roots but never on fine lateral roots (Gutjahr
et al. 2009) – and seminal studies of Giovannetti
et al. (1993) and Nagahashi and Douds (1997)
pointing at the presence of wall-associated
hyphopodium-stimulating
signals.
More
recently, one such signal has been identified in
monomeric cutin. This deduction came from
the observation of mutants in ram2 (Gobbato
et al. 2012), a glycerol-3-phosphate acyltransferase that is highly induced by RAM1 during
AM symbiosis (Harrison 2012) and is involved
in the biosynthesis of cutin precursors (Wang
et al. 2012; Vijayakumar et al. 2015). In fact,
root-bound cuticle monomers (Wang et al.
2012) that have also been reported to stimulate
AM hyphal branching (Nagahashi and Douds
2011) are less abundant in ram2 mutants.
Hyphopodium development is followed by
hyphal penetration in the sub-hyphopodial epidermal cell (Genre et al. 2005; Bonfante and
Genre 2010). Intracellular fungal accommodation is the central feature of AM symbiosis, and
plant cells have to change their architecture and
molecular composition in a process referred to
as host cell reprogramming (Do ¨rmann et al.
2014). Epidermal cells reorganize to accommodate the fungal symbiont with precise nuclear
movements, cytoplasm aggregation, and cytoskeleton remodeling. This cellular reorganization allows the assembling of a subcellular
column-shaped structure, the so-called prepenetration apparatus (PPA), that the plant cell
forms in anticipation of fungal infection (Genre
et al. 2005). PPA assembly may require 4–6 h
and starts with the movement of the epidermal
cell nucleus toward the hyphopodium. The
nucleus then moves away from the contact site
and traverses the plant cell vacuole inside a
broad cytoplasmic bridge. The resulting columnar cytoplasmic aggregation includes numerous Golgi stacks, extensive trans-Golgi
network, endoplasmic reticulum, cytoskeleton,
and secretory vesicles (Genre et al. 2005, 2008,
2012). Only at this stage a hyphopodiumderived hypha starts penetrating the epidermal
cell.
Endoplasmic reticulum and Golgi membranes that surround the penetrating hypha
are ideally positioned for the synthesis of the
perifungal membrane, which is believed to be
the main function of the PPA. In fact, intense
exocytic activity and the accumulation of
SNARE and exocyst proteins have been
observed around the penetrating hyphal tip
(Genre et al. 2008, 2012; Ivanov et al. 2012),
alongside the upregulation of the corresponding
genes (Ivanov et al. 2012; Zhang et al. 2015).
PPA formation was shown to be CSSPdependent (Genre et al. 2005; Gutjahr and Parniske 2013), and several GRAS and CAAT-box
transcription factors are active during this stage
(Hogekamp et al. 2011; Hogekamp and Kuster
2013), regulating a large number of genes
(Die ´dhiou and Diouf 2018). MtENOD11 is an
atypical cell wall-associated protein presumed
to limit cross-linking between other wall components (Journet et al. 2001). As such, MtENOD11 expression during AM colonization
may contribute to cell wall plasticity, especially
considering the lack of cell wall-degrading
enzymes in glomeromycotan genomes (Tisserant et al. 2012, 2013). Additional cell wall remodeling enzymes are expressed in roots during
AM colonization: a xyloglucan endotransglycosidase (van Buuren et al. 1999) and cellulose
synthase-like and expansin-like proteins
(Balestrini and Bonfante 2005; Siciliano et al.
2007). Vapyrin, a VAMP-associated protein, is
also expressed during early AM and SNF establishment (Pumplin et al. 2010; Murray et al.
2011).
Penetrating hyphae cross the epidermal cell
lumen strictly following the route traced by the
PPA and reach the root cortex. Overall, prepenetration responses in outer cortical cells
resemble those observed in epidermal cells
(Genre et al. 2008). By contrast, as AM hyphae
reach the inner cortex, a substantial change is
observed in both fungal growth pattern and
host cell responses: the fungus switches from
radial to longitudinal growth, and inner cortical cells develop broad PPA-like structures in
preparation of arbuscule accommodation
(Genre et al. 2008).
Arbuscule accommodation in cortical cells
involves the biogenesis of an extensive apoplastic compartment, the symbiotic interface (Bonfante 2001; Balestrini and Bonfante 2014),
which consists of the periarbuscular space, containing plant cell wall material and directly out154
L. Lanfranco et al.
et al. 2009) – and seminal studies of Giovannetti
et al. (1993) and Nagahashi and Douds (1997)
pointing at the presence of wall-associated
hyphopodium-stimulating
signals.
More
recently, one such signal has been identified in
monomeric cutin. This deduction came from
the observation of mutants in ram2 (Gobbato
et al. 2012), a glycerol-3-phosphate acyltransferase that is highly induced by RAM1 during
AM symbiosis (Harrison 2012) and is involved
in the biosynthesis of cutin precursors (Wang
et al. 2012; Vijayakumar et al. 2015). In fact,
root-bound cuticle monomers (Wang et al.
2012) that have also been reported to stimulate
AM hyphal branching (Nagahashi and Douds
2011) are less abundant in ram2 mutants.
Hyphopodium development is followed by
hyphal penetration in the sub-hyphopodial epidermal cell (Genre et al. 2005; Bonfante and
Genre 2010). Intracellular fungal accommodation is the central feature of AM symbiosis, and
plant cells have to change their architecture and
molecular composition in a process referred to
as host cell reprogramming (Do ¨rmann et al.
2014). Epidermal cells reorganize to accommodate the fungal symbiont with precise nuclear
movements, cytoplasm aggregation, and cytoskeleton remodeling. This cellular reorganization allows the assembling of a subcellular
column-shaped structure, the so-called prepenetration apparatus (PPA), that the plant cell
forms in anticipation of fungal infection (Genre
et al. 2005). PPA assembly may require 4–6 h
and starts with the movement of the epidermal
cell nucleus toward the hyphopodium. The
nucleus then moves away from the contact site
and traverses the plant cell vacuole inside a
broad cytoplasmic bridge. The resulting columnar cytoplasmic aggregation includes numerous Golgi stacks, extensive trans-Golgi
network, endoplasmic reticulum, cytoskeleton,
and secretory vesicles (Genre et al. 2005, 2008,
2012). Only at this stage a hyphopodiumderived hypha starts penetrating the epidermal
cell.
Endoplasmic reticulum and Golgi membranes that surround the penetrating hypha
are ideally positioned for the synthesis of the
perifungal membrane, which is believed to be
the main function of the PPA. In fact, intense
exocytic activity and the accumulation of
SNARE and exocyst proteins have been
observed around the penetrating hyphal tip
(Genre et al. 2008, 2012; Ivanov et al. 2012),
alongside the upregulation of the corresponding
genes (Ivanov et al. 2012; Zhang et al. 2015).
PPA formation was shown to be CSSPdependent (Genre et al. 2005; Gutjahr and Parniske 2013), and several GRAS and CAAT-box
transcription factors are active during this stage
(Hogekamp et al. 2011; Hogekamp and Kuster
2013), regulating a large number of genes
(Die ´dhiou and Diouf 2018). MtENOD11 is an
atypical cell wall-associated protein presumed
to limit cross-linking between other wall components (Journet et al. 2001). As such, MtENOD11 expression during AM colonization
may contribute to cell wall plasticity, especially
considering the lack of cell wall-degrading
enzymes in glomeromycotan genomes (Tisserant et al. 2012, 2013). Additional cell wall remodeling enzymes are expressed in roots during
AM colonization: a xyloglucan endotransglycosidase (van Buuren et al. 1999) and cellulose
synthase-like and expansin-like proteins
(Balestrini and Bonfante 2005; Siciliano et al.
2007). Vapyrin, a VAMP-associated protein, is
also expressed during early AM and SNF establishment (Pumplin et al. 2010; Murray et al.
2011).
Penetrating hyphae cross the epidermal cell
lumen strictly following the route traced by the
PPA and reach the root cortex. Overall, prepenetration responses in outer cortical cells
resemble those observed in epidermal cells
(Genre et al. 2008). By contrast, as AM hyphae
reach the inner cortex, a substantial change is
observed in both fungal growth pattern and
host cell responses: the fungus switches from
radial to longitudinal growth, and inner cortical cells develop broad PPA-like structures in
preparation of arbuscule accommodation
(Genre et al. 2008).
Arbuscule accommodation in cortical cells
involves the biogenesis of an extensive apoplastic compartment, the symbiotic interface (Bonfante 2001; Balestrini and Bonfante 2014),
which consists of the periarbuscular space, containing plant cell wall material and directly out154
L. Lanfranco et al.