, Volume 26, Issue 2, pp 133–140 | Cite as

Arbuscular mycorrhiza improve growth, nitrogen uptake, and nitrogen use efficiency in wheat grown under elevated CO2

  • Xiancan Zhu
  • Fengbin Song
  • Shengqun Liu
  • Fulai LiuEmail author
Original Article


Effects of the arbuscular mycorrhizal (AM) fungus Rhizophagus irregularis on plant growth, carbon (C) and nitrogen (N) accumulation, and partitioning was investigated in Triticum aestivum L. plants grown under elevated CO2 in a pot experiment. Wheat plants inoculated or not inoculated with the AM fungus were grown in two glasshouse cells with different CO2 concentrations (400 and 700 ppm) for 10 weeks. A 15N isotope labeling technique was used to trace plant N uptake. Results showed that elevated CO2 increased AM fungal colonization. Under CO2 elevation, AM plants had higher C concentration and higher plant biomass than the non-AM plants. CO2 elevation did not affect C and N partitioning in plant organs, while AM symbiosis increased C and N allocation into the roots. In addition, plant C and N accumulation, 15N recovery rate, and N use efficiency (NUE) were significantly higher in AM plants than in non-AM controls under CO2 enrichment. It is concluded that AM symbiosis favors C and N partitioning in roots, increases C accumulation and N uptake, and leads to greater NUE in wheat plants grown at elevated CO2.


Arbuscular mycorrhiza C/N partitioning C/N accumulation 15N recovery rate Nitrogen use efficiency Triticum aestivum



This study was financially supported by the Key Research Program of the Chinese Academy of Sciences (KZZD-EW-TZ-16) and the China Scholarship Council. We are thankful for the assistance provided by Xiangnan Li and Fan Fan in the experiment.


  1. 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 Phytol 165:351–371CrossRefPubMedGoogle Scholar
  2. Aljazairi S, Arias C, Nogues S (2015) Carbon and nitrogen allocation and partitioning in traditional and modern wheat genotypes under pre-industrial and future CO2 conditions. Plant Biol 17:647–659CrossRefPubMedGoogle Scholar
  3. Baslam M, Erice G, Goicoechea N (2012) Impact of arbuscular mycorrhizal fungi (AMF) and atmospheric CO2 concentration on the biomass production and partitioning in the forage legume alfalfa. Symbiosis 58:171–181CrossRefGoogle Scholar
  4. Baslam M, Antolin MC, Gogorcena Y, Munoz F, Goicoechea N (2014) Changes in alfalfa forage quality and stem carbohydrates induced by arbuscular mycorrhizal fungi and elevated atmospheric CO2. Ann Appl Biol 164:190–199CrossRefGoogle Scholar
  5. Bloom AJ, Burger M, Kimball BA, Pinter PJ (2014) Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nat Clim Chang 4:437–440CrossRefGoogle Scholar
  6. Bunce JA (2001) Direct and acclamatory responses of stomatal conductance to elevated carbon dioxide in four herbaceous crop species in the field. Glob Chang Biol 7:323–331CrossRefGoogle Scholar
  7. Cavagnaro TR, Sokolow SK, Jackson LE (2007) Mycorrhizal effects on growth and nutrition of tomato under elevated atmospheric carbon dioxide. Funct Plant Biol 34:730–736CrossRefGoogle Scholar
  8. Cavagnaro TR, Gleadow RM, Miller RE (2011) Plant nutrient acquisition and utilization in a high carbon dioxide world. Funct Plant Biol 38:87–96CrossRefGoogle Scholar
  9. Chen X, Tu C, Burton MG, Watson DM, Burkey KO, Hu S (2007) Plant nitrogen acquisition and interactions under elevated carbon dioxide: impact of endophytes and mycorrhizae. Glob Chang Biol 13:1238–1249CrossRefGoogle Scholar
  10. Cheng L, Bllker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084CrossRefPubMedGoogle Scholar
  11. Compant S, van der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol 73:197–214PubMedGoogle Scholar
  12. Drake BG, Gonzalez-Meler MA, Long SP (1997) More efficient plants: consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639CrossRefPubMedGoogle Scholar
  13. Drigo B, Kowalchuk GA (2013) Rhizosphere responses to elevated CO2. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere. Volume 1 & 2. John Wiley & Sons, Inc, HobokenGoogle Scholar
  14. Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ, Boschker HTS, Bodelier PLE, Whiteley AS, van Veen JA, Kowalchuk GA (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci U S A 107:10938–10942PubMedCentralCrossRefPubMedGoogle Scholar
  15. Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bucking H (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 109:2666–2671PubMedCentralCrossRefPubMedGoogle Scholar
  16. Gamper H, Hartwig UA, Leuchtmann A (2005) Mycorrhizas improve nitrogen nutrition of Trifolium repens after 8 yr of selection under elevated atmospheric CO2 partial pressure. New Phytol 167:531–542CrossRefPubMedGoogle Scholar
  17. Gavito ME, Curtis PS, Mikkelsen TN, Jakobsen I (2000) Atmospheric CO2 and mycorrhiza effects on biomass allocation and nutrient uptake of nodulated pea (Pisum sativum L.) plants. J Exp Bot 51:1931–1938CrossRefPubMedGoogle Scholar
  18. Gianinazzi S, Gollotte A, Binet M, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530CrossRefPubMedGoogle Scholar
  19. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  20. Goicoechea N, Baslam M, Erice G, Irigoyen JJ (2014) Increased photosynthetic acclimation in alfalfa associated with arbuscular mycorrhizal fungi (AMF) and cultivated in greenhouse under elevated CO2. J Plant Physiol 171:1774–1781CrossRefPubMedGoogle Scholar
  21. Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823CrossRefPubMedGoogle Scholar
  22. He Z, Xiong J, Kent AD, Deng Y, Xue K, Wang G, Wu L, Van Nostrand JD, Zhou J (2014) Distinct responses of soil microbial communities to elevated CO2 and O3 in a soybean agro-ecosystem. ISME J 8:714–726PubMedCentralCrossRefPubMedGoogle Scholar
  23. IPCC (2013) Fifth assessment report on climate change 2013: the physical science basis. Final draft underlying scientific-technical assessment. Intergovernmental Panel on Climate Change, Working group l, GenevaGoogle Scholar
  24. Johnson NC, Gehring CA (2007) Mycorrhizas: symbiotic mediators of rhizosphere and ecosystems processes. In: Cardon ZG, Whitback J (eds) The rhizosphere: an ecological perspective. Elsevier, New York, pp 73–100CrossRefGoogle Scholar
  25. Kormanik PP, Bryan WC, Schultz RC (1980) Procedures and equipment for staining large numbers of plant root samples for endomycorrhizal assay. Can J Microbiol 26:536–538CrossRefPubMedGoogle Scholar
  26. Liu ZL, Li YJ, Hou HY, Zhu XC, Rai V, He XY, Tian CJ (2013) Differences in the arbuscular mycorrhizal fungi-improved rice resistance to low temperature at two N levels: aspects of N and C metabolism on the plant side. Plant Physiol Biochem 71:87–95CrossRefPubMedGoogle Scholar
  27. Mitsutoshi K, Takayoshi K, Hiroyuki T, Yutaka M (2005) Elevated CO2 and limited nitrogen nutrition can restrict excitation energy dissipation in photosystem II of Japanese white birch (Betula platyphylla var. japonica) leaves. Physiol Plant 125:64–73CrossRefGoogle Scholar
  28. Mohan JE, Cowden CC, Baas P, Dawadi A, Frankson PT, Helmick K, Hughes E, Khan S, Lang A, Machmuller M, Taylor M, Witt CA (2014) Mycorrhizal fungi mediation of terrestrial ecosystem responses to global change: mini-review. Fungal Ecol 10:3–19CrossRefGoogle Scholar
  29. NOAA-ESRL (2015) National oceanic and atmospheric administration-earth system research laboratory. Atmospheric CO2 for Feb. 2015.
  30. Pacholski A, Manderscheid R, Weigel HJ (2015) Effects of free air CO2 enrichment on root growth of barley, sugar beet and wheat growth in a rotation under different nitrogen supply. Eur J Agron 63:36–46CrossRefGoogle Scholar
  31. Rillig MC, Wright SF, Allen MF, Field CB (1999) Rise in carbon dioxide changes soil structure. Nature 400:628CrossRefGoogle Scholar
  32. Rillig MC, Treseder KK, Allen MF (2002) Global change and mycorrhizal fungi. In: van der Heijden MGA, Sanders I (eds) Mycorrhizal ecology. Springer Verlag, Berlin, pp 135–160CrossRefGoogle Scholar
  33. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, LondonGoogle Scholar
  34. Staddon PL (2005) Mycorrhizal fungi and environmental change: the need for a mycocentric approach. New Phytol 167:635–637CrossRefPubMedGoogle Scholar
  35. Staddon PL, Fitter AH, Robinson D (1999) Effects of mycorrhizal colonization and elevated atmospheric carbon dioxide on carbon fixation and below-ground carbon partitioning in Plantago lanceolata. J Exp Bot 50:853–860CrossRefGoogle Scholar
  36. Treseder KK, Egerton-Warburton LM, Allen MF, Cheng Y, Oechel WC (2003) Alteration of soil carbon pools and communities of mycorrhizal fungi in chaparral exposed to elevated carbon dioxide. Ecosystems 6:786–796CrossRefGoogle Scholar
  37. Xu Z, Shimizu H, Yagasaki Y, Ito S, Zheng Y, Zhou G (2013) Interactive effects of elevated CO2, drought, and warming on plants. J Plant Growth Regul 32:692–707CrossRefGoogle Scholar
  38. Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421CrossRefGoogle Scholar
  39. Zavalloni C, Vicca S, Buscher M, de la Providencia IE, de Boulois HD, Declerck S, Nijs I, Ceulemans R (2012) Exposure to warming and CO2 enrichment promotes greater above-ground biomass, nitrogen, phosphorus and arbuscular mycorrhizal colonization in newly established grasslands. Plant Soil 359:121–136CrossRefGoogle Scholar
  40. Zhu XC, Song FB, Liu FL, Liu SQ, Tian CJ (2015) Carbon and nitrogen metabolism in arbuscular mycorrhizal maize plants under low-temperature stress. Crop Pasture Sci 66(1):62–70Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Xiancan Zhu
    • 1
    • 2
  • Fengbin Song
    • 1
  • Shengqun Liu
    • 1
  • Fulai Liu
    • 2
    Email author
  1. 1.Northeast Institute of Geography and AgroecologyChinese Academy of SciencesChangchunPeople’s Republic of China
  2. 2.Department of Plant and Environmental Sciences, Faculty of ScienceUniversity of CopenhagenTaastrupDenmark

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