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Unearthing the roots of ectomycorrhizal symbioses

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.

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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.

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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).

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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.

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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

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