Plant Physiol. (1998) 116: 1201-1207
UPDATE ON PLANT-MICROBE INTERACTIONS
Regulation of Root and Fungal Morphogenesis in Mycorrhizal
Symbioses1
Susan Jane Barker*,
Denis Tagu, and
Gabriele Delp
Department of Plant Science, Waite Campus, The University of
Adelaide, Glen Osmond, SA, 5064 Australia (S.J.B., G.D.); and Institut
National de la Recherche Agronomique, Nancy, Microbiologie
Forestière, 54280 Champenoux, France (D.T.)
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INTRODUCTION |
The root-fungus symbioses called
mycorrhizas have been known and studied since the last century.
Currently, four main types of mycorrhiza are recognized, based
primarily on the fungal partner in the association and the types of
mycorrhizal structures that develop. In all mutualistic types, the
mycorrhizal association contributes significantly to the mineral
nutrition of the plant host, in exchange for photosynthate. Very few
plant species studied do not form some kind of mycorrhizal association;
the majority exhibit VAM symbioses, whereas the temperate timber plants
are predominantly ectomycorrhizal (Smith and Read, 1997
). In this Update, we will focus on these two mycorrhizal associations.
With the renaissance in the study of plant-microbe interactions and plant nutrition that is being brought about by the application of
molecular techniques, progress in understanding the molecular controls
of the other mycorrhizal associations should soon be expected.
Molecular biological research on mycorrhizas has addressed two types of
questions about the interaction: what are the details of nutritional
exchange and how do the two partners communicate to enable development
of the symbiosis? Recent progress in cloning nutrient-transporter genes
has enabled research that is beginning to address exactly what
biochemicals are exchanged at which locations in mycorrhizas (Harrison,
1997; Smith and Read, 1997). Here we will briefly discuss these
processes but will focus mainly on progress toward understanding the
molecular communications that occur during establishment of the
symbioses, and where possible, we will indicate the commonalities
between the two mycorrhizal types. Mycorrhizal fungi are able to
achieve an intimate association with their host without a significant
defense response by the plant. Understanding how this is achieved at
the molecular level is anticipated to contribute specifically to
research on controlling plant-parasite interactions, as well as to
contribute more generally to research on cell-cell communications.
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DESCRIPTION OF ENDO- AND ECTOMYCORRHIZAS |
Structure and Function
Endomycorrhizal symbiosis was given the name
"vesicular-arbuscular" because of characteristic structures formed
in the symbiotic root. Arbuscules are intricately branched fungal
hyphae surrounded by possibly modified, invaginated plant plasma
membranes that form within cortical cells. Vesicles are intracellular
fungal "storage" structures that contain lipids and nuclei and are
thought to act as propagules. It should be noted that the fungus never contacts the plant cell cytoplasm. Figure
1A shows a confocal microscopic image of
an arbuscule. Clearly visible is the characteristic enlarged (due to
chromatin decondensation but not DNA replication) and centralized plant
nucleus (Bonfante and Perotto, 1995) that is surrounded by the branched
arbuscular structure; this image emphasizes the intimate and
genetically communicative nature of the interaction.
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| Figure 1.
Distinctive features of mycorrhizas revealed by
microscopy. A, Extended focus confocal microscope image of VAM
arbuscule (Glomus "City Beach" WUM16) in a leek root
cell embedded in London Resin White and stained with trypan blue.
Optical slice is 1 µm. A, Arbuscule; FN, fungal nucleus; PN, plant
nucleus; CW, plant cell wall; and IH, intracellular hypha. The image
was kindly provided by Ms. Sandy Dickson (The University of Adelaide).
B, Transverse section through a Pisolithus
tinctorius/Eucalyptus pilularis ectomycorrhizal symbiosis, stained with 0.05% toluidine blue in 1% sodium borate. M,
Mantle; HN, Hartig net; and C, cortex. The image was kindly provided by
Professors R.L. Peterson (University of Guelph, Canada) and A. Ashford
(University of New South Wales, Australia).
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Usually, ectomycorrhizas are formed between fine roots and dikaryotic
mycelia originating from the fusion of two different monokaryotic
hyphae germinated from spores. Ectomycorrhizas are characterized by the
presence of a fungal sheath (the mantle), which adheres to the root
surface and consists of aggregated hyphae (Fig. 1B). This mycelium is
linked to extramatrical hyphae that explore the substrate and are
responsible for the mineral nutrition and water uptake of the symbiotic
tissues. From the inner zone of the mantle, some hyphae penetrate
between the root cells to form an interface called the Hartig net,
where metabolites are exchanged. The hyphae always remain apoplastic
and can colonize the epidermal (angiosperms; Fig. 1B) and the cortical
cell (gymnosperms) layers. Root cells surrounded by hyphae are still
alive, as in arbuscules.
The nutritive exchange that occurs between the mycorrhizal partners has
been the main focus of research until the last decade. In exchange for
fixed carbon of still unknown biochemical form, the most important
benefit for the VAM plant is the increased availability of phosphorus
and some other elements such as zinc in poor soils. The effect on water
relations if any is still being debated. Nutrient transfer in VAM
symbioses is commonly indicated to occur at the arbuscular interface;
however, the exact role of the arbuscule has not been demonstrated.
Similarly, ectomycorrhizal symbiosis is important above all for
phosphorus and nitrogen nutrition of the plant (Smith and Read, 1997).
There is redundancy in the metabolic processes of each partner in
ectomycorrhizal roots, implying that a molecular dialogue occurs to
regulate and optimize these processes, as exemplified by the
assimilation of inorganic nitrogen. The fact that no general rules can
be proposed for the functioning of nitrogen metabolism in
ectomycorrhizas is probably the consequence of the great diversity of
the species involved in this symbiosis. In ectomycorrhizas,
carbohydrates provided by the plant are necessary for the development
of abundant extramatrical mycelium and for fruit body formation. In
temperate and boreal forests, approximately 20% of the plant carbon is
drained from the root to the symbiotic organ. This provokes a
significant modification in the carbon metabolism of the plant cells
because the mycorrhiza represents a new sink. Suc is transported to the
symbiotic tissues but it is likely that root apoplastic invertases
provide the mycelium with Glc and Fru (Smith and Read, 1997). Current
research is focused on cloning the plant and fungal transporter genes
and ATPases that may drive the transport processes in endo- and
ectomycorrhizas, to understand more clearly the locations and
biochemical form in which nutrients are exchanged (Harrison, 1997).
Partners and Evolution
In the modern world, 95% of plant species are classified in
families that are characteristically mycorrhizal, although mycorrhizal status has been examined for only about 3% of the total (Smith and
Read, 1997). The VAM symbiosis is an interaction between the majority
of land plants and members of the fungal order Glomales (Zygomycota).
There are less than 200 described fungal species that form VAM
symbioses and these are classified in six genera (Smith and Read,
1997). There is very little host specificity in their ability to
colonize, although not all combinations show mutualistic nutrient
exchange (Smith and Smith, 1996). Recent fossil evidence supports the
existence of mycorrhizas in the earliest vascular land plants that
lived more than 400 million years ago in the early Devonian period,
whereas molecular phylogenetic research indicates that the most
primitive VAM fungi diverged from a closely related nonmycorrhizal
taxon at about the same time (462-353 million years ago; Simon et al.,
1993; Remy et al., 1994). It is therefore possible that the
colonization of land and evolution of the whole land flora was achieved
by plants in symbiosis with co-evolving VAM fungi.
Relatively little is known about VAM fungal genetics, because these
species are obligate symbionts with no confirmed sexual stage. Spores
are multinucleate, containing thousands of nuclei, and evidence from
minisatellite amplification of DNA from single-spore cultures indicates
that spores are heterokaryotic (Zézé et al., 1997). nDNA
content has been determined for two species, being about 0.26 pg for
Glomus versiforme and 0.755 pg for Gigaspora margarita (Bianciotto and Bonfante, 1992). However, the ploidy of
the nuclei is unknown; therefore, these values cannot be equated with
genome size. Analogous to the proposed massive loss of genetic content
by the chloroplast and mitochondrial genomes during endosymbiotic evolution, it has been speculated that VAM fungi may have lost an
essential function to the ancestral land plant genome, thus exchanging
the ability to replicate independently for the unquestionably successful ecological niche. Considerable further research on these
enigmatic fungi is required to obtain a clear picture of their biology
and life cycle (Smith and Read, 1997).
Evidence for the evolution of other mycorrhizal types is that these are
more recent. The ectomycorrhizal symbiosis occurs mainly between woody
plants and filamentous fungi. This interaction involves only 5% of the
seed plants but the wide geographic range of trees makes the
ectomycorrhizal symbiosis important for plant biomass. Pinaceae,
Fagaceae, Myrtaceae, and Dipterocarpaceae are the predominant
ectomycorrhizal families (Smith and Read, 1997). In contrast with VAM
fungi, ectomycorrhiza-forming fungi are numerous (more than 5000 species), belong to the Ascomycotina or Basidiomycotina, and have
well-described sexual cycles. Some of their fruit bodies are edible
(e.g. Boletus, truffles), whereas others are highly toxic
(Amanita). Their interaction with plants is of intermediate specificity between that of VAMs and that of pathogenic fungi. As with
VAMs, several parts of a single root system can be colonized by
different ectomycorrhizal fungal species, and furthermore, two
neighboring plants can be connected by a mycelium of the same fungus.
Ectomycorrhizal fungi probably evolved from saprophytic fungi after the
Paleozoic era and still have saprophytic capacities. Molecular studies
suggest that the Holobasidiomycotina (including the ectomycorrhizal
Basidiomycetes) radiated 130 million years ago and, despite the lack of
precise paleontological data, it can be speculated that ectomycorrhizas
have a Mesozoic origin (Selosse and Le Tacon, 1998).
Most tropical tree families and many temperate trees are VAM plants.
Although they are of the genera that are ectomycorrhizal at maturity,
some form VAM symbioses as seedlings (e.g. Eucalyptus) and,
in the case of legumes, nitrogen-fixing nodules as well (e.g. Casuarina, Alnus). The idea that nodulation may
have evolved by co-opting a subset of plant VAM genetic processes
followed from studies of legume nodulation mutants, some of which are
also nonmycorrhizal (see below), and is now being widely canvassed
(Gianinazzi-Pearson, 1996). This idea should also be considered both
for other mycorrhizal types and for parasitic symbioses, such as
nematode infections that also may suppress plant defense responses (see
below; Williamson and Hussey, 1996) and for which there is preliminary
evidence of a small (to date) molecular overlap (Tagu and Barker,
1997).
The evolution of completely nonmycorrhizal taxa appears to have
occurred several times (e.g. Cruciferae, Chenopodiaceae,
Caryophyllaceae) but is nevertheless a rare phenomenon. The molecular
geneticists' model plant, Arabidopsis thaliana, is a
crucifer and no mycorrhizal ecotype has been reported. Mutational
analysis might enable determination of the mechanism involved in
preventing endomycorrhizal colonization of this species. Those
experiments would have the added advantage of generating material that
could subsequently be used to rapidly investigate the genetic basis for
successful colonization.
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DEVELOPMENT: MORPHOLOGICAL AND MOLECULAR DESCRIPTION |
Overview
As with many host-microbe interactions, it is possible to describe
the colonization process as beginning with a signaling between the two
partners followed by their development as a symbiosis, characterized by
an adhesion and the ingress of the fungus into host tissues. The nature
of the subsequent host response determines the fate of the interaction.
The colonization of a root by a mycorrhizal fungus begins with the
fixation of the mycelium to a root through appressoria (VAM) or hyphae
(ectomycorrhizas). This step is followed by internal root colonization
with intercellular growth (both symbioses) and intracellular growth
(VAM only), as well as effects on root meristems (see below).
Investigations during the past decade have begun the characterization
of molecules, genes, and proteins involved in signaling and
establishment of these symbioses. The current status of knowledge is
summarized in Figures 2 and 3.
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| Figure 2.
Cartoon illustration of VAM symbiotic morphologies
and regulatory points. Numbers 1 to 6 indicate molecular or genetic
control points described in the text. Ep, Epidermis; C, cortex; En,
endodermis; s, spore; eh, external hyph; ap, appressorium; ih,
intercellular hypha; a, arbuscule; ic, intracellular coil; and v,
vesicle. A, Arum type; B, Paris type. Note that most control points
have not been investigated in this symbiosis type.
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| Figure 3.
Schematic representation of ectomycorrhizal
development. Morphological events taking place during early (left) and
late (right) stages of ectomycorrhizal formation are indicated.
Molecules probably involved in these events are named. Note the
prominent role of fungal auxins.
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Precolonization Signaling
VAM spores can germinate in water to produce aseptate hyphae,
which however do not continue to grow unless in the presence of plant roots or root exudates. Spore germination can be influenced by
root chemicals and externally growing hyphae that originate from either
spores or a previous colonization, branch, or bend in the presence of
host roots, root exudate, or volatiles (control point 1, Fig. 2). It
has not yet been determined whether precontact stimulation is a
prerequisite for appressoria to form; indeed, as yet there is no clue
as to what does trigger appressoria formation (Douds et al., 1996;
Harrison, 1997). The chemical signals that have been shown to influence
the spore and hyphal responses include a variety of iso/flavonoids and
phenolics in common with other plant-microbe interactions (Bécard
et al., 1992; Harrison, 1997). Nonhost plant roots or extracts do not
stimulate fungal growth or chemotaxis and inhibitory compounds (likely
to be derived from glucosinolates) are extractable from
Brassica roots, but no inhibitors have been found in
representatives of other nonmycorrhizal families (Schreiner and Koide,
1993).
Signal exchange prior to establishing the ectomycorrhizal partnership
has also been demonstrated. Abietic acid extracted from Pinus root was able to induce spore germination at a very
low concentration (10
7 m) and this
effect seemed to be specific for the genus Suillus (Fries et
al., 1987). Horan and Chilvers (1990) demonstrated the presence of
root-diffusible molecules able to chemoattract ectomycorrhizal mycelia.
Many phenylpropanoids are accumulated in larch root cells upon
mycorrhization (Weiss et al., 1997) and root flavonoids are likely to
be important for signaling in ectomycorrhizal symbiosis. The fungal
partner also takes part in this signaling and an abundant indolic
compound, hypaphorine, has been purified from P. tinctorius (Béguiristain et al., 1995). Contact with eucalyptus roots
enhanced its concentration and, also, its presence provoked changes in eucalyptus root hair development and in the expression in roots of the
Egpar gene (which is also auxin-regulated), but the exact role of this molecule is still unknown.
Just after reaching the root surface, fungal cells enlarge and branch
intensively; two morphological steps shared with pathogenic species.
These early changes in fungal morphology may be switched on by the
scarcity of nutrients in the substrate surrounding the root; it is
known that virulence of pathogenic fungi can be induced by nitrogen
limitation.
Fungal Symbiotic Morphogenesis
Dormant spores of the VAM fungus Gigaspora rosea
have undetectable RNA content. Treatment to induce germination
coincidentally results in increased extractable RNAs, including
transcripts predicted to encode glyceraldehyde-3-phosphate
dehydrogenase, 
-tubulin, and P-type ATPases (Franken et al.,
1997). This research has provided a starting point for understanding
VAM fungal germination processes.
Once inside the root, there are two morphological forms of VAM
colonization, namely the "Arum" and "Paris" types (Fig. 2, control point 3). Many herbaceous plants exhibit the Arum colonization type (Fig. 2A), which involves extensive intercellular growth of the
fungus as it penetrates the root cortex, followed later in the
colonization by formation of arbuscules. All molecular research to date
has been done with Arum-type symbioses. However, a similar number of
herbaceous species undergo the contrasting Paris form of colonization
(Fig. 2B), in which growth into the root is slow, being primarily
intracellular, and the fungus forms coils inside each cell with rare or
minimally structured arbuscules (Gallaud, 1905, cited by Smith and
Smith, 1997). A parallel can be made with ectomycorrhizas, in which the
same mycelium can colonize either the epidermal layer only or also the
cortical layer, depending on the host plant. This demonstrates that the
plant controls the fungal growth habit, but the molecular mechanisms
for this are unknown (Smith and Smith, 1996, 1997). For both endo- and
ectomycorrhizas, the fungal ingress is always restricted to the
cortical tissues (Fig. 2, control point 6). The fungus may be prevented
from entering the stele because of its inability to degrade suberin and
lignin in the endodermal cell walls (Bonfante and Perotto, 1995). The overall extent of colonization is also controlled by plant metabolism; increasing plant phosphorus results in decreasing root colonization by
possibly several pathways, depending on the plant species (Smith and
Smith, 1996; Harrison, 1997). The controls on production of external
hyphae and the next generation of spores are completely unstudied.
An additional characteristic of the Arum symbiosis is accentuated by
the use of a rapid, synchronous, and extensive colonization procedure
(Rosewarne et al., 1997). Tomato and barley colonized by this modified
nurse-pot method undergo comparably staged development of symbiotic
structures, with maximal root infection containing arbuscules and
vesicles achieved within 10 d. Arbuscule structures have a limited
life span, with degeneration leaving the host cell intact. In the
modified nurse-pot procedure, two peaks of arbuscule formation are
observed during 28 d of growth subsequent to inoculation of tomato
with Glomus intraradices, indicating that arbuscule development may be a cyclic process, with timing controlled by the
fungus. Since this inoculation methodology produces extensive colonization, problems of low fungal biomass in the early stages of
colonization are overcome. Its application, together with PCR-based analyses of gene expression, should enable a molecular dissection of
the fungal side of the interaction.
In ectomycorrhizas, branched hyphae aggregate and bind to the root
surface. Binding occurs in the presence or absence of root hairs, and
in general the entire root surface is competent for fungal adhesion.
This may partially explain why the ectomycorrhizal symbiosis is not
species specific. By searching for proteins differentially synthesized
during ectomycorrhiza formation, it was found that a group of fungal
symbiosis-regulated acidic polypeptides were present in cell wall
preparations (Tagu and Martin, 1996); one of these had a sequence motif
typical of animal adhesins and was localized at the interfaces of the
mantle and Hartig net. Moreover, three expressed sequence tags from
P. tinctorius were characterized as encoding three different
hydrophobins (Tagu and Martin, 1996). These cell wall fungal proteins
are known to be involved in aerial growth, fruit body formation, and
appressorium development (Wessels, 1996). The observation that in
eucalypt ectomycorrhizas these three fungal RNAs were up-regulated
indicates that hydrophobins may also be important for root
colonization. These data suggest that adhesion is critical for
structure formation and is also probably necessary for the coordination
of morphogenesis and cell-to-cell signaling.
Root Symbiotic Morphogenesis: Role of Hormones
There is speculation in the literature that phytohormones may have
a "long-distance" signaling role in VAM symbiosis and that hormonal
gradients could be of primary importance in nodule meristem formation.
Increased cytokinin accumulation in alfalfa roots, linked with induced
expression of two early nodulin genes, namely MsENOD40
and MsENOD2, has been demonstrated to occur in VAM symbiosis
and nodulation but not in response to parasitic infection by
Rhizoctonia solani (van Rhijn et al., 1997). Although the
physiological role of increased cytokinin is not yet determined, this
indicates commonalities between signal transduction pathways in the two
mutualistic symbioses. Furthermore, ENOD40 peptide has a
demonstrated role in stimulating cell division that is enhanced by the
presence of cytokinin (John et al., 1997), and ENOD40
transcripts accumulate in dividing root stele pericycle cells that give
rise to lateral root primordia (Papadopoulou et al., 1996). Together, these results indicate a likely mechanism for the earlier observations that VAM plants have increased initiation of lateral roots associated with reduced growth of the primary apices and that the lateral root
effect operates at a distance from the site of colonization (Smith and
Read, 1997). They also support the developing concept that there exists
a set of fundamental genes the functions of which have been utilized in
various combinations during evolution to effect novel outcomes.
Analogous results have been obtained for ectomycorrhizas. For instance,
the overproduction of auxin by Hebeloma cylindrosporum mutant hyphae resulted, among several other effects, in the production of a large number of root meristems (Gay et al., 1994). The effect of
auxins on rhizogenesis can be interpreted as a preparation of the root
system for a better colonization by the mycelium. However, at later
stages of mycorrhiza formation, meristems of ensheathed roots are
blocked and growth is stopped. This dual effect of the presence of the
mycelium on root meristems could be explained by a gradient of auxins
or related compounds through transporters of auxins. Ectomycorrhizas
formed by the mycelium overproducing auxin have an overdeveloped Hartig
net and cortical cells are intracellularly colonized (Gay et al.,
1994), demonstrating the pleiotropic effect of auxin in mycorrhizas.
These whole root system responses may be considered as candidates for
the effects of changes in cytokinin/auxin balance.
Root Morphogenesis: Changes in Cytoskeleton
Fungal progression in roots provokes changes in cell shape and
cytoplasmic organization. Root cells undergoing ectomycorrhiza formation elongate, whereas arbuscule differentiation in VAM root cells
involves complete reorganization of the cytoplasm. These modifications
are undoubtedly linked to cytoskeleton rearrangements (Timonen et al.,
1993); for example, one eucalypt gene encoding an
-tubulin (EgTubA1) has been shown to be
up-regulated by ectomycorrhiza formation (Carnero Diaz et al., 1996).
Also, it has been shown that in transgenic tobacco roots, the promoter of the maize -tubulin gene Tub3a was specifically
activated in arbuscular cells (Bonfante et al., 1996). Whether changes
in cytoskeletal gene expression are a cause or the consequence of
mycorrhizal root morphogenesis needs further study.
Fungal Ingress and Plant Defense
The disruption of the middle lamella that occurs during
mycorrhizal fungal growth in roots is a wounding event, and so a major focus of research has been on known defense responses, with gene products examined, including chitinases, glucanases, flavonoid biosynthesis pathway enzymes, and phytoalexins. The main conclusion for
VAM is that, although small and transitory increases in expression of
genes involved in synthesis of pathogenesis-related proteins and
phytoalexins do occur, there is no evidence for any significant or
extended induction of a defense response by inter- or intracellular growth of the compatible VAM fungus (Harrison, 1997). For
ectomycorrhizas, host defenses are also less induced than for a
pathogenic attack: studies performed on in vitro cultures of spruce
cells demonstrated that elicitors prepared from ectomycorrhizal fungi
did induce defensive reactions, but plant chitinases were able to
inactivate these elicitors (Salzer et al., 1997), indicating that, as
for VAM, the host plant is able to regulate its colonization.
Is the fungus "invisible" to the plant or does it have an active
role in turning off plant defenses at the interface? The fact that a
mild induction of defense-response gene expression continues to occur
as the VAM fungus grows through the root, rather than only at the
appressorium, suggests that the VAM fungus does not elicit a general
signal through the plant root system to completely suppress plant root
defenses, but the recognition process must be initiated with each new
cell contact to result in suppression of the defense response (Fig. 2A,
control point 4). This observation explains why mycorrhizal plants are
not rendered hypersensitive to root pathogen attack: indeed,
mycorrhizal plants are reputedly less susceptible to root pathogen
infection, although how that is achieved has yet to be determined.
Research on the mycorrhizal status of legume nodulation mutants has
identified a set of early mutations that are nonmycorrhizal and either
block entry or stop hyphal growth shortly after ingress (Gianinazzi-Pearson, 1996; Harrison, 1997). Work with these mutants has
identified a further control point as being whether an appressorium is
successful in penetrating the root epidermis (Fig. 2A, control point
2). Cytological studies have shown that deposition of callose and
increased phenolics occur beneath appressoria formed on plant mutants
(Gollote et al., 1993; Peterson and Bradbury, 1995). A second class of
mutants has been described in which intercellular growth is permitted,
but arbuscules are aborted (Gianinazzi-Pearson, 1996). This is
indicated as control point 5 in Figure 2A, although it may be due to
failure of communication at control point 4. It will be interesting to
determine whether this mutant process is accomplished by the same
pathway as arbuscule senescence in the wild-type plant.
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CONCLUSIONS |
Mycorrhizal colonization of roots involves a sequence of steps
that have been well documented structurally but that are relatively poorly understood as biochemical processes, although a preliminary picture is beginning to emerge. There is clear evidence for host control of the colonization process, both from the existence of nonmycorrhizal taxa, mutants and subspecific variants, and in the way
in which the fungus develops within roots of normally mycorrhizal
species. Both the large number of developmental steps and the existence
of nonhosts with apparently different blocking steps leads to the
expectation that the process is controlled by a number of genes in both
organisms. The ancient origin of the symbiosis also suggests that the
genes would be present in all land plants, whether or not they form
mycorrhizas. Molecular and genetic researchers have begun to overcome
the experimental challenges associated with mycorrhizal research by
choosing appropriate host species. Unpublished research in several
laboratories on additional plant mutations in the mycorrhizal
colonization pathway, and research toward achieving transformation of
mycorrhizal fungi should soon provide novel insight into mechanisms
controlling the process. We expect that the next decade will see a much
improved understanding of the molecular controls and commonalities of
these most intimate associations.
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FOOTNOTES |
1
S.J.B. and G.D. acknowledge support from the
Australian Research Council Special Research Centre for Basic and
Applied Plant Molecular Biology.
*
Corresponding author; e-mail sbarker{at}waite.adelaide.edu.au; fax
61-8-8303-7109.
Received October 20, 1997;
accepted December 30, 1997.
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ABBREVIATIONS |
Abbreviation:
VAM, vesicular-arbuscular endomycorrhiza. Note
that since not all VAM fungi produce vesicles, the term arbuscular
mycorrhiza (AM) has been suggested as a more inclusive nomenclature.
Here we have retained the older term, which is familiar to a broader
audience .
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ACKNOWLEDGMENTS |
We would like to thank Marc André Selosse and Dr. Francis
Martin (both of Institut National de la Recherche Agronomique, Champenoux, France) and Professor Sally Smith (The University of
Adelaide, Glen Osmond, SA, Australia), for their comments concerning the manuscript, and Dr. Shelley Barker and Adam Vivian-Smith for their
assistance with figure preparation. In keeping with the Update style we have refrained from compacting all available
research publications into this review; we offer sincere apologies to
our noncited colleagues.
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Douds DD,
Pfeffer PE
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Extensive in vitro hyphal growth of vesicular-arbuscular mycorrhizal fungi in the presence of CO2 and flavonols.
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Bergero R,
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Rigau J,
Puigdoménech P
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Introduction
References