Opinion

Arbuscular mycorrhizal dialogues:

do you speak ‘plantish’ or ‘fungish’?
Paola Bonfante and Andrea Genre
Department of Life Science and Systems Biology, University of Turin, Turin, Italy

Plants rely on their associated microbiota for crucial hand, plants have to modulate their immune system in
physiological activities; realization of this interaction order to tolerate, stimulate, or counteract the activities of a
drives research to understand inter-domain communi- myriad of soil microbes, each producing their own signal
cation. This opinion article focuses on the arbuscular molecules [5]. In this context, where plants have to identify
mycorrhizal (AM) symbiosis, which involves the the surrounding microbes as friends or foes [6], arbuscular
Glomeromycota, fungi that can form a symbiosis with mycorrhizal (AM) (see Glossary) symbiosis is an excellent
most plants. Here we propose the hypothesis that the model to discuss the exchange of signaling molecules at the
molecules involved in inter-kingdom symbiotic signal- inter-kingdom level [7]: AM fungi are the most widespread
ing, such as strigolactones, cutin monomers, and chitin- fungal component of the plant microbiota, and most land
related molecules, also have key roles in development, plants support an AM symbiosis, irrespective of their
originally unrelated to symbiosis. Thus, the symbiotic phylogenetic position [8], suggesting the existence of a
role of these molecules relies on the co-evolved capacity conserved communication process.
of the AM partners to perceive and interpret them as Here, we summarize the characteristics of the best-
symbiotic signals. known plant and fungal molecules that trigger symbiotic
responses in the corresponding AM partner. Interestingly,
Plant and fungal symbiotic molecules the signaling molecules characterized so far (strigolac-
In cartoons, animals, plants, and mushrooms communicate tones, cutin monomers, chitin-related molecules) appear
with each other flawlessly. However, in real life, under- to have well-established developmental roles, unrelated
standing how individuals belonging to different domains of
life communicate, via ‘plantish’ or ‘fungish’ signals,
remains a hot topic in the field of plant–microbe interac- Glossary
tions. Plants and microbes exchange signals that regulate Arbuscular mycorrhiza (AM) fungi: among plant-associated microbes, the
each other’s metabolism and development, and ultimately widespread AM fungi play a key role in nutrient cycling and plant health due to
their ability to improve plant mineral nutrition. These fungi belong to an
condition their interactions. Several examples of inter-
ancient monophyletic phylum, the Glomeromycota, currently considered to be
specific communications have been identified in the hidden phylogenetically related to the Mucoromycotina. Unusually among fungi,
world of plant–microbe interactions. One long-known ex- Glomeromycota are obligate biotrophs, multinucleate, and apparently asexual.
Analysis of the genome sequence of Rhizophagus irregularis revealed
ample in legumes is the perception of Nod factors from additional unique features, for example, plant cell wall-degrading enzymes
rhizobial bacteria; this perception ultimately leads to the are very poorly represented, while small secreted proteins are abundant and,
generation of a novel symbiotic organ, the root nodule, as a result, are mostly expressed during the symbiotic phase.
Inter-kingdom symbiotic signaling: in AM host plants, a conserved signal
where symbiotic bacteria fix atmospheric nitrogen and transduction pathway mediates the perception of fungal signals. The proteins
convert it into organic compounds [1]. More recently, characterized so far include a membrane receptor-like kinase, a mevalonate
exciting new projects aim to introduce symbiotic nitrogen biosynthetic enzyme, nucleoporins, a cationic channel localized to the nuclear
envelope, and a nuclear calcium/calmodulin-dependent kinase. In legumes, the
fixation in cereals (https://www.jic.ac.uk/news/2012/07/ same proteins also participate in the signal transduction pathway mediating
cereals-self-fertilise/#) [2], which requires a deep under- the perception of the rhizobial Nod factor during nodulation via a common
standing of this inter-domain signal exchange. Recent data symbiotic signaling pathway. However, increasing evidence suggests the
existence of additional pathway(s).
by Liang et al. [3] indicate that indeed nonlegumes can MAMP-triggered immunity: plant immunity relies on cell-autonomous events
recognize rhizobial Nod factor, but this leads to a strong with some similarity to the innate immune system in animals. Plants use
suppression of the innate immune response. extracellular receptors to recognize microbe-associated molecular patterns
(MAMPs; e.g., bacterial flagellin) as well as endogenous molecules (such as
Plant–microbe communications rarely occur as one-to- wall oligomers released during pathogen attack), activating MAMP-triggered
one conversations: plants host a diverse microbiota, which immunity. A second level of perception drives effector-triggered immunity,
which uses intracellular receptors to recognize pathogen-secreted molecules
offers multiple ecological services to the green host. On the
called effectors. The high variability and specificity of effectors feeds plant–
one hand, benefits from one microbe may be obscured by pathogen co-evolution.
the simultaneous presence of another [4]; on the other Plant microbiota: similar to human microbiota, in plants, microbial commu-
nities thrive in tissues and on organ surfaces (e.g., in the rhizosphere and
Corresponding author: Bonfante, P. (paola.bonfante@unito.it). phyllosphere), cooperating in key metabolic processes and creating a network
Keywords: arbuscular mycorrhizal fungi; chitin; strigolactones; cutin monomers; of mutual relationships. To date, most research on plant microbiota has
signal molecules; receptors. focused on bacteria, identifying dominant communities of Actinobacteria,
Bacteroidetes, Firmicutes, and Proteobacteria. However, eukaryotes such as
1360-1385/ fungi, with lifestyles ranging from mutualism to parasitism and commensal-
ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2014.12.002 ism, also make up key components of the plant microbiota.

150 Trends in Plant Science, March 2015, Vol. 20, No. 3

 Opinion Trends in Plant Science March 2015, Vol. 20, No. 3

bud growth [12] through a well-characterized, receptor-

mediated pathway that probably interacts with other plant
hormones [13]. Strigolactone production is conserved from
Charales to Embryophytes, including the basal groups of
D ev liverworts and mosses [14]. These discoveries have revolu-
Hormones
t
tionized our view of strigolactone signaling: their function
e lo p m e n

el
op
Cell wall in the rhizosphere suddenly appearing to be a secondary

m e nt
Cucle
feature relying on their active release from the roots into
the soil [15]. Thus, 10 years after the seminal studies by the
ev

D groups of Kohki Akiyama [10] and Guillaume Bécard [11],

emerging data suggest that strigolactones function as
conserved determinants of plant development that were
P l a

recruited during the evolution of plant symbiotic and

al
n t

g parasitic interactions.
si
Fungal
i Despite this continued interest in strigolactones, our
s

g
n
a l
s knowledge of strigolactone perception by AM fungi
remains very limited. We only know that strigolactone
perception boosts fungal metabolism, leading to increased
TRENDS in Plant Science ATP production and mitochondrial division [11,16]. Prelim-
inary data from RNA sequencing (RNA-seq) of germinated
Figure 1. Our current view of the signaling between arbuscular mycorrhizal (AM)
fungi (shown on the right) and their host plants (shown on the left) suggests that spores of the AM fungus Gigaspora margarita treated with
molecules with a developmental role in each organism have been intercepted by the synthetic strigolactone GR24 confirm the upregulation
the respective partner and re-interpreted as symbiotic signals.
of mitochondrial genes (A. Salvioli and P. Bonfante, un-
published results). Interestingly, strigolactone treatment
to symbiosis, in the organisms that produce them also induced the proliferation of G. margarita endobacteria
(Figure 1). A particular case is represented by fungal [17]. Furthermore, by introducing the calcium sensor
lipo-chitooligosaccharides (LCOs): although their chemi- transactivator of transcription (TAT)-aequorin in the same
cal structure links them to chitin biosynthesis, LCOs are fungus, it has been demonstrated that GR24 causes rapid
not known to perform intrinsic functions in the AM fungi calcium transient in the fungal cytoplasm [18]. Finally,
and might therefore be specifically produced as signals to GR24 treatment of G. margarita and Rhizophagus irregu-
the plant host. laris [19] increases the release of short chito-oligosacchar-
ides (COs, presymbiotic fungal signals) as discussed below.
Host plant signals to AM fungi: hablas ‘plantish’? In short, recent data suggest that AM fungi might
Strigolactones, terpenoid lactones that derive from carot- perceive strigolactones through a calcium-mediated path-
enoid metabolism (Figure 2), were first studied as root- way and activate multiple responses involving fungal cell
exuded molecules that elicit the germination of parasitic wall-related metabolism (hyphal branching and chito-oli-
plants [9]; more recently, strigolactones returned to the gosaccharide production), and mitochondrial and endobac-
limelight as bioactive molecules that stimulate the branch- terial activity. However, fungal strigolactone receptors
ing and metabolism of presymbiotic hyphae in AM fungi remain unknown and analysis of the R. irregularis genome
[10,11]. Finally, strigolactones emerged as key plant hor- [20,21] has not revealed the existence of fungal homologs of
mones that repress shoot branching by controlling axillary the known strigolactone receptors in plants [13]. Thus, we

Plansh Fungish
Strigolactones Chin

Chito-
oligosaccharides
Lipo-chito-
oligosaccharides

Cun
monomers
Cun

Symbiosis
TRENDS in Plant Science

Figure 2. ‘Plantish’ and ‘fungish’ signals. The establishment of the arbuscular mycorrhizal (AM) symbiosis culminates in the development of arbuscules (central panel),
where the fungal and plant cells intertwine to create a symbiotic structure in its truest sense. Similarly, the chemical dialogue between the two symbionts is based on an
exchange of ‘plantish’ and ‘fungish’ words that get a novel meaning in the context of the symbiosis, as compared to the structural (cutin, chitin) or hormonal (strigolactone)
roles that the same – or closely related – molecules play in the producing organism.

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can only conclude that fungal and plant strigolactone molecules trigger GSE-like responses in the host roots,
receptor proteins likely differ in structure, which opens including Ca2+ spiking [19], and the regulation of symbio-
the possibility that AM fungi independently evolved sis-related genes [31,34].
strigolactone perception mechanisms. An interesting aspect of fungal signaling is that LCOs
Recent work identified cutin monomers as plant signals and COs both have structures closely related to chitin. This
that have a key role in the AM dialogue (Figure 2). These raises the question whether the production of such mole-
hydroxylated aliphatic acids are proposed to be released on cules occurs as a direct byproduct of fungal cell wall
the root surface as a necessary signal for hyphopodium biosynthesis or evolved from it via the generation of specific
differentiation from presymbiotic AM fungal hyphae metabolic pathways. In either case, molecules related to
[22,23]. Direct evidence showed that hyphopodium devel- fungal cell wall biogenesis play a role as inter-kingdom
opment requires the function of RAM2, a Medicago trun- messengers that only AM host plants recognize as symbi-
catula glycerol-3-phosphate acyl transferase involved in otic signals [19].
hydroxylated aliphatic acid biosynthesis, and is enhanced The idea that AM fungal signaling is based on chitin
by the application of exogenous cutin monomers. oligomers raises a critical specificity issue: since all fungi
Cutin polymer is the major component of the cuticle, the produce N-acetyl-glucosamine chains of various lengths,
waxy coating of aerial organs in land plants; cutin also has how can plants identify each fungus and raise the appro-
a well-known role as a signal to pathogenic fungi that priate response, discriminating between a symbiont and a
attack leaves, stems, and fruits [24]. A novel role for this pathogen? As a further complication, the major rhizobial
hydrophobic molecule in a hydrated, underground envi- signals, the Nod factors, have a striking structural simi-
ronment such as the surface of lateral roots may sound larity to LCOs, including the same N-acetyl-glucosamine
surprising. On the one hand, this suggests the existence of backbone [35]. Indeed, plants have large families of recep-
unpredicted similarities between symbiotic and pathogen- tors and receptor-like proteins that are predicted to bind
ic interactions, independent of the target organ [24,25]; on chitin-based molecules, including the bacterial Nod factors
the other hand, the fact that all plant clades that produce [36]. They all possess conserved lectin-like, chitin-binding
cutin (from liverworts to angiosperms) also develop AM LysM domains, but the specificity of each receptor for each
interactions [8] is a suggestive coincidence. So far, howev- chitin oligomer in native conditions remains to be fully
er, no evidence points to a direct relationship between understood. Overall, the picture will likely remain obscure
hyphopodium development and the presence of cutin on until we understand how these receptor proteins act, either
the root epidermis wall [26]. The closest analogy can alone or within complexes, in different plants and in the
probably be found in Colletotrichum trifolii, where cutin presence of different combinations of ligands [37]. At any
elicits appressorium formation through the activation of a rate, such a massive deployment of plant genomic
fungal protein kinase [27]. Anyway, we cannot exclude that resources, deriving from extensive gene duplication and
cutin monomers – not necessarily produced on the root neo-functionalization [38], can indicate a diversified per-
surface – indirectly influence hyphopodium development ception system, acting upstream of microbe-associated
by activating a signaling cascade within the plant cell. molecular pattern (MAMP)-triggered immunity and sym-
biotic responses, and representing a possible key to plant
Fungal signals to AM host plants: parlez-vous ‘fungish’? recognition of each interacting microbe.
Navazio and colleagues [28] provided the first evidence of
diffusible signals in the exudates of germinated glomer- Dr Dolittle in the rhizosphere? Plants and AM fungi
omycotan spores (GSE), showing that treating soybean speak to each other
cultured cells with concentrated GSE induced, within Although our knowledge of symbiotic signal exchanges in
minutes, a transient increase in cytosolic calcium concen- AM remains limited, an intriguing speculation appears
tration with a characteristic profile. The authors also reasonable: during their long co-evolution, glomeromy-
showed that GSE did not trigger the production of reactive cetes and their host plants seem to have developed the
oxygen species, a typical response to exudates from patho- ability to intercept structural or hormonal molecules from
genic fungi. Also, nitric oxide accumulates in the first their respective partners and interpret them as symbiotic
minutes after GSE application to M. truncatula roots messengers. Along this line, the similarity of strigolactone
[29] and GSE triggers nuclear Ca2+ spiking with the same and abiotic stress-induced Ca2+ transients recorded in G.
timing [30]. The first analyses of plant gene regulation margarita [18] suggests that fungi first perceived the
showed that Enod11, a M. truncatula nodulin expressed in ‘plantish’ strigolactones as natural xenobiotic compounds.
legume roots during early nodulation, was also upregu- It will be extremely interesting to understand whether
lated in response to diffusible fungal signals [31]. In this other plant-interacting fungi (including pathogens) have
case, the experimental setup did not allow a precise timing analogous responses.
of this response, but a later work [32] showed that 30 hours We can develop similar speculations about ‘fungish’ sig-
of treatment with GSE triggered Enod11 expression. On a nals: fungi produce chitin for a structural function, but the
longer time frame, the perception of diffusible fungal sig- host plant interprets chitin as a signal. Moreover, a more
nals induces reallocation of sugars within the plant, with complex picture surfaces in this case. First, AM fungi pos-
the accumulation of starch in the root system [33]. The sess several chitin synthases (according to [20,39]), possibly
most recent studies identified secreted molecules that are related to the different arrangement of chitin chains in the
supposed to play a role in fungal signaling to the host plant. thick, layered wall of spores or the thin, loose walls of
These include LCOs [32] and COs [19] (Figure 2). These arbuscule branches [40,41]. Which of these enzymes are
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responsible for CO and LCO biosynthesis? Can we compare spores of R. irregularis or G. margarita causes an increase
the long-chain chitin fibrils present in fungal walls with the in the production of short-chain COs, which in turn trigger
short (probably diffusible) COs that are recognized as a stronger Ca2+ spiking response in the root epidermis
MAMPs by LysM receptors [42]? How can chitin-based [19]. This chemical dialogue proves that, at this point in
molecules elicit both symbiotic (e.g., nuclear calcium spik- their long co-evolution, plants and glomeromycetes have
ing) and defense responses (e.g., expression of pathogene- learnt to understand each other.
sis-related proteins) as expected in the innate immune
response [43]? Replies to these questions are expected Acknowledgments
from the ongoing characterization of the plant receptor Research quoted in this report has been funded by the Projects of
and receptor-like protein families, which are predicted to National Interest (PRIN) Project PRO-ROOT. The authors are grateful to
bind chitin-based molecules [44], and from a deeper bio- Dr Jennifer Mach for revising the text.
chemical characterization of fungal and plant bioactive
molecules [45]. References
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