Common mycorrhizal networks (CMNs) formed by arbuscular mycorrhizal fungi (AMF) interconnect plants of the same and/or different species, redistributing nutrients and draining carbon (C) from the different plant partners at different rates. Here, we conducted a plant co-existence (intercropping) experiment testing the role of AMF in resource sharing and exploitation by simplified plant communities composed of two congeneric grass species (Panicum spp.) with different photosynthetic metabolism types (C3 or C4). The grasses had spatially separated rooting zones, conjoined through a root-free (but AMF-accessible) zone added with 15N-labeled plant (clover) residues. The plants were grown under two different temperature regimes: high temperature (36/32°C day/night) or ambient temperature (25/21°C day/night) applied over 49 days after an initial period of 26 days at ambient temperature. We made use of the distinct C-isotopic composition of the two plant species sharing the same CMN (composed of a synthetic AMF community of five fungal genera) to estimate if the CMN was or was not fed preferentially under the specific environmental conditions by one or the other plant species. Using the C-isotopic composition of AMF-specific fatty acid (C16:1ω5) in roots and in the potting substrate harboring the extraradical AMF hyphae, we found that the C3-Panicum continued feeding the CMN at both temperatures with a significant and invariable share of C resources. This was surprising because the growth of the C3 plants was more susceptible to high temperature than that of the C4 plants and the C3-Panicum alone suppressed abundance of the AMF (particularly Funneliformis sp.) in its roots due to the elevated temperature. Moreover, elevated temperature induced a shift in competition for nitrogen between the two plant species in favor of the C4-Panicum, as demonstrated by significantly lower 15N yields of the C3-Panicum but higher 15N yields of the C4-Panicum at elevated as compared to ambient temperature. Although the development of CMN (particularly of the dominant Rhizophagus and Funneliformis spp.) was somewhat reduced under high temperature, plant P uptake benefits due to AMF inoculation remained well visible under both temperature regimes, though without imminent impact on plant biomass production that actually decreased due to inoculation with AMF.

Laboratory of Fungal Biology Ecology Institute of Microbiology Czech Academy of Sciences Prague Czechia

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Aroca R., Porcel R., Ruiz-Lozano J. M. (2007). How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in PubMed

Augé R. M., Toler H. D., Saxton A. M. (2014). Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis. PubMed DOI PMC

Augé R. M., Toler H. D., Saxton A. M. (2015). Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. PubMed DOI

Bever J. D., Dickie I. A., Facelli E., Facelli J. M., Klironomos J., Moora M., et al. (2010). Rooting theories of plant community ecology in microbial interactions. PubMed DOI PMC

Bever J. D., Richardson S. C., Lawrence B. M., Holmes J., Watson M. (2009). Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. PubMed DOI

Bryla D. R., Eissenstat D. M. (2005). “Respiratory costs of mycorrhiza associations,” in

Bücking H., Kafle A. (2015). Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. DOI

Bücking H., Mensah J. A., Fellbaum C. R. (2016). Common mycorrhizal networks and their effect on the bargaining power of the fungal partner in the arbuscular mycorrhizal symbiosis. PubMed DOI PMC

Bukovská P., Bonkowski M., Konvalinková T., Beskid O., Hujslová M., Püschel D., et al. (2018). Utilization of organic nitrogen by arbuscular mycorrhizal fungi - is there a specific role for protists and ammonia oxidizers? PubMed DOI

Bunn R., Lekberg Y., Zabinski C. (2009). Arbuscular mycorrhizal fungi ameliorate temperature stress in thermophilic plants. PubMed DOI

Chandrasekaran M., Kim K., Krishnamoorthy R., Walitang D., Sundaram S., Joe M. M., et al. (2016). Mycorrhizal symbiotic efficiency on C3 and C4 plants under salinity stress - a meta-analysis. PubMed DOI PMC

Compant S., van der Heijden M. G. A., Sessitsch A. (2010). Climate change effects on beneficial plant-microorganism interactions. PubMed DOI

Compant S., van der Heijden M. G. A., Sessitsch A. (2013). “Soil warming effects on beneficial plant-microbe interactions,” in

R Core Team (2013).

Couillerot O., Ramirez-Trujillo A., Walker V., von Felten A., Jansa J., Maurhofer M., et al. (2013). Comparison of prominent PubMed DOI

Courty P. E., Doubková P., Calabrese S., Niemann H., Lehmann M. F., Vosátka M., et al. (2015). Species-dependent partitioning of C and N stable isotopes between arbuscular mycorrhizal fungi and their C3 and C4 hosts. DOI

Davison J., Moora M., Öpik M., Adholeya A., Ainsaar L., Ba A., et al. (2015). Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. PubMed DOI

Dessureault-Rompré J., Zebarth B. J., Georgallas A., Burton D. L., Grant C. A., Drurye C. F. (2010). Temperature dependence of soil nitrogen mineralization rate: comparison of mathematical models, reference temperatures and origin of the soils. DOI

Ehleringer J. R., Monson R. K. (1993). Evolutionary and ecological aspects of photosynthetic pathway variation. DOI

Fellbaum C. R., Gachomo E. W., Beesetty Y., Choudhari S., Strahan G. D., Pfeffer P. E., et al. (2012). Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. PubMed DOI PMC

Fellbaum C. R., Mensah J. A., Cloos A. J., Strahan G. E., Pfeffer P. E., Kiers E. T., et al. (2014). Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. PubMed DOI

Fitter A. H., Heinemeyer A., Staddon P. L. (2000). The impact of elevated CO2 and global climate change on arbuscular mycorrhizas: a mycocentric approach. DOI

Frostegård A., Tunlid A., Bååth E. (1991). Microbial biomass measured as total lipid phosphate in soils of different organic content. DOI

Hawkes C. V., Hartley I. P., Ineson P., Fitter A. H. (2008). Soil temperature affects carbon allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus. DOI

Heinemeyer A., Ineson P., Ostle N., Fitter A. H. (2006). Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows strong dependence on recent photosynthates and acclimation to temperature. PubMed DOI

Helgason T., Merryweather J. W., Denison J., Wilson P., Young J. P. W., Fitter A. H. (2002). Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. DOI

Hetrick B. A. D., Wilson G. W. T., Todd T. C. (1990). Differential responses of C3 and C4 grasses to mycorrhizal symbiosis, phosphorus fertilization, and soil-microorganisms. DOI

Hewitt E. J. (1966).

Hodge A., Fitter A. H. (2010). Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. PubMed DOI PMC

Hodge A., Storer K. (2015). Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. DOI

Hoeksema J. D., Chaudhary V. B., Gehring C. A., Johnson N. C., Karst J., Koide R. T., et al. (2010). A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. PubMed DOI

Jakobsen I., Rosendahl L. (1990). Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. DOI

Jansa J., Erb A., Oberholzer H. R., Šmilauer P., Egli S. (2014). Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. PubMed DOI

Jansa J., Mozafar A., Frossard E. (2005). Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. DOI

Jansa J., Smith F. A., Smith S. E. (2008). Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? PubMed

Johnson N. C., Wilson G. W. T., Wilson J. A., Miller R. M., Bowker M. A. (2015). Mycorrhizal phenotypes and the law of the minimum. PubMed DOI

Kiers E. T., Duhamel M., Beesetty Y., Mensah J. A., Franken O., Verbruggen E., et al. (2011). Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. PubMed DOI

Konvalinková T., Püschel D., Řezáčová V., Gryndlerová H., Jansa J. (2017). Carbon flow from plant to arbuscular mycorrhizal fungi is reduced under phosphorus fertilization. DOI

Koske R. E., Gemma J. N. (1989). A modified procedure for staining roots to detect VA-mycorrhizas. DOI

Krak K., Janoušková M., Caklová P., Vosátka M., Štorchová H. (2012). Intraradical dynamics of two coexisting isolates of the arbuscular mycorrhizal fungus PubMed DOI PMC

Latef A. A. H. A., Hashem A., Rasool S., Abd Allah E. F., Alqarawi A. A., Egamberdieva D., et al. (2016). Arbuscular mycorrhizal symbiosis and abiotic stress in plants: a review. DOI

Leigh J., Hodge A., Fitter A. H. (2009). Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. PubMed DOI

Lekberg Y., Hammer E. C., Olsson P. A. (2010). Plants as resource islands and storage units - adopting the mycocentric view of arbuscular mycorrhizal networks. PubMed DOI

Lekberg Y., Rosendahl S., Michelsen A., Olsson P. A. (2013). Seasonal carbon allocation to arbuscular mycorrhizal fungi assessed by microscopic examination, stable isotope probing and fatty acid analysis. DOI

Lenoir I., Fontaine J., Sahraoui A. L. H. (2016). Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. PubMed DOI

Lobell D. B., Gourdji S. M. (2012). The influence of climate change on global crop productivity. PubMed DOI PMC

López-Mondéjar R., Brabcová V., Štursová M., Davidová A., Jansa J., Cajthaml T., et al. (2018). Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling. PubMed DOI PMC

McGonigle T. P., Miller M. H., Evans D. G., Fairchild G. L., Swan J. A. (1990). A new method which gives an objective-measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. PubMed DOI

Millar N. S., Bennett A. E. (2016). Stressed out symbiotes: hypotheses for the influence of abiotic stress on arbuscular mycorrhizal fungi. PubMed DOI PMC

Mohan J. E., Cowden C. C., Baas P., Dawadi A., Frankson P. T., Helmick K., et al. (2014). Mycorrhizal fungi mediation of terrestrial ecosystem responses to global change: mini-review. DOI

Nakano A., Takahashi K., Kimura M. (1999). The carbon origin of arbuscular mycorrhizal fungi estimated from δ13C values of individual spores. DOI

Newsham K. K., Fitter A. H., Watkinson A. R. (1995). Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. DOI

Ohno T., Zibilske L. M. (1991). Determination of low concentrations of phosphorus in soil extracts using malachite green. DOI

Olsson P. A. (1999). Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. DOI

Pinto H., Sharwood R. E., Tissue D. T., Ghannoum O. (2014). Photosynthesis of C3 C3-C4 and C4 grasses at glacial CO2. PubMed DOI PMC

Pollastri S., Savvides A., Pesando M., Lumini E., Volpe M. G., Ozudogru E. A., et al. (2018). Impact of two arbuscular mycorrhizal fungi on PubMed DOI

Püschel D., Janoušková M., Hujslová M., Slavíková R., Gryndlerová H., Jansa J. (2016). Plant-fungus competition for nitrogen erases mycorrhizal growth benefits of PubMed DOI PMC

Querejeta J. I., Barea J. M., Allen M. F., Caravaca F., Roldán A. (2003). Differential response of delta δ13C and water use efficiency to arbuscular mycorrhizal infection in two aridland woody plant species. PubMed DOI

Řezáčová V., Konvalinková T., Jansa J. (2017a). “Carbon fluxes in mycorrhizal plants,” in

Řezáčová V., Slavíková R., Konvalinková T., Hujslová M., Gryndlerová H., Gryndler M., et al. (2017b). Imbalanced carbon-for-phosphorus exchange between European arbuscular mycorrhizal fungi and non-native

Řezáčová V., Slavíková R., Zemková L., Konvalinková T., Procházková V., Št’ovíček V., et al. (2018). Mycorrhizal symbiosis induces plant carbon reallocation differently in C3 and C4 DOI

Rillig M. C., Wright S. F., Shaw M. R., Field C. B. (2002). Artificial climate warming positively affects arbuscular mycorrhizae but decreases soil aggregate water stability in an annual grassland. DOI

Roth R., Paszkowski U. (2017). Plant carbon nourishment of arbuscular mycorrhizal fungi. PubMed DOI

Saia S., Benítez E., García-Garrido J., Settanni L., Amato G., Giambalvo D. (2014). The effect of arbuscular mycorrhizal fungi on total plant nitrogen uptake and nitrogen recovery from soil organic material. DOI

Schüßler A., Walker C. (2010).

Slavíková R., Püschel D., Janoušková M., Hujslová M., Konvalinková T., Gryndlerová H., et al. (2017). Monitoring CO PubMed DOI

Smith S. E., Jakobsen I., Grønlund M., Smith F. A. (2011). Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. PubMed DOI PMC

Smith S. E., Read D. J. (2008).

Smith S. E., Smith F. A., Jakobsen I. (2004). Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. DOI

Spatafora J. W., Chang Y., Benny G. L., Lazarus K., Smith M. E., Berbee M. L., et al. (2016). A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. PubMed DOI PMC

Sumner J. L., Morgan E. D., Evans H. C. (1969). The effect of growth temperature on the fatty acid composition of fungi in the order Mucorales. PubMed DOI

Svenningsen N. B., Watts-Williams S. J., Joner E. J., Battini F., Efthymiou A., Cruz-Paredes C., et al. (2018). Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. PubMed DOI PMC

Thonar C., Erb A., Jansa J. (2012). Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communities–marker design, verification, calibration and field validation. PubMed DOI

Tobar R., Azcón R., Barea J. M. (1994). Improved nitrogen uptake and transport from 15N-labeled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. DOI

Treseder K. K. (2016). Model behavior of arbuscular mycorrhizal fungi: predicting soil carbon dynamics under climate change. DOI

van der Heijden M. G. A., Klironomos J. N., Ursic M., Moutoglis P., Streitwolf-Engel R., Boller T., et al. (1998). Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. DOI

van der Heijden M. G. A., Martin F. M., Selosse M. A., Sanders I. R. (2015). Mycorrhizal ecology and evolution: the past, the present, and the future. PubMed DOI

Vandenkoornhuyse P., Ridgway K. P., Watson I. J., Fitter A. H., Young J. P. W. (2003). Co-existing grass species have distinctive arbuscular mycorrhizal communities. PubMed DOI

Vigo C., Norman J. R., Hooker J. E. (2000). Biocontrol of the pathogen DOI

Voříšková A., Jansa J., Püschel D., Krüger M., Cajthaml T., Vosátka M., et al. (2017). Real-time PCR quantification of arbuscular mycorrhizal fungi: does the use of nuclear or mitochondrial markers make a difference? PubMed DOI

Voznesenskaya E. V., Franceschi V. R., Kiirats O., Freitag H., Edwards G. E. (2001). Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. PubMed DOI

Wagg C., Jansa J., Schmid B., van der Heijden M. G. A. (2011). Belowground biodiversity effects of plant symbionts support aboveground productivity. PubMed DOI

Walder F., Niemann H., Lehmann M. F., Boller T., Wiemken A., Courty P. E. (2013). Tracking the carbon source of arbuscular mycorrhizal fungi colonizing C3 and C4 plants using carbon isotope ratios (δ13C). DOI

Walder F., Niemann H., Natarajan M., Lehmann M. F., Boller T., Wiemken A. (2012). Mycorrhizal networks: common goods of plants shared under unequal terms of trade. PubMed DOI PMC

Walder F., van der Heijden M. G. A. (2015). Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. PubMed DOI

Waller S. S., Lewis J. K. (1979). Occurrence of C3 and C4 photosynthetic pathways in North American grasses. DOI

Wang G. H., Sheng L. C., Zhao D., Sheng J. D., Wang X. R., Liao H. (2016). Allocation of nitrogen and carbon is regulated by nodulation and mycorrhizal networks in soybean/maize intercropping system. PubMed DOI PMC

Welc M., Bünemann E. K., Fliessbach A., Frossard E., Jansa J. (2012). Soil bacterial and fungal communities along a soil chronosequence assessed by fatty acid profiling. DOI

Weremijewicz J., Sternberg L. D. L. O., Janos D. P. (2016). Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. PubMed DOI

Zhu X. C., Song F. B., Liu S. Q., Liu T. D. (2011). Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. DOI

Mycorrhiza governs plant-plant interactions through preferential allocation of shared nutritional resources: A triple (13C, 15N and 33P) labeling study

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