bound receptors into the nucleus, where gene
expression is modulated. The LRR receptor-like
kinase LjSYMRK is believed to interact with so
far unidentified Myc factor receptor(s) (Gobbato 2015). In its cytoplasmic domain, the M.
truncatula homolog of LjSYMRK, MtDMI2,
interacts with a 3-hydroxy-3-methylglutarylCoA reductase (HMGR1) involved in mevalonate synthesis (Kevei et al. 2007). Mevalonate is
therefore believed to be produced in the vicinity of the cytoplasmic face of the plasma membrane (Venkateshwaran et al. 2015) and acts as
an intermediate messenger. The following
group of known CSSP proteins are localized
on the nuclear envelope. They include three
nucleoporins (NUP85, NUP133, and NENA;
Kanamori et al. 2006; Saito et al. 2007; Groth
et al. 2010), the ATP-powered Ca
2+ pump
(MtMCA8; Capoen et al. 2011), a cyclic
nucleotide-gated channel (MtCNGC15s; Charpentier et al. 2016), and the cationic channels
LjCASTOR (MtDMI1) and LjPOLLUX (Ane ´
et al. 2004; Charpentier et al. 2008). Nucleoporins were proposed to be involved in the targeting of CSSP channels and pumps to the inner
nuclear membrane (Kanamori et al. 2006; Saito
et al. 2007; Groth et al. 2010), whereas the
latter are directly involved in generating
nuclear Ca
2+ spiking: a series of repeated oscillations in Ca
2+ concentration (Ane ´ et al. 2004;
Imaizumi-Anraku et al. 2005; Capoen et al.
2011; Venkateshwaran et al. 2012). In more
detail, CNGC15 channels are predicted to
release Ca
2+ from the nuclear envelope lumen,
a release compensated by the opposite flow of
K
+ ions through CASTOR (Parniske 2008; Venkateshwaran et al. 2012). MCA8 activity contributes to the restoration of Ca
2+ concentration
at the end of each peak.
The last group of CSSP proteins resides in
the nucleoplasm: Ca
2+ spiking is supposed to
activate a Ca
2+
- and calmodulin-dependent
protein kinase (LjCCaMK; Miller et al. 2013),
which in turn phosphorylates its interacting
partner, CYCLOPS (Yano et al. 2008). Activated
CYCLOPS regulates gene expression either
directly or through the action of other transcription factors like NSP1, NSP2, and RAM1
(Oldroyd 2013). Importantly, the identified
CSSP actors only constitute subsets of the
whole transduction pathway, leaving gaps that
still hamper the definition of a complete picture
of the signaling process (Genre and Russo
2016).
Beside canonical CSSP members, recent
evidence showed a role for additional players:
the Nod factor receptor MtLYK3 (LjNFR1) –
but not MtNFP (LjNFR5) – is required for
AM-specific activation of the CSSP and
subsequent colonization (Miyata et al. 2014;
Zhang et al. 2015). Furthermore, Myc-LCOinduced responses were shown to be NFPdependent, indicating the involvement of this
receptor in both Nod- and Myc-LCO perception
(Op den Camp et al. 2011). Although nfp
mutants exhibit normal Ca
2+ spiking and AM
colonization (Maillet et al. 2011; Genre et al.
2013; Zhang et al. 2015), such mutants do not
display nuclear Ca
2+ spiking in response to
Myc-LCOs (Sun et al. 2015). Taken together,
these findings point to possible partial overlaps
and crosstalks between Nod and Myc signaling
in legumes.
By contrast, studies in non-legumes are
opening new perspectives in the characterization of AM-specific CSSP activation. A dual role
has been demonstrated for the rice receptorlike kinase CERK1. This gene is required for
both chitin-triggered immunity and AM colonization (Miya et al. 2007; Shimizu et al. 2010).
In defense-related chitin perception, OsCERK1
acts with its LysM co-receptor OsCEBiP (Kaku
et al. 2006; Shimizu et al. 2010), but OsCEBiP is
not required for AM symbiosis (Miyata et al.
2014), suggesting the involvement of additional
players in Myc factor perception. In short,
legumes and non-legumes appear to differ in
their perception of Myc-LCO and Myc-CO signals, outlining a more complex scenario, where
different plant species respond to different
components in the mix of signals produced by
AM fungi (Sun et al. 2015).
Since CSSP activation is required for the
transcription of genes involved in both AM
and SNF, it is not fully clear how this pathway
can discriminate between the two signals and
induce different developmental programs. Evidence points to a differential regulation of
CCaMK by Ca
2+ and calmodulin. In fact, the
CaM-binding domain is redundant for AM but
152
L. Lanfranco et al.
expression is modulated. The LRR receptor-like
kinase LjSYMRK is believed to interact with so
far unidentified Myc factor receptor(s) (Gobbato 2015). In its cytoplasmic domain, the M.
truncatula homolog of LjSYMRK, MtDMI2,
interacts with a 3-hydroxy-3-methylglutarylCoA reductase (HMGR1) involved in mevalonate synthesis (Kevei et al. 2007). Mevalonate is
therefore believed to be produced in the vicinity of the cytoplasmic face of the plasma membrane (Venkateshwaran et al. 2015) and acts as
an intermediate messenger. The following
group of known CSSP proteins are localized
on the nuclear envelope. They include three
nucleoporins (NUP85, NUP133, and NENA;
Kanamori et al. 2006; Saito et al. 2007; Groth
et al. 2010), the ATP-powered Ca
2+ pump
(MtMCA8; Capoen et al. 2011), a cyclic
nucleotide-gated channel (MtCNGC15s; Charpentier et al. 2016), and the cationic channels
LjCASTOR (MtDMI1) and LjPOLLUX (Ane ´
et al. 2004; Charpentier et al. 2008). Nucleoporins were proposed to be involved in the targeting of CSSP channels and pumps to the inner
nuclear membrane (Kanamori et al. 2006; Saito
et al. 2007; Groth et al. 2010), whereas the
latter are directly involved in generating
nuclear Ca
2+ spiking: a series of repeated oscillations in Ca
2+ concentration (Ane ´ et al. 2004;
Imaizumi-Anraku et al. 2005; Capoen et al.
2011; Venkateshwaran et al. 2012). In more
detail, CNGC15 channels are predicted to
release Ca
2+ from the nuclear envelope lumen,
a release compensated by the opposite flow of
K
+ ions through CASTOR (Parniske 2008; Venkateshwaran et al. 2012). MCA8 activity contributes to the restoration of Ca
2+ concentration
at the end of each peak.
The last group of CSSP proteins resides in
the nucleoplasm: Ca
2+ spiking is supposed to
activate a Ca
2+
- and calmodulin-dependent
protein kinase (LjCCaMK; Miller et al. 2013),
which in turn phosphorylates its interacting
partner, CYCLOPS (Yano et al. 2008). Activated
CYCLOPS regulates gene expression either
directly or through the action of other transcription factors like NSP1, NSP2, and RAM1
(Oldroyd 2013). Importantly, the identified
CSSP actors only constitute subsets of the
whole transduction pathway, leaving gaps that
still hamper the definition of a complete picture
of the signaling process (Genre and Russo
2016).
Beside canonical CSSP members, recent
evidence showed a role for additional players:
the Nod factor receptor MtLYK3 (LjNFR1) –
but not MtNFP (LjNFR5) – is required for
AM-specific activation of the CSSP and
subsequent colonization (Miyata et al. 2014;
Zhang et al. 2015). Furthermore, Myc-LCOinduced responses were shown to be NFPdependent, indicating the involvement of this
receptor in both Nod- and Myc-LCO perception
(Op den Camp et al. 2011). Although nfp
mutants exhibit normal Ca
2+ spiking and AM
colonization (Maillet et al. 2011; Genre et al.
2013; Zhang et al. 2015), such mutants do not
display nuclear Ca
2+ spiking in response to
Myc-LCOs (Sun et al. 2015). Taken together,
these findings point to possible partial overlaps
and crosstalks between Nod and Myc signaling
in legumes.
By contrast, studies in non-legumes are
opening new perspectives in the characterization of AM-specific CSSP activation. A dual role
has been demonstrated for the rice receptorlike kinase CERK1. This gene is required for
both chitin-triggered immunity and AM colonization (Miya et al. 2007; Shimizu et al. 2010).
In defense-related chitin perception, OsCERK1
acts with its LysM co-receptor OsCEBiP (Kaku
et al. 2006; Shimizu et al. 2010), but OsCEBiP is
not required for AM symbiosis (Miyata et al.
2014), suggesting the involvement of additional
players in Myc factor perception. In short,
legumes and non-legumes appear to differ in
their perception of Myc-LCO and Myc-CO signals, outlining a more complex scenario, where
different plant species respond to different
components in the mix of signals produced by
AM fungi (Sun et al. 2015).
Since CSSP activation is required for the
transcription of genes involved in both AM
and SNF, it is not fully clear how this pathway
can discriminate between the two signals and
induce different developmental programs. Evidence points to a differential regulation of
CCaMK by Ca
2+ and calmodulin. In fact, the
CaM-binding domain is redundant for AM but
152
L. Lanfranco et al.