TGA1 and TGA4 Transcription Factors as Important Regulatory Components of the Nitrate Response of Arabidopsis Thaliana Roots. Plant J. 2014, 80, 12618.
  21. Zhong, L.; Chen, D.; Min, D.; Li, W.; Xu, Z.; Zhou, Y.; Li, L.; Chen, M.; Ma, Y. AtTGA4, a BZIP Transcription Factor, Confers Drought Resistance by Enhancing Nitrate Transport and Assimilation in Arabidopsis Thaliana. Biochem. Biophys. Res. Commun. 2015, 457, 433–439.
  22. Marschner, H. Marschner’s Mineral Nutrition of Higher Plants; Elsevier: Amsterdam, The Netherlands, 2012; ISBN 9780123849052.
  23. Taylor, A.R.; Bloom, A.J. Ammonium, Nitrate, and Proton Fluxes along the Maize Root. Plant Cell Environ. 1998, 21, 1255–1263.
  24. Bloom, A.J.; Meyerhoff, P.A.; Taylor, A.R.; Rost, T.L. Root Development and Absorption of Ammonium and Nitrate from the Rhizosphere. J. Plant Growth Regul. 2002, 21, 416–431.
  25. Gu, R.; Duan, F.; An, X.; Zhang, F.; von Wirén, N.; Yuan, L. Characterization of AMT-Mediated High-Affinity Ammonium Uptake in Roots of Maize (Zea mays L.). Plant Cell Physiol. 2013, 54, 1515–1524.
  26. Zhao, S.; Li, C.-I.; Guo, Y.; Sheng, Q.; Shyr, Y. RnaSeqSampleSize: Real Data Based Sample Size Estimation for RNA Sequencing. BMC Bioinform. 2018, 19, 191.
  27. Meyer, C.; Stitt, M. Nitrate Reduction and Signalling. In Plant Nitrogen; Springer: Berlin/Heidelberg, Germany, 2001; pp. 37–59.
  28. Wang, Y.-Y.; Cheng, Y.-H.; Chen, K.-E.; Tsay, Y.-F. Nitrate Transport, Signaling, and Use Efficiency. Annu. Rev. Plant Biol. 2018, 69, 85–122.
  29. Masclaux-Daubresse, C.; Daniel-Vedele, F.; Dechorgnat, J.; Chardon, F.; Gaufichon, L.; Suzuki, A. Nitrogen Uptake, Assimilation and Remobilization in Plants: Challenges for Sustainable and Productive Agriculture. Ann. Bot. 2010, 105, 1141–1157.
  30. Asibi, A.E.; Chai, Q.; Coulter, J.A. Mechanisms of Nitrogen Use in Maize. Agronomy 2019, 9, 775.
  31. Sakakibara, H.; Kawabata, S.; Hase, T.; Sugiyama, T. Differential Effects of Nitrate and Light on the Expression of Glutamine Synthetases and Ferredoxin-Dependent Glutamate Synthase in Maize. Plant Cell Physiol. 1992, 33, 1193–1198.
  32. Martin, A.; Lee, J.; Kichey, T.; Gerentes, D.; Zivy, M.; Tatout, C.; Dubois, F.; Balliau, T.; Valot, B.; Davanture, M.; et al. Two Cytosolic Glutamine Synthetase Isoforms of Maize Are Specifically Involved in the Control of Grain Production. Plant Cell 2006, 18, 3252–3274.
  33. Liseron-Monfils, C.; Bi, Y.-M.; Downs, G.S.; Wu, W.; Signorelli, T.; Lu, G.; Chen, X.; Bondo, E.; Zhu, T.; Lukens, L.N.; et al. Nitrogen Transporter and Assimilation Genes Exhibit Developmental Stage-Selective Expression in Maize (Zea mays L.) Associated with Distinct Cis -Acting Promoter Motifs. Plant Signal. Behav. 2013, 8, e26056.
  34. Suzuki, A.; Knaff, D.B. Glutamate Synthase: Structural, Mechanistic and Regulatory Properties, and Role in the Amino Acid Metabolism. Photosynth. Res. 2005, 83, 191–217.
  35. Lemaitre, T.; Gaufichon, L.; Boutet-Mercey, S.; Christ, A.; Masclaux-Daubresse, C. Enzymatic and Metabolic Diagnostic of Nitrogen Deficiency in Arabidopsis thaliana Wassileskija Accession. Plant Cell Physiol. 2008, 49, 1056–1065.
  36. Tabuchi, M.; Abiko, T.; Yamaya, T. Assimilation of Ammonium Ions and Reutilization of Nitrogen in Rice (Oryza sativa L.). J. Exp. Bot. 2007, 58, 2319–2327.
  37. Uauy, C.; Distelfeld, A.; Fahima, T.; Blechl, A.; Dubcovsky, J. A NAC Gene Regulating Senescence Improves Grain Protein, Zinc, and Iron Content in Wheat. Science 2006, 314, 1298–1301.
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