Differently from model fungi (Neurospora,
Aspergillus) and plants (Arabidopsis), the
genetics of arbuscular mycorrhizas, intended
as the sum of interacting plants and fungi, is
therefore a very recent domain of science. Parniske (2004) was one of the first to use the term
genetics in his highly quoted review “Molecular
genetics of the arbuscular mycorrhizal symbiosis.”
In this context, the aim of this chapter is to
provide a review of the multiple interactions
that are included in the term “arbuscular
mycorrhizas” and present an updated view of
our knowledge on the molecular genetics of
AMs, covering the genomes of AM fungi, the
cellular and molecular responses of the host
plant, as well as the fungal and plant natural
variation that contributes to the outcome of
this fascinating interaction.
II. A New Look at the Interacting
Partners: From Two to Many
Arbuscular mycorrhizas (AMs) are traditionally described as the symbiosis resulting from
the interaction between the roots of land plants
and soil fungi. Even if AM host plants can
survive if deprived of their fungal symbionts,
this condition is virtually unknown in natural
ecosystems, where AM fungi are associated as
helper microorganisms in most of the environments so far investigated (Davison et al. 2015,
2018). On the other hand, AM fungi are still
considered to be unculturable in the absence
of their host: being auxotrophic for lipids
(Jiang et al. 2017; Luginbuehl et al. 2017; Keymer et al. 2017), they strictly depend on their
green hosts for growth and reproduction, which
gives them the status of obligate biotrophs.
From an evolutionary point of view, the ecological success of AM fungi demonstrates that the
advantages of such a strict association with
plants have overcome the risks arising from
the loss of saprotrophic capabilities (Bonfante
and Genre 2010). Recent findings have however
demonstrated that the interaction is more complex than a one-to-one relationship, since roots
may simultaneously host many AM fungi and
also other microbes. In addition to the Glomeromycotina, some members of the related subphylum of Mucoromycotina (Spatafora et al.
2016) have been demonstrated to colonize
early-diverging plants, i.e. liverworts and hornworts, and lycophytes (Bidartondo et al. 2011;
Desiro ` et al. 2013; Rimington et al. 2015). In
addition, a typology of AM fungi, usually identified as Glomus tenuis (the fine endophyte),
has been recently suggested to be related with
the Mucoromycotina (Orchard et al. 2017),
broadening therefore the taxonomic spectrum
of aseptate fungi which colonize land plants.
The colonization process of AM fungi
belonging to the Glomeromycotina has been
described in detail by using light and electron
microscopy (Bonfante 2018), while more recent
information is based on the use of in vivo confocal microscopy (McLean et al. 2017; Lanfranco et al. 2018; Pimprikar and Gutjahr
2018). By contrast, the colonization processes
by Mucoromycotina are still to be defined:
these fungi may establish different interactions
with plants; some of them also establish ectomycorrhizas (Fassi et al. 1969) and have been
detected mostly by using molecular tools, while
morphology suggests that they form characteristic intracellular swellings (Bidartondo et al.
2011). In the light of the hypothesis that G.
tenuis is actually belonging to Mucoromycotina, a few observations dating back to the
1980s described how the cellular features of
these fungi and their interaction with the plant
host are impressively similar to those of Glomeromycotina (Gianinazzi-Pearson et al. 1981).
Since many reports revealed that a single plant
may be simultaneously colonized by both
Mucoromycotina
and
Glomeromycotina
(Desiro ` et al. 2013), it will be crucial to develop
cellular tools to clearly distinguish between the
two fungal subphyla during their growth in
planta. Lastly, many AM fungi host obligate
endobacteria which live inside their cytoplasm
and have an impact on fungal biology (Bonfante and Desiro ` 2017; Salvioli et al. 2016).
The bacteria living in Glomeromycotina
appear to be common to many Mucoromycota,
since related microbes have been detected in
Rhizopus, Mortierella, as well as Endogone species, suggesting that their presence predates the
144
L. Lanfranco et al.
Aspergillus) and plants (Arabidopsis), the
genetics of arbuscular mycorrhizas, intended
as the sum of interacting plants and fungi, is
therefore a very recent domain of science. Parniske (2004) was one of the first to use the term
genetics in his highly quoted review “Molecular
genetics of the arbuscular mycorrhizal symbiosis.”
In this context, the aim of this chapter is to
provide a review of the multiple interactions
that are included in the term “arbuscular
mycorrhizas” and present an updated view of
our knowledge on the molecular genetics of
AMs, covering the genomes of AM fungi, the
cellular and molecular responses of the host
plant, as well as the fungal and plant natural
variation that contributes to the outcome of
this fascinating interaction.
II. A New Look at the Interacting
Partners: From Two to Many
Arbuscular mycorrhizas (AMs) are traditionally described as the symbiosis resulting from
the interaction between the roots of land plants
and soil fungi. Even if AM host plants can
survive if deprived of their fungal symbionts,
this condition is virtually unknown in natural
ecosystems, where AM fungi are associated as
helper microorganisms in most of the environments so far investigated (Davison et al. 2015,
2018). On the other hand, AM fungi are still
considered to be unculturable in the absence
of their host: being auxotrophic for lipids
(Jiang et al. 2017; Luginbuehl et al. 2017; Keymer et al. 2017), they strictly depend on their
green hosts for growth and reproduction, which
gives them the status of obligate biotrophs.
From an evolutionary point of view, the ecological success of AM fungi demonstrates that the
advantages of such a strict association with
plants have overcome the risks arising from
the loss of saprotrophic capabilities (Bonfante
and Genre 2010). Recent findings have however
demonstrated that the interaction is more complex than a one-to-one relationship, since roots
may simultaneously host many AM fungi and
also other microbes. In addition to the Glomeromycotina, some members of the related subphylum of Mucoromycotina (Spatafora et al.
2016) have been demonstrated to colonize
early-diverging plants, i.e. liverworts and hornworts, and lycophytes (Bidartondo et al. 2011;
Desiro ` et al. 2013; Rimington et al. 2015). In
addition, a typology of AM fungi, usually identified as Glomus tenuis (the fine endophyte),
has been recently suggested to be related with
the Mucoromycotina (Orchard et al. 2017),
broadening therefore the taxonomic spectrum
of aseptate fungi which colonize land plants.
The colonization process of AM fungi
belonging to the Glomeromycotina has been
described in detail by using light and electron
microscopy (Bonfante 2018), while more recent
information is based on the use of in vivo confocal microscopy (McLean et al. 2017; Lanfranco et al. 2018; Pimprikar and Gutjahr
2018). By contrast, the colonization processes
by Mucoromycotina are still to be defined:
these fungi may establish different interactions
with plants; some of them also establish ectomycorrhizas (Fassi et al. 1969) and have been
detected mostly by using molecular tools, while
morphology suggests that they form characteristic intracellular swellings (Bidartondo et al.
2011). In the light of the hypothesis that G.
tenuis is actually belonging to Mucoromycotina, a few observations dating back to the
1980s described how the cellular features of
these fungi and their interaction with the plant
host are impressively similar to those of Glomeromycotina (Gianinazzi-Pearson et al. 1981).
Since many reports revealed that a single plant
may be simultaneously colonized by both
Mucoromycotina
and
Glomeromycotina
(Desiro ` et al. 2013), it will be crucial to develop
cellular tools to clearly distinguish between the
two fungal subphyla during their growth in
planta. Lastly, many AM fungi host obligate
endobacteria which live inside their cytoplasm
and have an impact on fungal biology (Bonfante and Desiro ` 2017; Salvioli et al. 2016).
The bacteria living in Glomeromycotina
appear to be common to many Mucoromycota,
since related microbes have been detected in
Rhizopus, Mortierella, as well as Endogone species, suggesting that their presence predates the
144
L. Lanfranco et al.