Skip to main content

Advertisement

SpringerLink
Log in

Impacts of elevated atmospheric CO2 on arbuscular mycorrhizal fungi and their role in moderating plant allometric partitioning

  • Short Note
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Elevated atmospheric CO2 concentration (eCO2) effects on plants depend on several factors including plant photosynthetic physiology (e.g. C3, C4), soil nutrient availability and plants’ co-evolved soil-dwelling fungal symbionts, namely arbuscular mycorrhizal (AM) fungi. Complicated interactions among these components will determine the outcomes for plants. Therefore, clearer understanding is needed of how plant growth and nutrient uptake, along with root-colonising AM fungal communities, are simultaneously impacted by eCO2. We conducted a factorial growth chamber experiment with a C3 and a C4 grass species (± AM fungi and ± eCO2). We found that eCO2 increased plant biomass allocation towards the roots, but only in plants without AM fungi, potentially associated with an eCO2-driven increase in plant nutrient requirements. Furthermore, our data suggest a difference in the identities of root-colonising fungal taxa between ambient CO2 and eCO2 treatments, particularly in the C4 grass species, although this was not statistically significant. As AM fungi are ubiquitous partners of grasses, their response to increasing atmospheric CO2 is likely to have important consequences for how grassland ecosystems respond to global change.

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

Availability of data and material

The data that support the findings of this study are openly available in figshare repository at https://doi.org/10.6084/m9.figshare.12749864 (Frew et al. 2020). Raw DNA sequencing data are available under NCBI accession number PRJNA650012; representative sequences of each virtual taxon are available from GenBank accession numbers MT835028-MT835100.

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 Phytol 165:351–372

    PubMed  Google Scholar 

  • Alberton O, Kuyper TW, Gorissen A (2005) Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO2. New Phytol 167:859–868

    CAS  PubMed  Google Scholar 

  • Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383

    CAS  PubMed  Google Scholar 

  • Bowes G (1993) Facing the inevitable: plants and increasing atmospheric CO2. Annu Rev Plant Biol 44:309–332

    CAS  Google Scholar 

  • Camacho C, Coulouris G, Avagyan V et al (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421

    PubMed  PubMed Central  Google Scholar 

  • Chagnon PL, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491

    CAS  PubMed  Google Scholar 

  • Ciais P, Sabine C, Bala G, et al (2014) Carbon and other biogeochemical cycles. In: Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, pp 465–570

  • CM Iversen 2010 Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems New Phytol 346–357 https://doi.org/10.1111/j.1469-8137.2009.03122.x@10.1002/(ISSN)1469-8137(CAT)VirtualIssues(VI)ScalingRootProcessesGlobalImpacts

  • Compant S, Van Der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant–microorganism interactions. FEMS Microbiol Ecol 73:197–214

    CAS  PubMed  Google Scholar 

  • Cotton TEA, Fitter AH, Miller RM et al (2015) Fungi in the future: interannual variation and effects of atmospheric change on arbuscular mycorrhizal fungal communities. New Phytol 205:1598–1607

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong Y, Wang Z, Sun H et al (2018) The response patterns of arbuscular mycorrhizal and ectomycorrhizal symbionts under elevated CO2: a meta-analysis. Front Microbiol 9:1248

    PubMed  PubMed Central  Google Scholar 

  • Drigo B, Kowalchuk GA, Knapp BA et al (2013) Impacts of 3 years of elevated atmospheric CO2 on rhizosphere carbon flow and microbial community dynamics. Glob Change Biol 19:621–636

    Google Scholar 

  • Dumbrell AJ, Ashton PD, Aziz N et al (2011) Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190:794–804

    CAS  PubMed  Google Scholar 

  • Field KJ, Cameron DD, Leake JR et al (2012) Contrasting arbuscular mycorrhizal responses of vascular and non-vascular plants to a simulated Palaeozoic CO2 decline. Nat Commun 3:835

    PubMed  Google Scholar 

  • Fox J, Weisberg S (2011) An R Companion to Applied Regression, 2nd edn. Sage Publications, Thousand Oaks, CA

    Google Scholar 

  • Frew A, Price JN (2019) Mycorrhizal-mediated plant-herbivore interactions in a high CO2 world. Funct Ecol 33:1376–1385

    Google Scholar 

  • Frew A, Price JN, Oja J et al (2020) Arbuscular mycorrhizal fungi moderate changes in plant allometric partitioning and nutrient concentration under elevated atmospheric CO2. Figshare Digit Respository. https://doi.org/10.6084/m9.figshare.12749864.10.6084/m9.figshare.12749864

  • Ghannoum O, von Caemmerer S, Ziska L, Conroy JP (2001) The growth response of C4 plants to rising atmospheric CO2 partial pressure: a reassessment. Plant Cell Environ 23:931–942

    Google Scholar 

  • Grace EJ, Cotsaftis O, Tester M et al (2009) Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes. New Phytol 181:938–949

    CAS  PubMed  Google Scholar 

  • Groves R, Whalley R (2002) Grass and grassland ecology in Australia. Flora Aust 43:157–182

    Google Scholar 

  • Güsewell S (2004) N : P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    PubMed  Google Scholar 

  • Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789

    CAS  PubMed  Google Scholar 

  • Jin J, Tang C, Sale P (2015) The impact of elevated carbon dioxide on the phosphorus nutrition of plants: a review. Ann Bot 116:987–999

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson NC, Graham JH (2013) The continuum concept remains a useful framework for studying mycorrhizal functioning. Plant Soil 363:411–419

    CAS  Google Scholar 

  • Johnson NC, Wolf J, Reyes MA et al (2005) Species of plants and associated arbuscular mycorrhizal fungi mediate mycorrhizal responses to CO2 enrichment. Glob Change Biol 11:1156–1166

    Google Scholar 

  • Johnson SN, Gherlenda AN, Frew A, Ryalls JM (2016) The importance of testing multiple environmental factors in legume–insect research: replication, reviewers, and rebuttal. Front Plant Sci 7:489

    PubMed  PubMed Central  Google Scholar 

  • Koide RT, Li M (1989) Appropriate controls for vesicular–arbuscular mycorrhiza research. New Phytol 111:35–44

    Google Scholar 

  • Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    CAS  PubMed  Google Scholar 

  • Maček I, Clark DR, Šibanc N et al (2019) Impacts of long-term elevated atmospheric CO2 concentrations on communities of arbuscular mycorrhizal fungi. Mol Ecol 28:3445–3458

    PubMed  PubMed Central  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG et al (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115:495–501

    CAS  PubMed  Google Scholar 

  • Monz CA, Hunt HW, Reeves FB, Elliott ET (1994) The response of mycorrhizal colonization to elevated CO2 and climate change in Pascopyrum smithii and Bouteloua gracilis. Plant Soil 165:75–80

    CAS  Google Scholar 

  • Niu Y, Chai R, Dong H et al (2013) Effect of elevated CO2 on phosphorus nutrition of phosphate-deficient Arabidopsis thaliana (L.) Heynh under different nitrogen forms. J Exp Bot 64:355–367

    CAS  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Legendre P, et al (2015) vegan: Community Ecology Package. http://CRAN.R-project.org/package=vegan

  • Öpik M, Vanatoa A, Vanatoa E et al (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241

    PubMed  Google Scholar 

  • Reich PB, Hobbie SE, Lee TD, Pastore MA (2018) Unexpected reversal of C3 versus C4 grass response to elevated CO2 during a 20-year field experiment. Science 360:317–320

    CAS  PubMed  Google Scholar 

  • Reich PB, Tilman D, Craine J et al (2001) Do species and functional groups differ in acquisition and use of C, N and water under varying atmospheric CO2 and N availability regimes? A field test with 16 grassland species. New Phytol 150:435–448

    CAS  Google Scholar 

  • Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584

    PubMed  PubMed Central  Google Scholar 

  • Saks Ü, Davison J, Öpik M et al (2014) Root-colonizing and soil-borne communities of arbuscular mycorrhizal fungi in a temperate forest understorey. Botany 92:277–285

    Google Scholar 

  • Sharp D, Simon BK (2002) AusGrass: grasses of Australia. CSIRO, Melbourne, Australia

    Google Scholar 

  • Shipley B, Meziane D (2002) The balanced-growth hypothesis and the allometry of leaf and root biomass allocation. Funct Ecol 16:326–331

    Google Scholar 

  • Sikes BA, Cottenie K, Klironomos JN (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol 97:1274–1280

    Google Scholar 

  • Šmilauer P, Šmilauerová M, Kotilínek M, Košnar J (2020) Foraging speed and precision of arbuscular mycorrhizal fungi under field conditions: an experimental approach. Mol Ecol 29:1574–1587

    PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. Academic Press, Amsterdam, the Netherlands & Boston, MA

  • Spatafora JW, Chang Y, Benny GL et al (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Staddon PL, Fitter AH (1998) Does elevated atmospheric carbon dioxide affect arbuscular mycorrhizas? Trends Ecol Evol 13:455–458

    CAS  PubMed  Google Scholar 

  • Terrer C, Jackson RB, Prentice IC et al (2019) Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass. Nat Clim Change 9:684–689

    CAS  Google Scholar 

  • Terrer C, Vicca S, Hungate BA et al (2016) Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353:72–74

    CAS  PubMed  Google Scholar 

  • Thirkell TJ, Campbell M, Driver J et al (2020) Cultivar-dependent increases in mycorrhizal nutrient acquisition by barley in response to elevated CO2. Plants People Planet. https://doi.org/10.1002/ppp3.10174

    Article  Google Scholar 

  • Thirkell TJ, Pastok D, Field KJ (2020) Carbon for nutrient exchange between arbuscular mycorrhizal fungi and wheat varies according to cultivar and changes in atmospheric carbon dioxide concentration. Glob Change Biol 26:1725–1738

    Google Scholar 

  • Vandenkoornhuyse P, Mahé S, Ineson P et al (2007) Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. Proc Natl Acad Sci 104:16970–16975

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vasar M, Andreson R, Davison J et al (2017) Increased sequencing depth does not increase captured diversity of arbuscular mycorrhizal fungi. Mycorrhiza 27:761–773

    CAS  PubMed  Google Scholar 

  • Vasar M, Davison J, Neuenkamp L et al (2021) User-friendly bioinformatics pipeline gDAT (graphical downstream analysis tool) for analysing rDNA sequences. Mol Ecol Resour. https://doi.org/10.1111/1755-0998.13340

    Article  PubMed  Google Scholar 

  • Veresoglou SD, Anderson IC, de Sousa NMF et al (2016) Resilience of fungal communities to elevated CO2. Microb Ecol 72:493–495

    CAS  PubMed  Google Scholar 

  • Veresoglou SD, Menexes G, Rillig MC (2012) Do arbuscular mycorrhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010. Mycorrhiza 22:227–235

    PubMed  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wand SJE, Midgley GF, Jones MH, Curtis PS (1999) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Glob Change Biol 5:723–741

    Google Scholar 

  • Wang Y, Naumann U, Wright ST, Warton DI (2012) mvabund–an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3:471–474

    Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Google Scholar 

Download references

Acknowledgements

AF was supported by a Charles Sturt University Faculty of Science Postdoctoral Research Fellowship. MÖ and MV were supported by the European Regional Development Fund (Centre of Excellence EcolChange). The authors thank Joshua Hodges, John Davison, and the technical teams at Charles Sturt University and the University of Tartu for their support.

Funding

AF was supported by a Charles Sturt University Faculty of Science Postdoctoral Research Fellowship. MÖ and MV were supported by the European Regional Development Fund (Centre of Excellence EcolChange).

Author information

Authors and Affiliations

  1. Centre for Crop Health, School of Sciences, University of Southern Queensland, Toowoomba, QLD, Australia

    Adam Frew

  2. Institute for Land, Water and Society, Charles Sturt University, Albury, NSW, Australia

    Adam Frew & Jodi N Price

  3. Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia

    Jane Oja, Martti Vasar & Maarja Öpik

Authors
  1. Adam Frew
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jodi N Price
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jane Oja
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martti Vasar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maarja Öpik
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AF, JNP and MÖ conceived the study. AF and JNP conducted the study. AF, JO, MV and MÖ conducted molecular and bioinformatic analyses. AF conducted the statistical analyses, and all authors contributed to writing the manuscript.

Corresponding author

Correspondence to Adam Frew.

Ethics declarations

Consent for publication

All authors confirm their approval for submission of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 288 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Frew, A., Price, J.N., Oja, J. et al. Impacts of elevated atmospheric CO2 on arbuscular mycorrhizal fungi and their role in moderating plant allometric partitioning. Mycorrhiza 31, 423–430 (2021). https://doi.org/10.1007/s00572-021-01025-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-021-01025-6

Keywords

Search

Navigation