One of the most fundamental requirements for forest
trees to flourish is the ability to acquire limited nutrients,
such as nitrogen and phosphorus, and water from soil.
As the levels of bioavailable inorganic nutrients in for-
est soils are often too low to sustain plant growth, most
trees rely on mycorrhizal fungal symbioses for their
nutrition
1,2
. As such, the establishment of the mycor-
rhizal lifestyle was a pivotal event in the evolutionary
history of land plants
3,4
. Subsequently, soil-borne mycor-
rhizal fungi, such as arbuscular mycorrhizal fungi and
ectomycorrhizal fungi (BOX 1), helped to shape plant
communities through mutualistic relationships with
rhizoid-based rooting systems and roots
5–8
(BOX 2).
A remarkable number of ectomycorrhizal basidiomy-
cetes and ascomycetes (more than 20,000 species) have
established symbioses with ~6,000 tree species, includ-
ing pines, beeches, oaks, eucalypts, dipterocarps and
poplars, whereas arbuscular mycorrhizal glomeromycetes
have established symbioses with ~200,000 plant species,
including poplars, eucalypts and some gymnosperms
2,6,9
.
Thus, these symbioses have a broad influence on forest
ecosystems. For example, extensive forests across the tem-
perate, boreal, subtropical and mountainous ecoregions
of the Northern Hemisphere and Southern Hemisphere
are composed of tree species that have been colonized by
ectomycorrhizal fungi
1,2,10
. In each of these forests, tril-
lions of plant rootlets are colonized and interconnected
by the mycelium of hundreds of different species of ecto-
mycorrhizal fungi, forming extraradicular mycorrhizal net-
works that have been informally termed the ‘wood-wide
web’ (REFS 11–13).
It is important to note that ectomycorrhizal fungi
occupy a dual niche; that is, the soil and the host
root. Similarly to their saprotrophic ancestors, ecto-
mycorrhizal fungi have access to mineral nutrients in
the soil that are efficiently absorbed by the perennial
absorbing mycelial network and partly translocated to
the host root
1,9,14
. However, ectomycorrhizal fungi have
lost much of the ability of saprotrophic fungi to efficiently
decay the lignocellulose that accumulates in wood and
soil organic matter
15
. Adaptation to the ectomycorrhizal
lifestyle has not only involved loss of functions; ecto-
mycorrhizal fungi have also gained some of the mech-
anisms that are used by biotrophic plant pathogens
to colonize root tissues and capture host glucose
16–18
(although ectomycorrhizal fungi lack the parasitic mor-
phological structures that are specific to pathogens, such
as the haustorium). These adaptations suggest that ecto-
mycorrhizal symbiosis provides a useful model for the
study of the evolution of nutritional modes in fungi
19,20
.
Although the vast majority of ectomycorrhizal fungi
share a typical anatomical pattern — a hyphal network
(known as the Hartig net) that forms inside root cells,
a sheathing mantle around rootlets and extramatri-
cal hyphae that explore the rhizosphere and nearby soil
niches
14,21
(FIG. 1) — the phenotypic diversity of these fungi
is broad, owing to variation in morphology, anatomy,
physiology, host species and ecological specialization
2,6,9,21
.
However, only a small number of ectomycorrhizal sym-
bioses have been studied at a molecular level, as studies
have mainly focused on the model associations between
Laccaria bicolor and poplars, Hebeloma cylindrosporum
Unearthing the roots of
ectomycorrhizal symbioses
Francis Martin
1
, Annegret Kohler
1
, Claude Murat
1
, Claire Veneault-Fourrey
2
and David S. Hibbett
3
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.
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.
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.
3
Biology Department, Clark
University, Lasry Center for
Bioscience, 950 Main Street,
Worcester, Massachusetts
01610, USA.
Correspondence to F.M.
francis.martin@inra.fr
doi:10.1038/nrmicro.2016.149
Published online 31 Oct 2016
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