Plant and fungal partners in arbuscular mycorrhizal symbiosis trade mineral nutrients for carbon, with the outcome of this relationship for plant growth and nutrition being highly context-dependent and changing with the availability of resources as well as with the specific requirements of the different partners. Here we studied how the model legume Medicago truncatula, inoculated or not with a mycorrhizal fungus Rhizophagus irregularis, responded to a gradient of light intensities applied over different periods of time, in terms of growth, phosphorus nutrition and the levels of root colonization by the mycorrhizal fungus. Short-term (6 d) shading, depending on its intensity, resulted in a rapid decline of phosphorus uptake to the shoots of mycorrhizal plants and simultaneous accumulation of phosphorus in the roots (most likely in the fungal tissues), as compared to the non-mycorrhizal controls. There was, however, no significant change in the levels of mycorrhizal colonization of roots due to short-term shading. Long-term (38 d) shading, depending on its intensity, provoked a multitude of plant compensatory mechanisms, which were further boosted by the mycorrhizal symbiosis. Mycorrhizal growth- and phosphorus uptake benefits, however, vanished at 10% of the full light intensity applied over a long-term. Levels of root colonization by the mycorrhizal fungus were significantly reduced by long-term shading. Our results indicate that even short periods of shade could have important consequences for the functioning of mycorrhizal symbiosis in terms of phosphorus transfer between the fungus and the plants, without any apparent changes in root colonization parameters or mycorrhizal growth response, and call for more focused research on temporal dynamics of mycorrhizal functioning under changing environmental conditions.

Laboratory of Fungal Biology Institute of Microbiology Academy of Sciences of the Czech Republic Prague Czech Republic

Laboratory of Fungal Biology Institute of Microbiology Academy of Sciences of the Czech Republic Prague Czech Republic ; Department of Mycorrhizal Symbioses Institute of Botany Academy of Sciences of the Czech Republic Průhonice Czech Republic

Zobrazit více v PubMed

Burleigh S. H., Bechmann I. E. (2002). Plant nutrient transporter regulation in arbuscular mycorrhizas. Plant Soil 244 247–251 10.1023/A:1020227232140 DOI

Burleigh S. H., Harrison M. J. (1999). “Mt4 a phosphorus starvation-inducible cDNA from Medicago truncatula, which is down-regulated both by phosphorus fertilization and arbuscular-mycorrhizal colonization,” in Phosphorus in Plant Biology: Regulatory Roles in Molecular, Cellular, Organismic, and Ecosystem Processes, eds Lynch J. P., Deikman J. (Rockville, MD: American Society of Plant Biologists; ), 359–360.

Cirino G. G., Souza R. A. F., Adams D. K., Artaxo P. (2014). The effect of atmospheric aerosol particles and clouds on net ecosystem exchange in the Amazon. Atmos. Chem. Phys. 14 6523–6543 10.5194/acp-14-6523-2014 DOI

Drigo B., Pijl A. S., Duyts H., Kielak A., Gamper H. A., Houtekamer M. J., et al. (2010). Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc. Natl. Acad. Sci. U.S.A. 107 10938–10942 10.1073/pnas.0912421107 PubMed DOI PMC

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. Proc. Natl. Acad. Sci. U.S.A. 109 2666–2671 10.1073/pnas.1118650109 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. New Phytol. 203 646–656 10.1111/nph.12827 PubMed DOI

Fitter A. H., Helgason T., Hodge A. (2011). Nutritional exchanges in the arbuscular mycorrhizal symbiosis: implications for sustainable agriculture. Fungal Biol. Rev. 25 68–72 10.1016/j.fbr.2011.01.002 DOI

Frossard E., Achat D. L., Bernasconi S. M., Bunemann E. K., Fardeau J. C., Jansa J., et al. (2011). “The use of tracers to investigate phosphate cycling in soil-plant systems,” in Phosphorus in Action: Biological Processes in Soil Phosphorus Cycling, eds ünemann, E.B, Oberson, A., Frossard A. (Berlin: Springer; ), 59–91 10.1007/978-3-642-15271-9_3 DOI

Gehring C. A. (2003). Growth responses to arbuscular mycorrhizae by rain forest seedlings vary with light intensity and tree species. Plant Ecol. 167 127–139 10.1023/A:1023989610773 DOI

George T., Singleton P. W., Vankessel C. (1993). The use of 15N natural abundance and nitrogen yield of nonnodulating isolines to estimate nitrogen fixation by soybeans (Glycine max L) across 3 elevations. Biol. Fertil. Soils 15 81–86 10.1007/BF00336422 DOI

Grimoldi A. A., Kavanova M., Lattanzi F. A., Schaufele R., Schnyder H. (2006). Arbuscular mycorrhizal colonization on carbon economy in perennial ryegrass: quantification by 13CO2/12CO2 steady-state labelling and gas exchange. New Phytol. 172 544–553 10.1111/j.1469-8137.2006.01853.x PubMed DOI

Grman E. (2012). Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi. Ecology 93 711–718 10.1890/11-1358.1 PubMed DOI

Gryndler M., Vejsadová H., Vančura V. (1992). The effect of magnesium-ions on the vesicular arbuscular mycorrhizal infection of maize roots. New Phytol. 122 455–460 10.1111/j.1469-8137.1992.tb00073.x PubMed DOI

Hammer E. C., Pallon J., Wallander H., Olsson P. A. (2011). Tit for tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiol. Ecol. 76 236–244 10.1111/j.1574-6941.2011.01043.x PubMed DOI

Heinemeyer A., Ridgway K. P., Edwards E. J., Benham D. G., Young J. P. W., Fitter A. H. (2003). Impact of soil warming and shading on colonization and community structure of arbuscular mycorrhizal fungi in roots of a native grassland community. Glob. Chang. Biol. 10 52–64 10.1111/j.1365-2486.2003.00713.x DOI

Huve K., Merbach W., Remus R., Luttschwager D., Wittenmayer L., Hertel K., et al. (2007). Transport of phosphorus in leaf veins of Vicia faba L. J. Plant Nutr. Soil Sci. 170 14–23 10.1002/jpin.200625057 DOI

Jakobsen I., Rosendahl L. (1990). Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol. 115 77–83 10.1111/j.1469-8137.1990.tb00924.x DOI

Jansa J. (2002). Effect of Soil Tillage on Arbuscular Mycorrhizal Fungi and on their Role in Nutrient Uptake by Crops. Ph.D. thesis, Swiss Federal Institute of Technology (ETH), Zürich.

Javot H., Penmetsa R. V., Terzaghi N., Cook D. R., Harrison M. J. (2007). A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 104 1720–1725 10.1073/pnas.0608136104 PubMed DOI PMC

Jeschke W. D., Kirkby E. A., Peuke A. D., Pate J. S., Hartung W. (1997). Effects of P deficiency on assimilation and transport of nitrate and phosphate in intact plants of castor bean (Ricinus communis L). J. Exp. Bot. 48 75–91 10.1093/Jxb/48.1.75 DOI

Johnson N. C., Graham J. H. (2013). The continuum concept remains a useful framework for studying mycorrhizal functioning. Plant Soil 363 411–419 10.1007/s11104-012-1406-1 DOI

Johnson N. C., Graham J. H., Smith F. A. (1997). Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 135 575–586 10.1046/j.1469-8137.1997.00729.x DOI

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. New Phytol. 205 1473–1484 10.1111/nph.13172 PubMed DOI

Kaschuk G., Kuyper T. W., Leffelaar P. A., Hungria M., Giller K. E. (2009). Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol. Biochem. 41 1233–1244 10.1016/j.soilbio.2009.03.005 DOI

Kaschuk G., Leffelaar P. A., Giller K. E., Alberton O., Hungria M., Kuyper T. W. (2010). Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses. Soil Biol. Biochem. 42 125–127 10.1016/j.soilbio.2009.10.017 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. Science 333 880–882 10.1126/science.1208473 PubMed DOI

Knegt B., Jansa J., Franken O., Engelmoer D. J. P., Werner G. D. A., Bücking H., et al. (2015). Host plant quality mediates competition between arbuscular mycorrhizal fungi. Fungal Ecol. 10.1016/j.funeco.2014.09.011 DOI

Korhonen J., Kytoviita M. M., Siikamaki P. (2004). Are resources allocated differently to symbiosis and reproduction in Geranium sylvaticum under different light conditions? Can. J. Bot. 82 89–95 10.1139/B03-142 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. FEMS Microbiol. Ecol. 74 336–345 10.1111/j.1574-6941.2010.00956.x PubMed DOI

Lendenmann M., Thonar C., Barnard R. L., Salmon Y., Werner R. A., Frossard E., et al. (2011). Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi. Mycorrhiza 21 689–702 10.1007/s00572-011-0371-5 PubMed DOI

Martens S. N., Breshears D. D., Meyer C. W. (2000). Spatial distributions of understory light along the grassland/forest continuum: effects of cover, height, and spatial pattern of tree canopies. Ecol. Modell. 126 79–93 10.1016/S0304-3800(99)00188-X DOI

McCormick M. P., Thomason L. W., Trepte C. R. (1995). Atmospheric effects of the Mt-Pinatubo eruption. Nature 373 399–404 10.1038/373399a0 DOI

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. New Phytol. 115 495–501 10.1111/j.1469-8137.1990.tb00476.x PubMed DOI

Millar J. A., Ballhorn D. J. (2013). Effect of mycorrhizal colonization and light limitation on growth and reproduction of lima bean (Phaseolus lunatus L.). J. Appl. Bot. Food Q. 86 172–179 10.5073/Jabfq.2013.086.023 DOI

Mortimer P. E., Perez-Fernandez M. A., Valentine A. J. (2009). Arbuscular mycorrhizae affect the N and C economy of nodulated Phaseolus vulgaris (L.) during NH4+ nutrition. Soil Biol. Biochem. 41 2115–2121 10.1016/j.soilbio.2009.07.021 DOI

Ohno T., Zibilske L. M. (1991). Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci. Soc. Am. J. 55 892–895 10.2136/sssaj1991.03615995005500030046x DOI

Olsson P. A., Rahm J., Aliasgharzad N. (2010). Carbon dynamics in mycorrhizal symbioses is linked to carbon costs and phosphorus benefits. FEMS Microbiol. Ecol. 72 123–131 10.1111/j.1574-6941.2009.00833.x PubMed DOI

Paul E. A., Kucey R. M. N. (1981). Carbon flow in plant microbial associations. Science 213 473–474 10.1126/science.213.4506.473 PubMed DOI

Pearson J. N., Jakobsen I. (1993a). The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labeling with 32P and 33P. New Phytol. 124 489–494 10.1111/j.1469-8137.1993.tb03840.x DOI

Pearson J. N., Jakobsen I. (1993b). Symbiotic exchange of carbon and phosphorus between cucumber and 3 arbuscular mycorrhizal fungi. New Phytol. 124 481–488 10.1111/j.1469-8137.1993.tb03839.x DOI

Rausch C., Daram P., Brunner S., Jansa J., Laloi M., Leggewie G., et al. (2001). A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414 462–466 10.1038/35106601 PubMed DOI

Reinhard S., Weber E., Martin P., Marschner H. (1994). Influence of phosphorus supply and light-intensity on mycorrhizal response in Pisum-Rhizobium-Glomus symbiosis. Experientia 50 890–896 10.1007/Bf01923475 DOI

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. New Phytol. 162 511–524 10.1111/j.1469-8137.2004.01039.x DOI

Somasegaran P., Hoben H. J. (1994). Handbook for Rhizobia: Methods in Legume-Rhizobium Technology. New York: Springer; 10.1007/978-1-4613-8375-8 DOI

Son C. L., Smith F. A., Smith S. E. (1988). Effect of light-intensity on root-growth, mycorrhizal infection and phosphate-uptake in onion (Allium cepa L). Plant Soil 111 183–186 10.1007/Bf02139935 DOI

Son C. L., Smith S. E. (1988). Mycorrhizal growth-responses - interactions between photon irradiance and phosphorus-nutrition. New Phytol. 108 305–314 10.1111/j.1469-8137.1988.tb04167.x PubMed DOI

Thonar C., Schnepf A., Frossard E., Roose T., Jansa J. (2011). Traits related to differences in function among three arbuscular mycorrhizal fungi. Plant Soil 339 231–245. 10.1007/s11104-010-0571-3

Tuomi J., Kytoviita M. M., Hardling R. (2001). Cost efficiency of nutrient acquisition and the advantage of mycorrhizal symbiosis for the host plant. Oikos 92 62–70 10.1034/j.1600-0706.2001.920108.x DOI

Viereck N., Hansen P. E., Jakobsen I. (2004). Phosphate pool dynamics in the arbuscular mycorrhizal fungus Glomus intraradices studied by in vivo 31P NMR spectroscopy. New Phytol. 162 783–794 10.1111/j.1469-8137.2004.01048.x PubMed DOI

Voisin A. S., Cazenave A. B., Duc G., Salon C. (2013). Pea nodule gradients explain C nutrition and depressed growth phenotype of hypernodulating mutants. Agron. Sustain. Dev. 33 829–838 10.1007/s13593-013-0146-9 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. Plant Physiol. 159 789–797 10.1104/pp.112.195727 PubMed DOI PMC

Wang X. R., Pan Q. A., Chen F. X., Yan X. L., Liao H. (2011). Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21 173–181 10.1007/s00572-010-0319-1 PubMed DOI

Wright D. P., Scholes J. D., Read D. J. (1998). Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ. 21 209–216 10.1046/j.1365-3040.1998.00280.x DOI

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

Dead Rhizophagus irregularis biomass mysteriously stimulates plant growth

Correlative evidence for co-regulation of phosphorus and carbon exchanges with symbiotic fungus in the arbuscular mycorrhizal Medicago truncatula

Abiotic contexts consistently influence mycorrhiza functioning independently of the composition of synthetic arbuscular mycorrhizal fungal communities

Real-time PCR quantification of arbuscular mycorrhizal fungi: does the use of nuclear or mitochondrial markers make a difference?

Monitoring CO2 emissions to gain a dynamic view of carbon allocation to arbuscular mycorrhizal fungi

Plant-fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply

Lights Off for Arbuscular Mycorrhiza: On Its Symbiotic Functioning under Light Deprivation

Organic Nitrogen-Driven Stimulation of Arbuscular Mycorrhizal Fungal Hyphae Correlates with Abundance of Ammonia Oxidizers