Arbuscular Mycorrhiza Stimulates Biological Nitrogen Fixation in Two Medicago spp. through Improved Phosphorus Acquisition
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article
PubMed
28396674
PubMed Central
PMC5366336
DOI
10.3389/fpls.2017.00390
Knihovny.cz E-resources
- Keywords
- arbuscular mycorrhiza, competition, legumes, nitrogen acquisition, phosphorus uptake, rhizobia, root symbioses, synergies,
- Publication type
- Journal Article MeSH
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
Laboratory of Fungal Biology Institute of Microbiology Czech Academy of Sciences Prague Czechia
See more in 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. Biol. Fertil. Soils 22 10–15. 10.1007/BF00384426 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 (Phaseolus lunatus L.). PLoS ONE 11:e0154116 10.1371/journal.pone.0154116 PubMed DOI PMC
Barea J. M., Pozo M. J., Azcón R., Azcón-Aguilar C. (2005). Microbial co-operation in the rhizosphere. J. Exp. Bot. 56 1761–1778. 10.1093/jxb/eri197 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. Plant Physiol. 70 446–450. 10.1104/pp.70.2.446 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. New Phytol. 205 1503–1514. 10.1111/nph.13239 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. Plant Soil 175 57–66. 10.1007/BF02413010 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. Field Crop Res. 156 161–171. 10.1016/j.fcr.2013.11.004 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. New Phytol. 169 157–167. 10.1111/j.1469-8137.2005.01568.x PubMed DOI
Gange A. C., Ayres R. L. (1999). On the relation between arbuscular mycorrhizal colonization and plant ‘benefit’. Oikos 87 615–621. 10.2307/3546829 DOI
Garau G., Reeve W. G., Brau L., Deiana P., Yates R. J., James D., et al. (2005). The symbiotic requirements of different Medicago spp. suggest the evolution of Sinorhizobium meliloti and S. medicae with hosts differentially adapted to soil pH. Plant Soil 276 263–277. 10.1007/s11104-005-0374-0 DOI
Giovannetti M., Mosse B. (1980). Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 84 489–500. 10.1111/j.1469-8137.1980.tb04556.x DOI
Jakobsen I. (1985). The role of phosphorus in nitrogen fixation by young pea plants (Pisum sativum). Physiol. Plant. 64 190–196. 10.1111/j.1399-3054.1985.tb02334.x 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. Plant Cell Environ. 28 928–938. 10.1111/j.1365-3040.2005.01345.x DOI
Jakobsen I., Rosendahl L. (1990). Carbon flow into soil and external hyphea from roots of mycorrhizal cucumber plants. New Phytol. 115 77–83. 10.1111/j.1469-8137.1990.tb00924.x DOI
Jansa J., Finlay R., Wallander H., Smith F. A., Smith S. E. (2011). Role of mycorrhizal symbioses in phosphorus cycling. Soil Biol. 26 137–168. 10.1007/978-3-642-15271-9_6 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. Agronomie 23 481–488. 10.1051/agro:2003013 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. Ecol. Appl. 13 1164–1176. 10.1007/s12275-015-5108-2 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
Kleinert A., Venter M., Kossmann J., Valentine A. (2014). The reallocation of carbon in P deficient lupins affects biological nitrogen fixation. J. Plant Physiol. 171 1619–1624. 10.1016/j.jplph.2014.07.017 PubMed DOI
Koske R. E., Gemma J. N. (1989). A modified procedure for staining roots to detect VA-mycorrhizas. Mycol. Res. 92 486–505. 10.1016/S0953-7562(89)80195-9 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. J. Integr. Plant Biol. 47 549–559. 10.1111/j.1744-7909.2005.00072.x DOI
Larimer A. L., Bever J. D., Clay K. (2010). The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51 139–148. 10.1007/s13199-010-0083-1 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. Ecology 95 1045–1054. 10.1890/13-0025.1 PubMed DOI
Linderman R. G., Davis E. A. (2004). Varied response of marigold (Tagetes spp.) genotypes to inoculation with different arbuscular mycorrhizal fungi. Sci. Hortic. 99 67–78. 10.1016/S0304-4238(03)00081-5 DOI
Lynch J. P. (2007). Roots of the second green revolution. Aust. J. Bot. 55 493–512. 10.1071/BT06118 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 Qual. 86 172–179.
Morandi D., Prado E., Sagan M., Duc G. (2005). Characterisation of new symbiotic Medicago truncatula (Gaertn.) mutants, and phenotypic or genotypic complementary information on previously described mutants. Mycorrhiza 15 283–289. 10.1007/s00572-004-0331-4 PubMed DOI
Morgan J. A. W., Bending G. D., White P. J. (2005). Biological costs and benefits to plant-microbe interactions in the rhizosphere. J. Exp. Bot. 56 1729–1739. 10.1093/jxb/eri205 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. Soil Biol. Biochem. 40 1019–1027. 10.1016/j.soilbio.2007.11.014 DOI
Mortimer P. E., Pérez-Fernández 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
Nibau C., Gibbs D. J., Coates J. C. (2008). Branching out in new directions: the control of root architecture by lateral root formation. New Phytol. 179 595–614. 10.1111/j.1469-8137.2008.02472.x PubMed 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
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
Püschel D., Janoušková M., Hujslová M., Slavíková R., Gryndlerová H., Jansa J. (2016). Plant–fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply. Ecol. Evol. 6 4332–4346. 10.1002/ece3.2207 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. Ann. Bot. 118 593–605. 10.1093/aob/mcw073 PubMed DOI PMC
Raven J. A., Edwards D. (2001). Roots: evolutionary origins and biogeochemical significance. J. Exp. Bot. 52 381–401. 10.1093/jexbot/52.suppl_1.381 PubMed DOI
Reinhard S., Martin P., Marschner H. (1993). Interactions in the tripartite symbiosis of pea (Pisum sativum L.), Glomus and Rhizobium under nonlimiting phosphorus supply. J. Plant Physiol. 141 7–11. 10.1016/S0176-1617(11)80844-8 DOI
Řezáčová V., Konvalinková T., Jansa J. (2017). “Carbon fluxes in mycorrhizal plants,” in Mycorrhiza eds Varma A., Prasad R., Tuteja N. (Cham: Springer International Publishing; ).
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. PLoS ONE 9:e90738 10.1371/journal.pone.0090738 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. Mycorrhiza 27 35–51. 10.1007/s00572-016-0731-2 PubMed DOI
Smith S. E., Read D. J. (2008). Mycorrhizal Symbiosis. Cambridge: Academic Press.
Somasegaran P., Hoben H. J. (1994). Handbook for Rhizobia: Methods in Legume-Rhizobium Technology. New York, NY: Springer; 10.1007/978-1-4613-8375-8 DOI
Treseder K. K. (2004). A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol. 164 347–355. 10.1111/j.1469-8137.2004.01159.x PubMed DOI
Vadez V., Lasso J. H., Beck D. P., Drevon J. J. (1999). Variability of N2-fixation in common bean (Phaseolus vulgaris L.) under P deficiency is related to P use efficiency. Euphytica 106 231–242. 10.1023/A:1003512519558 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. ISME J. 10 389–399. 10.1038/ismej.2015.120 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
Arbuscular Mycorrhiza Mediates Efficient Recycling From Soil to Plants of Nitrogen Bound in Chitin
Dead Rhizophagus irregularis biomass mysteriously stimulates plant growth
Appropriate nonmycorrhizal controls in arbuscular mycorrhiza research: a microbiome perspective