identified. By contrast, symbiosis-specific
phosphate importers – PT4 in Medicago truncatula and PT11 in rice (Javot et al. 2007; Pumplin and Harrison 2009; Kobae et al. 2010) –
have been localized to the PAM. M. truncatula
pt4 deletion induces a premature arbuscule collapse and symbiosis abortion (Javot et al. 2007),
suggesting that host cells monitor phosphate
delivery from arbuscules and induce arbuscule
degeneration if it is not sufficient. Similarly,
nitrogen has also proven to act as a signal
supporting arbuscule survival (Javot et al.
2011). Ammonium transporters are transcriptionally induced in mycorrhized roots and
localize in the periarbuscular membrane
(Kobae et al. 2010; Koegel et al. 2013). In fact,
an ammonium transporter 2 family protein
AMT2-3 has been identified in M. truncatula,
whose mutation induces premature arbuscule
degeneration (Yang et al. 2012; BreuillinSessoms et al. 2015). In the same context,
PAM-associated H
+ -ATPases of the MtHA1
family (Krajinski et al. 2014; Hogekamp et al.
2011; Gaude et al. 2012) are believed to generate
the proton gradient required for the import of
different nutrients from the periarbuscular
space.
A few studies have analyzed the molecular
bases of carbon transfer from the host plant to
the AM fungus. The sugar transporter MtST1
was found to be expressed in Medicago truncatula root tissues colonized by AM fungi (Harrison 1996). Radiolabelling studies suggest that
glucose can be absorbed by intraradical but not
extraradical hyphae (Bago et al. 2000; Douds
et al. 2000). Glucose transfer requires the
expression of invertases and sucrose synthases
in mycorrhizal roots, suggesting sucrose as a
possible source of the hexoses delivered to the
fungus. In parallel, a high-affinity monosaccharide transporter (MST2) has been identified in
arbuscules and intraradical hyphae of Rhizophagus irregularis (Helber et al. 2011). Once
the assimilated sugars reach the fungal cytoplasm, they are converted into glycogen and
trehalose and exported to the extraradical
mycelium (Pfeffer et al. 1999).
Even if the main form of carbon storage in
AM fungi is represented by triacylglycerols
(TAGs), extraradical hyphae and fungal spores
are not capable of de novo fatty acid synthesis
(Pfeffer et al. 1999; Gobbato et al. 2013). Indeed,
studies revealed that host plants also provide
fatty acids to AM fungi, likely in the form of
palmitic acid (Wewer et al. 2014). This scenario
is supported by the upregulation of several
genes involved in lipid biosynthesis and secretion in arbusculated cells. They include the
acyl-ACP (acyl carrier protein) thioesterase
FatM and the glycerol-3-phosphate acyltransferase RAM2, both required for the establishment of a functional AM symbiosis (Gobbato
et al. 2013; Luginbuehl et al. 2017). FatM has
been suggested to produce palmitic acid from
palmitoyl-ACP in the chloroplast (Bravo et al.
2017), whereas RAM2 has been shown to preferentially use palmitoyl-coenzyme A as a substrate to produce 2-monopalmitin (Luginbuehl
et al. 2017). Interestingly, RAM1-dependent
expression has been reported for the ABCG
lipid exporters STR and STR2, which localize
to the branch domain of the PAM (Gutjahr et al.
2012; Bravo et al. 2017; Luginbuehl et al. 2017).
The functional lifetime of arbuscules has
been estimated a few days (Kobae and Hata
2010) after which senescence processes are
initiated. Coupled with their non-synchronous
formation, this relatively short time of activity
leads to the coexistence of symbiotic structures
at different stages within the same area of the
root. Arbuscule collapse and degeneration
involves the rapid shrinkage of arbuscule
branches and PAM, including the dismantling
of its associated proteins (Kobae and Hata
2010). Abundant vesicles and endoplasmic
reticulum cisternae persist around the collapsing PAM, alongside peroxisomes, possibly
assisting lipid breakdown or protecting the
host cell from oxidative damage (Pumplin and
Harrison 2009). As senescence proceeds, progressively larger branches and the arbuscule
trunk become septate and collapse, eventually
leading to the disappearance of the arbuscule
from its host cell (Luginbuehl and Oldroyd
2017). The MYB1 transcription factor is
required for the expression of several M. truncatula genes associated with arbuscule collapse.
MYB1 was shown to interact with DELLAs and
NSP1 to form a transcription factor complex
156
L. Lanfranco et al.
phosphate importers – PT4 in Medicago truncatula and PT11 in rice (Javot et al. 2007; Pumplin and Harrison 2009; Kobae et al. 2010) –
have been localized to the PAM. M. truncatula
pt4 deletion induces a premature arbuscule collapse and symbiosis abortion (Javot et al. 2007),
suggesting that host cells monitor phosphate
delivery from arbuscules and induce arbuscule
degeneration if it is not sufficient. Similarly,
nitrogen has also proven to act as a signal
supporting arbuscule survival (Javot et al.
2011). Ammonium transporters are transcriptionally induced in mycorrhized roots and
localize in the periarbuscular membrane
(Kobae et al. 2010; Koegel et al. 2013). In fact,
an ammonium transporter 2 family protein
AMT2-3 has been identified in M. truncatula,
whose mutation induces premature arbuscule
degeneration (Yang et al. 2012; BreuillinSessoms et al. 2015). In the same context,
PAM-associated H
+ -ATPases of the MtHA1
family (Krajinski et al. 2014; Hogekamp et al.
2011; Gaude et al. 2012) are believed to generate
the proton gradient required for the import of
different nutrients from the periarbuscular
space.
A few studies have analyzed the molecular
bases of carbon transfer from the host plant to
the AM fungus. The sugar transporter MtST1
was found to be expressed in Medicago truncatula root tissues colonized by AM fungi (Harrison 1996). Radiolabelling studies suggest that
glucose can be absorbed by intraradical but not
extraradical hyphae (Bago et al. 2000; Douds
et al. 2000). Glucose transfer requires the
expression of invertases and sucrose synthases
in mycorrhizal roots, suggesting sucrose as a
possible source of the hexoses delivered to the
fungus. In parallel, a high-affinity monosaccharide transporter (MST2) has been identified in
arbuscules and intraradical hyphae of Rhizophagus irregularis (Helber et al. 2011). Once
the assimilated sugars reach the fungal cytoplasm, they are converted into glycogen and
trehalose and exported to the extraradical
mycelium (Pfeffer et al. 1999).
Even if the main form of carbon storage in
AM fungi is represented by triacylglycerols
(TAGs), extraradical hyphae and fungal spores
are not capable of de novo fatty acid synthesis
(Pfeffer et al. 1999; Gobbato et al. 2013). Indeed,
studies revealed that host plants also provide
fatty acids to AM fungi, likely in the form of
palmitic acid (Wewer et al. 2014). This scenario
is supported by the upregulation of several
genes involved in lipid biosynthesis and secretion in arbusculated cells. They include the
acyl-ACP (acyl carrier protein) thioesterase
FatM and the glycerol-3-phosphate acyltransferase RAM2, both required for the establishment of a functional AM symbiosis (Gobbato
et al. 2013; Luginbuehl et al. 2017). FatM has
been suggested to produce palmitic acid from
palmitoyl-ACP in the chloroplast (Bravo et al.
2017), whereas RAM2 has been shown to preferentially use palmitoyl-coenzyme A as a substrate to produce 2-monopalmitin (Luginbuehl
et al. 2017). Interestingly, RAM1-dependent
expression has been reported for the ABCG
lipid exporters STR and STR2, which localize
to the branch domain of the PAM (Gutjahr et al.
2012; Bravo et al. 2017; Luginbuehl et al. 2017).
The functional lifetime of arbuscules has
been estimated a few days (Kobae and Hata
2010) after which senescence processes are
initiated. Coupled with their non-synchronous
formation, this relatively short time of activity
leads to the coexistence of symbiotic structures
at different stages within the same area of the
root. Arbuscule collapse and degeneration
involves the rapid shrinkage of arbuscule
branches and PAM, including the dismantling
of its associated proteins (Kobae and Hata
2010). Abundant vesicles and endoplasmic
reticulum cisternae persist around the collapsing PAM, alongside peroxisomes, possibly
assisting lipid breakdown or protecting the
host cell from oxidative damage (Pumplin and
Harrison 2009). As senescence proceeds, progressively larger branches and the arbuscule
trunk become septate and collapse, eventually
leading to the disappearance of the arbuscule
from its host cell (Luginbuehl and Oldroyd
2017). The MYB1 transcription factor is
required for the expression of several M. truncatula genes associated with arbuscule collapse.
MYB1 was shown to interact with DELLAs and
NSP1 to form a transcription factor complex
156
L. Lanfranco et al.