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360
Development of the arbuscular mycorrhizal symbiosis
Maria J Harrison
The arbuscular mycorrhizal (AM) symbiosis formed between
plant roots and fungi is one of the most widespread symbiotic
associations found in plants, yet our understanding of events
underlying its development are limited. The recent integration
of biochemical, molecular and genetic approaches into
analyses of the symbiosis is providing new insights into
various aspects of its development. In the past year there
have been advances in our understanding of the signals
required for the formation of appressoria, the molecular
changes in the root in response to colonisation, and
components of the signal transduction pathways common to
both the AM and Rhizobium symbioses.
Addresses
The Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway,
Ardmore, Oklahoma, 73402 USA;e-mail: mjharrison@noble.org
Current Opinion in Plant Biology 1998, 1:360–365
http://biomednet.com/elecref/1369526600100360
Current Biology Ltd ISSN 1369-5266
Abbreviations
AM
arbuscular mycorrhizal
Mt4
Medicago truncatula 4
Introduction
Over 80% of vascular flowering plants are capable
of entering into symbiotic associations with arbuscular
mycorrhizal (AM) fungi, and in natural environments the
roots of many plants are really symbiotic organs termed
mycorrhizae. The fungi that form these associations are
members of the zygomycetes and the current classification
places them all into one Order, the Glomales [1]. The AM
association is a relatively non-specific, highly compatible,
long lasting mutualism from which both partners derive
benefit. The plant supplies the fungus with carbon, on
which it is entirely dependent. The fungal contribution
is more complex — it is clear that the fungus assists the
plant with the acquisition of phosphate and other mineral
nutrients from the soil, and it is also apparent that it may
influence the plant’s resistance to invading pathogens [2].
In addition to its ecological significance, the association
may also have applications in agriculture, particularly in
sustainable systems [3], where the intimate link between
the soil and the plant created by the mycorrhiza, and its
impact on nutrient movement, plant and soil nutrition and
soil conservation, may be fully exploited.
Development of the symbiosis is associated with significant alterations in the interior morphology of the
root cortex and in the physiology of the plant. These
aspects have been reviewed elsewhere in detail [4–7]. In
brief, the interaction begins when fungal hyphae, arising
from spores or from adjacent colonised roots, contact the
root surface. Here they differentiate to form appressoria
via which they penetrate the root (Figure 1). Once
inside the root, the fungus may grow both inter- and
intra-cellularly throughout the cortex but does not invade the vasculature or the meristematic regions. The
types of internal structures that develop depend on the
plant/fungal combination and may include intracellular,
differentiated hyphae called arbuscules and/or intracellular
coils [8•]. Although the fungal hypha penetrates the
cortical cell wall to form the arbuscule within the cell,
it does not penetrate the plant plasma membrane and
this extends to surround the arbuscule (Figure 1). In
addition to internal growth within the root, the fungus
also maintains external mycelia which ramify out into the
soil. These external hyphae access phosphate which is
then transported to the internal structures and eventually
released to the root. The interface between the fungal
arbuscule and the cortical cell is probably important for
nutrient transfer between the symbionts, but this has not
yet been demonstrated directly [9]. In comparison to other
plant/microbe interactions, we still know relatively little
about the molecular events underlying development of
the AM symbiosis. The obligate, biotrophic nature of the
fungi has contributed to the difficulties with molecular and
genetic analyses of these associations and it is only recently
that such approaches have been applied. This review
surveys the most recent molecular genetic and biochemical
studies of the association and their contributions to basic
knowledge of the AM symbiosis.
Signals for the development of the AM
symbiosis
The formation of the symbiosis requires the co-ordinate
development of both the fungus and the plant and is
assumed to require an interchange of signals. As AM
fungal spores are capable only of germination and limited
hyphal growth in the absence of the plant, it seems
likely that plant signals are essential for the initial stages
of the symbiosis. Root exudates have been shown to
stimulate growth and branching of the AM fungal hyphae
and low concentrations of certain flavonoid/isoflavonoid
compounds, which are major components of some plant
root exudates, are also capable of promoting hyphal growth
[10,11]. Recent data suggest that AM fungi have a receptor
for the flavonoid/isoflavonoid compounds. Flavonoids,
particularly isoflavonoids are known to have estrogenic
activity and the estrogen 17β-estradiol was shown to
stimulate AM fungal hyphal growth in a similar manner to
that of the isoflavonoid biochanin A, while antiestrogens
competitively inhibited the biochanin A-mediated growth
stimulation. The data are consistent with the presence
of a fungal receptor in which the A and C rings of
the flavonoid and the hydroxyl group at position A-7
Development of the arbuscular mycorrhizal symbiosis Harrison
361
Figure 1
rh
a
Arbuscule
Plant plasma
membrane
Interface
compartment
h
e
Peri-arbuscular
membrane
ap
e
a
Cortical cell
Current Opinion in Plant Biology
Roots colonised with a mycorrhizal fungus and a diagrammatic representation of a cell containing an arbuscule. The upper left panel shows a
Medicago truncatula root colonised with an arbuscular mycorrhizal fungus, Glomus versiforme. An appressorium (ap) and hypha (h) penetrating
the root are visible. Arbuscules (a), slightly out of the focal plane are visible in the inner cortex. Root hairs are also shown (rh) and the epidermis
is labelled (e). The lower panel shows arbuscules in the inner cortical cells of a M. truncatula root. The right hand side panel is a diagram
showing the features of an arbuscule within a cortical cell. The peri-arbuscule membrane is continuous with the plant plasma membrane and
surrounds the arbuscule. The space between the membrane and the arbuscule is referred to as the interface compartment. The roots were
stained with Cholorazol Black E to allow visualisation of the fungus. The magnification of the upper panel is x300 and the lower panel x600.
are likely to be important features for recognition of
the molecule ([12]; Figure 2). Despite the evidence that
flavonoid/isoflavonoids promote growth of these fungi it
seems unlikely that they are essential for development
of the association, as maize mutants lacking flavonoids
are still able to form the symbiosis [13]. In addition,
isoflavonoids are unlikely to be a universal signal, as they
are found only in a subset of the plants capable of forming
the symbiosis. Instead, such compounds probably signal
the presence of a root and the fungus can respond by
increasing hyphal growth and branching to enhance the
possibility of contacting the root.
On contact with the root, the fungus differentiates to
form appressoria on the surface of the epidermal cells.
These structures have only been observed on plant
roots and they do not form on synthetic surfaces even
in the presence of growth-stimulating exudates [10,14].
Recently it was demonstrated that the mycorrhizal fungus,
Gigaspora margarita was able to form appressoria on
purified carrot epidermal cell wall fragments [15•]. These
elegant experiments indicate that the cell wall alone is
sufficient to stimulate formation of appressoria and signals
secreted from the roots are not necessary. In addition,
the cell walls of the non-host, sugar beet, do not permit
appressoria development and, therefore, topology of the
epidermis is not sufficient to induce appressoria and
endogenous signals must be present in host wall. This is
supported further by observations that appressoria form
only on epidermal cell wall fragments and not on cell
walls from other parts of the root such as the cortex
or vasculature. The appressoria that form on the host
cell wall fragments do not develop complete penetration
hyphae which suggests that the next stage of development
requires an intact cell [15•]. Thus the epidermal cell wall
signals appressoria formation; the next task will be to
elucidate the specific cell wall component(s) that trigger
the response.
362
Plant–microbe interactions
Following the formation of appressoria, the fungus penetrates the root and proceeds to colonise the cortex and
differentiate to form arbuscules. Plant mutants on which
the fungus is able to form appressoria but unable to
penetrate the root have been identified in a number
of legumes [16–19]. Some of these mutants may be
lacking a signal for entry and the cloning of the mutated
genes has the potential to provide insight into signalling
at this stage of the symbiosis. The nature of the
signals involved in the later stages of the association
is entirely unknown; however, it is conceivable that
the more common secondary metabolites are involved.
Flavonoids increase in mycorrhizal legume roots and
sesquiterpenoid cyclohexenone derivatives were shown
recently to accumulate during mycorrhizal development in
many members of the Poaceae [20,21,22•]. Other possible
candidates for later signals include hormones. Induction
of cytokinins in mycorrhizae has been reported previously
and this was confirmed recently in alfalfa, where significant
induction of ZR (trans-zeatin riboside) type cytokinins was
observed in mycorrhizal roots [23,24•]. At the moment,
signals derived from the fungus are entirely unknown.
Figure 2
HO
7
8
A
O
1'
2'
C
B
6
5
OH
5'
3'
OCH3
4'
O
Current Opinion in Plant Biology
Chemical structure of biochanin A showing the numbering system
used to identify carbon atoms and rings.
Molecular events associated with the
development of the mycorrhiza
The identification of plant mutants unable to form a
complete symbiosis indicates that development of the
association is controlled, at least in part, by the plant.
The nature of this control, however, is currently unknown
[16]. There has been recent progress in the identification
of genes showing differential expression in mycorrhizal
roots and although it will require extensive analyses to
determine whether these genes have a significant role in
the symbiosis, they currently provide information on the
molecular events occurring during formation of the association. In addition they may serve as molecular markers for
different developmental stages in the symbiosis. A mycorrhizal inducible β-tubulin gene was identified in maize and
expression of promoter–reporter gene fusions in tobacco
indicated that this gene is induced in the cells in which
arbuscules are developing [25]. This is consistent with
alterations in the cytoskeleton which occur as the internal
structure of the cell is reorganising to accommodate the
arbuscule and to develop the peri-arbuscular membrane
(Figure 1). The cell wall of the arbuscule and the
peri-arbuscular membrane that surrounds it are separated
by a narrow interface compartment that is continuous
with the plant cell wall although it differs in structure
([26]; Figure 1). Antibody probes and stains have revealed
that the compartment is a complex mixture of molecules
including xyloglucans, arabinogalactans, β-D-1→4 glucans
and hydroxy rich glycoproteins [27–28]. The significance
of this molecular composition is currently unknown but
it has been speculated that some of the components may
act as signals [5]. Potential candidates might include small
oligosaccharides or arabinogalactan proteins, both of which
are known to act as signaling molecules in other systems.
The importance of cell wall signals in the early stages
of the AM symbiosis [15•] indicates that these types of
signals should not be overlooked.
One of the major alterations in the cortical cells in
which the arbuscules form is the massive extension
of the plasma membrane to form the peri-arbuscular
membrane ([29]; Figure 1). Given that the exchange of
nutrients is assumed to occur at this interface, it might
be expected that membrane transport mechanisms will
be induced. Consistent with this suggestion, a cDNA
representing a mycorrhizal inducible plasma membrane
ATPase was identified recently in barley [30] and a novel
gene, predicted to encode a membrane anchored protein
with structural similarities to phospholamban, a vertebrate
protein that regulates the activity of a Ca2+-ATPase,
is induced in mycorrhizal pea [31]. The induction of
an ATPase gene is consistent with biochemical data
indicating increases in plasma membrane ATPase activity
in mycorrhizal roots of some species [32] and with
earlier studies that demonstrated high levels of ATPase
activity on the peri-arbuscular membrane [33]. The
putative function of ATPases on this membrane is to
provide energy for nutrient transfer processes; however,
transport proteins involved in nutrient movement at the
arbuscular interface are currently unknown. A mycorrhizal
inducible sugar transporter has been identified in Medicago
truncatula [34] and a gene encoding a member of the
membrane intrinsic protein gene family is induced in
parsley mycorrhizae. Members of this family have been
shown to facilitate the movement of water and other small
molecules [35].
Phosphate regulates the symbiosis between AM fungi
and plants and the extent of colonisation in the roots is
inversely correlated with the phosphate status of the plant
[36,37]. Since the symbiosis usually results in increased
levels of phosphate in the plant some of the plant
genes showing differential expression in mycorrhizal roots
may be regulated in response to phosphate, rather than
signals from the fungus. There is, however, evidence
for independent regulation of expression of one gene,
Mt4, via both of these stimuli. Mt4 is a novel cDNA
representing a root specific gene from M. truncatula [38•].
Mt4 transcripts are induced in response to phosphate
Development of the arbuscular mycorrhizal symbiosis Harrison
starvation and down-regulated by phosphate or in response
to colonisation by a mycorrhizal fungus. It was initially
assumed that down regulation in the symbiosis was
a consequence of increased phosphate; however, Mt4
expression is also down regulated in a symbiotic plant
mutant in which colonisation is limited to growth on
the surface of the root and in which phosphate transfer
does not occur. This suggests that the Mt4 gene is
regulated independently by two signals, phosphate and
an unknown component(s) of the mycorrhizal fungus.
Two phosphate transporters and an acid phosphatase show
similar patterns of expression in response to phosphate
starvation and colonisation by mycorrhizal fungi, but
it is unknown whether they also show independent
regulation in response to the two signals [39]. Together,
these data indicate that, in general, phosphate starvation
inducible genes are down regulated in the early stages
of the symbiosis, ahead of significant levels of phosphate
entering the root. Has the symbiosis co-evolved to the
extent that the plant ‘anticipates’ an increased supply of
phosphate before it is delivered? Certainly the symbionts
have co-existed for the extensive periods of time that
might be necessary for this to occur. Fossil evidence
indicates that arbuscular mycorrhizae were present in
Devonian land plants and thus plants and AM fungi have
been associated for over 400 million years [40].
In comparison with the plant, even less is known about
the molecular changes in the fungal symbiont as the
association develops. The recent identification of genes
expressed in the spores [41] coupled with the continuing
identification of fungal genes expressed during the
symbiotic phase of the life cycle [42,43] will be essential
in unravelling aspects of AM fungal development.
Conserved signalling pathways in the
Rhizobium-legume and mycorrhizal
symbioses
It has been speculated that the Rhizobium–legume
(bacterial–plant) symbiosis evolved from the much older
mycorrhizal (fungal–plant) symbiosis and emerging similarities in the molecular events occurring during their
development lend support to this idea [44]. The observation that a number of nodulation mutants are also
mycorrhizal mutants indicates the presence of genes
essential for both symbioses; however, the identity of the
genes responsible is unknown [16–19]. Recent studies
indicate that a number of the nodulin genes induced
during nodule development are also induced in the
mycorrhizal symbiosis, although their function in the latter
is unclear. In Vicia faba, one of the four leghaemoglobin
genes induced in nodules is also induced in mycorrhizal
roots [45] and three other nodulin genes, PsENOD12,
MsENOD2 and MsENOD40 are induced in mycorrhizal pea
and alfalfa roots, respectively [5,24•]. In mycorrhizal alfalfa
roots, MsENOD40 transcripts are localised to the pericycle,
epidermis and cortex as seen in roots inoculated with
363
Rhizobia, and co-localise with cells containing immature
arbuscules. The MsENOD2 transcripts are present in
cells containing mature arbuscules, whereas in nodules
these transcripts are localised in the nodule parenchyma.
Induction of MsENOD2 and 40 occurs in response to
cytokinin, which is elevated in roots during nodulation and
has been shown recently to increase in mycorrhizal alfalfa
roots [24•]. On the basis of these data the authors suggest
that the downstream signalling events are conserved
between the two symbioses; however, it is equally possible
that the similarity lies only in the increase in cytokinin and
the pathways prior to cytokinin induction are distinct.
Further support for conserved signalling pathways is
provided by studies of PsENOD5 and 12A expression in
mycorrhizal and nodulated pea and pea mutants [46•].
As in nodule development, PsENOD5 and PsENOD12A
are induced in the early stages of the pea mycorrhizal
symbiosis. Further experiments using the pea sym8
mutant, which is blocked in early stages of both nodulation
and mycorrhiza formation, demonstrated that a functional
Sym8 was necessary for expression of the downstream
PsENOD5 and PsENOD12A genes in both symbioses. Sym
8, therefore, is a common step in the signal transduction
pathways for both of these symbioses. It seems unlikely
that the initial signals for the two symbioses will be the
same; however, at some point — probably shortly after the
initial signal — the signal pathways converge and a number
of downstream events are conserved.
Conclusions
As the application of molecular approaches to analyses of
this symbiosis is relatively recent, it can be anticipated
that the first few years will include groundwork to support
future advances. In the past year molecular approaches
have contributed to our understanding of some aspects
of the symbiosis and generated molecular tools essential
for future analyses. Thus, the end of the lag phase is
approaching and the next few years should see a rapid
increase in our understanding of the events underlying the
AM symbiosis. The identification of mycorrhizal mutants
is accelerating and the continued cloning of genes induced
during the symbiosis will contribute to a molecular
picture of the events accompanying development of the
association. These genes will also serve as tools; both for
the analysis of altered developmental processes in the
mutants, and as a starting point for the analysis of signal
transduction pathways operating in the symbiosis. The
symbiosis is a complex system and it will be important
to use integrated approaches to obtain a complete
understanding of the events underlying its development
and functioning.
Acknowledgements
The author would like to thank K Korth for critical reading of the
manuscript. Financial support was provided by The Samuel Roberts Noble
Foundation.
364
Plant–microbe interactions
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arbuscular mycorrhizal fungus, Gigaspora rosea. Mycologia
1997, 89:293-297.
42.
Harrison MJ, van Buuren ML: A phosphate transporter from the
mycorrhizal fungus Glomus versiforme. Nature 1995, 378:626629.
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Burleigh SH, Harrison MJ: A cDNA from the arbuscular
mycorrhizal fungus Glomus versiforme with homology to
a cruciform DNA-binding protein from Ustilago maydis.
Mycorrhiza 1998, 7:in press.
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Fruhling
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M, Roussel H, Gianinazzi-Pearson V, Puhler
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A, Perlick AM:
The Vicia faba leghemoglobin gene VfLb29 is induced in root
nodules and in roots colonized by the arbuscular mycorrhizal
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10:124-131.
38.
•
39.
Liu H, Trieu AT, Blaylock LA, Harrison MJ: Cloning and
characterization of two phosphate transporters from Medicago
truncatula roots: Regulation in response to phosphate and
to colonization by arbuscular mycorrhizal (AM) fungi. Mol
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Remy W, Taylor TN, Hass H, Kerp H: Four hundred-million-yearold vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA
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41.
Franken P, Lapopin L, Meyer-Gauen G, Gianinazzi-Pearson V:
RNA accumulation and genes expressed in spores of the
365
Albrecht C, Geurts R, Lapeyrie F, Bisseling T: Endomycorrhizae
and rhizobial nod factors activate signal transduction pathways
inducing PsENOD5 and PsENOD12 expression in which Sym8
is a common step. Plant J 1998, in press.
This paper provides direct evidence for signal transduction pathway components shared in the Rhizobium and mycorrhizal symbioses. In pea, PsENOD
5 and PsENOD 12A are induced in the early stages of both symbioses.
Studies with symbiotic mutants indicate that these genes are not induced in
the sym8 mutant. Thus a functional Sym8 gene product is required for the
induction of PsENOD 5 and 12A gene expression in both symbioses and
represents a common component of the signalling pathways.
46.
•
Development of the arbuscular mycorrhizal symbiosis
Maria J Harrison
The arbuscular mycorrhizal (AM) symbiosis formed between
plant roots and fungi is one of the most widespread symbiotic
associations found in plants, yet our understanding of events
underlying its development are limited. The recent integration
of biochemical, molecular and genetic approaches into
analyses of the symbiosis is providing new insights into
various aspects of its development. In the past year there
have been advances in our understanding of the signals
required for the formation of appressoria, the molecular
changes in the root in response to colonisation, and
components of the signal transduction pathways common to
both the AM and Rhizobium symbioses.
Addresses
The Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway,
Ardmore, Oklahoma, 73402 USA;e-mail: mjharrison@noble.org
Current Opinion in Plant Biology 1998, 1:360–365
http://biomednet.com/elecref/1369526600100360
Current Biology Ltd ISSN 1369-5266
Abbreviations
AM
arbuscular mycorrhizal
Mt4
Medicago truncatula 4
Introduction
Over 80% of vascular flowering plants are capable
of entering into symbiotic associations with arbuscular
mycorrhizal (AM) fungi, and in natural environments the
roots of many plants are really symbiotic organs termed
mycorrhizae. The fungi that form these associations are
members of the zygomycetes and the current classification
places them all into one Order, the Glomales [1]. The AM
association is a relatively non-specific, highly compatible,
long lasting mutualism from which both partners derive
benefit. The plant supplies the fungus with carbon, on
which it is entirely dependent. The fungal contribution
is more complex — it is clear that the fungus assists the
plant with the acquisition of phosphate and other mineral
nutrients from the soil, and it is also apparent that it may
influence the plant’s resistance to invading pathogens [2].
In addition to its ecological significance, the association
may also have applications in agriculture, particularly in
sustainable systems [3], where the intimate link between
the soil and the plant created by the mycorrhiza, and its
impact on nutrient movement, plant and soil nutrition and
soil conservation, may be fully exploited.
Development of the symbiosis is associated with significant alterations in the interior morphology of the
root cortex and in the physiology of the plant. These
aspects have been reviewed elsewhere in detail [4–7]. In
brief, the interaction begins when fungal hyphae, arising
from spores or from adjacent colonised roots, contact the
root surface. Here they differentiate to form appressoria
via which they penetrate the root (Figure 1). Once
inside the root, the fungus may grow both inter- and
intra-cellularly throughout the cortex but does not invade the vasculature or the meristematic regions. The
types of internal structures that develop depend on the
plant/fungal combination and may include intracellular,
differentiated hyphae called arbuscules and/or intracellular
coils [8•]. Although the fungal hypha penetrates the
cortical cell wall to form the arbuscule within the cell,
it does not penetrate the plant plasma membrane and
this extends to surround the arbuscule (Figure 1). In
addition to internal growth within the root, the fungus
also maintains external mycelia which ramify out into the
soil. These external hyphae access phosphate which is
then transported to the internal structures and eventually
released to the root. The interface between the fungal
arbuscule and the cortical cell is probably important for
nutrient transfer between the symbionts, but this has not
yet been demonstrated directly [9]. In comparison to other
plant/microbe interactions, we still know relatively little
about the molecular events underlying development of
the AM symbiosis. The obligate, biotrophic nature of the
fungi has contributed to the difficulties with molecular and
genetic analyses of these associations and it is only recently
that such approaches have been applied. This review
surveys the most recent molecular genetic and biochemical
studies of the association and their contributions to basic
knowledge of the AM symbiosis.
Signals for the development of the AM
symbiosis
The formation of the symbiosis requires the co-ordinate
development of both the fungus and the plant and is
assumed to require an interchange of signals. As AM
fungal spores are capable only of germination and limited
hyphal growth in the absence of the plant, it seems
likely that plant signals are essential for the initial stages
of the symbiosis. Root exudates have been shown to
stimulate growth and branching of the AM fungal hyphae
and low concentrations of certain flavonoid/isoflavonoid
compounds, which are major components of some plant
root exudates, are also capable of promoting hyphal growth
[10,11]. Recent data suggest that AM fungi have a receptor
for the flavonoid/isoflavonoid compounds. Flavonoids,
particularly isoflavonoids are known to have estrogenic
activity and the estrogen 17β-estradiol was shown to
stimulate AM fungal hyphal growth in a similar manner to
that of the isoflavonoid biochanin A, while antiestrogens
competitively inhibited the biochanin A-mediated growth
stimulation. The data are consistent with the presence
of a fungal receptor in which the A and C rings of
the flavonoid and the hydroxyl group at position A-7
Development of the arbuscular mycorrhizal symbiosis Harrison
361
Figure 1
rh
a
Arbuscule
Plant plasma
membrane
Interface
compartment
h
e
Peri-arbuscular
membrane
ap
e
a
Cortical cell
Current Opinion in Plant Biology
Roots colonised with a mycorrhizal fungus and a diagrammatic representation of a cell containing an arbuscule. The upper left panel shows a
Medicago truncatula root colonised with an arbuscular mycorrhizal fungus, Glomus versiforme. An appressorium (ap) and hypha (h) penetrating
the root are visible. Arbuscules (a), slightly out of the focal plane are visible in the inner cortex. Root hairs are also shown (rh) and the epidermis
is labelled (e). The lower panel shows arbuscules in the inner cortical cells of a M. truncatula root. The right hand side panel is a diagram
showing the features of an arbuscule within a cortical cell. The peri-arbuscule membrane is continuous with the plant plasma membrane and
surrounds the arbuscule. The space between the membrane and the arbuscule is referred to as the interface compartment. The roots were
stained with Cholorazol Black E to allow visualisation of the fungus. The magnification of the upper panel is x300 and the lower panel x600.
are likely to be important features for recognition of
the molecule ([12]; Figure 2). Despite the evidence that
flavonoid/isoflavonoids promote growth of these fungi it
seems unlikely that they are essential for development
of the association, as maize mutants lacking flavonoids
are still able to form the symbiosis [13]. In addition,
isoflavonoids are unlikely to be a universal signal, as they
are found only in a subset of the plants capable of forming
the symbiosis. Instead, such compounds probably signal
the presence of a root and the fungus can respond by
increasing hyphal growth and branching to enhance the
possibility of contacting the root.
On contact with the root, the fungus differentiates to
form appressoria on the surface of the epidermal cells.
These structures have only been observed on plant
roots and they do not form on synthetic surfaces even
in the presence of growth-stimulating exudates [10,14].
Recently it was demonstrated that the mycorrhizal fungus,
Gigaspora margarita was able to form appressoria on
purified carrot epidermal cell wall fragments [15•]. These
elegant experiments indicate that the cell wall alone is
sufficient to stimulate formation of appressoria and signals
secreted from the roots are not necessary. In addition,
the cell walls of the non-host, sugar beet, do not permit
appressoria development and, therefore, topology of the
epidermis is not sufficient to induce appressoria and
endogenous signals must be present in host wall. This is
supported further by observations that appressoria form
only on epidermal cell wall fragments and not on cell
walls from other parts of the root such as the cortex
or vasculature. The appressoria that form on the host
cell wall fragments do not develop complete penetration
hyphae which suggests that the next stage of development
requires an intact cell [15•]. Thus the epidermal cell wall
signals appressoria formation; the next task will be to
elucidate the specific cell wall component(s) that trigger
the response.
362
Plant–microbe interactions
Following the formation of appressoria, the fungus penetrates the root and proceeds to colonise the cortex and
differentiate to form arbuscules. Plant mutants on which
the fungus is able to form appressoria but unable to
penetrate the root have been identified in a number
of legumes [16–19]. Some of these mutants may be
lacking a signal for entry and the cloning of the mutated
genes has the potential to provide insight into signalling
at this stage of the symbiosis. The nature of the
signals involved in the later stages of the association
is entirely unknown; however, it is conceivable that
the more common secondary metabolites are involved.
Flavonoids increase in mycorrhizal legume roots and
sesquiterpenoid cyclohexenone derivatives were shown
recently to accumulate during mycorrhizal development in
many members of the Poaceae [20,21,22•]. Other possible
candidates for later signals include hormones. Induction
of cytokinins in mycorrhizae has been reported previously
and this was confirmed recently in alfalfa, where significant
induction of ZR (trans-zeatin riboside) type cytokinins was
observed in mycorrhizal roots [23,24•]. At the moment,
signals derived from the fungus are entirely unknown.
Figure 2
HO
7
8
A
O
1'
2'
C
B
6
5
OH
5'
3'
OCH3
4'
O
Current Opinion in Plant Biology
Chemical structure of biochanin A showing the numbering system
used to identify carbon atoms and rings.
Molecular events associated with the
development of the mycorrhiza
The identification of plant mutants unable to form a
complete symbiosis indicates that development of the
association is controlled, at least in part, by the plant.
The nature of this control, however, is currently unknown
[16]. There has been recent progress in the identification
of genes showing differential expression in mycorrhizal
roots and although it will require extensive analyses to
determine whether these genes have a significant role in
the symbiosis, they currently provide information on the
molecular events occurring during formation of the association. In addition they may serve as molecular markers for
different developmental stages in the symbiosis. A mycorrhizal inducible β-tubulin gene was identified in maize and
expression of promoter–reporter gene fusions in tobacco
indicated that this gene is induced in the cells in which
arbuscules are developing [25]. This is consistent with
alterations in the cytoskeleton which occur as the internal
structure of the cell is reorganising to accommodate the
arbuscule and to develop the peri-arbuscular membrane
(Figure 1). The cell wall of the arbuscule and the
peri-arbuscular membrane that surrounds it are separated
by a narrow interface compartment that is continuous
with the plant cell wall although it differs in structure
([26]; Figure 1). Antibody probes and stains have revealed
that the compartment is a complex mixture of molecules
including xyloglucans, arabinogalactans, β-D-1→4 glucans
and hydroxy rich glycoproteins [27–28]. The significance
of this molecular composition is currently unknown but
it has been speculated that some of the components may
act as signals [5]. Potential candidates might include small
oligosaccharides or arabinogalactan proteins, both of which
are known to act as signaling molecules in other systems.
The importance of cell wall signals in the early stages
of the AM symbiosis [15•] indicates that these types of
signals should not be overlooked.
One of the major alterations in the cortical cells in
which the arbuscules form is the massive extension
of the plasma membrane to form the peri-arbuscular
membrane ([29]; Figure 1). Given that the exchange of
nutrients is assumed to occur at this interface, it might
be expected that membrane transport mechanisms will
be induced. Consistent with this suggestion, a cDNA
representing a mycorrhizal inducible plasma membrane
ATPase was identified recently in barley [30] and a novel
gene, predicted to encode a membrane anchored protein
with structural similarities to phospholamban, a vertebrate
protein that regulates the activity of a Ca2+-ATPase,
is induced in mycorrhizal pea [31]. The induction of
an ATPase gene is consistent with biochemical data
indicating increases in plasma membrane ATPase activity
in mycorrhizal roots of some species [32] and with
earlier studies that demonstrated high levels of ATPase
activity on the peri-arbuscular membrane [33]. The
putative function of ATPases on this membrane is to
provide energy for nutrient transfer processes; however,
transport proteins involved in nutrient movement at the
arbuscular interface are currently unknown. A mycorrhizal
inducible sugar transporter has been identified in Medicago
truncatula [34] and a gene encoding a member of the
membrane intrinsic protein gene family is induced in
parsley mycorrhizae. Members of this family have been
shown to facilitate the movement of water and other small
molecules [35].
Phosphate regulates the symbiosis between AM fungi
and plants and the extent of colonisation in the roots is
inversely correlated with the phosphate status of the plant
[36,37]. Since the symbiosis usually results in increased
levels of phosphate in the plant some of the plant
genes showing differential expression in mycorrhizal roots
may be regulated in response to phosphate, rather than
signals from the fungus. There is, however, evidence
for independent regulation of expression of one gene,
Mt4, via both of these stimuli. Mt4 is a novel cDNA
representing a root specific gene from M. truncatula [38•].
Mt4 transcripts are induced in response to phosphate
Development of the arbuscular mycorrhizal symbiosis Harrison
starvation and down-regulated by phosphate or in response
to colonisation by a mycorrhizal fungus. It was initially
assumed that down regulation in the symbiosis was
a consequence of increased phosphate; however, Mt4
expression is also down regulated in a symbiotic plant
mutant in which colonisation is limited to growth on
the surface of the root and in which phosphate transfer
does not occur. This suggests that the Mt4 gene is
regulated independently by two signals, phosphate and
an unknown component(s) of the mycorrhizal fungus.
Two phosphate transporters and an acid phosphatase show
similar patterns of expression in response to phosphate
starvation and colonisation by mycorrhizal fungi, but
it is unknown whether they also show independent
regulation in response to the two signals [39]. Together,
these data indicate that, in general, phosphate starvation
inducible genes are down regulated in the early stages
of the symbiosis, ahead of significant levels of phosphate
entering the root. Has the symbiosis co-evolved to the
extent that the plant ‘anticipates’ an increased supply of
phosphate before it is delivered? Certainly the symbionts
have co-existed for the extensive periods of time that
might be necessary for this to occur. Fossil evidence
indicates that arbuscular mycorrhizae were present in
Devonian land plants and thus plants and AM fungi have
been associated for over 400 million years [40].
In comparison with the plant, even less is known about
the molecular changes in the fungal symbiont as the
association develops. The recent identification of genes
expressed in the spores [41] coupled with the continuing
identification of fungal genes expressed during the
symbiotic phase of the life cycle [42,43] will be essential
in unravelling aspects of AM fungal development.
Conserved signalling pathways in the
Rhizobium-legume and mycorrhizal
symbioses
It has been speculated that the Rhizobium–legume
(bacterial–plant) symbiosis evolved from the much older
mycorrhizal (fungal–plant) symbiosis and emerging similarities in the molecular events occurring during their
development lend support to this idea [44]. The observation that a number of nodulation mutants are also
mycorrhizal mutants indicates the presence of genes
essential for both symbioses; however, the identity of the
genes responsible is unknown [16–19]. Recent studies
indicate that a number of the nodulin genes induced
during nodule development are also induced in the
mycorrhizal symbiosis, although their function in the latter
is unclear. In Vicia faba, one of the four leghaemoglobin
genes induced in nodules is also induced in mycorrhizal
roots [45] and three other nodulin genes, PsENOD12,
MsENOD2 and MsENOD40 are induced in mycorrhizal pea
and alfalfa roots, respectively [5,24•]. In mycorrhizal alfalfa
roots, MsENOD40 transcripts are localised to the pericycle,
epidermis and cortex as seen in roots inoculated with
363
Rhizobia, and co-localise with cells containing immature
arbuscules. The MsENOD2 transcripts are present in
cells containing mature arbuscules, whereas in nodules
these transcripts are localised in the nodule parenchyma.
Induction of MsENOD2 and 40 occurs in response to
cytokinin, which is elevated in roots during nodulation and
has been shown recently to increase in mycorrhizal alfalfa
roots [24•]. On the basis of these data the authors suggest
that the downstream signalling events are conserved
between the two symbioses; however, it is equally possible
that the similarity lies only in the increase in cytokinin and
the pathways prior to cytokinin induction are distinct.
Further support for conserved signalling pathways is
provided by studies of PsENOD5 and 12A expression in
mycorrhizal and nodulated pea and pea mutants [46•].
As in nodule development, PsENOD5 and PsENOD12A
are induced in the early stages of the pea mycorrhizal
symbiosis. Further experiments using the pea sym8
mutant, which is blocked in early stages of both nodulation
and mycorrhiza formation, demonstrated that a functional
Sym8 was necessary for expression of the downstream
PsENOD5 and PsENOD12A genes in both symbioses. Sym
8, therefore, is a common step in the signal transduction
pathways for both of these symbioses. It seems unlikely
that the initial signals for the two symbioses will be the
same; however, at some point — probably shortly after the
initial signal — the signal pathways converge and a number
of downstream events are conserved.
Conclusions
As the application of molecular approaches to analyses of
this symbiosis is relatively recent, it can be anticipated
that the first few years will include groundwork to support
future advances. In the past year molecular approaches
have contributed to our understanding of some aspects
of the symbiosis and generated molecular tools essential
for future analyses. Thus, the end of the lag phase is
approaching and the next few years should see a rapid
increase in our understanding of the events underlying the
AM symbiosis. The identification of mycorrhizal mutants
is accelerating and the continued cloning of genes induced
during the symbiosis will contribute to a molecular
picture of the events accompanying development of the
association. These genes will also serve as tools; both for
the analysis of altered developmental processes in the
mutants, and as a starting point for the analysis of signal
transduction pathways operating in the symbiosis. The
symbiosis is a complex system and it will be important
to use integrated approaches to obtain a complete
understanding of the events underlying its development
and functioning.
Acknowledgements
The author would like to thank K Korth for critical reading of the
manuscript. Financial support was provided by The Samuel Roberts Noble
Foundation.
364
Plant–microbe interactions
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