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Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Nitrogen supply in combination of nitrate and ammonium enhances harnessing of elevated atmospheric CO2 through improved nitrogen and carbon metabolism in wheat (Triticum aestivum)

Muhammad Asif A C , Seray Zora B , Yasemin Ceylan A , Raheela Rehman A and Levent Ozturk A D
+ Author Affiliations
- Author Affiliations

A Faculty of Engineering and Natural Sciences, Sabanci University, Tuzla, 34956 Istanbul, Turkey.

B Department of Bioengineering, Faculty of Chemistry and Metallurgy, Yildiz Technical University, Istanbul, Turkey.

C Department of Plant Breeding and Genetics, University of Agriculture Faisalabad, University Main Rd, Faisalabad, Punjab 38000, Pakistan.

D Corresponding author. Email: Lozturk@sabanciuniv.edu

Crop and Pasture Science 71(2) 101-112 https://doi.org/10.1071/CP19308
Submitted: 31 July 2019  Accepted: 21 November 2019   Published: 27 February 2020

Abstract

Elevated carbon dioxide (e-CO2) levels from ambient (a-CO2) enhance plant biomass production and yield. However, this response is highly dependent on the availability and possibly the form of nitrogen (N) supply to plants. This study aimed to investigate changes in C and N metabolism of wheat (Triticum aestivum L.) in response to e-CO2 and N source. e-CO2 enhanced net CO2 assimilation but at highly variable rates depending on the form of N supply. Under e-CO2, net CO2 assimilation rate was in the order NO3 > NH4NO3 > NH4+ > urea. Plants supplied with ammonium and nitrate (i.e. NH4NO3) performed better in terms of biomass production and expressed a higher biomass enhancement ratio by e-CO2 than plants receiving sole applications of NO3, NH4+ or urea. Supply of NH4NO3 also resulted in lower intercellular CO2, higher photoassimilate translocation to roots and lower accumulation of free amino acids than other N forms, indicating a better exploitation of the e-CO2 environment. Our results conclude that major physiological pathways of photosynthesis and protein and carbohydrate metabolism are differentially influenced by e-CO2 depending on the source of N supply. A balanced supply of NO3 and NH4+ to plant roots is the key to harnessing e-CO2 while minimising its adverse effects on quality of the produce.

Additional keywords: climate change, crop productivity, nitrogen form, nutritional quality.


References

Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165, 351–372.
What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2.Crossref | GoogleScholarGoogle Scholar | 15720649PubMed |

Amthor JS (2001) Effects of atmospheric CO2 concentration on wheat yield: review of results from experiments using various approaches to control CO2 concentration. Field Crops Research 73, 1–34.
Effects of atmospheric CO2 concentration on wheat yield: review of results from experiments using various approaches to control CO2 concentration.Crossref | GoogleScholarGoogle Scholar |

Andrews M, Condron LM, Kemp PD, Topping JF, Lindsey K, Hodge S, Raven JA (2019) Elevated CO2 effects on nitrogen assimilation and growth of C3 vascular plants are similar regardless of N-form assimilated. Journal of Experimental Botany 70, 683–690.
Elevated CO2 effects on nitrogen assimilation and growth of C3 vascular plants are similar regardless of N-form assimilated.Crossref | GoogleScholarGoogle Scholar | 30403798PubMed |

Aranjuelo I, Cabrerizo PM, Arrese-Igor C, Aparicio-Tejo PM (2013) Pea plant responsiveness under elevated [CO2] is conditioned by the N source (N2 fixation versus NO3– fertilization). Environmental and Experimental Botany 95, 34–40.
Pea plant responsiveness under elevated [CO2] is conditioned by the N source (N2 fixation versus NO3 fertilization).Crossref | GoogleScholarGoogle Scholar |

Asif M, Yilmaz O, Ozturk L (2017) Potassium deficiency impedes elevated carbon dioxide-induced biomass enhancement in well watered or drought-stressed bread wheat. Journal of Plant Nutrition and Soil Science 180, 474–481.
Potassium deficiency impedes elevated carbon dioxide-induced biomass enhancement in well watered or drought-stressed bread wheat.Crossref | GoogleScholarGoogle Scholar |

Asif M, Tunc CE, Yazici MA, Tutus Y, Rehman R, Rehman A, Ozturk L (2019) Effect of predicted climate change on growth and yield performance of wheat under varied nitrogen and zinc supply. Plant and Soil 434, 231–244.
Effect of predicted climate change on growth and yield performance of wheat under varied nitrogen and zinc supply.Crossref | GoogleScholarGoogle Scholar |

Barber MJ, Notton BA (1990) Spinach nitrate reductase. Effects of ionic strength and pH on the full and partial enzyme activities. Plant Physiology 93, 537–540.
Spinach nitrate reductase. Effects of ionic strength and pH on the full and partial enzyme activities.Crossref | GoogleScholarGoogle Scholar | 16667499PubMed |

Bloom AJ, Smart DR, Nguyen DT, Searles PS (2002) Nitrogen assimilation and growth of wheat under elevated carbon dioxide. Proceedings of the National Academy of Sciences of the United States of America 99, 1730–1735.
Nitrogen assimilation and growth of wheat under elevated carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 11818528PubMed |

Bloom AJ, Burger M, Asensio JSR, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328, 899–903.
Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 20466933PubMed |

Bloom AJ, Rubio-Asensio JS, Randall L, Rachmilevitch S, Cousins AB, Carlisle EA (2012) CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants. Ecology 93, 355–367.
CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants.Crossref | GoogleScholarGoogle Scholar | 22624317PubMed |

Carlisle E, Myers S, Raboy V, Bloom A (2012) The effects of inorganic nitrogen form and CO2 concentration on wheat yield and nutrient accumulation and distribution. Frontiers in Plant Science 3, 195
The effects of inorganic nitrogen form and CO2 concentration on wheat yield and nutrient accumulation and distribution.Crossref | GoogleScholarGoogle Scholar | 22969784PubMed |

Chaillou S, Vessey JK, Morot-Gaudry JF, Raper CD, Henry LT, Boutin JP (1991) Expression of characteristics of ammonium nutrition as affected by pH of the root medium. Journal of Experimental Botany 42, 189–196.
Expression of characteristics of ammonium nutrition as affected by pH of the root medium.Crossref | GoogleScholarGoogle Scholar | 11537730PubMed |

Cox WJ, Reisenauer HM (1973) Growth and ion uptake by wheat supplied nitrogen as nitrate, or ammonium, or both. Plant and Soil 38, 363–380.
Growth and ion uptake by wheat supplied nitrogen as nitrate, or ammonium, or both.Crossref | GoogleScholarGoogle Scholar |

Cramer M, Lewis OAM (1993) The Influence of nitrate and ammonium nutrition on the growth of wheat (Triticum aestivum) and maize (Zea mays) plants. Annals of Botany 72, 359–365.
The Influence of nitrate and ammonium nutrition on the growth of wheat (Triticum aestivum) and maize (Zea mays) plants.Crossref | GoogleScholarGoogle Scholar |

Criddle RS, Ward MR, Huffaker RC (1988) Nitrogen uptake by wheat seedlings, interactive effects of four nitrogen sources, NO3–, NO2–, NH4+, and urea. Plant Physiology 86, 166–175.
Nitrogen uptake by wheat seedlings, interactive effects of four nitrogen sources, NO3, NO2, NH4+, and urea.Crossref | GoogleScholarGoogle Scholar | 11538231PubMed |

Cui H, Shi Z, Cai J, Jiang D, Cao W, Dai T (2011) Effects of atmospheric CO2 concentration enhancement and nitrogen application rate on wheat grain yield and quality. Journal of Applied Ecology 22, 979–984.

FAO (2017) World fertilizer trends and outlook to 2020. Summary Report. Food and Agriculture Organization of the United Nations, Rome. Available at: http://www.fao.org/3/a-i6895e.pdf (accessed 23 December 2018).

Feng GQ, Li Y, Cheng ZM (Max) (2014) Plant molecular and genomic responses to stresses in projected future CO2 environment. Critical Reviews in Plant Sciences 33, 238–249.
Plant molecular and genomic responses to stresses in projected future CO2 environment.Crossref | GoogleScholarGoogle Scholar |

Fernando N, Hirotsu N, Panozzo J, Tausz M, Norton RM, Seneweera S (2017) Lower grain nitrogen content of wheat at elevated CO2 can be improved through post-anthesis NH4+ supplement. Journal of Cereal Science 74, 79–85.
Lower grain nitrogen content of wheat at elevated CO2 can be improved through post-anthesis NH4+ supplement.Crossref | GoogleScholarGoogle 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 & Environment 22, 1177–1199.
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.Crossref | GoogleScholarGoogle Scholar |

Geissler N, Hussin S, Koyro HW (2009) Elevated atmospheric CO2 concentration ameliorates effects of NaCl salinity on photosynthesis and leaf structure of Aster tripolium L. Journal of Experimental Botany 60, 137–151.
Elevated atmospheric CO2 concentration ameliorates effects of NaCl salinity on photosynthesis and leaf structure of Aster tripolium L.Crossref | GoogleScholarGoogle Scholar | 19036838PubMed |

Gray SB, Dermody O, Klein SP, Locke AM, McGrath JM, Paul RE, Rosenthal DM, Ruiz-Vera UM, Siebers MH, Strellner R, Ainsworth EA, Bernacchi CJ, Long SP, Ort DR, Leakey AD (2016) Intensifying drought eliminates the expected benefits of elevated carbon dioxide for soybean. Nature Plants 2, 16132
Intensifying drought eliminates the expected benefits of elevated carbon dioxide for soybean.Crossref | GoogleScholarGoogle Scholar | 27595230PubMed |

Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Molle IS, White P (2012) Functions of macronutrients. In ‘Marschner’s mineral nutrition of higher plants’. (Ed. P Marschner) pp. 135–189. (Academic Press: Cambridge, MA, USA)

Högy P, Wieser H, Köhler P, Schwadorf K, Breuer J, Franzaring J, Muntifering R, Fangmeier A (2009) Effects of elevated CO2 on grain yield and quality of wheat, results from a 3-year free-air CO2 enrichment experiment. Plant Biology 11, 60–69.
Effects of elevated CO2 on grain yield and quality of wheat, results from a 3-year free-air CO2 enrichment experiment.Crossref | GoogleScholarGoogle Scholar | 19778369PubMed |

IPCC (2013) Climate change 2013, the physical science basis. In ‘Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change’. (Eds TF Stocker, D Qin, GK Plattner et al.) (Cambridge University Press: Cambridge, UK)

Jin J, Armstrong R, Tang C (2019) Impact of elevated CO2 on grain nutrient concentration varies with crops and soils—a long-term FACE study. The Science of the Total Environment 651, 2641–2647.
Impact of elevated CO2 on grain nutrient concentration varies with crops and soils—a long-term FACE study.Crossref | GoogleScholarGoogle Scholar | 30463119PubMed |

Kirschbaum MUF (2011) Does enhanced photosynthesis enhance growth? Lessons learned from CO2 enrichment studies. Plant Physiology 155, 117–124.
Does enhanced photosynthesis enhance growth? Lessons learned from CO2 enrichment studies.Crossref | GoogleScholarGoogle Scholar |

Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations, six important lessons from FACE. Journal of Experimental Botany 60, 2859–2876.
Elevated CO2 effects on plant carbon, nitrogen, and water relations, six important lessons from FACE.Crossref | GoogleScholarGoogle Scholar |

Li F, Kang S, Zhang J (2004) Interactive effects of elevated CO2, nitrogen and drought on leaf area, stomatal conductance, and evapotranspiration of wheat. Agricultural Water Management 67, 221–233.
Interactive effects of elevated CO2, nitrogen and drought on leaf area, stomatal conductance, and evapotranspiration of wheat.Crossref | GoogleScholarGoogle Scholar |

Li B, Xin W, Sun S, Sun S, Shen Q, Xu G (2006) Physiological and molecular responses of nitrogen-starved rice plants to re-supply of different nitrogen sources. Plant and Soil 287, 145–159.
Physiological and molecular responses of nitrogen-starved rice plants to re-supply of different nitrogen sources.Crossref | GoogleScholarGoogle Scholar |

Lopes MS, Araus JL (2006) Nitrogen source and water regime effects on durum wheat photosynthesis and stable carbon and nitrogen isotope composition. Physiologia Plantarum 126, 435–445.
Nitrogen source and water regime effects on durum wheat photosynthesis and stable carbon and nitrogen isotope composition.Crossref | GoogleScholarGoogle Scholar |

Lopes MS, Nogués S, Araus JL (2004) Nitrogen source and water regime effects on barley photosynthesis and isotope signature. Functional Plant Biology 31, 995
Nitrogen source and water regime effects on barley photosynthesis and isotope signature.Crossref | GoogleScholarGoogle Scholar |

Madan P, Jagadish SVK, Craufurd PQ, Fitzgerald M, Lafarge T, Wheeler TR (2012) Effect of elevated CO2 and high temperature on seed-set and grain quality of rice. Journal of Experimental Botany 63, 3843–3852.
Effect of elevated CO2 and high temperature on seed-set and grain quality of rice.Crossref | GoogleScholarGoogle Scholar | 22438302PubMed |

Matt P, Geiger M, Walch-Liu P, Engels C, Krapp A, Stitt M (2001) Elevated carbon dioxide increases nitrate uptake and nitrate reductase activity when tobacco is growing on nitrate, but increases ammonium uptake and inhibits nitrate reductase activity when tobacco is growing on ammonium nitrate. Plant, Cell & Environment 24, 1119–1137.
Elevated carbon dioxide increases nitrate uptake and nitrate reductase activity when tobacco is growing on nitrate, but increases ammonium uptake and inhibits nitrate reductase activity when tobacco is growing on ammonium nitrate.Crossref | GoogleScholarGoogle Scholar |

Mérigout P, Gaudon V, Quilleré I, Briand X, Daniel-Vedele F (2008a) Urea use efficiency of hydroponically grown maize and wheat. Journal of Plant Nutrition 31, 427–443.
Urea use efficiency of hydroponically grown maize and wheat.Crossref | GoogleScholarGoogle Scholar |

Mérigout P, Lelandais M, Bitton F, Renou JP, Briand X, Meyer C, Daniel-Vedele F (2008b) Physiological and transcriptomic aspects of urea uptake and assimilation in Arabidopsis plants. Plant Physiology 147, 1225–1238.
Physiological and transcriptomic aspects of urea uptake and assimilation in Arabidopsis plants.Crossref | GoogleScholarGoogle Scholar | 18508958PubMed |

Mitchell RAC, Mitchell VJ, Driscoll SP, Franklin J, Lawlor DW (1993) Effects of increased CO2 concentration and temperature on growth and yield of winter wheat at two levels of nitrogen application. Plant, Cell & Environment 16, 521–529.
Effects of increased CO2 concentration and temperature on growth and yield of winter wheat at two levels of nitrogen application.Crossref | GoogleScholarGoogle Scholar |

Nasraoui-Hajaji A, Gouia H (2014) Photosynthesis sensitivity to NH4+-N change with nitrogen fertilizer type. Plant, Soil and Environment 60, 274–279.
Photosynthesis sensitivity to NH4+-N change with nitrogen fertilizer type.Crossref | GoogleScholarGoogle Scholar |

NOAA (2019) ESRL Global Monitoring Division. Global Greenhouse Gas Reference Network. National Oceanic & Atmospheric Administration, US Department of Commerce, Washington, DC. https//www.esrl.noaa.gov/gmd/ccgg/trends/gl_full.html (accessed 17 April 2019).

Norby RJ, Cotrufo MF, Ineson P, O’Neill EG, Canadell JG (2001) Elevated CO2, litter chemistry, and decomposition, a synthesis. Oecologia 127, 153–165.
Elevated CO2, litter chemistry, and decomposition, a synthesis.Crossref | GoogleScholarGoogle Scholar | 24577644PubMed |

Qian X, Shen QR, Xu GH, Wang J, Zhou M (2004) Nitrogen form effects on yield and nitrogen uptake of rice crop grown in aerobic soil. Journal of Plant Nutrition 27, 1061–1076.
Nitrogen form effects on yield and nitrogen uptake of rice crop grown in aerobic soil.Crossref | GoogleScholarGoogle Scholar |

Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440, 922–925.
Nitrogen limitation constrains sustainability of ecosystem response to CO2.Crossref | GoogleScholarGoogle Scholar | 16612381PubMed |

Roosta HR, Schjoerring JK (2007) Effects of ammonium toxicity on nitrogen metabolism and elemental profile of cucumber plants. Journal of Plant Nutrition 30, 1933–1951.
Effects of ammonium toxicity on nitrogen metabolism and elemental profile of cucumber plants.Crossref | GoogleScholarGoogle Scholar |

Rosenthal DM, Locke AM, Khozaei M, Raines CA, Long SP, Ort DR (2011) Over-expressing the C3 photosynthesis cycle enzyme sedoheptulose-1-7 bisphosphatase improves photosynthetic carbon gain and yield under fully open air CO2 fumigation (FACE). BMC Plant Biology 11, 123
Over-expressing the C3 photosynthesis cycle enzyme sedoheptulose-1-7 bisphosphatase improves photosynthetic carbon gain and yield under fully open air CO2 fumigation (FACE).Crossref | GoogleScholarGoogle Scholar | 21884586PubMed |

Rubio-Asensio JS, Bloom AJ (2017) Inorganic nitrogen form: a major player in wheat and Arabidopsis responses to elevated CO2. Journal of Experimental Botany 68, 2611–2625.

Sadasivam S, Manickam A (1996) Proteins and amino acids. In ‘Biochemical methods’. pp. 32–97. (New Age International: New Delhi)

Siddiqi MY, Malhotra B, Min X, Glass AD (2002) Effects of ammonium and inorganic carbon enrichment on growth and yield of a hydroponic tomato crop. Journal of Plant Nutrition and Soil Science 165, 191–197.
Effects of ammonium and inorganic carbon enrichment on growth and yield of a hydroponic tomato crop.Crossref | GoogleScholarGoogle Scholar |

Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition, the physiological and molecular background. Plant, Cell & Environment 22, 583–621.
The interaction between elevated carbon dioxide and nitrogen nutrition, the physiological and molecular background.Crossref | GoogleScholarGoogle Scholar |

Tausz M, Bilela S, Bahrami H, Armstrong R, Fitzgerald G, Oeary G, Simon J, Tausz-Posch S, Rennenberg H (2017) Nitrogen nutrition and aspects of root growth and function of two wheat cultivars under elevated [CO2]. Environmental and Experimental Botany 140, 1–7.
Nitrogen nutrition and aspects of root growth and function of two wheat cultivars under elevated [CO2].Crossref | GoogleScholarGoogle Scholar |

Thompson M, Gamage D, Hirotsu N, Martin A, Seneweera S (2017) Effects of elevated carbon dioxide on photosynthesis and carbon partitioning: a perspective on root sugar sensing and hormonal crosstalk. Frontiers in Physiology 8, 578
Effects of elevated carbon dioxide on photosynthesis and carbon partitioning: a perspective on root sugar sensing and hormonal crosstalk.Crossref | GoogleScholarGoogle Scholar | 28848452PubMed |

Van Oosten JJ, Besford RT (1994) Sugar feeding mimics effect of acclimation to high CO2- rapid down regulation of RuBisCO small subunit transcripts but not of the large subunit transcripts. Journal of Plant Physiology 143, 306–312.
Sugar feeding mimics effect of acclimation to high CO2- rapid down regulation of RuBisCO small subunit transcripts but not of the large subunit transcripts.Crossref | GoogleScholarGoogle Scholar |

Van Oosten JJ, Wilkins D, Besford RT (1994) Regulation of the expression of photosynthetic nuclear genes by CO2 is mimicked by regulation by carbohydrates, a mechanism for the acclimation of photosynthesis to high CO2? Plant, Cell & Environment 17, 913–923.
Regulation of the expression of photosynthetic nuclear genes by CO2 is mimicked by regulation by carbohydrates, a mechanism for the acclimation of photosynthesis to high CO2?Crossref | GoogleScholarGoogle Scholar |

Wang XT, Below FE (1995) Tillering, nutrient accumulation, and yield of winter wheat as influenced by nitrogen form. Journal of Plant Nutrition 18, 1177–1189.
Tillering, nutrient accumulation, and yield of winter wheat as influenced by nitrogen form.Crossref | GoogleScholarGoogle Scholar |

Wang L, Feng Z, Schjoerring JK (2013) Effects of elevated atmospheric CO2 on physiology and yield of wheat (Triticum aestivum L.), a meta-analytic test of current hypotheses. Agriculture, Ecosystems & Environment 178, 57–63.
Effects of elevated atmospheric CO2 on physiology and yield of wheat (Triticum aestivum L.), a meta-analytic test of current hypotheses.Crossref | GoogleScholarGoogle Scholar |

Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. The Biochemical Journal 57, 508–514.

Zong YZ, Shangguan ZP (2014) Nitrogen deficiency limited the improvement of photosynthesis in maize by elevated CO2 under drought. Journal of Integrative Agriculture 13, 73–81.
Nitrogen deficiency limited the improvement of photosynthesis in maize by elevated CO2 under drought.Crossref | GoogleScholarGoogle Scholar |