lining the fungal cell wall (Balestrini and Bonfante 2014), and periarbuscular membrane
(PAM; Harrison 2012), continuous with the
host cell plasmalemma.
The process of arbuscule accommodation
in cortical cells is the most striking feature of
AM development and requires a broad reorganization of the host cells in strict coordination
with fungal development: hyphal penetration
associates with nuclear movement at the center
of the cell (Bonfante 2001), engulfed by a broad
PPA (Genre et al. 2008). This anticipates the
formation of the arbuscule trunk and the PAM
trunk domain (Pumplin and Harrison 2009),
characterized by a set of proteins that is analogous to that of the plasma membrane. Later on,
smaller PPA-like aggregates organize in the
areas where the arbuscule branches and their
associated PAM branch domain develop (Genre
et al. 2008), harboring a specific set of proteins
devoted to nutrient exchange (Pumplin and
Harrison 2009), whose genes are only expressed
during this phase of arbuscule development
(McLean et al. 2017).
The extensive, repeated branching of
arbuscule hyphae requires a very intense membrane synthesis (Pumplin and Harrison 2009)
and a polarized exocytic process that dwarfs
the analogous mechanisms described in outer
cell layers and positions AM-specific membrane proteins in the PAM. An important transcriptional response drives such cellular
changes, and the roles of individual genes are
gradually being revealed (McLean et al. 2017;
Hogekamp et al. 2011; Gaude et al. 2012; Hogekamp and Kuster 2013).
In response to CSSP activation, several
transcription factors are expressed during
either early or later stages of arbuscule formation (Bucher et al. 2014; Luginbuehl and Oldroyd 2017; Die ´dhiou and Diouf 2018; Pimprikar
and Gutjahr 2018), in turn regulating the
expression of genes involved in nutrient transfer, primary and specialized metabolism, membrane and cell wall modifications, secretion,
and signal transduction (Hohnjec et al. 2005;
Gaude et al. 2012; Hogekamp and Kuster 2013;
Handa et al. 2015). The BLUE COPPERBINDING PROTEIN 1 localizes to the peripheral plasma membrane and PAM trunk domain
(Pumplin and Harrison 2009; Pumplin et al.
2012; Ivanov and Harrison 2014). By contrast,
the GRAS-domain transcription factor, RAM1,
is regulated by DELLA proteins and required
for arbuscule branch development (Gobbato
et al. 2013; Park et al. 2015; Rich et al. 2015;
Pimprikar et al. 2016). RAM1 regulates the
expression of exocytic markers such as the
EXO70I subunit of the exocyst complex
(Zhang et al. 2015b). Indeed, several proteins
involved in membrane dynamics are expressed
during the PAM branch domain development,
such as the symbiosis-specific t-SNARE
SYP132A (Huisman et al. 2016; Pan et al.
2016), VAPYRIN, involved in membrane fusion
processes (Feddermann et al. 2010; Pumplin
et al. 2010; Murray et al. 2011), and two
symbiosis-specific v-SNARES of the VAMP721
group (Ivanov et al. 2012).
Other GRAS-domain proteins, such as
RAD1 (Xue et al. 2015) and DIP1 (Yu et al.
2014), play a role in arbuscule development by
interacting with RAM1 and DELLAs, suggesting
the existence of a large transcription factor
complex (Floss et al. 2016). Furthermore,
another GRAS protein, MIG1 (MYCORRHIZAINDUCED GRAS 1), was proposed to control
radial expansion of cortical cells during arbuscule formation and interact with DELLA1 to
regulate AM root development (Heck et al.
2016; Luginbuehl and Oldroyd 2017). AMupregulated transcription factors also include
AP2 (APETALA2)-EREBP, an ethyleneresponsive element binding protein with a role
in arbuscule development (Devers et al. 2013),
and MtERF1, specifically expressed in arbusculated cells and required for arbuscule maturation (Devers et al. 2013).
AM fungi provide the host plant with a
more efficient access to soil mineral nutrients,
in particular phosphate and ammonium. After
absorption, phosphorus (P) and nitrogen (N)
are translocated along the extraradical and
intraradical mycelium in the form of polyphosphate and arginine. From arbuscules, they are
released into the periarbuscular space as phosphate (Javot et al. 2007) and ammonium
(Tanaka and Yano 2005), respectively.
AM fungal exporters for nutrients bound to
the periarbuscular space have not yet been
7 Genetics and Genomics Decipher Partner Biology in Arbuscular Mycorrhizas
155
(PAM; Harrison 2012), continuous with the
host cell plasmalemma.
The process of arbuscule accommodation
in cortical cells is the most striking feature of
AM development and requires a broad reorganization of the host cells in strict coordination
with fungal development: hyphal penetration
associates with nuclear movement at the center
of the cell (Bonfante 2001), engulfed by a broad
PPA (Genre et al. 2008). This anticipates the
formation of the arbuscule trunk and the PAM
trunk domain (Pumplin and Harrison 2009),
characterized by a set of proteins that is analogous to that of the plasma membrane. Later on,
smaller PPA-like aggregates organize in the
areas where the arbuscule branches and their
associated PAM branch domain develop (Genre
et al. 2008), harboring a specific set of proteins
devoted to nutrient exchange (Pumplin and
Harrison 2009), whose genes are only expressed
during this phase of arbuscule development
(McLean et al. 2017).
The extensive, repeated branching of
arbuscule hyphae requires a very intense membrane synthesis (Pumplin and Harrison 2009)
and a polarized exocytic process that dwarfs
the analogous mechanisms described in outer
cell layers and positions AM-specific membrane proteins in the PAM. An important transcriptional response drives such cellular
changes, and the roles of individual genes are
gradually being revealed (McLean et al. 2017;
Hogekamp et al. 2011; Gaude et al. 2012; Hogekamp and Kuster 2013).
In response to CSSP activation, several
transcription factors are expressed during
either early or later stages of arbuscule formation (Bucher et al. 2014; Luginbuehl and Oldroyd 2017; Die ´dhiou and Diouf 2018; Pimprikar
and Gutjahr 2018), in turn regulating the
expression of genes involved in nutrient transfer, primary and specialized metabolism, membrane and cell wall modifications, secretion,
and signal transduction (Hohnjec et al. 2005;
Gaude et al. 2012; Hogekamp and Kuster 2013;
Handa et al. 2015). The BLUE COPPERBINDING PROTEIN 1 localizes to the peripheral plasma membrane and PAM trunk domain
(Pumplin and Harrison 2009; Pumplin et al.
2012; Ivanov and Harrison 2014). By contrast,
the GRAS-domain transcription factor, RAM1,
is regulated by DELLA proteins and required
for arbuscule branch development (Gobbato
et al. 2013; Park et al. 2015; Rich et al. 2015;
Pimprikar et al. 2016). RAM1 regulates the
expression of exocytic markers such as the
EXO70I subunit of the exocyst complex
(Zhang et al. 2015b). Indeed, several proteins
involved in membrane dynamics are expressed
during the PAM branch domain development,
such as the symbiosis-specific t-SNARE
SYP132A (Huisman et al. 2016; Pan et al.
2016), VAPYRIN, involved in membrane fusion
processes (Feddermann et al. 2010; Pumplin
et al. 2010; Murray et al. 2011), and two
symbiosis-specific v-SNARES of the VAMP721
group (Ivanov et al. 2012).
Other GRAS-domain proteins, such as
RAD1 (Xue et al. 2015) and DIP1 (Yu et al.
2014), play a role in arbuscule development by
interacting with RAM1 and DELLAs, suggesting
the existence of a large transcription factor
complex (Floss et al. 2016). Furthermore,
another GRAS protein, MIG1 (MYCORRHIZAINDUCED GRAS 1), was proposed to control
radial expansion of cortical cells during arbuscule formation and interact with DELLA1 to
regulate AM root development (Heck et al.
2016; Luginbuehl and Oldroyd 2017). AMupregulated transcription factors also include
AP2 (APETALA2)-EREBP, an ethyleneresponsive element binding protein with a role
in arbuscule development (Devers et al. 2013),
and MtERF1, specifically expressed in arbusculated cells and required for arbuscule maturation (Devers et al. 2013).
AM fungi provide the host plant with a
more efficient access to soil mineral nutrients,
in particular phosphate and ammonium. After
absorption, phosphorus (P) and nitrogen (N)
are translocated along the extraradical and
intraradical mycelium in the form of polyphosphate and arginine. From arbuscules, they are
released into the periarbuscular space as phosphate (Javot et al. 2007) and ammonium
(Tanaka and Yano 2005), respectively.
AM fungal exporters for nutrients bound to
the periarbuscular space have not yet been
7 Genetics and Genomics Decipher Partner Biology in Arbuscular Mycorrhizas
155