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Living in harmony in the wood underground:ectomycorrhizal genomicsFrancis Martin, Annegret Kohler and Sebastien Duplessis
The ectomycorrhizal symbiosis involving trees and soil
fungi is a process of major ecological importance in forest
ecosystems. The establishment of an effective symbiosis
encompasses a series of complex and overlapping
developmental processes in the colonizing mycelium and roots
of host trees. Regulated gene expression is an important
mechanism for controlling ectomycorrhizal symbiosis
development and functioning. Gene profiling studies led to the
identification of genes that are required for fungal attachment,
plant defense, and symbiosis-related metabolism. They
showed that changes in morphology associated with
mycorrhizal development were accompanied by changes in
transcript patterns, but no ectomycorrhiza-specific genes were
detected. Comparison of the genomes of pathogenic and
saprobic fungi with the recently released ectomycorrhizal
Laccaria genome is providing crucial insights into the genetic
makeup of plant–fungus interactions.
Addresses
UMR 1136 INRA/UHP, Interactions Arbres/Micro-Organismes, IFR 110,
Centre INRA de Nancy, 54280 Champenoux, France
Corresponding author: Martin, Francis ([email protected])
Current Opinion in Plant Biology 2007, 10:204–210
This review comes from a themed issue on
Genome studies and molecular genetics
Edited by Stefan Jansson and Edward S Buckler
Available online 8th February 2007
1369-5266/$ – see front matter
# 2007 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2007.01.006
IntroductionMycorrhizal symbioses — the union of roots and soil fungi
— are widespread: boreal, temperate, montane and trop-
ical forests all have them, as do grasslands and tundras.
Within days of their emergence in the upper soil profiles,
up to 95% of short roots of most terrestrial plants are
colonized by mycorrhizal fungi. The fungal symbionts
send out extensive webs of fine threads of mycelia, which
link with and extend the reach of plant roots. Host plants
are then able to harness mycorrhizal symbionts very
efficiently for their nutritional benefit. They hijack the
formidable web of saprotrophic hyphae of mycorrhizal
fungi permeating the soil horizons, litter and decaying
wood debris. The prospecting mycelium delivers soil
minerals, particularly phosphorus and nitrogen, to the
Current Opinion in Plant Biology 2007, 10:204–210
host roots; the plants reward them with energizing
photoassimilates. In addition, these fungal threads link
one plant to another, transferring nutrients not only
among fungi but also from plant to plant, shaping the
biological makeup of whole communities [1].
It is widely thought that the activity of mycorrhizal fungi
affected the evolution of early land plants [2,3]. There are
therefore important ecological benefits to be gained from
understanding the molecular evolution of mycorrhizal
symbioses. Although research over the past decade has
broadened our knowledge of the ecological roles of
mycorrhizal symbioses [1], our understanding of the
mechanisms that govern the establishment and function-
ing of arbuscular endomycorrhiza (AM) and ectomycor-
rhizal (ECM) symbioses has only recently significantly
improved. What could be the molecular basis of such a
progressive, highly organized ontogenic process? What is
the role of rhizospheric chemicals and cellular signals in
symbiosis development? How many gene networks con-
trol mycorrhiza development, as distinct from providing
the housekeeping functions of the fungal and plant cells?
This review focuses on the molecular processes involved
in the development of ECM symbiosis. Recent reviews
[4–6] summarize the progress made in understanding AM
symbiosis.
The quest for master symbiotic genes in theectomycorrhizal symbiosisEctomycorrhizal fungi are best known for their fruiting
structures (e.g. toadstools) that often grow next to tree
trunks in woodlands. Although a relatively small number
of plants (around 8000) form ECM, the ecological import-
ance of these symbioses is amplified by their wide occu-
pancy of biomes [1,3]. Through mutualistic symbioses
with ECM fungi, tree species have been able to acquire
metabolic capabilities that have allowed the utilization of
otherwise unavailable ecological niches. The mechan-
isms involved in the development of symbiosis are likely
to be similar if not identical in the numerous ectomycor-
rhizal morphotypes and in mutualistic and some bio-
trophic parasitic symbioses. The identification of these
primary genetic determinants is a daunting task. It
involves the typical gene-to-phenotype approach (i.e.
the identification of traits by characterization of gene
expression and subsequent gene inactivation). It should
be kept in mind, however, that this powerful approach
might be restricted by the fact that symbiosis develop-
ment and activity might be determined partly by complex
epistatic interactions among different genes showing
subtle quantitative variation.
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Ectomycorrhizal genomics Martin, Kohler and Duplessis 205
The pathways triggering the development of the ecto-
mycorrhizal hyphal networks (i.e. mantle sheath, apoplas-
tic Hartig net and soil fungal mats) involve a cascade of
nuclear gene expression, including the expression of
genes that encode developmental proteins, enzymes
and transporters that regulate the details of symbiosis
development [7]. These genes respond to rhizospheric
and apoplastic signals released by the plant partner,
positional information mediated by sensory molecules
and nutritional cues [7–9]. In the wake of the first tran-
script profiling of the Eucalyptus–Pisolithus symbiosis [10],
hundreds of genes that are preferentially expressed in
symbiotic tissues have been identified using cDNA
arrays, amplified fragment length polymorphism (AFLP)
or suppression subtractive hybridization (SSH) [11–14,
15��,16��]. These studies have confirmed that dramatic
alterations in gene expression take place during, and are
likely to be required for, symbiosis development; how-
ever, plant and fungal genetic switches that are necessary
for ECM development remain unidentified to date.
Legume mutants have been key to identifying the
genetic switches in AM development [4,6,17]. Impaired
genes such as those encoding the SYMRK/NORK/DMI2
receptor kinase, the DMI1 ion channel and DMI3
calcium- and calmodulin-dependent kinase are collec-
tively referred to as the ‘common’ SYM genes. These
genes define a partial overlap between the genetic pro-
grams for AM endosymbiosis and those for the nitrogen-
fixing root nodule symbiosis. The evolutionary implica-
tion is that the younger bacterial symbiosis has recruited
perception functions from the ancient AM symbiosis. It is
tempting to speculate that the recent ectomycorrhizal
symbioses (which first evolved around 180 million years
ago) have also recruited the AM symbiosis SYM genes for
signaling and the early steps of the symbiosis (e.g. intra-
radicular accommodation).
These DMI genes are found in the genome of Populustrichocarpa [18��], a tree hosting both AM and ECM
symbioses. Their inactivation using RNAi will confirm
whether or not perennial tree species and legumes have
evolved similar mechanisms to interact with mycorrhizal
fungi. Although many pieces of the puzzle remain to be
elucidated, it seems inescapable that the cross-talk
between rhizospheric metabolites, the hormonal balance
and signalling networks involving Ca2+ play important
roles in coordinating the execution of the appropriate
responses. It will be fascinating to learn more about the
multiple facets of this communication network. In this
regard, advances in the elucidation of symbiosis signalling
pathways can be accelerated by the identification of more
target genes by transcript profiling [15��,16��] and inser-
tional mutagenesis [22].
Interestingly, a quantitative trait locus (QTL) linked to
ectomycorrhizal infection rate on the male P. trichocarpa
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genetic map was localized close to a locus previously
shown to be involved in the interaction between Populusand the foliar rust fungus Melampsora larici populina [20].
This evidence provides a genetic indication that the
ectomycorrhizal trait could be associated with loci and
genes that might be common to the interaction with
mutualistic root and pathogenic leaf fungi [19].
Transcript alteration in symbiotic tissueTo examine gene activity changes that are associated with
the development of the Eucalyptus–Pisolithus and Betula–Paxillus symbioses, expression profiling using cDNA arrays
were performed during the development of ectomycor-
rhiza [15��,16��]. RNAs used for cDNA array hybridiz-
ations were derived from nonmycorrhizal roots, free-
living mycelium and colonized roots collected during
the early, middle and late stages of symbiosis development.
Thus, these time points for RNA collection correspond to
the various stages of ectomycorrhiza development: i) early
hyphae–root contacts, ii) root surface colonization, mantle
formation, root penetration and subsequent Hartig net
formation, and iii) mature symbiotic organ. These inves-
tigations confirmed that changes in morphology that are
associated with mycorrhizal development were accom-
panied by changes in transcript patterns and that these
changes commenced at the time of contact between the
two partners, long before the formation of functional
ectomycorrhiza.
Clustering algorithms revealed groups of transcripts that
have both related regulation patterns and expression
amplitudes (Figure 1). Developmental reprogramming
was observed in roots and hyphae, although the magnitude
of transcriptome alteration appears to be much larger in the
mycelium (�10–20% of the analyzed transcripts) than in
root cells (�2% of the transcripts) [10,14,15��,16��]. Induc-
tion of common gene networks takes place in ectomycor-
rhizal systems, as demonstrated by the observation
that several cellular functions are similarly regulated in
the investigated symbiotic models. For example, many
cellular functions were found to be upregulated upon
symbiosis development, including fungal cell division
and proliferation, differentiation and signaling, synthesis
of cell wall and extracellular matrices, plant defense or
stress responses and primary metabolism (i.e. glycolytic
respiration, amino acid biosynthesis and the activity of
transporters).
At the different developmental stages studied, the devel-
opment of the symbioses between Pisolithus–Eucalyptus,Paxillus–Betula, Pisolithus–Populus, Laccaria–Populus, Lac-caria–Pseudotsuga and Tuber–Tilia do not induce the
expression of ectomycorrhiza-specific genes [10–14,
15��,16��]. Overall, the induction or repression rates of
the ectomycorrhiza-regulated genes were moderate and
rarely exceeded five-fold upregulation or downregulation.
An analysis of around 9500 unique transcripts (i.e. 20% of
Current Opinion in Plant Biology 2007, 10:204–210
206 Genome studies and molecular genetics
Figure 1
The main expression patterns of plant and fungal symbiosis-regulated genes during the development of the ectomycorrhizal symbiosis, as revealed by
transcript profiling studies. Transcriptional responses of fungal and root tissues progressing through the development of ectomycorrhiza were
investigated in the Betula–Paxillus and Eucalyptus–Pisolithus interactions using cDNA arrays [15��,16��]. We have derived groups of coordinately
expressed genes using hierarchical and non-hierarchical clustering algorithms. Major temporal patterns of induction or repression were observed with
distinct groups of genes that have early, middle and late transcription responses to fungal colonization (after [15��]).
the total gene set) of P. trichocarpa confirmed the lack of
host ectomycorrhiza-specific genes (A Kohler et al. unpub-
lished). The apparent lack of ectomycorrhiza-specific
genes and the moderate induction of symbiosis-regulated
genes are striking, and suggest that ontogenic and meta-
Current Opinion in Plant Biology 2007, 10:204–210
bolic programs that lead to the development of symbiosis
are driven by the differential expression of pre-existing
transcription factors and/or transduction pathways, rather
than by the expression of symbiosis-specific gene arrays.
A more complete analysis of this crucial question awaits the
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Ectomycorrhizal genomics Martin, Kohler and Duplessis 207
completion of larger sets of ECM expression profiles on a
wider range of associations using whole-genome microar-
rays and high-throughput quantitative PCR of transcrip-
tion factors.
By comparing two closely related strains of Paxillus invo-lutus, Le Quere et al. [21] showed that loss of symbiotic
ability was associated with the lack of plant-induced gene
expression of symbiosis-regulated genes. The observed
changes in expression are likely to be due to changes in
promoter element sequences and expression levels of
transcription factors. Tunlid and coworkers also showed
that the lack of mutualism was associated with structural
changes in the products of two of the differentially
regulated genes, the gene encoding the conconamycin-
induced protein CIPC1 and that encoding the metallo-
chaperone CCHA [21]. A further challenge will be to
investigate the function of these proteins and how the
observed nucleotide substitutions alter symbiotic com-
patibility.
The ectomycorrhiza-regulated genes that have been
identified using transcriptomics are primary targets for
gene inactivation, but homologous recombination and
RNA interference procedures are not yet available for
ECM fungi. In a breakthrough study, Agrobacterium-
mediated transformation was recently used for random
insertional mutagenesis to generate mutants of the ecto-
mycorrhizal basidiomycete Hebeloma cylindrosporum that
were impaired in their symbiotic capability [22]. Light
and scanning electron microscopy observations of pine
roots inoculated with nonmycorrhizal (myc null) mutants
suggested that these mutants were blocked at early stages
of interaction, confirming that master genes are essential
for symbiosis development.
Toward the promised land: how to land andescape host surveillanceBefore contact, the hyphae of ECM fungi growing in the
rhizosphere induce an intense short-root formation, pro-
viding a means of increasing contact sites and niches for
hosting the colonizing hyphae. The molecular basis for this
coup d’etat is unknown, but it is clear that the mycobiont
alters auxin-regulated developmental pathways, meriste-
matic activity and cell shape through the action of secreted
molecules, such as auxins and hypaphorin, an indole-3-
acetic acid (IAA) antagonist [7,8,23,24]. Several ectomy-
corrhiza-regulated genes in host tissues are involved in
auxin metabolism, calcium signaling pathways and tran-
scriptional regulation, thus supporting this hypothesis
[10,14,15��,16��].
After contact, mycorrhizal fungi must be equipped to
evade or overcome the constitutive barriers and inducible
defenses of its host, and must possess the developmental
and metabolic features needed to exploit the nutritional
environment provided by that host. Some nonspecific,
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broad-spectrum responses (e.g. those involving metal-
lothioneins, chitinases, glutathione S-transferases and
peroxidases) are clearly mounted in plant hosts when
ectomycorrhizal fungi approach the host roots [25] and
as they penetrate the root and digest their way through
the apoplastic space [15��,16��]. These induced defense
responses might limit the fungal invasion of root tissues.
Future research should explore the molecular mechan-
isms that orchestrate the escape of the symbionts from the
host defense system. For example, we do not know how
ECM fungi avoid clearance by the innate immune system
of the host and persist for large periods of time in host
tissues.
Novel metabolic networks for a fair tradeAs expected from an alliance aimed to better exploit the
scarce nutrients of soil horizons, symbiosis induces
dramatic changes in nutrient content and metabolic fluxes
in root and fungal tissues [26]. To survive in planta, the
developing mycobiont must express the channels, pumps
and transporters at the appropriate time, the correct
location and at the right levels [27�,28]. ECM fungi
activate and regulate the anabolic and catabolic enzymes
involved in nutrition and growth over a sustained period
to complete the symbiosis development [15��,16��]. It has
been a general observation that these metabolic altera-
tions are also accompanied by mineral and nutrient-
related changes in plant gene expression.
Owing to large expressed sequence tag (EST) sets
[12,28] and available Populus [18��] and Laccaria (http://
genome.jgi-psf.org/Lacbi1/Lacbi1.home.html) genome
sequences, several genes encoding transporters [29–
33,34�] and channels [35] have been cloned and their
expression during ECM development investigated. The
observed upregulation of several of these genes is likely to
reflect the intense metabolite fluxes occurring between the
symbiotic partners and reveal a complex interplay of fungal
and plant transporter activities. An important challenge
will be to determine how the different transporters are
reallocated at the plant–fungal interface to sustain the
intense and opposite fluxes of phosphorus and nitrogen
compounds (fungus to plant) and carbon assimilates
(plant to fungus).
An additional challenge for further research will be to
identify the ‘dispatch centre’, if any, that coordinates the
fluxes of cargo vesicle that translocate transporter proteins
to the plasma membranes of the symbiotic interfaces.
Functional specialization of the hyphal webcompartmentsThe fungal symbiont differentiates three main hyphal
networks: (i) the mantle and intraradical Hartig net of the
ectomycorrhizal tips with their mutualistic activities, (ii)
the rhizomorphic web linking the latter tissues to (iii)
Current Opinion in Plant Biology 2007, 10:204–210
208 Genome studies and molecular genetics
fungal mats that proliferate on nutrient-rich sources
in the different soil horizons. These compartments
with contrasted metabolic activities should efficiently
solve logistics issues. In microcosms mimicking forest
soil conditions, Wright et al. [36��] and Morel et al.[37�] identified striking differential expression in the
various fungal compartments of the Betula–Paxillusassociation (i.e. mycelial patches growing on nutrient
sources, extramatrical hyphae, rhizomorphs draining
metabolites to the symbiotic tissues and ectomycorrhizal
tips). The pattern of differential expression of genes (e.g.
nitrogen-assimilating enzymes) might be influenced by
multiple factors, such as the level of nutrients within the
nutrient patches, the extent of metabolite translocation
versus assimilation within the extramatrical mycelium,
and the microenvironment in which the rhizomorph and
mycorrhizal root tips are situated. Interestingly, both
Wright et al. [36��] and Morel et al. [37�] showed that
urea was the principal nitrogen compound in hyphae, and
suggested that the urea cycle could be activated in
extramatrical mycelium of P. involutus under nitrogen-
limited conditions; it might also play a key role in both
nitrogen translocation between the hyphal webs and in
nitrogen transport between partners [27�].
These novel transcriptomics data clearly confirmed the
physiological heterogeneity and functional specialization
among the different compartments of the fungal webs
[38]. The identification of signals that coordinate these
activities is a major focus for further research. Whether
gene expression of metabolic genes is controlled by sugar-
and amino-acid-dependent regulation, as reported for
free-living mycelium [9], by symbiosis-related develop-
mental signals [7], the external microenvironment
[36��,37�] or, as is likely, by a complex blend of these
different signals is currently unknown.
What makes a good ectomycorrhizal fungus?The ECM fungi are found in many ascomycetous and
basidiomycetous clades, suggesting that this mutualistic
habit has evolved several times during the evolution of the
Mycota kingdom, probably from saprotrophic ancestors
[39].
On the genomic level, there are basically three compatible
mechanisms that can account for the multiple emergences
of and adaptations to symbiosis in fungi: differences in the
regulation of gene expression through the activity of a core
set of transcription factors; the presence of novel genes; and
gene loss and deletions [40]. The mechanism(s) involved
are likely to be identified in the coming years through
comparative genomics, because a large amount of infor-
mation from the genome sequences of fungal saprotrophs,
pathogens and symbionts is now available through the
Fungal Genome Initiative at the Broad Institute (http://
www.broad.mit.edu/annotation/fungi/fgi/) and the Com-
munity Sequencing Programme of the US Department
Current Opinion in Plant Biology 2007, 10:204–210
of Energy Joint Genome Institute (http://www.jgi.doe.gov/
CSP/index.html). There are currently 115 completed or
ongoing fungal genome projects [41,42].
In the wake of the Populus genome sequencing project
[18��], the sequencing of the genome of the ECM basi-
diomycete Laccaria bicolor was accomplished, using the
whole-genome shotgun approach, by the US Department
of Energy Joint Genome Institute (Laccaria Genome Por-
tal; [http://genome.jgi-psf.org/Lacbi1/Lacbi1.home.html])
and the Laccaria Genome Consortium, and publicly
released in July 2006.
The Laccaria genome is much larger (�65 Mb) than that
of the other fungi whose genomic sequences have been
published [41–45]. A total of around 20 000 genes encod-
ing proteins (i.e. 37% of the whole-genome sequence)
were identified using automated annotation and manual
curation. These genes contain many short introns and, as
expected from previous EST analysis [12], 50% of them
are of unknown function. Predicted genes, supporting
evidence, and structural and functional annotations are
available through interactive visualization and analysis
tools from the JGI Laccaria Genome Portal.
This genome sequence, from a major mycorrhizal clade,
reveals an organism equipped to take advantage of tran-
sient occurrences of high-nutrient niches within a bulk
low-nutrient environment. Not only the roots of the host–
plant but also dead organic matter and microscale ‘hot
spots’ of the rhizospheric soil might provide such niches.
Ongoing analysis of the Laccaria genome reveals that this
ECM basidiomycete has both saprotrophic and mutualistic
abilities (F Martin et al., unpublished). By elucidating the
genomes of close relatives that have differing saprotrophic
or symbiotic properties, such as the basidiomycetous gill
mushrooms L. bicolor and Coprinopsis cinerea, we will be
able to catalogue the genetic differences that might
underlie their different life habits. Hence, we should
achieve a deeper understanding of the processes by which
fungi colonize wood, interact with their host trees in their
ecosystem and perform vital functions in the carbon and
nitrogen cycles.
ConclusionsTranscriptomics of the ectomycorrhizal symbiosis offers
new insights into our understanding of both biotrophic
interactions and fungal and root development. The
integration of knowledge arising from whole-genome
sequencing with information provided by transcrip-
tomics and advanced functional analysis of target genes,
such as transporters, will help us understand how
fungi have learned to interact with plants in a balanced
way.
A view that is gaining increasing support among research-
ers studying plant–microbe interactions is the hypothesis
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Ectomycorrhizal genomics Martin, Kohler and Duplessis 209
that plant fungal pathogens might have arisen by the
recruitment and exploitation of gene networks of ancient
symbiotic pathways; the symbionts themselves being
derived from saprotrophic ancestors. The gene networks
that control the saprotrophic/biotrophic phase switch,
recognition mechanisms, host penetration and in plantaaccommodation are often alike in biotrophic parasites and
mutualistic symbionts. Analysis of the molecular mech-
anisms that lead to ECM symbiosis should thus lead to a
better understanding of plant–pathogen interactions. It
will be far harder to define genes that influence symbiont
fitness. Any gene that provides the mycobiont with a
growth advantage could easily influence how beneficial a
particular strain is within a given host. Therefore, dis-
secting the molecular mechanisms of symbiosis fitness
requires both the identification of the functions of indi-
vidual genes and knowledge of how genes interact to form
complex traits, such as those expressed in a mutualistic
symbiosis. It is difficult to predict the total number of
genes involved in symbiosis and, hence, the scope for
each mycorrhizal association to be unique. There are
more than 8000 different ectomycorrhizal associations,
and each and every ectomycorrhizal type might express a
specific set of genes. Despite this, a variety of morpho-
logical and molecular common parameters can be used to
classify ectomycorrhizal symbioses into discrete molecu-
lar classes for further investigation [15��,16��]. In the
future, symbiotic molecular phenotypes might be corre-
lated to ecological phenotypes.
Finally, knowledge of the regulatory mechanisms that
allow fungal symbionts to promote plant growth in nutri-
ent-scarce environments will provide the information
needed to manage sustainable forest ecosystems in a
biosphere threatened by global climate changes.
AcknowledgementsSpecial thanks go to the former and present members of our research groupfor their great contributions to our work and for stimulating discussions.Investigations carried out in our laboratory were supported by grants fromthe INRA, Genoscope (project ForEST) and the Region Lorraine. TheLaccaria genome project was performed under the auspices of the USDepartment of Energy’s Office of Science, Biological and EnvironmentalResearch Program, the University of California, Lawrence LivermoreNational Laboratory and INRA.
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� of special interest�� of outstanding interest
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16.��
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18.��
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27.�
Chalot M, Blaudez D, Brun A: Ammonia: a candidate for nitrogentransfer at the mycorrhizal interface. Trends Plant Sci 2006,11:263-266.
The data reviewed herein provide strong biochemical evidence thatammonium might play a role in nitrogen translocation between ectomy-corrhizal partners. Together with the papers by Laczko et al. [26] and Selleet al. [34�], this paper re-visits the text book view on pathways that areinvolved in nutrient exchanges in mycorrhizal symbioses.
28. Lambilliotte R, Cooke R, Samson D, Fizames C, Gaymard F,Plassard C, Tatry MV, Berger C, Laudie M, Legeai F et al.:Large-scale identification of genes in the fungus Hebelomacylindrosporum paves the way to molecular analyses ofectomycorrhizal symbiosis. New Phytol 2004, 164:505-513.
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34.�
Selle A, Willmann M, Grinze N, Geßler A, Weiß M, Nehls U: Thehigh-affinity poplar ammonium importer PttAMT1.2 and its rolein ectomycorrhizal symbiosis. New Phytol 2005, 168:697-706.
This study shows an increased ammonium uptake capacity of mycor-rhizal Populus roots through the mycorrhiza-dependent upregulation ofan ammonium transporter. It also suggests, together with the expressionof putative ammonium exporter genes in the ectomycorrhizal fungusAmanita muscaria, that ammonium could be a major nitrogen sourcedelivered from the fungus to the plant in symbiosis. Also see annotationChalot et al. [27�].
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36.��
Wright DP, Johansson T, Le Quere A, Soderstrom B, Tunlid A:Spatial patterns of gene expression in the extramatricalmycelium and mycorrhizal root tips formed by theectomycorrhizal fungus Paxillus involutus in associationwith birch (Betula pendula) seedlings in soil microcosms.New Phytol 2005, 167:579-596.
Using soil microcosms of increased ecological complexity, more geno-mics studies of the kind discussed herein will advance our understandingof mycorrhizal symbioses in situ. The authors investigated the geneexpression of the mycobiont in the major hyphal compartments (i.e.symbiotic root tissues, the web of rhizomorphic hyphae permeatingthe soil and the fungal patches proliferating on nutrient sources). Pre-ferentially expressed genes were identified in these various compart-ments, illustrating the physiological heterogeneity of the fungal mycelia. Itis a major touchstone for future research.
37.�
Morel M, Jacob C, Kohler A, Johansson T, Martin F, Chalot M,Brun A: Identification of genes differentially expressed inextraradical mycelium and ectomycorrhizal roots duringPaxillus involutus–Betula pendula ectomycorrhizal symbiosis.Appl Environ Microbiol 2005, 71:382-391.
Together with the work described by Wright et al. [36��], this study usessoil microcosms to investigate functional specialization among the dif-ferent compartments of the fungal webs in ectomycorrhizal symbiosis.This transcriptomics analysis shows the overlooked importance of theurea cycle in nitrogen translocation in ectomycorrhizal systems.
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