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Cellular programs for arbuscular mycorrhizal symbiosis
Maria J Harrison
In arbuscular mycorrhizal (AM) symbiosis, AM fungi colonize
root cortical cells to obtain carbon from the plant, while
assisting the plant with the acquisition of mineral nutrients from
the soil. Within the root cells, the fungal hyphae inhabit
membrane-bound compartments that the plant establishes to
accommodate the fungal symbiont. Recent data provide new
insights into the events associated with development of the
symbiosis including signaling for the formation of a cellular
apparatus that guides hyphal growth through the cell. Plant
genes that play key roles in a cellular program for the
accommodation of microbial symbionts have been identified.
In the inner cortical cells, tightly regulated changes in gene
expression accompanied by a transient reorientation of
secretion, enables the cell to build and populate the
periarbuscular membrane with its unique complement of
transporter proteins. Similarities between the cellular events for
development of the periarbuscular membrane and cell plate
formation are emerging.
Address
Boyce Thompson Institute for Plant Research, Tower Road, Ithaca,
NY 14853, USA
Corresponding author: Harrison, Maria J. ([email protected])
Current Opinion in Plant Biology 2012, 15:691–698
This review comes from a themed issue on Cell biology
Edited by Keiko U Torii and Masao Tasaka
For a complete overview see the Issue and the Editorial
Available online 1st October 2012
1369-5266/$ – see front matter, # 2012 Elsevier Ltd. All rights
reserved.
http://dx.doi.org/10.1016/j.pbi.2012.08.010
Introduction
The arbuscular mycorrhizal (AM) symbiosis is formed by
plants and fungi from the Glomeromycota. The ability to
form AM symbiosis occurred early in the plant lineage and
was retained in many plant families. As a result of its
widespread distribution, AM symbiosis has a global impact
on plant phosphorus nutrition and on the carbon cycle [1].
AM symbiosis is an endosymbiosis, that is, a symbiosis
where one organism lives within the cells of another.
During AM symbiosis, the fungus enters the root through
the epidermal cells and grows into the cortex where it
establishes highly branched hyphae called arbuscules
within the cortical cells. At all stages of development,
the hyphae that grow through, or differentiate within,
plant cells are always surrounded by a plant membrane.
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This is referred to as the perifungal membrane around
intracellular hyphae or the periarbuscular membrane
(PAM) around the arbuscule. The arbuscule is the site
of phosphate delivery to the plant and phosphate transporters in the PAM capture phosphate released from the
arbuscule and transport it into the cortical cell [2–5]. The
site of carbon transfer to the fungus is still unclear but
analysis of an AM fungal hexose transporter implicates
the arbuscule in this process [6].
Diffusible signals initiate the symbiosis before physical
contact between the symbionts. Strigolactones, secreted
from the roots of phosphate-deprived plants [7], activate
AM fungal metabolism and this results in hyphal branching in proximity to the root [8,9]. Following contact with
the root surface, the fungus forms a hyphopodium
through which it penetrates the epidermis. Entry into
the epidermal cell and subsequently the root cortex, is
controlled by a plant signaling pathway, referred to as the
common symbiosis signaling pathway (CSSP), so named
because in legumes, this pathway is required also for the
formation of symbiosis with rhizobia (Box 1). In CSSP
loss-of-function mutants, the AM fungus is unable to
enter epidermal or cortical cells. The current understanding of signaling through the CSSP has been obtained
mostly from analyses of the rhizobium-legume symbiosis
(RLS) (Box 1). Here, rhizobial Nod factors are perceived
by LysM-domain receptor kinases and downstream signaling through the CSSP activates calcium spiking in root
cells and gene expression changes necessary for RLS
[10,11]. Calcium spiking and transient increases in cytosolic calcium levels also occur in root cells treated with
exudates from AM fungi [12–14], and it was shown
recently that AM fungi secrete a mixture of sulphated
and non-sulphated lipochitooligosaccharides (referred to
as Myc-LCOs) with structures very similar to Nod factors
[15]. This suggests that activation of the CSSP for AM
symbiosis may occur in a similar manner to activation by
Nod factors. Currently, the full complement of receptors
for Myc-LCOs is unknown. In Medicago truncatula, lateral
root branching, which is one of the activities stimulated
by Myc-LCOs is mediated partly through a Nod factor
receptor, NFP [15], and in Parasponia, the ortholog of
NFP is required for RLS and for arbuscule formation in
AM symbiosis [16]. However, nfp and L. japonicus Nod
factor receptor mutants nfr1 and nfr5, all form AM
symbiosis [17,18], therefore in legumes, additional
receptors must be involved in Myc-LCO perception for
AM symbiosis. In M. truncatula the LysM-domain receptor family contains at least 17 members [19], one of
which is induced during AM symbiosis [20] and any of
which could be Myc-LCO receptors.
Current Opinion in Plant Biology 2012, 15:691–698
692 Cell biology
Box 1 Common symbiosis signaling pathway (CSSP)
The CSSP is a signaling pathway required for AM symbiosis and
rhizobium-legume symbiosis (RLS) and several recent reviews
provide in depth coverage of this pathway [10,11]. As the AM
symbiosis is the older of the two symbioses, it is assumed that the
CSSP arose for AM symbiosis and was later coopted for RLS.
Components of the CSSP were identified largely through genetic
analyses of RLS. The pathway is comprised of a receptor kinase
(SYMRK in L. japonicus, DMI2 in M. truncatula), ion channel(s)
(CASTOR and POLLUX in L. japonicus, DMI1 in M. truncatula), a
calcium calmodulin-dependent protein kinase (CCaMK), three
components of the nuclear pore complex (NUP85, NUP135 and
NENA in L. japonicus), a nuclear protein of unknown function
(CYCLOPS in L. japonicus, IPD3 in M. truncatula) and a transcription factor, NSP2 of M. truncatula. It is assumed that for each
symbiosis, signals perceived by unique receptors activate the
signaling pathway and a combination of outputs, common to both
symbioses and unique to each individual symbiosis, are obtained via
signaling through different sets of transcription factors. A detailed
understanding of signaling through the pathway has been obtained
from analyses of RLS. In RLS, rhizobial lipochitooligosaccharide
molecules called Nod factors are perceived by LysM-domain
receptor kinases (NFR1, NFR5 in L. japonicus, NFP and LYK3 in M.
truncatula) which then activate signaling through the CSSP. Calcium
spiking is a central component of the CSSP and the spiking signal is
likely decoded by CCaMK to activate NSP2 and also transcription
factors unique to RLS, to result in changes in gene expression and
RLS. The ion channels, receptor kinases and nuclear pore
components are required to enable calcium spiking. Recently a
sarco/endoplasmic reticulum calcium ATPase required for spiking
was identified that is potentially another component of the CSSP
[58].
develops around the nucleus and under the contact site.
Subsequently, the nucleus migrates to the opposite side
of the epidermal cell and a broad cytoplasmic column,
containing the PPA, links the nucleus with its original
position below the hyphopodium. FM4-64 labeling
suggests that plasma membrane invagination occurs
under the hyphopodium contact point and the penetrating hypha then grows across the cell, following the path
defined by the PPA. Live cell imaging and electron
microscopy analyses indicated that Golgi bodies were
abundant under the hyphopodium and in the vicinity
of the penetrating hypha, as were trans-Golgi networks
(TGN). In addition, EXO-84, a marker of the exocytotic
pathway, and VAMP proteins that mark secretory
vesicles, accumulated in the vicinity of the hyphopodium,
and around the growing hyphal tip [25]. These data point
to substantial secretory activity in the PPA, likely associated with the synthesis of the perifungal membrane and
matrix that envelop the hypha as it grows through the cell
(Figure 1).
A similar reorganization of the ER and nuclear migration
was observed in the outer cortical cells before hyphal
growth through the cell and also in the inner cortical cells
preparing for arbuscule formation [14,22,25,26,27]
(Box 2).
Calcium signaling and hyphal growth through
epidermal and cortical cells
Which genes and which cellular processes are activated
by the CSSP, or by other signaling pathways, to enable
AM symbiosis? Here, recent advances that lead to our
current understanding of the cellular programs used to
accommodate fungal symbionts during AM symbiosis are
reviewed. Some aspects of the programs are controlled by
the CSSP and fall within the remit of a general accommodation program for endosymbionts, proposed originally by Parniske several years ago [21].
Cellular events during hyphal penetration of
epidermal and cortical cells
Two striking aspects of AM symbiosis are the extent to
which root cells reorganize their internal structure to
accommodate the fungal symbiont and the fact that the
first changes occur before intracellular growth of the
fungal hypha, suggesting that the cells prepare for infection [22,23]. As observed previously for pre-infection
threads formed during RLS [24], the cellular reorganization defines the future path of hyphal growth through the
cell. By using fluorescent protein fusions and confocal
microscopy, the cellular alterations that occur in preparation for AM symbiosis have been analyzed in detail,
particularly in epidermal cells in contact with a hyphopodium [23]. Here it was observed that the nucleus of
the epidermal cell moves toward the hyphopodium contact site and a dense assemblage of ER, actin and microtubules, named the prepenetration apparatus (PPA),
Current Opinion in Plant Biology 2012, 15:691–698
What induces PPA formation? PPAs were not observed in
the CSSP mutants dmi2 or dmi3 [23] and constitutive
expression of a gain-of-function CCaMK variant induces
cytoplasmic aggregates which appear similar to PPAs
[27]. Consequently, PPA formation is induced in
response to signaling through the CSSP. In RLS, the
analogous structure, the pre-infection thread, can be
induced by Nod factors [24].
Analyses of calcium spiking during the pre-infection
phase and also during hyphal growth through epidermal
and outer cortical cells, revealed differences in the spiking signatures during these two phases. Epidermal cells in
contact with a hyphopodium showed calcium spiking, as
did the underlying outer cortical cells and in both cases,
spiking was associated with nuclear migration toward the
contact site and cytoplasmic aggregation [14,26]. A
distinct increase in the frequency of the calcium spikes
was observed as the fungus penetrated the cells. Detailed
observations of outer cortical cells indicated that highfrequency spiking occurred only in the penetrated cell
and was no longer detected once hyphal growth through
the cell was complete (Figure 1). Similar analyses of RLS
showed that growth of the infection thread across the
outer cortical cells is also associated with high-frequency
calcium spiking and the spiking signature was the same as
that observed in root hair cells treated with Nod factors.
Furthermore, the spiking signature observed in the outer
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Cellular programs for AM symbiosis Harrison 693
Figure 1
hypha
Hyphopodium
Penetrating
PPA
Golgi
CSSP
ER
Vapryin/PAM1
punctate bodies
TGN
TGN
CCaMK
Hypothetical Myc-LCO
receptor
TG
N
Myc-LCO
gene expression
(VAPYRIN)
Ca2+
Current Opinion in Plant Biology
Growth of a fungal hypha through an epidermal cell is guided by the plant pre-penetration apparatus (PPA) that spans the cell. The PPA consists of
cytoplasm containing a dense assemblage of ER, cytoskeletal components (not shown) and organelles of the secretory system. It functions to guide the
hypha through the cell and secretion of the peri-fungal membrane (shown as an orange dotted line) and a matrix with composition similar to a primary cell
wall (white space between the peri-fungal membrane and the penetrating hypha) is achieved through the secretory organelles within the PPA. The PPA
forms in the cells underlying hyphopodia, before hyphal growth through the cell and its formation is triggered by signaling through the common symbiosis
signaling pathway (CSSP). Although not yet shown directly, it is likely that Myc-LCOs produced by the fungus, induce formation of the PPA. Receptors that
perceive Myc-LCOs and activate the CSSP for PPA formation have not been identified and are shown as ‘hypothetical receptors’.
cortical cells during infection thread growth was the same
as that observed during transcellular hyphal growth [26].
Consequently, it is likely that spiking in these cells is
induced by Nod factors and Myc-LCOs produced by the
respective symbionts. Do low-frequency and high-frequency calcium spiking induce different changes in gene
expression associated with the preparative and penetration events? This is unknown but previous studies
suggested that a minimum number of calcium spikes is
necessary to induce gene expression changes [28], which
would be most readily attained by high-frequency
calcium spiking. A calcium spiking signature common
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to both symbioses can be expected to induce similar
gene expression changes but how are gene expression
patterns specific to each inducer [17] achieved? Currently, the answer to this is unclear but CCaMK may
provide some specificity as this multi-domain protein
does not function identically in the two symbioses
[29,30]. Thus, a high-frequency calcium spiking signal
induced by Nod factors and Myc-LCOs, may activate
CCaMK and lead to both common and unique changes
in gene expression depending on the environment.
Additionally, specificity may arise from signaling independent of the CSSP [31–34].
Current Opinion in Plant Biology 2012, 15:691–698
694 Cell biology
Box 2 Prepenetration apparatus (PPA) formation in the inner
cortical cells
PPA-like structures are also observed in the inner cortical cells
before arbuscule formation and their morphology varies depending
on the morpho-type of the mycorrhiza. In Arum-type symbioses, the
PPA develops below the hyphal contact point and the nucleus
migrates to the middle of the cell where it remains during arbuscule
branching. In the Paris-type symbioses, where the fungal hyphae
take an intracellular path through the inner cortical cells, the PPAs
are particularly striking. As many as 5 cells ahead of the advancing
hyphae show a polarized organization with a broad aggregation of
ER that links the potential contact point to a centrally located nucleus
and furthermore connects to the opposite side of the cell where the
hypha will exit the cell. Time lapse imaging demonstrated that these
PPAs define the path of hyphal growth as the fungus passed through
each cell, sometimes forming large coils within the cell. These results
suggest that either a diffusible signal or cell-to-cell communication
ahead of the growing hypha initiates PPA formation [22,25]. PPA
formation in the cortical cells is associated with significant enlargement of the nuclei [22,59] which may be necessary for the significant
transcriptional activity that occurs during arbuscule development, or
alternatively a reflection of endoreduplication [59,60]. The latter
provides further support for the hypothesis of recruitment of the cell
division program to enable periarbuscular membrane formation, as
discussed later in this review.
Vapyrin/PAM1, a gene induced by Myc-LCOs
that is required for hyphal entry into cells
While links between signaling and preparative cellular
events have been made, we know relatively little about
genes activated by the CSSP that function in cellular
processes for the accommodation of the fungus. The
Vapyrin gene of M. truncatula and its ortholog, PAM1
of Petunia hybrida are required for both AM symbiosis and
RLS and may be the first candidate [35,36,37]. During
AM symbiosis, Vapyrin is induced transiently in epidermal cells and then in cortical cells during hyphal growth
into the cell [35]. It is likely that this occurs via MycLCOs as Vapryin transcripts are elevated in roots exposed
to Myc-LCOs [17] and induction requires the CSSP
[36]. However, Vapyin expression is not restricted to
the penetrated cell but occurs also in adjacent cells, so if it
is induced by the high-frequency calcium spiking, the
signal must be further transduced to the neighboring
cells. In Vapryin RNAi lines, 50% of the hyphopodia fail
to penetrate epidermal cells [35,36] and hyphae that
gain access to the inner cortex are unable to enter the
cortical cells, so arbuscule formation is abolished. The
phenotype of pam1 is similar, although some hyphae
manage to penetrate cortical cells but fail to develop
arbuscules [37]. The minor differences in phenotypes
in M. truncatula and Petunia may result from differences
in the fungal symbionts or environmental conditions.
Currently, it is unclear how Vapyrin/PAM1 functions to
enable hyphal penetration of cells. The Vapyrin/PAM1
protein is a novel combination of two previously
described protein domains, a VAMP Associated Protein
(VAP)/major sperm protein (MSP) domain and an ankyrin
repeat domain; both domains are generally involved in
protein–protein interactions. Vapyrin/PAM-GFP fusions
Current Opinion in Plant Biology 2012, 15:691–698
revealed that the protein was present mostly as small
puncta some of which move rapidly in the cell and it is
possible that Vapyrin/PAM1 associates with proteins on
vesicles involved in building the perimicrobial membranes [35,37]. Alternatively, MSP domains are known
to self-oligomerize and Vapyrin puncta may be aggregates, possibly with a role in the development of the PPA.
Currently, it is not known if PPAs form correctly in
vapryin/pam1 mutants.
Cellular activities in the inner cortical cells;
accommodation of the arbuscule and
development of the periarbuscular membrane
The prepenetration apparatus and the phenotype of
vapryin/pam1 mutants indicate a cellular program common to epidermal and cortical cells that enables hyphal
growth into cells. However, in the inner cortical cells,
additional events are necessary to enable arbuscule development including a substantial reorganization of cellular components and expression of a unique
transcriptional program [38,39], which is not activated
directly via the CCSP [27]. Currently, signals and
regulators of this specific cortical cell program are
unknown and only a few genes with potential roles in
this program are known. In addition to Vapryin/PAM1, an
ABC transporter STR/STR2 [40,41] and a secreted subtilisin protease, SbtM1 that localizes in the periarbuscular
space [42], are required to enable arbuscule development. In both cases, their substrates and their exact roles
are unknown.
During arbuscule formation, the hypha enters the inner
cortical cells and is guided to the middle of the cell by a
PPA where arbuscule branching commences [22]. The
signal that induces branching and terminal differentiation
of the fungus is currently unknown. During arbuscule
branching, the ER envelops the developing arbuscule and
cytoskeletal components reorganize and bundle around
the arbuscule branches [22,43–45]. Golgi bodies, which
are particularly numerous, are positioned adjacent to
arbuscule branch nodes [44], and markers suggest exocytosis at the hyphal tips [25]. Again, this arrangement of
the cytoskeleton, organelles and markers point to
secretory activities, likely associated with development
of the PAM and matrix in the periarbuscular space.
The PAM has two broad domains: the domain around the
arbuscule trunk, which shares protein markers with the
plasma membrane of the cell and a domain around the
arbuscule branches, which contains a unique set of
proteins including symbiotic phosphate transporters such
as M. truncatula MtPT4 and rice OsPT11 [3,44]. The
striking polarity of MtPT4 prompted investigations of the
mechanism underlying its targeting to the branch-domain
of the PAM. This led to an unexpected finding that
several different plasma membrane-resident phosphate
transporter and carbohydrate transporter proteins could
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Cellular programs for AM symbiosis Harrison 695
be targeted to the PAM if expressed ectopically from the
MtPT4 promoter [46]. Subsequent analyses revealed
that the final destination of these membrane proteins
depended on the time at which they were expressed
relative to arbuscule formation; expression before arbuscule formation resulted in location in the plasma membrane while expression coincident with arbuscule
formation resulted in location in the PAM. These results
suggested that during arbuscule formation the secretory
pathway is redirected to the developing PAM [46] a
finding that is also consistent with the positioning of the
majority of the secretory organelles [25,44] Thus, the cell
simultaneously builds and populates the PAM by reorienting secretory flow in the cell and activating transcription of genes encoding PAM-resident proteins.
Additionally, alterations in the ER of colonized cells
further controls which proteins enter the secretory system
[46]. Currently, it is unclear when default secretion to
the plasma membrane is reestablished but this probably
occurs once PAM development is complete.
Although the cell builds the PAM by redirecting secretion,
there is still a requirement for some specific vesicle trafficking components. In M. truncatula, two SNAREs
Figure 2
Arbuscule
TGN
N
TGN
TGN
Vapryin/PAM1 punctate bodies
MtPT4
Vesicles containing VAMP 721d and e
Periarbuscular membrane
STR/STR2
Layer of ER-rich cytoplasm
Golgi
TGN
TGN
Arrows indicate the direction of secretion
Current Opinion in Plant Biology
During arbuscule development, a layer of cytoplasm containing ER, cytoskeleton (not shown) and the tonoplast (not shown) surrounds the arbuscule
(for detailed images of cytoskeleton and tonoplast, see [43,44,61]). Golgi bodies are abundant and locate at the branch nodes. Vapyrin/PAM1 punctate
mobile bodies are abundant in the cell; Vapyrin/PAM1 is required for arbuscule formation but its cellular function is unknown. Vesicles containing
VAMP721d/e are located around the hyphal branches. VAMP721d/e likely function in SNARE-mediated vesicle fusion to the periarbuscular membrane.
The periarbuscular membrane is physically continuous with the plasma membrane of the cell but the domain around the arbuscule branches contains
a unique set of proteins including phosphate transporters (MtPT4, OsPT11) and ABC transporters (STR/STR2) that are not present in the plasma
membrane. Vapyrin/PAM1 punctate mobile bodies are abundant in the colonized cells; their function is unknown. During arbuscule branching, the
default secretory pathway, which is normally directed to the plasma membrane, is reoriented to the periarbuscular membrane.
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Current Opinion in Plant Biology 2012, 15:691–698
696 Cell biology
(soluble N-ethylmaleimide sensitive factor attachment
protein receptor), VAMP721d and VAMP721e, likely play
a role in periarbuscular membrane development [47].
The VAMP72 family of vSNAREs, of which VAMP721d/e
are members, are located on the membranes of exocytotic
vesicles and together with tSNAREs located on the target
membrane; they mediate the fusion of vesicles and target
membranes. VAMP721d/e are expressed in the inner cortical cells and knockdown via RNAi resulted in aberrant
arbuscules with a trunk and very few short branches. GFPVAMP721 fusion proteins were visible in the vicinity of the
arbuscule and it seems likely that they are located on
vesicles where they mediate fusion to the PAM. Potential
cargo of the VAMP721d/e vesicles would include PAMresident proteins, MtPT4 [48], an ABC transporter, STR/
STR2 [40,41] and a secreted subtilisin protease, SbtM1
[42]. VAMP721d/e are required also for symbiosome
formation during RLS [47] indicating commonalities in
exocytotic events in these two endosymbioses (Figure 2).
and rhizobia-legume symbiosis continue to emerge, supporting the idea of a basic cellular program for the
accommodation of endosymbionts [21], with individual
specializations.
The arbuscule is a transient structure and the PAM and
matrix are rapidly built and later deconstructed as the
cortical cell returns to its original state [49]. Development
of the PAM has several parallels with cell plate formation
during cytokinesis. In both cases, polarized secretion of
large amounts of membrane occurs in a short space of time
and this is achieved through the transient reorientation of
default secretory flow [46,50,51]. Consistent with this,
reorganization of the cytoskeleton and proliferation of
Golgi, and secretory machinery are features common to
both processes [25,45,52,53]. VAMP721 proteins are
required in both of these processes [54] and the M.
truncatula VAMP 721d/e proteins localize to the cell plate
in meristematic cells [47]. Additionally, both processes
require a transient reduction in vacuole volume and
morphology [44,55,56]. Given these emerging similarities, it seems possible that some aspects of the program for accommodation of the arbuscule may have
evolved from the cellular program for cell plate formation.
A similar proposal has been made for infection thread
growth during RLS, which is coupled to cell cycle reactivation and cell division processes [57].
Summary and conclusions
In summary, the cellular programs for AM symbiosis are
beginning to be revealed. The current data suggest that
the fungal symbiont activates the CSSP to induce complex cellular changes necessary to enable its growth into
the epidermal and cortical cells. In the cortical cells, an
additional cellular program operates to accommodate the
arbuscule and signals that activate this program are
unknown. So far, only a handful of proteins that operate
in these cellular accommodation programs have been
identified and in most cases, their precise roles are
unclear. It may be useful to turn to other cellular programs, such as cell plate formation, for additional clues.
Commonalities in the cellular programs for AM symbiosis
Current Opinion in Plant Biology 2012, 15:691–698
Acknowledgements
Financial support was provided by the National Science Foundation IOS0842720 and IOS-0820005. Figures 1 and 2 were drawn by M. Swartwood
Towne.
References and recommended reading
Papers of particular interest, published within the period of review,
have been highlighted as:
of special interest
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Current Opinion in Plant Biology 2012, 15:691–698
698 Cell biology
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