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Plant Physiol. (1998) 116: 1201–1207
Update on Plant-Microbe Interaction
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.)
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.
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 [email protected];
fax 61– 8 – 8303–7109.
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.
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
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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Barker et al.
Plant Physiol. Vol. 116, 1998
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
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
mm. 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).
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
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
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Development of Mycorrhizal Symbioses
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.
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
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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.
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
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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Barker et al.
Plant Physiol. Vol. 116, 1998
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.
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 plantmicrobe 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 (1027 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 accu-
mulated 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 germina-
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Development of Mycorrhizal Symbioses
tion coincidentally results in increased extractable RNAs,
including transcripts predicted to encode glyceraldehyde3-phosphate dehydrogenase, b-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 ex-
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plain 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 upregulated 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-tocell 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. Ectomycorrhi-
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Barker et al.
zas 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
a-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 a-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
Plant Physiol. Vol. 116, 1998
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.
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.
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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Development of Mycorrhizal Symbioses
Received October 20, 1997; accepted December 30, 1997.
Copyright Clearance Center: 0032–0889/98/116/1201/07.
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