2015) and does not respond transcriptionally to
AM germinating spore exudates. Together
these results suggest that the karrikin receptor
complex plays a role in symbiotic signaling
even if the involvement of karrikin-like molecules of fungal or plant origin remains to be
investigated (Gutjahr et al. 2015; Waters et al.
2017).
The discovery of a rice and maize Nacetylglucosamine
transporter
(NOPE1)
required for AM signaling and colonization
points to the role of additional diffusible plant
molecules in the activation of pre-symbiotic
fungal reprogramming (Nadal et al. 2017). Elucidating the exact molecular function of NOPE1
and its substrate will shed light on long predicted new molecular actors in AM signaling
(Bonfante and Requena 2011).
Even if fungal receptors for strigolactones
remain unknown (Waters et al. 2017), recent
data suggest the activation of a calciummediated pathway (Moscatiello et al. 2014)
and – intriguingly – the release of presymbiotic fungal signals (Genre et al. 2013).
In fact, AM fungi release water-soluble
molecules collectively known as Myc factors
(mycorrhizal factors) (Bonfante and Genre
2015). Myc factor perception triggers plant
symbiotic responses (Bonfante and Requena
2011) through a Ca
2+
-mediated signal transduction pathway. Responses include transcriptional regulation, starch accumulation in roots,
and lateral root formation (Kosuta et al. 2003,
2008; Ola ´h et al. 2005; Kuhn et al. 2010; Chabaud et al. 2011; Mukherjee and Ane ´ 2011;
Maillet et al. 2011; Genre et al. 2013), overall
preparing the plant to a successful symbiotic
association.
The first evidence of diffusible Myc factors
was found in the exudates of germinated spores
(GSE), which triggered a transient increase in
cytosolic calcium concentration of soybean
cultured cells (Navazio et al. 2007). The GSE
was later shown to contain different chitinrelated oligomers that are responsible for such
plant responses: these include lipo-chito-oligosaccharides (Myc-LCOs; Maillet et al. 2011) and
tetra- and penta-chito-oligosaccharides (MycCOs; Genre et al. 2013).
Myc-LCOs were purified from sterile exudates of mycorrhizal carrot roots and identified
as putative Myc factors by their induction of the
early symbiotic gene MtENOD11 in Medicago
plants. Furthermore, such LCOs stimulate root
hair branching (a typical Nod factor-related
response) in Vicia sativa (Maillet et al. 2011).
In fact, LCOs have a striking structural similarity to rhizobial Nod factors (De ´narie ´ et al.
1996).
Myc-COs have been isolated from distantly
related AM fungi, Rhizophagus irregularis and
Gigaspora rosea (Genre et al. 2013). They are
the most effective elicitors of nuclear Ca
2+
spiking patterns that resemble the irregular spiking
triggered by GSE. Myc-COs are active in both
legumes and non-legumes at very low concentration, down to 10
À8 M (Genre et al. 2013; Sun
et al. 2015), and can be considered as universal
AM-specific elicitors.
1. The Common Symbiotic Signaling Pathway
The study of Myc factor signaling mechanisms
in legumes such as Medicago truncatula and
Lotus japonicus has mostly come as a followup of analogous research on symbiotic nitrogen fixation (SNF; De ´narie ´ and Cullimore 1993;
Maillet et al. 2011). Since the latter evolved
almost 400 million years later than the oldest
known AM-related interactions, it is currently
acknowledged that legumes and rhizobia have
adapted the pre-existing AM signaling pathway
to control the new interaction. Indeed, several
legume mutants that cannot transduce Nod factor signals are equally impaired in the early
development of SNF and AM (Sagan et al.
1995; Catoira et al. 2000; Oldroyd and Downie
2006; Kosuta et al. 2008; Parniske 2008). Once
characterized, the corresponding genes have
been associated in the so-called common symbiotic signaling pathway (CSSP), a signal transduction pathway that mediates AM and – in
legumes – SNF establishment (Oldroyd 2013;
Gobbato 2015). Phylogenetic studies have
demonstrated that key CSSP genes are present
throughout eudicots, monocots, basal land
plants, and charophytes (Banba et al. 2008;
Gutjahr et al. 2008; Chen et al. 2009; Wang
et al. 2010; Delaux et al. 2013, 2015).
The CSSP mediates fungal and bacterial
signal transduction from plasma membrane7 Genetics and Genomics Decipher Partner Biology in Arbuscular Mycorrhizas
151
AM germinating spore exudates. Together
these results suggest that the karrikin receptor
complex plays a role in symbiotic signaling
even if the involvement of karrikin-like molecules of fungal or plant origin remains to be
investigated (Gutjahr et al. 2015; Waters et al.
2017).
The discovery of a rice and maize Nacetylglucosamine
transporter
(NOPE1)
required for AM signaling and colonization
points to the role of additional diffusible plant
molecules in the activation of pre-symbiotic
fungal reprogramming (Nadal et al. 2017). Elucidating the exact molecular function of NOPE1
and its substrate will shed light on long predicted new molecular actors in AM signaling
(Bonfante and Requena 2011).
Even if fungal receptors for strigolactones
remain unknown (Waters et al. 2017), recent
data suggest the activation of a calciummediated pathway (Moscatiello et al. 2014)
and – intriguingly – the release of presymbiotic fungal signals (Genre et al. 2013).
In fact, AM fungi release water-soluble
molecules collectively known as Myc factors
(mycorrhizal factors) (Bonfante and Genre
2015). Myc factor perception triggers plant
symbiotic responses (Bonfante and Requena
2011) through a Ca
2+
-mediated signal transduction pathway. Responses include transcriptional regulation, starch accumulation in roots,
and lateral root formation (Kosuta et al. 2003,
2008; Ola ´h et al. 2005; Kuhn et al. 2010; Chabaud et al. 2011; Mukherjee and Ane ´ 2011;
Maillet et al. 2011; Genre et al. 2013), overall
preparing the plant to a successful symbiotic
association.
The first evidence of diffusible Myc factors
was found in the exudates of germinated spores
(GSE), which triggered a transient increase in
cytosolic calcium concentration of soybean
cultured cells (Navazio et al. 2007). The GSE
was later shown to contain different chitinrelated oligomers that are responsible for such
plant responses: these include lipo-chito-oligosaccharides (Myc-LCOs; Maillet et al. 2011) and
tetra- and penta-chito-oligosaccharides (MycCOs; Genre et al. 2013).
Myc-LCOs were purified from sterile exudates of mycorrhizal carrot roots and identified
as putative Myc factors by their induction of the
early symbiotic gene MtENOD11 in Medicago
plants. Furthermore, such LCOs stimulate root
hair branching (a typical Nod factor-related
response) in Vicia sativa (Maillet et al. 2011).
In fact, LCOs have a striking structural similarity to rhizobial Nod factors (De ´narie ´ et al.
1996).
Myc-COs have been isolated from distantly
related AM fungi, Rhizophagus irregularis and
Gigaspora rosea (Genre et al. 2013). They are
the most effective elicitors of nuclear Ca
2+
spiking patterns that resemble the irregular spiking
triggered by GSE. Myc-COs are active in both
legumes and non-legumes at very low concentration, down to 10
À8 M (Genre et al. 2013; Sun
et al. 2015), and can be considered as universal
AM-specific elicitors.
1. The Common Symbiotic Signaling Pathway
The study of Myc factor signaling mechanisms
in legumes such as Medicago truncatula and
Lotus japonicus has mostly come as a followup of analogous research on symbiotic nitrogen fixation (SNF; De ´narie ´ and Cullimore 1993;
Maillet et al. 2011). Since the latter evolved
almost 400 million years later than the oldest
known AM-related interactions, it is currently
acknowledged that legumes and rhizobia have
adapted the pre-existing AM signaling pathway
to control the new interaction. Indeed, several
legume mutants that cannot transduce Nod factor signals are equally impaired in the early
development of SNF and AM (Sagan et al.
1995; Catoira et al. 2000; Oldroyd and Downie
2006; Kosuta et al. 2008; Parniske 2008). Once
characterized, the corresponding genes have
been associated in the so-called common symbiotic signaling pathway (CSSP), a signal transduction pathway that mediates AM and – in
legumes – SNF establishment (Oldroyd 2013;
Gobbato 2015). Phylogenetic studies have
demonstrated that key CSSP genes are present
throughout eudicots, monocots, basal land
plants, and charophytes (Banba et al. 2008;
Gutjahr et al. 2008; Chen et al. 2009; Wang
et al. 2010; Delaux et al. 2013, 2015).
The CSSP mediates fungal and bacterial
signal transduction from plasma membrane7 Genetics and Genomics Decipher Partner Biology in Arbuscular Mycorrhizas
151