Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Unearthing the roots of ectomycorrhizal symbioses

Nature Reviews Microbiology volume 14, pages 760–773 (2016)Cite this article

Subjects

Key Points

  • During the diversification of Fungi and the rise of conifer-dominated and angiosperm-dominated forests, ectomycorrhizal symbioses have enabled trees to colonize boreal and temperate regions.

  • Ectomycorrhizal fungi have evolved on several independent occasions from diverse saprotrophic lineages.

  • A large-scale loss of plant cell wall degradative enzymes — and, consequently, degradative abilities — has occurred in all ectomycorrhizal fungal lineages. However, the degradative enzymes that have been retained vary between each independent lineage and may correspond to a variation in capabilities for the decay of organic matter.

  • Genome analyses have shown how, through contraction and loss of major gene families, ectomycorrhizal fungi have become highly reliant on the availability of photoassimilates from their plant host, while preserving plant cell integrity by avoiding the release of degradative enzymes.

  • Ectomycorrhizal fungi use diffusible signalling molecules to manipulate the morphology and metabolism of host roots so that they provide a more suitable environment for fungal invasion.

  • The ectomycorrhizal fungus Laccaria bicolor has been used as a model for the study of protein effectors that manipulate host plant hormone receptors and related signalling pathways to dampen plant defences and facilitate fungal colonization.

Abstract

During the diversification of Fungi and the rise of conifer-dominated and angiosperm- dominated forests, mutualistic symbioses developed between certain trees and ectomycorrhizal fungi that enabled these trees to colonize boreal and temperate regions. The evolutionary success of these symbioses is evident from phylogenomic analyses that suggest that ectomycorrhizal fungi have arisen in approximately 60 independent saprotrophic lineages, which has led to the wide range of ectomycorrhizal associations that exist today. In this Review, we discuss recent genomic studies that have revealed the adaptations that seem to be fundamental to the convergent evolution of ectomycorrhizal fungi, including the loss of some metabolic functions and the acquisition of effectors that facilitate mutualistic interactions with host plants. Finally, we consider how these insights can be integrated into a model of the development of ectomycorrhizal symbioses.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The Populus spp.–Laccaria bicolor ectomycorrhizal symbiosis: an in vitro model system.
Figure 2: Evolution of ectomycorrhizal and orchid mycorrhizal symbioses.
Figure 3: The evolution of saprotrophic and ectomycorrhizal lifestyles in the subphylum Agaricomycotina.
Figure 4: Proposed model for the regulation of jasmonate signalling in poplar by MiSSP7.
Figure 5: A model for the establishment of ectomycorrhizal symbioses.

Similar content being viewed by others

References

  1. Read, D. J., Leake, J. R. & Perez-Moreno, J. Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can. J. Bot. 82, 1243 (2004).

    Article  CAS  Google Scholar 

  2. Smith, S. E. & Read, D. J. (eds) Mycorrhizal Symbiosis (Academic Press, 2008).

    Google Scholar 

  3. Pirozynski, K. A. & Malloch, D. W. The origin of land plants: a matter of mycotrophism. Biosystems 6, 153–164 (1975).

    Article  CAS  PubMed  Google Scholar 

  4. Simon, L., Bousquet, J., Lévesque, R. C. & Lalonde, M. Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363, 67–69 (1993).

    Article  Google Scholar 

  5. Selosse, M. A. & Le Tacon, F. The land flora: a phototroph–fungus partnership? Trends Ecol. Evol. 13, 15–20 (1998).

    Article  CAS  PubMed  Google Scholar 

  6. Brundrett, M. C. Coevolution of roots and mycorrhizas of land plants. New Phytol. 154, 275–304 (2002).

    Article  Google Scholar 

  7. Bidartondo, M. I. et al. The dawn of symbiosis between plants and fungi. Biol. Lett. 7, 574–577 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Strullu-Derrien, C. et al. Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant–fungus symbioses. New Phytol. 203, 964–979 (2014). This study is notable because it shows that early plants were colonized by species in the Mucoromycotina and Glomeromycota, which overturns the long-held paradigm that the early endophytes were exclusively in the Glomeromycota.

    Article  PubMed  Google Scholar 

  9. Van Der Heijden, M. G. A., Martin, F., Selosse, M. A. & Sanders, I. R. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 205, 1406–1423 (2015).

    Article  CAS  PubMed  Google Scholar 

  10. Soudzilovskaia, N. A. et al. Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry. Global Ecol. Biogeogr. 24, 371–382 (2015).

    Article  Google Scholar 

  11. Simard, S. W. et al. Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388, 579–582 (1997).

    Article  CAS  Google Scholar 

  12. Selosse, M.-A., Richard, F., He, X. & Simard, S. W. Mycorrhizal networks: des liaisons dangereuses? Trends Ecol. Evol. 21, 621–628 (2006).

    Article  PubMed  Google Scholar 

  13. Klein, T., Siegwolf, R. T. W. & Körner, C. Belowground carbon trade among tall trees in a temperate forest. Science 352, 342–344 (2016).

    Article  CAS  PubMed  Google Scholar 

  14. Finlay, R. Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J. Exp. Bot. 59, 1115–1126 (2008).

    Article  CAS  PubMed  Google Scholar 

  15. Treseder, K. K., Torn, M. S. & Masiello, C. A. An ecosystem-scale radiocarbon tracer to test use of litter carbon by ectomycorrhizal fungi. Soil Biol. Biochem. 38, 1077 (2006).

    Article  CAS  Google Scholar 

  16. Martin, F. et al. Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytol. 151, 145–154 (2001).

    Article  CAS  Google Scholar 

  17. Spanu, P. D. The genomics of obligate (and nonobligate) biotrophs. Annu. Rev. Phytopathol. 50, 91–109 (2012).

    Article  CAS  PubMed  Google Scholar 

  18. Bonfante, P. & Genre, A. Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1, 48 (2010).

    Article  CAS  PubMed  Google Scholar 

  19. Martin, F. et al. Sequencing the fungal tree of life. New Phytol. 190, 818–821 (2011).

    Article  CAS  PubMed  Google Scholar 

  20. Tedersoo, L., May, T. W. & Smith, M. E. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20, 217–263 (2010).

    Article  PubMed  Google Scholar 

  21. Peterson, R. L. & Massicotte, H. B. Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces. Can. J. Bot. 82, 1074–1088 (2004).

    Article  Google Scholar 

  22. Duplessis, S., Courty, P. E., Tagu, D. & Martin, F. Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol. 165, 599–611 (2005).

    Article  CAS  PubMed  Google Scholar 

  23. Larsen, P. E. et al. Multi-omics approach identifies molecular mechanisms of plant–fungus mycorrhizal interaction. Front. Plant Sci. 6, 1061 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Martin, F. & Selosse, M.-A. The Laccaria genome: a symbiont blueprint decoded. New Phytol. 180, 379–390 (2008).

    Article  CAS  PubMed  Google Scholar 

  25. Plett, J. M. & Martin, F. Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. Trends Genet. 27, 14–22 (2011).

    Article  CAS  PubMed  Google Scholar 

  26. Grigoriev, I. V. et al. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res. 42, D699–D704 (2014).

    Article  CAS  PubMed  Google Scholar 

  27. Matheny, P. B. & Hibbett, D. S. The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses. BMC Biol. 7, 13 (2009). The Bayesian relaxed molecular clock analyses that are carried out in this study show that there have been at least eight independent origins of ectomycorrhizal associations involving angiosperms, and at least six-to-eight origins of associations with gymnosperms.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Matheny, P. B. et al. Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae. J. Biogeogr. 36, 577–592 (2009).

    Article  Google Scholar 

  29. Skrede, I. et al. Evolutionary history of Serpulaceae (Basidiomycota): molecular phylogeny, historical biogeography and evidence for a single transition of nutritional mode. BMC Evol. Biol. 11, 230 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Rineau, F. et al. Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus. ISME J. 7, 2010 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Bödeker, I. T. M. et al. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytol. 203, 245 (2014).

    Article  CAS  PubMed  Google Scholar 

  32. Högberg, M. N. & Högberg, P. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol. 154, 791 (2002).

    Article  Google Scholar 

  33. Clemmensen, K. E. et al. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615 (2013).

    Article  CAS  PubMed  Google Scholar 

  34. Rytioja, J. et al. Plant-polysaccharide-degrading enzymes from Basidiomycetes. Microbiol. Mol. Biol. Rev. 78, 614–649 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Floudas, D. et al. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336, 1715–1719 (2012). This study maps the detailed evolution of wood-degrading enzymes by using a large set of genomes from wood-decaying fungi and shows that a key peroxidase and other enzymes that are involved in lignin decay were present in the common ancestor of the Agaricomycetes.

    Article  CAS  PubMed  Google Scholar 

  36. Nagy, L. G. et al. Comparative genomics of early-diverging mushroom-forming fungi provides insights into the origins of lignocellulose decay capabilities. Mol. Biol. Evol. 33, 959–970 (2016).

    Article  CAS  PubMed  Google Scholar 

  37. Hori, C. et al. Genome wide analysis of polysaccharides degrading enzymes in 11 white- and brown-rot Polyporales provides insight into mechanisms of wood decay. Mycologia 105, 1412–1427 (2013).

    Article  CAS  PubMed  Google Scholar 

  38. Lundell, T. K., Mäkelä, M. R., de Vries, R. P. & Hildén, K. S. Genomics, lifestyles and future prospects of wood-decay and litter-decomposing basidiomycota. Adv. Bot. Res. 70, 329–370 (2014).

    Article  Google Scholar 

  39. Ruiz-Dueñas, F. J. et al. Lignin-degrading peroxidases in Polyporales: an evolutionary survey based on 10 sequenced genomes. Mycologia 105, 1428–1444 (2013).

    Article  CAS  PubMed  Google Scholar 

  40. Martin, F. et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452, 88–92 (2008). This study describes the first genome from an ectomycorrhizal symbiont, and the predicted gene inventory of L. bicolor indicates previously unknown mechanisms of symbiosis that operate in biotrophic mycorrhizal fungi.

    Article  CAS  PubMed  Google Scholar 

  41. Martin, F. et al. Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464, 1033–1038 (2010).

    Article  CAS  PubMed  Google Scholar 

  42. Tisserant, E. et al. The genome of an arbuscular mycorrhizal fungus provides insights into the oldest plant symbiosis. Proc. Natl Acad. Sci. USA 110, 20117–20122 (2013).

    Article  CAS  PubMed  Google Scholar 

  43. Kohler, A. et al. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat. Genet. 47, 410–415 (2015). This works takes advantage of large-scale comparative genomics to show that the ectomycorrhizal lifestyle evolved in fungi through the repeated evolution of a 'symbiosis toolkit', with decreased numbers of PCWDEs and lineage-specific suites of mycorrhiza-induced genes.

    Article  CAS  PubMed  Google Scholar 

  44. Peter, M. et al. Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum. Nat. Commun. 7, 12662 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Kracher, D. et al. Extracellular electron transfer systems fuel cellulose oxidative degradation. Science 352, 1098–1101 (2016).

    Article  CAS  PubMed  Google Scholar 

  46. Bödeker, I. T. M., Nygren, C. M. R., Taylor, A. F. S., Olson, A. & Lindahl, B. D. Class II peroxidase-encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi. ISME J. 3, 1387–1395 (2009).

    Article  CAS  PubMed  Google Scholar 

  47. Talbot, J. M., Allison, S. D. & Treseder, K. K. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct. Ecol. 22, 955–963 (2008).

    Article  Google Scholar 

  48. Shah, F. et al. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol. 209, 1705–1719 (2015). This works demonstrates that several ectomycorrhizal fungi are able to decompose plant litter through the use of the Fenton reaction.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lindahl, B. D. & Tunlid, A. Ectomycorrhizal fungi — potential organic matter decomposers, yet not saprotrophs. New Phytol. 205, 1443–1447 (2015).

    Article  CAS  PubMed  Google Scholar 

  50. Wolfe, B. E., Tulloss, R. E. & Pringle, A. The irreversible loss of a decomposition pathway marks the single origin of an ectomycorrhizal symbiosis. PLoS ONE 7, e39597 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Felten, J. et al. The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol. 151, 1991–2005 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Martin, F., Kohler, A. & Duplessis, S. Living in harmony in the wood underground ectomycorrhizal genomics. Curr. Opin. Plant Biol. 10, 204–210 (2007).

    Article  CAS  PubMed  Google Scholar 

  53. Luo, Z. B. et al. Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol. 151, 1902–1917 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Tschaplinski, T. J. et al. Populus trichocarpa and Populus deltoides exhibit different metabolomic responses to colonization by the symbiotic fungus Laccaria bicolor. Mol. Plant Microbe Interact. 27, 546–556 (2014).

    Article  CAS  PubMed  Google Scholar 

  55. Veneault-Fourrey, C. & Martin, F. Mutualistic interactions on a knife-edge between saprotrophy and pathogenesis. Curr. Opin. Plant Biol. 14, 444–450 (2011).

    Article  PubMed  Google Scholar 

  56. Vayssieres, A. et al. Development of the poplar–Laccaria bicolor ectomycorrhiza modifies root auxin metabolism, signaling, and response. Plant Physiol. 169, 890–902 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Krause, K. et al. Biosynthesis and secretion of indole-3-acetic acid and its morphological effects on Tricholoma vaccinum–spruce ectomycorrhiza. Appl. Environ. Microbiol. 81, 7003–7011 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Plett, J. M. et al. Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots. New Phytol. 202, 270–286 (2014).

    Article  CAS  PubMed  Google Scholar 

  59. Ditengou, F. A. et al. Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture. Nat. Commun. 6, 6279 (2015). This works suggests that volatile sesquiterpenes have a key role in the development of the ectomycorrhizal symbiosis by stimulating the formation of short roots.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Sukumar, P. et al. Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions. Plant Cell Environ. 36, 909–919 (2013).

    Article  CAS  PubMed  Google Scholar 

  61. Doré, J. et al. Comparative genomics, proteomics and transcriptomics give new insight into the exoproteome of the basidiomycete Hebeloma cylindrosporum and its involvement in ectomycorrhizal symbiosis. New Phytol. 208, 1169–1187 (2015).

    Article  CAS  PubMed  Google Scholar 

  62. Plett, J. M. et al. The mutualist Laccaria bicolor expresses a core gene regulon during the colonization of diverse host plants and a variable regulon to counteract host-specific defenses. Mol. Plant Microbe Interact. 28, 261–273 (2014).

    Article  CAS  Google Scholar 

  63. Garcia, K., Doidy, J., Zimmermann, S. D., Wipf, D. & Courty, P. E. Take a trip through the plant and fungal transportome of mycorrhiza. Trends Plant Sci. http://dx.doi.org/10.1016/j.tplants.2016.07.010 (2016).

  64. Doré, J., Marmeisse, R., Combier, J. P. & Gay, G. A fungal conserved gene from the Basidiomycete Hebeloma cylindrosporum is essential for efficient ectomycorrhiza formation. Mol. Plant Microbe Interact. 27, 1059–1069 (2014).

    Article  CAS  PubMed  Google Scholar 

  65. Liao, H. L. et al. Metatranscriptomic analysis of ectomycorrhizal roots reveals genes associated with Piloderma–Pinus symbiosis: improved methodologies for assessing gene expression in situ. Environ. Microbiol. 16, 3730–3742 (2014).

    Article  CAS  PubMed  Google Scholar 

  66. Plett, J. M. et al. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr. Biol. 21, 1197 (2011).

    Article  CAS  PubMed  Google Scholar 

  67. Plett, J. M. et al. The effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses JA-responsive genes. Proc. Natl Acad. Sci. USA 111, 8299 (2014). This study shows that the symbiotic effector MiSSP7 from the ectomycorrhizal fungus L. bicolor interacts with the jasmonate co-receptor in planta to enable the development of symbiosis.

    Article  CAS  PubMed  Google Scholar 

  68. Kazan, K. & Manners, J. M. JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci. 17, 22–31 (2012).

    Article  CAS  PubMed  Google Scholar 

  69. Goossens, J., Fernandez-Calvo, P., Schweizer, F. & Goossens, A. Jasmonates: signal transduction components and their roles in environmental stress responses. Plant Mol. Biol. 91, 673–689 (2016).

    Article  CAS  PubMed  Google Scholar 

  70. Zuccaro, A. et al. Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog. 7, e1002290 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Lahrmann, U. et al. Mutualistic root endophytism is not associated with the reduction of saprotrophic traits and requires a noncompromised plant innate immunity. New Phytol. 207, 841–857. This works demonstrate the importance of indole-carboxylic acid derivatives as potential key players in the maintenance of a mutualistic interaction with root endophytes.

    Article  CAS  PubMed  Google Scholar 

  72. Fesel, P. H. & Zuccaro, A. Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis. Curr. Opin. Microbiol. 32, 103–112 (2016).

    Article  PubMed  Google Scholar 

  73. Kloppholz, S., Kuhn, H. & Requena, N. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21, 1204–1209 (2011). This study characterizes the symbiotic secreted effector SP7 from the arbuscular mycorrhizal fungus G. intraradices (now classified as R. irregularis ) and shows that it promotes the colonization of the host plant.

    Article  CAS  PubMed  Google Scholar 

  74. Garcia, K., Delaux, P. M., Cope, K. R. & Ané, J. M. Molecular signals required for the establishment and maintenance of ectomycorrhizal symbiosis. New Phytol. 208, 79–87 (2015).

    Article  PubMed  Google Scholar 

  75. Weßling, R. et al. Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe 16, 364–375 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Lo Presti, L. et al. Fungal effectors and plant susceptibility. Annu. Rev. Plant Biol. 66, 513–545 (2015).

    Article  CAS  PubMed  Google Scholar 

  77. Plett, J. M. & Martin, F. Reconsidering mutualistic plant–fungal interactions through the lens of effector biology. Curr. Opin. Plant Biol. 26, 45–50 (2015).

    Article  PubMed  Google Scholar 

  78. Veneault-Fourrey, C. et al. Genomic and transcriptomic analysis of Laccaria bicolor CAZome reveals insights into polysaccharides remodelling during symbiosis establishment. Fungal Genet. Biol. 72, 168–181 (2014).

    Article  CAS  PubMed  Google Scholar 

  79. Mankel, A., Krause, K. & Kothe, E. Identification of a hydrophobin gene that is developmentally regulated in the ectomycorrhizal fungus Tricholoma terreum. Appl. Environ. Microbiol. 68, 1408–1413 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Tagu, D. et al. Immuno-localization of hydrophobin HYDPt-1 from the ectomycorrhizal basidiomycete Pisolithus tinctorius during colonization of Eucalyptus globulus roots. New Phytol. 149, 127–135 (2000).

    Article  Google Scholar 

  81. Plett, J. M. et al. Phylogenetic, genomic organization and expression analysis of hydrophobin genes in the ectomycorrhizal basidiomycete Laccaria bicolor. Fungal Genet. Biol. 49, 199–209 (2012).

    Article  CAS  PubMed  Google Scholar 

  82. Pellegrin, C., Morin, E., Martin, F. & Veneault-Fourrey, C. Comparative analysis of secretomes from ectomycorrhizal fungi with an emphasis on small secreted proteins. Front. Microbiol. 6, 1278 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  83. Lionetti, V. & Métraux, J.-P. Plant cell wall in pathogenesis, parasitism and symbiosis. Front. Plant Sci. 5, 612 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  84. Cope, K. et al. Poplar as a model for dissecting early mycorrhizal signaling in woody perennials. 2016 International Society for Molecular Plant–Microbe Interactions Congress http://www.ismpmi.org/congress/2016/abstracts/pages/abstractdetail.aspx?LID=358 (2016).

  85. Delaux, P. M., Séjalon-Delmas, N., Bécard, G. & Ané, J. M. Evolution of the plant–microbe symbiotic 'toolkit'. Trends Plant Sci. 18, 298–304 (2013).

    Article  CAS  PubMed  Google Scholar 

  86. Parniske, M. Arbuscular mycorrhiza: the mother of plant-root endosymbioses. Nat. Rev. Microbiol. 6, 763–775 (2008).

    Article  CAS  PubMed  Google Scholar 

  87. Kottke, I. & Oberwinkler, F. The cellular structure of the Hartig net: coenocytic & transfer cell-like organization. Nordic J. Bot. 7, 85–95 (1987).

    Article  Google Scholar 

  88. Agerer, R. (ed) Descriptions of Ectomycorrhizae (Einhorn-Verlag, 1996–2012).

  89. Krings, M., Taylor, T. N., Taylor, E. L., Dotzler, N. & Walker, C. Arbuscular mycorrhizal-like fungi in Carboniferous arborescent lycopsids. New Phytol. 191, 311–314 (2011).

    Article  PubMed  Google Scholar 

  90. LePage, B. A., Currah, R. S., Stockey, R. A. & Rothwell, G. W. Fossil ectomycorrhizae from the Middle Eocene. Am. J. Bot. 84, 410–412 (1997).

    Article  CAS  PubMed  Google Scholar 

  91. Wang, H. et al. Rosid radiation and the rapid rise of angiosperm-dominated forest. Proc. Natl Acad. Sci. USA 106, 3853–3858 (2009).

    Article  CAS  PubMed  Google Scholar 

  92. Rice, A. V. & Currah, R. S. Oidiodendron maius: saprobe in Sphagnum peat, mutualist in ericaceous roots. Soil Biol. 9, 227–246 (2006).

    Article  Google Scholar 

  93. Sasaki-Sekimoto, Y. et al. Basic helix–loop–helix transcription factors jasmonate-associated MYC2-like1 (JAM1), JAM2, and JAM3 are negative regulators of jasmonate responses in Arabidopsis. Plant Physiol. 163, 291–304 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Xin, X. F. & He, S. Y. Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu. Rev. Phytopathol. 51, 473–498 (2013).

    Article  CAS  PubMed  Google Scholar 

  95. Gimenez-Ibanez, S. et al. The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis. PLoS Biol. 12, e1001792 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Jiang, S. S. et al. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLoS Pathog. 9, e1003715 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Plett, J. M. & Martin, F. Poplar root exudates contain compounds that induce the expression of MiSSP7 in Laccaria bicolor. Plant Signal. Behav. 7, 12–15 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Hacquard, S. et al. Laser microdissection and microarray analysis of Tuber melanosporum ectomycorrhizas reveal functional heterogeneity between mantle and Hartig net compartments. Environ. Microbiol. 15, 1853–1869 (2013).

    Article  CAS  PubMed  Google Scholar 

  99. Garcia, K. & Zimmermann, S. D. The role of mycorrhizal associations in plant potassium nutrition. Front. Plant Sci. 5, 337 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  100. Becquer, A. et al. From soil to plant, the journey of P through trophic relationships and ectomycorrhizal association. Front. Plant Sci. 5, 548 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  101. López, M. F. et al. The sugar porter gene family of Laccaria bicolor: function in ectomycorrhizal symbiosis and soil-growing hyphae. New Phytol. 180, 365–378 (2008).

    Article  CAS  PubMed  Google Scholar 

  102. Xu, H. et al. Overexpression of Laccaria bicolor aquaporin JQ585595 alters root water transport properties in ectomycorrhizal white spruce (Picea glauca) seedlings. New Phytol. 205, 757–770 (2015).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Many of the findings discussed in this manuscript were obtained within the framework of the Mycorrhizal Genomics Initiative (MGI) consortium and the Oak Ridge National Laboratory Plant–Microbe Interfaces project. The authors thank I. Grigoriev, J. Tuskan, M. Doktycz, J. Plett, E. Morin, Y. Daguerre, C. Pellegrin, L. Nagy, D. Floudas, M. Peter and J. Labbé for exciting discussions and interactions in relation to this manuscript. The MGI is supported by the French National Institute for Agricultural Research (INRA), the US Department of Energy (DOE) Joint Genome Institute (JGI; Office of Science of the US Department of Energy under contract number DE-AC02-05CH11231), the Region Lorraine Research Council and the European Commission (European Regional Development Fund (ERDF)). Research in the laboratory of F.M. is funded by the Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE; grant ANR-11-LABX-0002-01), the US DOE through the Oak Ridge National Laboratory Scientific Focus Area for Genomics Foundational Sciences (Plant Microbe Interfaces Project).

Author information

Authors and Affiliations

  1. Institut national de la recherche agronomique (INRA), Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (ARBRE), Centre INRA-Lorraine, 54280, Champenoux, France

    Francis Martin, Annegret Kohler & Claude Murat

  2. Université de Lorraine, Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Laboratoire d'excellence Recherches Avancées sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (ARBRE), 54500, Vandoeuvre-lès-Nancy, France

    Claire Veneault-Fourrey

  3. Biology Department, Clark University, Lasry Center for Bioscience, 950 Main Street, Worcester, 01610, Massachusetts, USA

    David S. Hibbett

Authors
  1. Francis Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Annegret Kohler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claude Murat
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Claire Veneault-Fourrey
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David S. Hibbett
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francis Martin.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Glossary

Rhizoid-based rooting systems

Simple hair-like protuberances that extend from the epidermal cells of certain plants. Rhizoids are similar in structure and function to the root hairs of vascular land plants.

Basidiomycetes

(Formally known as Basidiomycota). A division or phylum within the kingdom Fungi that, together with the ascomycetes (formally known as Ascomycota), constitute the subkingdom Dikarya (often referred to as 'higher fungi'). Basidiomycetes reproduce sexually through the formation of specialized club-shaped end cells, known as basidia, that contain meiospores.

Ascomycetes

(Formally known as Ascomycota). A division or phylum in the kingdom Fungi that, together with the basidiomycetes, form the subkingdom Dikarya. Members of the Ascomycota are commonly known as the sac fungi. The defining feature of ascomycetes is the ascus, a microscopic sexual structure in which meiospores, known as ascospores, are formed.

Glomeromycetes

(Formally known as Glomeromycota). One of the seven currently recognized phyla in the kingdom Fungi. The 230 recognized species are all obligate symbionts of land plants that form arbuscular mycorrhizal associations.

Mycorrhizal networks

Underground networks of hyphae that are produced by mycorrhizal fungi. Mycorrhizal networks connect individual plants together and transfer water, carbon and other nutrients.

Saprotrophic fungi

Fungi that obtain their nutrition from non-living organic material.

Rhizosphere

The soil that surrounds and is influenced by the roots of a plant.

Protocorms

Tuber-shaped bodies with trichomes that are produced by the young seedlings of various orchids and other plants that have associated mycorrhizal fungi.

Apoplastic space

In plants, the apoplastic space, or apoplast, is formed by the continuum of cell walls of adjacent cells as well as the extracellular space. It is the space outside of the plasma membrane.

Rhizodermis

The epidermis that is formed by the outermost layer of primary cells in the plant root.

Root cortex

The outermost layer of the plant root, which is bound on the outside by the epidermis (or rhizodermis) and on the inside by the endodermis. The root cortex is usually composed of large thin-walled parenchyma cells.

Laccases

Enzymes that carry out a one-electron oxidation on phenols and similar molecules. Laccases are part of a larger group of enzymes that are termed the multicopper enzymes and that occur widely in fungi (but are also found in many plants and bacteria).

White-rot fungi

Fungi that decay wood by breaking down lignin and cellulose.

Auriculariales

An order of the kingdom Fungi in the class Agaricomycetes. Species in the Auriculariales often differentiate gelatinous fruit bodies and are thus commonly named 'jelly fungi'.

Brown-rot fungi

Fungi that decay wood by breaking down hemicellulose and cellulose, leaving the lignin behind.

Endophyte

A bacterium or fungus that lives inside a plant host without causing apparent disease.

Agaricomycetidae

A subclass of fungi in the phylum Basidiomycota.

Sesquiterpenes

A class of volatile hydrocarbons that consist of three isoprene units.

Middle lamella

In plants, the middle lamella is formed by a pectin layer that cements the cell walls of adjoining cells together.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martin, F., Kohler, A., Murat, C. et al. Unearthing the roots of ectomycorrhizal symbioses. Nat Rev Microbiol 14, 760–773 (2016). https://doi.org/10.1038/nrmicro.2016.149

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro.2016.149

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing