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.
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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.
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
Alberton O, Kuyper TW, Gorissen A (2005) Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO2. New Phytol 167:859–868
Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383
Bowes G (1993) Facing the inevitable: plants and increasing atmospheric CO2. Annu Rev Plant Biol 44:309–332
Camacho C, Coulouris G, Avagyan V et al (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421
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
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://email@example.com/(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
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
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
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
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
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
Fox J, Weisberg S (2011) An R Companion to Applied Regression, 2nd edn. Sage Publications, Thousand Oaks, CA
Frew A, Price JN (2019) Mycorrhizal-mediated plant-herbivore interactions in a high CO2 world. Funct Ecol 33:1376–1385
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
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
Groves R, Whalley R (2002) Grass and grassland ecology in Australia. Flora Aust 43:157–182
Güsewell S (2004) N : P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266
Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789
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
Johnson NC, Graham JH (2013) The continuum concept remains a useful framework for studying mycorrhizal functioning. Plant Soil 363:411–419
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
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
Koide RT, Li M (1989) Appropriate controls for vesicular–arbuscular mycorrhiza research. New Phytol 111:35–44
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
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
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
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
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
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
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
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
Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584
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
Sharp D, Simon BK (2002) AusGrass: grasses of Australia. CSIRO, Melbourne, Australia
Shipley B, Meziane D (2002) The balanced-growth hypothesis and the allometry of leaf and root biomass allocation. Funct Ecol 16:326–331
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
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
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
Staddon PL, Fitter AH (1998) Does elevated atmospheric carbon dioxide affect arbuscular mycorrhizas? Trends Ecol Evol 13:455–458
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
Terrer C, Vicca S, Hungate BA et al (2016) Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353:72–74
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
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
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
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
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
Veresoglou SD, Anderson IC, de Sousa NMF et al (2016) Resilience of fungal communities to elevated CO2. Microb Ecol 72:493–495
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
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
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
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
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14
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.
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).
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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 (2021). https://doi.org/10.1007/s00572-021-01025-6
- Allometric partitioning
- Arbuscular mycorrhizal fungi