Skip to main content
SpringerLink
Log in

Elevated CO2 alters tissue balance of nitrogen metabolism and downregulates nitrogen assimilation and signalling gene expression in wheat seedlings receiving high nitrate supply

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Tissue and canopy-level evidence suggests that elevated carbon dioxide (EC) inhibits shoot nitrate assimilation in plants and thereby affects nitrogen (N) and protein content of the economic produce. It is speculated that species or genotypes relying more on root nitrate assimilation can adapt better under EC due to the improved/steady supply of reductants required for nitrate assimilation. A study was conducted to examine the effect of EC on N assimilation and associated gene expression in wheat seedlings. Wheat genotypes, BT-Schomburgk (BTS) with comparatively high leaf nitrate reductase (NR) activity and Gluyas Early (GE) with high root NR activity were grown in hydroponic culture for 30 days with two different nitrate levels (0.05 mM and 5 mM) in the climate controlled growth chambers maintained at either ambient (400 ± 10 μmol mol−1) or EC (700 ± 10 μmol mol−1) conditions. Exposure to EC downregulated the activity of enzyme NR and glutamate synthase (GOGAT) in leaf tissues, whereas in roots, activities of both the enzymes were upregulated by exposure to EC. In addition, EC downregulated N assimilation and signalling gene expression under high N availability. Root N assimilation was less affected in comparison with shoot N assimilation; thereby, the proportion of root contribution towards total assimilation was higher. The results suggest that EC could alter and re-programme N assimilation and signalling in wheat seedlings. The genotype and tissue-specific effects of EC on N assimilation also warrants the need for identification of suitable genotypes and revision of fertiliser regime for tapping the beneficial effects of EC conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adavi SB, Sathee L (2019) Elevated CO2-induced production of nitric oxide differentially modulates nitrate assimilation and root growth of wheat seedlings in a nitrate dose-dependent manner. Protoplasma 256:147–159

    CAS  PubMed  Google Scholar 

  • Agüera E, Ruano D, Cabello P, de la Haba P (2006) Impact of atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in cucumber (Cucumis sativus L.) plants. J Plant Physiol 163:809–817

    PubMed  Google Scholar 

  • Amthor JS (2001) Effects of atmospheric CO2 concentration on wheat yield: review of results from experiments using various approaches to control CO2 concentration. F Crop Res 73:1–34

    Google Scholar 

  • Arp WJ, Drake BG (1991) Increased photosynthetic capacity of Scirpus olneyi after 4 years of exposure to elevated CO2. Plant Cell Environ 14:1003–1006

    CAS  Google Scholar 

  • Backhausen JE, Emmerlich A, Holtgrefe S, Horton P, Nast G, Rogers JJM, Müller-Röber B, Scheibe R (1998) Transgenic potato plants with altered expression levels of chloroplast NADP-malate dehydrogenase: interactions between photosynthetic electron transport and malate metabolism in leaves and in isolated intact chloroplasts. Planta 207:105–114

    CAS  Google Scholar 

  • Beidler KV, Taylor BN, Strand AE, Cooper ER, Schönholz M, Pritchard SG (2015) Changes in root architecture under elevated concentrations of CO2 and nitrogen reflect alternate soil exploration strategies. New Phytol 205:1153–1163

    CAS  PubMed  Google Scholar 

  • Benlloch-Gonzalez M, Berger J, Bramley H, Rebetzke G, Palta JA (2014) The plasticity of the growth and proliferation of wheat root system under elevated CO2. Plant Soil 374:963–976

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bloom AJ, Smart DR, Nguyen DT, Searles PS (2002) Nitrogen assimilation and growth of wheat under elevated carbon dioxide. Proc Natl Acad Sci 99:1730–1735

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bloom AJ, Burger M, Asensio JSR, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science (80- ) 328:899–903

    CAS  Google Scholar 

  • Bloom AJ, Burger M, Kimball BA, Pinter PJ Jr (2014) Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nat Clim Chang 4:477–480

    CAS  Google Scholar 

  • Buchner P, Tausz M, Ford R, Leo A, Fitzgerald GJ, Hawkesford MJ, Tausz-Posch S (2015) Expression patterns of C-and N-metabolism related genes in wheat are changed during senescence under elevated CO2 in dry-land agriculture. Plant Sci 236:239–249

    CAS  PubMed  Google Scholar 

  • Bunce JA (2002) Carbon dioxide concentration at night affects translocation from soybean leaves. Ann Bot 90:399–403

    CAS  PubMed  PubMed Central  Google Scholar 

  • Conroy J, Hocking P (1993) Nitrogen nutrition of C3 plants at elevated atmospheric CO2 concentrations. Physiol Plant 89:570–576

    CAS  Google Scholar 

  • de Mothes MA, Knoppik D (1994) Effects of long-term enhanced CO2 partial pressure on gas exchange parameters and saccharide pools in wheat leaves. Photosynth (Czech Republic) 30(3):435–445

    Google Scholar 

  • Dong J, Li X, Chu W, Duan Z (2017) High nitrate supply promotes nitrate assimilation and alleviates photosynthetic acclimation of cucumber plants under elevated CO2. Sci Hortic (Amsterdam) 218:275–283

    CAS  Google Scholar 

  • Downes MT (1978) An improved hydrazine reduction method for the automated determination of low nitrate levels in freshwater. Water Res 12:673–675

    CAS  Google Scholar 

  • Foyer CH, Noctor G, Hodges M (2011) Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. J Exp Bot 62:1467–1482

    CAS  PubMed  Google Scholar 

  • Geiger M, Walch-Liu P, Engels C, Harnecker J, Schulze ED, Ludewig F, Sonnewald U, Scheible WR, Stitt M (1998) Enhanced carbon dioxide leads to a modified diurnal rhythm of nitrate reductase activity in older plants, and a large stimulation of nitrate reductase activity and higher levels of amino acids in young tobacco plants. Plant Cell Environ 21:253–268

    CAS  Google Scholar 

  • Geiger M, Haake V, Ludewig F, Sonnewald U, Stitt M (1999) The nitrate and ammonium nitrate supply have a major influence on the response of photosynthesis, carbon metabolism, nitrogen metabolism and growth to elevated carbon dioxide in tobacco. Plant Cell Environ 22:1177–1199

    Google Scholar 

  • Grimmer C, Komor E (1999) Assimilate export by leaves of Ricinus communis L. growing under normal and elevated carbon dioxide concentrations: the same rate during the day, a different rate at night. Planta 209:275–281

    CAS  PubMed  Google Scholar 

  • Hachiya T, Sugiura D, Kojima M, Sato S, Yanagisawa S, Sakakibara H, Terashima I, Noguchi K (2014) High CO2 triggers preferential root growth of Arabidopsis thaliana via two distinct systems under low pH and low N stresses. Plant Cell Physiol 55:269–280

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hawkesford M, Horst W, Kichey T et al (2012) Functions of macronutrients. In: Marschner’s mineral nutrition of higher plants. pp. 135–189

  • He X, Qu B, Li W, Zhao X, Teng W, Ma W, Ren Y, Li B, Li Z, Tong Y (2015) The nitrate-inducible NAC transcription factor TaNAC2-5A controls nitrate response and increases wheat yield. Plant Physiol 169:1991–2005. https://doi.org/10.1104/pp.15.00568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

    CAS  Google Scholar 

  • Ho C-H, Lin S-H, Hu H-C, Tsay Y-F (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194

    CAS  PubMed  Google Scholar 

  • Hocking PJ, Meyer CP (1991) Carbon dioxide enrichment decreases critical nitrate and nitrogen concentrations in wheat. J Plant Nutr 14:571–584

    Google Scholar 

  • Igamberdiev AU, Bykova NV, Lea PJ, Gardeström P (2001) The role of photorespiration in redox and energy balance of photosynthetic plant cells: a study with a barley mutant deficient in glycine decarboxylase. Physiol Plant 111:427–438

    CAS  PubMed  Google Scholar 

  • Iversen CM (2010) Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems. New Phytol 186:346–357

    PubMed  Google Scholar 

  • Jackson RB, Reynolds HL (1996) Nitrate and ammonium uptake for single-and mixed-species communities grown at elevated CO2. Oecologia 105:74–80

    CAS  PubMed  Google Scholar 

  • Jauregui I, Aparicio-Tejo PM, Avila C, Cañas R, Sakalauskiene S, Aranjuelo I (2016) Root--shoot interactions explain the reduction of leaf mineral content in Arabidopsis plants grown under elevated [CO2] conditions. Physiol Plant 158:65–79

    CAS  PubMed  Google Scholar 

  • Jayawardena DM, Heckathorn SA, Bista DR, Mishra S, Boldt JK, Krause CR (2017) Elevated CO2 plus chronic warming reduce nitrogen uptake and levels or activities of nitrogen-uptake and-assimilatory proteins in tomato roots. Physiol Plant 159:354–365

    CAS  PubMed  Google Scholar 

  • Jones JB (1987) Kjeldahl nitrogen determination—what’s in a name. J Plant Nutr 10(9–16):1675–1682

    CAS  Google Scholar 

  • Jin Z, Zhu Y, Li X, Dong Y, An Z (2015) Soil N retention and nitrate leaching in three types of dunes in the Mu Us desert of China. Sci Rep 5:14222

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kimball BA, Morris CF, Pinter PJ et al (2001) Elevated CO2, drought and soil nitrogen effects on wheat grain quality. New Phytol 150:295–303

    CAS  Google Scholar 

  • Klepper L, Flesher D, Hageman RH (1971) Generation of reduced nicotinamide adenine dinucleotide for nitrate reduction in green leaves. Plant Physiol 48:580–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kruse J, Hetzger I, Hänsch R, Mendel RR, Walch-Liu P, Engels C, Rennenberg H (2002) Elevated p CO2 favours nitrate reduction in the roots of wild-type tobacco (Nicotiana tabacum cv. Gat.) and significantly alters N-metabolism in transformants lacking functional nitrate reductase in the roots. J Exp Bot 53:2351–2367

    CAS  PubMed  Google Scholar 

  • la Mata L, la Haba P, Alamillo JM et al (2013) Elevated CO2 concentrations alter nitrogen metabolism and accelerate senescence in sunflower (Helianthus annuus L.) plants. Plant. Soil Environ 59:303–308

    Google Scholar 

  • Larios B, Agüera E, Cabello P et al (2004) The rate of CO2 assimilation controls the expression and activity of glutamine synthetase through sugar formation in sunflower (Helianthus annuus L.) leaves. J Exp Bot 55:69–75

    CAS  PubMed  Google Scholar 

  • Lekshmy S, Vanita J, Sangeeta K et al (2009) Effect of elevated carbon dioxide on kinetics of nitrate uptake in wheat roots. Indian J Plant Physiol 14:16–22

    CAS  Google Scholar 

  • Lekshmy S, Jain V, Khetarpal S et al (2016) Influence of elevated carbon dioxide and ammonium nutrition on growth and nitrogen metabolism in wheat (Triticum aestivum). Indian J Agric Sci 86:25–30

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2- ΔΔCT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Mahmoud D, Pandey R, Sathee L, et al (2020) Regulation of expression of genes associated with nitrate response by osmotic stress and combined osmotic and nitrogen deficiency stress in bread wheat (Triticum aestivum L.). Plant Physiol Reports 1–16

  • Mariscal V, Moulin P, Orsel M, Miller AJ, Fernández E, Galván A (2006) Differential regulation of the Chlamydomonas Nar1 gene family by carbon and nitrogen. Protist 157:421–433

    CAS  PubMed  Google Scholar 

  • Martin T, Oswald O, Graham IA (2002) Arabidopsis seedling growth, storage lipid mobilization, and photosynthetic gene expression are regulated by carbon: nitrogen availability. Plant Physiol 128:472–481

    CAS  PubMed  PubMed Central  Google Scholar 

  • McNally SF, Hirel B, Gadal P et al (1983) Glutamine synthetases of higher plants: evidence for a specific isoform content related to their possible physiological role and their compartmentation within the leaf. Plant Physiol 72:22–25

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miller AJ, Fan X, Shen Q, Smith SJ (2008) Amino acids and nitrate as signals for the regulation of nitrogen acquisition. J Exp Bot 59:111–119

    CAS  PubMed  Google Scholar 

  • Mohanty B, Fletcher JS (1980) Ammonium influence on nitrogen assimilating enzymes and protein accumulation in suspension cultures of Paul’s Scarlet rose. Physiol Plant 48:453–459

    CAS  Google Scholar 

  • Nair TVR, Abrol YP (1973) Nitrate reductase activity in developing wheat ears. Experientia 29:1480–1481

    CAS  Google Scholar 

  • Nie GY, Long SP, Garcia RL et al (1995) Effects of free-air CO2 enrichment on the development of the photosynthetic apparatus in wheat, as indicated by changes in leaf proteins. Plant Cell Environ 18:855–864

    CAS  Google Scholar 

  • O’Brien JA, Vega A, Bouguyon E et al (2016) Nitrate transport, sensing, and responses in plants. Mol Plant 9:837–856

    PubMed  Google Scholar 

  • Padhan BK, Sathee L, Meena HS, Adavi SB (2020) CO2 elevation accelerates phenology and alters carbon / nitrogen metabolism vis-à-vis ROS abundance in bread wheat. Front Plant Sci 11:1–18. https://doi.org/10.3389/fpls.2020.01061

    Article  Google Scholar 

  • Pleijel H, Uddling J (2011) Yield vs. quality trade-offs for wheat in response to carbon dioxide and ozone. Glob Chang Biol 18:596–605

    Google Scholar 

  • Porter JR, Xie L, Challinor AJ, Cochrane K, Howden SM, Iqbal MM, Lobell DB, Travasso MI (2014) Food security and food production systems. In: Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Field CB, VR Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, L.L.White LL (eds.)]. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA: 485–533

  • Qaderi MM, Reid DM (2008) Combined effects of temperature and carbon dioxide on plant growth and subsequent seed germinability of Silene noctiflora. Int J Plant Sci 169:1200–1209

    CAS  Google Scholar 

  • Quesada A, Fernández E et al (2000) Involvement of chloroplast and mitochondria redox valves in nitrate assimilation. Trends Plant Sci 5:463–464

    CAS  PubMed  Google Scholar 

  • Rachmilevitch S, Cousins AB, Bloom AJ (2004) Nitrate assimilation in plant shoots depends on photorespiration. Proc Natl Acad Sci 101:11506–11510

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rahayu YS, Walch-Liu P, Neumann G, Römheld V, von Wirén N, Bangerth F (2005) Root-derived cytokinins as long-distance signals for NO3--induced stimulation of leaf growth. J Exp Bot 56:1143–1152

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Schroeder PD, Radcliffe DE, Cabrera ML (2004) Rainfall timing and poultry litter application rate effects on phosphorus loss in surface runoff. J Environ Qual 33:2201–2209

    CAS  PubMed  Google Scholar 

  • Shimono H, Bunce JA (2009) Acclimation of nitrogen uptake capacity of rice to elevated atmospheric CO2 concentration. Ann Bot 103:87–94

    CAS  PubMed  Google Scholar 

  • Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621

    CAS  Google Scholar 

  • Taub DR, Wang X (2008) Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. J Integr Plant Biol 50:1365–1374

    CAS  PubMed  Google Scholar 

  • Tuba Z, Szente K, Koch J (1994) Response of photosynthesis, stomatal conductance, water use efficiency and production to long-term elevated CO2 in winter wheat. J Plant Physiol 144:661–668

    CAS  Google Scholar 

  • Uprety DC, Dwivedi N, Jain V, Mohan R (2002) Effect of elevated carbon dioxide concentration on the stomatal parameters of rice cultivars. Photosynthetica 40:315–319

    CAS  Google Scholar 

  • Vicente R, Pérez P, Martínez-Carrasco R, Feil R, Lunn JE, Watanabe M, Arrivault S, Stitt M, Hoefgen R, Morcuende R (2016) Metabolic and transcriptional analysis of durum wheat responses to elevated CO2 at low and high nitrate supply. Plant Cell Physiol 57:2133–2146. https://doi.org/10.1093/pcp/pcw131

    Article  CAS  PubMed  Google Scholar 

  • Walch-Liu P, Neumann G, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 51:227–237

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Yang T, Hao L, Yao S, Zhao Y, Lu W, Xiao K (2016) TabHLH1, a bHLHtype transcription factor gene in wheat, improves plant tolerance to P and N deprivation via regulation of nutrient transporter gene transcription and ROS homeostasis. Plant Physiol Biochem 104:99–113

    CAS  PubMed  Google Scholar 

  • Zerihun A, Gutschick VP, Bassirirad H (2000) Compensatory roles of nitrogen uptake and photosynthetic N-use efficiency in determining plant growth response to elevated CO2: evaluation using a functional balance model. Ann Bot 86:723–730

    CAS  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the ICAR-Indian Agricultural Research Institute for providing the necessary facilities.

Funding

This work was financially supported by the ICAR-Indian Agricultural Research Institute for funding (institute project-CRSCIARISIL20144047279). SAB was a recipient of ICAR-Junior research fellowship support, during the course of the study.

Author information

Author notes

  1. Sandeep B. Adavi and Lekshmy Sathee contributed equally to this work.

Authors and Affiliations

  1. Division of Plant Physiology, ICAR-Indian Agricultural Research Institute, New Delhi, India

    Sandeep B. Adavi & Lekshmy Sathee

Authors
  1. Sandeep B. Adavi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lekshmy Sathee
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SAB and LS conducted the experiments. LS finalised the experiments, designed primers and did the expression profiling and statistical analysis. LS and SAB together prepared the manuscript.

Corresponding author

Correspondence to Lekshmy Sathee.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Additional information

Handling Editor: Néstor Carrillo

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 4450 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Adavi, S.B., Sathee, L. Elevated CO2 alters tissue balance of nitrogen metabolism and downregulates nitrogen assimilation and signalling gene expression in wheat seedlings receiving high nitrate supply. Protoplasma 258, 219–233 (2021). https://doi.org/10.1007/s00709-020-01564-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-020-01564-3

Keywords

Search

Navigation