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Magnesium supports nitrogen uptake through regulating NRT2.1/2.2 in soybean

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Abstract

Aims

Nitrogen (N) and magnesium (Mg) are two of the essential elements for plant growth. Application of Mg may increase N use efficiency in plants, but the mechanisms underlying Mg and N interaction are not well understood. The objectives of this study were to assess how Mg supply affects N uptake in soybean, and to further investigate underlying molecular mechanisms.

Methods

Soybean (Glycine max L.) seedlings were provided with various concentrations of Mg under different N conditions in hydroponic cultures. Biomass, nutrient and sugar concentrations, and gene expression were determined. Tissue specificity of gene expression was performed in hairy-root transformants.

Results

Increasing Mg supply enhanced N concentration and total N uptake in soybean. The promotive effect is due to the enhanced uptake of nitrate but not ammonium. Moreover, elevating nitrate supply can partially restore growth retardation and leaf chlorosis caused by low Mg availability. A comparative transcriptomic study revealed that two Nitrate Transporter 2 (NRT2) family genes NRT2.1 and NRT2.2 were positively regulated by Mg in roots. Both NRT2.1 and 2.2 are mainly expressed in the exodermis and epidermis of soybean roots, suggesting roles in nitrate uptake. In addition, under low-Mg conditions, expression of NRT2.1 and 2.2 and subsequent N uptake were restored upon exogenous addition of sucrose, implying the possibility that Mg may regulate NRT2.1/2.2 expression through facilitation of sucrose allocation.

Conclusions

The results of this study indicate that Mg promotes N uptake through positive regulation of NRT2.1/2.2 expression in soybean roots. This Mg-induced gene expression appears to act through-facilitation of sucrose allocation from shoots to roots.

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Abbreviations

DW:

Dry weight

Mg:

Magnesium

N:

Nitrogen

N2 :

Dinitrogen

NUE:

Nitrogen use efficiency

References

  • Afza R, Hardarson G, Zapata F, Danso SKA (1987) Effects of delayed soil and foliar N fertilization on yield and N2 fixation of soybean. Plant Soil 97(3):361–368

    Google Scholar 

  • Amarasinghe BHRR, de Bruxelles GL, Braddon M, Onyeocha I, Forde BG, Udvardi MK (1998) Regulation of GmNRT2 expression and nitrate transport activity in roots of soybean (Glycine max). Planta 206(1):44–52

    CAS  PubMed  Google Scholar 

  • Andrews (1986) The partitioning of nitrate assimilation between root and shoot of higher plants. Plant Cell Environ 9(7):511–519

    CAS  Google Scholar 

  • Bloom AJ (2006) Assimilation of mineral nutrients. In: Taiz L, Zeiger E (eds) Plant physiology, 3rd edn. Sinauer Associates, Inc., Sunderland, pp 290–313

  • Bloom AJ (2015) Photorespiration and nitrate assimilation: a major intersection between plant carbon and nitrogen. Photosynth Res 123(2):117–128

    CAS  PubMed  Google Scholar 

  • Bloom AJ, Sukrapanna SS, Warner RL (1992) Root respiration associated with ammonium and nitrate absorption and assimilation by barley. Plant Physiol 99:1294–1301

    CAS  PubMed  PubMed Central  Google Scholar 

  • Briskin DP (1990) The plasma membrane H+-ATPase of higher plant cells: biochemistry and transport function. Biochim Biophys Acta 1019(2):95–109

    CAS  Google Scholar 

  • Cakmak I, Kirkby EA (2008) Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol Plant 133:692–704

    CAS  PubMed  Google Scholar 

  • Chen LY, Liao H (2017) Engineering crop nutrient efficiency for sustainable agriculture. J Integr Plant Biol 59(10):710–735

    PubMed  Google Scholar 

  • Chen XP, Cui ZL, Vitousek PM, Cassman KG, Matson PA, Bai JS, Meng QF, Hou P, Yue SC, Römheld V, Zhang FS (2011) Integrated soil-crop system management for food security. Proc Natl Acad Sci U S A 108(16):6399–6404

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen ZC, Peng WT, Li J, Liao H (2018) Functional dissection and transport mechanism of magnesium in plants. Semin Cell Dev Biol 74:142–152

    CAS  PubMed  Google Scholar 

  • Chiou TJ, Bush DR (1998) Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci U S A 95(8):4784–4788

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442(7105):939–942

    PubMed  Google Scholar 

  • De Jong F, Thodey K, Lejay LV, Bevan MW (2014) Glucose elevates NITRATE TRANSPORTER2.1 protein levels and nitrate transport activity independently of its HEXOKINASE1-mediated stimulation of NITRATE TRANSPORTER2.1 expression. Plant Physiol 164(1):308–320

    PubMed  Google Scholar 

  • Dromantienė R, Pranckietienė I, Šidlauskas G, Smalstienė V (2017) The effect of Mg and S on photosynthesis products and nitrogen content in winter wheat. In: Raupelienė A (ed) Proceedings of the 8th International Scientific Conference Rural Development, Aleksandras Stulginskis University, Kaunas, pp 42–46

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78(1):9–19

    PubMed  Google Scholar 

  • Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63(9):3367–3377

    CAS  PubMed  Google Scholar 

  • Fan XR, Tang Z, Tan YW, Zhang Y, Luo BB, Yang M, Lian XM, Shen QR, Miller AJ, Xu GH (2016) Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. Proc Natl Acad Sci U S A 113(26):7118–7123

    CAS  PubMed  PubMed Central  Google Scholar 

  • von der Fecht-Bartenbach J, Bogner M, Dynowski M, Ludewig U (2010) CLC-b-mediated NO3/H+ exchange across the tonoplast of Arabidopsis vacuoles. Plant Cell Physiol 51(6):960–968

    PubMed  Google Scholar 

  • Feng HM, Yan M, Fan XR, Li BZ, Shen QR, Miller AJ, Xu GH (2011) Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status. J Exp Bot 62(7):2319–2332

    CAS  PubMed  Google Scholar 

  • Goulding K, Jarvis S, Whitmore A (2008) Optimizing nutrient management for farm systems. Philos Trans R Soc Lond Ser B Biol Sci 363(1491):667–680

    CAS  Google Scholar 

  • Grzebisz W (2013) Crop response to magnesium fertilization as affected by nitrogen supply. Plant Soil 368(1–2):23–39

    CAS  Google Scholar 

  • Grzebisz W, Przygocka-Cyna K, Szczepaniak W, Diatta J, Potarzycki J (2010) Magnesium as a nutritional tool of nitrogen efficient management-plant production and environment. J Elem 15(4):771–788

    Google Scholar 

  • Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KW, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327(5968):1008–1010

    CAS  PubMed  Google Scholar 

  • Guo WB, Zhao J, Li XX, Qin L, Yan XL, Liao H (2011) A soybean β-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. Plant J 66:541–552

    CAS  PubMed  Google Scholar 

  • Hansson M, Lundqvist J, Sirijovski N, Al-Karadaghi S, Subunits IMC (2013) Magnesium chelatase: the molecular motor of chlorophyll biosynthesis. In: Ferreira GC (ed) Handbook of porphyrin science. World Scientific Publishing, Singapore, pp 41–84

    Google Scholar 

  • Hermans C, Verbruggen N (2005) Physiological characterization of mg deficiency in Arabidopsis thaliana. J Exp Bot 56:2153–2161

    CAS  PubMed  Google Scholar 

  • Hikosaka K, Terashima I (1996) Nitrogen partitioning among photosynthetic components and its consequence in sun and shade plants. Funct Ecol 10(3):335–343

    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(9):2369–2387

    CAS  PubMed  Google Scholar 

  • Huang ZA, Jiang DA, Yang Y, Sun JW, Jin SH (2004) Effects of nitrogen deficiency on gas exchange, chlorophyll fluorescence and antioxidant enzymes in leaves of rice plants. Photosynthetica 42:357–364

    CAS  Google Scholar 

  • Kalaji HM, Dąbrowski P, Cetner MD, Izabela A, Samborska IA, Łukasik I, Brestic M, Zivcak M, Tomasz H, Mojski J, Kociel H, Panchal BM (2017) A comparison between different chlorophyll content meters under nutrient deficiency conditions. J Plant Nutr 40(7):1024–1034

    CAS  Google Scholar 

  • Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62(4):1399–1409

    CAS  PubMed  Google Scholar 

  • Kiba T, Feria-Bourrellier AB, Lafouge F, Lezhneva L, Boutet-Mercey S, Orsel M, Bréhaut V, Miller A, Daniel-Vedele F, Sakakibara H, Krapp A (2012) The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell 24(1):245–258

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lawlor DW, Lemaire G, Gastal F (2001) Nitrogen, plant growth and crop yield. In: Lea PJ, Morot-Gaudry JF (eds) Plant Nitrogen. Springer, Berlin, pp 343–367

    Google Scholar 

  • Li W, Wang Y, Okamoto M, Crawford NM, Siddiqi MY, Glass AD (2007) Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiol 143(1):425–433

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu XJ, Zhang Y, Han WX, Tang AH, Shen JL, Cui ZL, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang FS (2013) Enhanced nitrogen deposition over China. Nature 494(7438):459–462

    CAS  PubMed  Google Scholar 

  • Maathuis FJ (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12(3):250–258

    CAS  PubMed  Google Scholar 

  • Makino A, Osmond B (1991) Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat. Plant Physiol 96:355–362

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mengel K, Kirkby EA, Kosegarten H, Appel T (2001) Nitrogen. In: Mengel K, Kirkby EA, Kosegarten H, Appel T (eds) Principles of plant nutrition, 5th edn. Kluwer Academic Publishers, Dordrecht, pp 397–434

    Google Scholar 

  • Mueller ND, Lassaletta L, Runck BC, Billen G, Garnier J, Gerber JS (2017) Declining spatial efficiency of global cropland nitrogen allocation. Global Biogeochem CY 31(2):245–257

    CAS  Google Scholar 

  • Peng WT, Zhang LD, Zhou Z, Fu C, Chen ZC, Liao H (2018) Magnesium promotes root nodulation through facilitation of carbohydrate allocation in soybean. Physiol Plant 163(3):372–385

    CAS  Google Scholar 

  • Potarzycki J (2011) Effect of magnesium or zinc supplementation at the background of nitrogen rate on nitrogen management by maize canopy cultivated in monoculture. Plant Soil Environ 57(1):19–25

    CAS  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    CAS  PubMed  Google Scholar 

  • Salsac L (1987) Nitrate and ammonium nutrition in plants. Plant Physiol Biochem 25:805–812

    Google Scholar 

  • Salvagiotti F, Cassman KG, Specht JE, Walters DT, Weiss A, Dobermann A (2008) Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review. Field Crops Res 108(1):1–13

    Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178–183

    CAS  PubMed  Google Scholar 

  • Shen Y, Ryde U (2005) Reaction mechanism of porphyrin metallation studied by theoretical methods. Chem Eur J 11(5):1549–1564

    CAS  PubMed  Google Scholar 

  • Shoemaker RC, Polzin K, Labate J, Specht J, Brummer EC, Olson T, Young N, Concibido V, Wilcox J, Tamulonis JP, Kochert G, Boerma HR (1996) Genome duplication in soybean (Glycine subgenus soja). Genetics 144(1):329–338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sinclair TR, De Wit CT (1975) Photosynthate and nitrogen requirements for seed production by various crops. Science 189(4202):565–567

    CAS  PubMed  Google Scholar 

  • Singh RJ, Hymowitz T (1999) Soybean genetic resources and crop improvement. Genome 42(4):605–616

    CAS  Google Scholar 

  • Sorgonà A, Lupini A, Mercati F, Di Dio L, Sunseri F, Abenavoli MR (2011) Nitrate uptake along the maize primary root: an integrated physiological and molecular approach. Plant Cell Environ 34(7):1127–1140

    PubMed  Google Scholar 

  • Spiertz JHJ (2010) Nitrogen, sustainable agriculture and food security: a review. Agron Sustain Dev 30:43–55

    CAS  Google Scholar 

  • Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2(3):178–186

    CAS  PubMed  Google Scholar 

  • Szulc P (2010) Effects of differentiated levels of nitrogen fertilization and the method of magnesium application on the utilization of nitrogen by two different maize cultivars for grain. Pol J Environ Stud 19(2):407–412

    CAS  Google Scholar 

  • Tilman D, Balzer C, Hill J, Befort BL (2011) Global food demand and the sustainable intensification of agriculture. Proc Natl Acad Sci U S A 108(50):20260–20264

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uchida R (2000) Essential nutrients for plant growth: nutrient functions and deficiency symptoms. In: Silva JA, Uchida R (eds) Plant nutrient management in Hawaii’s soils. College of Tropical Agriculture and Human Resources, University of Hawaii, Honolulu, pp 31–55

    Google Scholar 

  • Verbruggen N, Hermans C (2013) Physiological and molecular responses to magnesium nutritional imbalance in plants. Plant Soil 368:87–99

    CAS  Google Scholar 

  • Vidal EA, Gutiérrez RA (2008) A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Curr Opin Plant Biol 11(5):521–529

    CAS  PubMed  Google Scholar 

  • Walker CJ, Weinstein JD (1994) The magnesium-insertion step of chlorophyll biosynthesis is a two-stage reaction. Biochem J 299(1):277–284

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17(8):458–467

    CAS  PubMed  Google Scholar 

  • Wang YY, Cheng YH, Chen KE, Tsay YF (2018) Nitrate transport, signaling, and use efficiency. Annu Rev Plant Biol 69:85–122

    CAS  PubMed  Google Scholar 

  • Willows RD (2003) Biosynthesis of chlorophylls from protoporphyrin IX. Nat Prod Rep 20(3):327–341

    CAS  PubMed  Google Scholar 

  • Wu W, Ma BL (2015) Integrated nutrient management (INM) for sustaining crop productivity and reducing environmental impact: a review. Sci Total Environ 512:415–427

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Yang N, Jiang JL, Xie HL, Bai MY, Xu QZ, Wang XG, Yu XM, Chen ZC, Guan YF (2017) Metabolomics reveals distinct carbon and nitrogen metabolic responses to magnesium deficiency in leaves and roots of soybean [Glycine max (Linn.) Merr.]. Front Plant Sci 8:2091

    PubMed  PubMed Central  Google Scholar 

  • Zhang X (2017) A plan for efficient use of nitrogen fertilizers. Nature 543(7645):322–323

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (grant number 31872171); and the China National Key Program for Research and Development (grant number 2016YFD0100700); and the China National Key Program for Research and Development (grant number 2016YFD0100401). We thank Dr. Thomas Walk and Golden Fidelity LLC for careful review of the manuscript.

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Correspondence to Zhi Chang Chen.

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Peng, W.T., Qi, W.L., Nie, M.M. et al. Magnesium supports nitrogen uptake through regulating NRT2.1/2.2 in soybean. Plant Soil 457, 97–111 (2020). https://doi.org/10.1007/s11104-019-04157-z

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