Plant-mediated partner discrimination in ectomycorrhizal mutualisms
Although ectomycorrhizal fungi have well-recognized effects on ecological processes ranging from plant community dynamics to carbon cycling rates, it is unclear if plants are able to actively influence the structure of these fungal communities. To address this knowledge gap, we performed two complementary experiments to determine (1) whether ectomycorrhizal plants can discriminate among potential fungal partners, and (2) to what extent the plants might reward better mutualists. In experiment 1, split-root Larix occidentalis seedlings were inoculated with spores from three Suillus species (S. clintonianus, S. grisellus, and S. spectabilis). In experiment 2, we manipulated the symbiotic quality of Suillus brevipes isolates on split-root Pinus muricata seedlings by changing the nitrogen resources available, and used carbon-13 labeling to track host investment in fungi. In experiment 1, we found that hosts can discriminate in multi-species settings. The split-root seedlings inhibited colonization by S. spectabilis whenever another fungus was available, despite similar benefits from all three fungi. In experiment 2, we found that roots and fungi with greater nitrogen supplies received more plant carbon. Our results suggest that plants may be able to regulate this symbiosis at a relatively fine scale, and that this regulation can be integrated across spatially separated portions of a root system.
KeywordsEctomycorrhiza Larix occidentalis Partner choice Pinus muricata Stable isotope enrichment Suillus
We thank Nhu Nguyen for collecting and logistical assistance with experiment 1. We thank Ford Denison, Tad Fukami, members of the Peay lab, Thomas Kuyper, and four anonymous reviewers for feedback on prior versions of this manuscript. Thanks also to Don Herman, who provided essential assistance with the isotope enrichment part of experiment 2.
P.K. designed experiment 1, which was conducted by S.H. and J.H. L.B. designed and carried out experiment 2 with support from K.P. and A.K. L.B. analyzed the data and composed the manuscript, with writing and editing assistance from P.K., and additional revisions from all co-authors.
S. Hortal received a Hawkesbury Institute for the Environment Research Exchange Program grant. L. Bogar received support for this research from a National Science Foundation (NSF) Graduate Research Fellowship Program grant, scholarships from the Mycological Society of San Francisco and the Phi Beta Kappa Northern California Association, and a predoctoral fellowship from the Stanford Center for Computational, Evolutionary, and Human Genomics. Further support was provided by an NSF-Division of Environmental Biology grant (1554375) to P. Kennedy.
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Conflict of interest
The authors declare that they have no conflict of interest.
- Ek H, Andersson S, Söderström B (1996) Carbon and nitrogen flow in silver birch and Norway spruce connected by a common mycorrhizal mycelium. 465–467. doi: https://doi.org/10.1007/s005720050148
- Finlay RD (1989) Functional aspects of phosphorus uptake and carbon translocation in incompatible ectomycorrhizal associations between Pinus sylvestris and Suillus grevillei and Boletinus cavipes. New Phytol 112:185–192. https://doi.org/10.1111/j.1469-8137.1989.tb02373.x
- Fukami T (2015) Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu Rev Ecol Evol Syst 46:1–23. https://doi.org/10.1146/annurev-ecolsys-110411-160340 CrossRefGoogle Scholar
- He X, Critchley C, Ng H, Bledsoe C (2005) Nodulated N2-fixing Casuarina cunninghamiana is the sink for net N transfer from non-N2-fixing Eucalyptus maculata via an ectomycorrhizal fungus Pisolithus sp. using 15NH4+ or 15NO3− supplied as ammonium nitrate. New Phytol 167:897–912. https://doi.org/10.1111/j.1469-8137.2005.01437.x CrossRefGoogle Scholar
- Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu Rev Ecol Evol Syst 39:215–236. https://doi.org/10.1146/annurev.ecolsys.39.110707.173423 CrossRefGoogle Scholar
- Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bucking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science (80- ) 333:880–882. https://doi.org/10.1126/science.1208473 CrossRefGoogle Scholar
- Marx D (1969) The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic infections. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59:153–163Google Scholar
- Molina R, Horton TR (2015) Mycorrhiza specificity: its role in the development and function of common mycelial networks. In: Horton TR (ed) Mycorrhizal Networks, 1st edn. Springer Netherlands, Dordrecht, pp 1–39Google Scholar
- Nylund J, Wallander H (1989) Effects of ectomycorrhiza on host growth and carbon balance in a semi-hydroponic cultivation system. New Phytol 112:389–398. https://doi.org/10.1111/j.1469-8137.1989.tb00328.x CrossRefGoogle Scholar
- Oldroyd GED, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144. https://doi.org/10.1146/annurev-genet-110410-132549 CrossRefGoogle Scholar
- Peay KG (2016) The mutualistic niche: mycorrhizal symbiosis and community dynamics. Annu Rev Ecol Evol Syst 47:143–164. https://doi.org/10.1146/annurev-ecolsys-121415-032100 CrossRefGoogle Scholar
- Plett JM, Daguerre Y, Wittulsky S, Vayssieres A, Deveau A, Melton SJ, Kohler A, Morrell-Falvey JL, Brun A, Veneault-Fourrey C, Martin F (2014) Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. Proc Natl Acad Sci U S A 111:8299–8304. https://doi.org/10.1073/pnas.1322671111 CrossRefGoogle Scholar
- R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from https://www.R-project.org/
- Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, San DiegoGoogle Scholar