Legumes establish root symbioses with rhizobia that provide plants with nitrogen (N) through biological N fixation (BNF), as well as with arbuscular mycorrhizal (AM) fungi that mediate improved plant phosphorus (P) uptake. Such complex relationships complicate our understanding of nutrient acquisition by legumes and how they reward their symbiotic partners with carbon along gradients of environmental conditions. In order to disentangle the interplay between BNF and AM symbioses in two Medicago species (Medicago truncatula and M. sativa) along a P-fertilization gradient, we conducted a pot experiment where the rhizobia-treated plants were either inoculated or not inoculated with AM fungus Rhizophagus irregularis 'PH5' and grown in two nutrient-poor substrates subjected to one of three different P-supply levels. Throughout the experiment, all plants were fertilized with 15N-enriched liquid N-fertilizer to allow for assessment of BNF efficiency in terms of the fraction of N in the plants derived from the BNF (%NBNF). We hypothesized (1) higher %NBNF coinciding with higher P supply, and (2) higher %NBNF in mycorrhizal as compared to non-mycorrhizal plants under P deficiency due to mycorrhiza-mediated improvement in P nutrition. We found a strongly positive correlation between total plant P content and %NBNF, clearly documenting the importance of plant P nutrition for BNF efficiency. The AM symbiosis generally improved P uptake by plants and considerably stimulated the efficiency of BNF under low P availability (below 10 mg kg-1 water extractable P). Under high P availability (above 10 mg kg-1 water extractable P), the AM symbiosis brought no further benefits to the plants with respect to P nutrition even as the effects of P availability on N acquisition via BNF were further modulated by the environmental context (plant and substrate combinations). As a response to elevated P availability in the substrate, the extent of root length colonization by AM fungi was reduced, the turning points occurring at about 8 and 10 mg kg-1 water extractable P for M. sativa and M. truncatula, respectively. Our results indicated competition for limited C resource between the two kinds of microsymbionts and thus degradation of AM symbiotic functioning under ample P supply.

Department of Mycorrhizal Symbioses Institute of Botany Czech Academy of Sciences Průhonice Czechia

Department of Mycorrhizal Symbioses Institute of Botany Czech Academy of SciencesPrůhonice Czechia; Laboratory of Fungal Biology Institute of Microbiology Czech Academy of SciencesPrague Czechia

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

Zobrazit více v PubMed

Ankomah A. B., Zapata F., Hardarson G., Danso S. K. A. (1996). Yield, nodulation, and N-2 fixation by cowpea cultivars at different phosphorus levels. DOI

Ballhorn D. J., Schadler M., Elias J. D., Millar J. A., Kautz S. (2016). Friend or foe - Light availability determines the relationship between mycorrhizal fungi, rhizobia and lima bean ( PubMed DOI PMC

Barea J. M., Pozo M. J., Azcón R., Azcón-Aguilar C. (2005). Microbial co-operation in the rhizosphere. PubMed DOI

Bethlenfalvay G. J., Pacovsky R. S., Bayne H. G., Stafford A. E. (1982). Interactions between nitrogen-fixation, mycorrhizal colonization, and host-plant growth in the Phaseolus-Rhizobium-Glomus symbiosis. PubMed DOI PMC

Bever J. D. (2015). Preferential allocation, physio-evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts. PubMed DOI

Bolger T. P., Pate J. S., Unkovich M. J., Turner N. C. (1995). Estimates of seasonal nitrogen-fixation of annual subterranean clover-based pastures using the 15N natural-abundance technique. DOI

Divito G. A., Sadras V. O. (2014). How do phosphorus, potassium and sulphur affect plant growth and biological nitrogen fixation in crop and pasture legumes? A meta-analysis. DOI

Edwards E. J., McCaffery S., Evans J. R. (2006). Phosphorus availability and elevated CO2 affect biological nitrogen fixation and nutrient fluxes in a clover-dominated sward. PubMed DOI

Gange A. C., Ayres R. L. (1999). On the relation between arbuscular mycorrhizal colonization and plant ‘benefit’. DOI

Garau G., Reeve W. G., Brau L., Deiana P., Yates R. J., James D., et al. (2005). The symbiotic requirements of different DOI

Giovannetti M., Mosse B. (1980). Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. DOI

Jakobsen I. (1985). The role of phosphorus in nitrogen fixation by young pea plants ( DOI

Jakobsen I., Chen B. D., Munkvold L., Lundsgaard T., Zhu Y. G. (2005). Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root hairless barley mutant. DOI

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

Jansa J., Finlay R., Wallander H., Smith F. A., Smith S. E. (2011). Role of mycorrhizal symbioses in phosphorus cycling. DOI

Jansa J., Mozafar A., Frossard E. (2003a). Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. DOI

Jansa J., Mozafar A., Kuhn G., Anken T., Ruh R., Sanders I. R., et al. (2003b). Soil tillage affects the community structure of mycorrhizal fungi in maize roots. DOI

Johnson N. C., Graham J. H., Smith F. A. (1997). Functioning of mycorrhizal associations along the mutualism-parasitism continuum. 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. 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? 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. 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

Kleinert A., Venter M., Kossmann J., Valentine A. (2014). The reallocation of carbon in P deficient lupins affects biological nitrogen fixation. PubMed DOI

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

Kuang R. B., Liao H., Yan X. L., Dong Y. S. (2005). Phosphorus and nitrogen interactions in field-grown soybean as related to genetic attributes of root morphological and nodular traits. DOI

Larimer A. L., Bever J. D., Clay K. (2010). The interactive effects of plant microbial symbionts: a review and meta-analysis. DOI

Larimer A. L., Clay K., Bever J. D. (2014). Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. PubMed DOI

Linderman R. G., Davis E. A. (2004). Varied response of marigold ( DOI

Lynch J. P. (2007). Roots of the second green revolution. DOI

Millar J. A., Ballhorn D. J. (2013). Effect of mycorrhizal colonization and light limitation on growth and reproduction of lima bean (

Morandi D., Prado E., Sagan M., Duc G. (2005). Characterisation of new symbiotic PubMed DOI

Morgan J. A. W., Bending G. D., White P. J. (2005). Biological costs and benefits to plant-microbe interactions in the rhizosphere. PubMed DOI

Mortimer P. E., Perez-Fernandez M. A., Valentine A. J. (2008). The role of arbuscular mycorrhizal colonization in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris. DOI

Mortimer P. E., Pérez-Fernández M. A., Valentine A. J. (2009). Arbuscular mycorrhizae affect the N and C economy of nodulated DOI

Nibau C., Gibbs D. J., Coates J. C. (2008). Branching out in new directions: the control of root architecture by lateral root formation. PubMed DOI

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

Paul E. A., Kucey R. M. N. (1981). Carbon flow in plant microbial associations. 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

Rao I. M., Miles J. W., Beebe S. E., Horst W. J. (2016). Root adaptations to soils with low fertility and aluminium toxicity. PubMed DOI PMC

Raven J. A., Edwards D. (2001). Roots: evolutionary origins and biogeochemical significance. PubMed DOI

Reinhard S., Martin P., Marschner H. (1993). Interactions in the tripartite symbiosis of pea ( DOI

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

Saia S., Amato G., Frenda A. S., Giambalvo D., Ruisi P. (2014). Influence of arbuscular mycorrhizae on biomass production and nitrogen fixation of berseem clover plants subjected to water stress. PubMed DOI PMC

Slavíková R., Püschel D., Janoušková M., Hujslová M., Konvalinková T., Gryndlerová H., et al. (2016). Monitoring CO2 emissions to gain a dynamic view of carbon allocation to arbuscular mycorrhizal fungi. PubMed DOI

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

Somasegaran P., Hoben H. J. (1994). DOI

Treseder K. K. (2004). A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. PubMed DOI

Vadez V., Lasso J. H., Beck D. P., Drevon J. J. (1999). Variability of N2-fixation in common bean ( DOI

van der Heijden M. G. A., de Bruin S., Luckerhoff L., van Logtestijn R. S. P., Schlaeppi K. (2016). A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. PubMed DOI PMC

Unraveling the diversity of hyphal explorative traits among Rhizophagus irregularis genotypes

Nutrient-dependent cross-kingdom interactions in the hyphosphere of an arbuscular mycorrhizal fungus

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

Arbuscular Mycorrhiza and Nitrification: Disentangling Processes and Players by Using Synthetic Nitrification Inhibitors

Establishing a quality management framework for commercial inoculants containing arbuscular mycorrhizal fungi

Organic nitrogen utilisation by an arbuscular mycorrhizal fungus is mediated by specific soil bacteria and a protist

Arbuscular Mycorrhiza Mediates Efficient Recycling From Soil to Plants of Nitrogen Bound in Chitin

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

Appropriate nonmycorrhizal controls in arbuscular mycorrhiza research: a microbiome perspective

Utilization of organic nitrogen by arbuscular mycorrhizal fungi-is there a specific role for protists and ammonia oxidizers?

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