Phytohormone-based signalling
Phytohormones such as SLs and karrikins (KARs) condition pre-symbiosis
rhizosphere communication with AMFs. Arabidopsis thaliana (a
non-mycorrhizal plant) SLs and KARs receptors D14 (Dwarf14) and KAI2
(Karrikin-insensitive 2; rice homolog of D14L) activate downstream
signaling through the MAX2 (More axillary growth 2) E3 ligase. MAX2
targets different members of the SMAX1-LIKE (Suppressor of MAX2-1-like)
family of transcriptional repressors for degradation (Q. Wang, Smith, &
Huang, 2022). The d14l and d3 mutants show impaired AMF
colonization (Gutjahr et al., 2015). Perception of AMF by the rice
α/β-fold hydrolase D14L (Dwarf14-Like; an evolutionary paralogue of D14)
leads to D3 (Dwarf3; a homolog of MAX2)-mediated signaling, stimulating
fungal metabolism, allowing rapid hyphal growth in roots and expanding
colonization. KAI2 functions are conserved in monocots (Meng et al.,
2022). SMAX1 operates downstream of the D14L/D3 receptor to negatively
regulate AMF symbiosis. Rice smax1 mutants show enhanced
expression of SL biosynthesis genes, indicating that SL-KAR crosstalk is
required for efficient AMF symbiosis (Choi et al., 2020).
Gibberellic acid (GA) and the associated GRAS family DELLA TFs mediate
transcriptional reprogramming during arbuscule development. GA binding
to its receptor induces the degradation of DELLA proteins that repress
GA signaling (Fig. 1A). The della mutants of M. truncatula(Floss, Levesque-Tremblay, Park, & Harrison, 2016) and rice (Yu et al.,
2014) exhibit impaired AMF symbiosis. Similarly, the exogenous
application of GA inhibited arbuscule branching in pea roots (El
Ghachtouli, Martin-Tanguy, Paynot, & Gianinazzi, 1996). Expression of
the MIG1 (Mycorrhiza-induced GRAS1) GRAS-type TF, which is a key
regulator of cortical cell expansion, is a prerequisite for arbuscule
development. The expression of dominant-active DELLA proteins rescues
the loss-of-arbuscule phenotype of the mig1 mutants. Hence, MIG1
and DELLA act together to promote cortical radial cell expansion (Fig.
1A) (Heck et al., 2016). The MIG1-DELLA-mediated positive regulation
cascade is fine-tuned by MIG3 (a MIG1 paralogue)-SCL3 (Scarecrow-like 3,
GRAS TF), which acts as a negative regulator of arbuscule development inM. truncatula (Seemann et al., 2022). Salicylic acid (SA) also
regulates root/microbiome interactions in response to nutrient
deficiency (Kim et al., 2022). Rhizobia- and AMF-induced microbial
signals are transduced via nuclear-localized calcium oscillations,
generated by CNGC15 (Cyclic-nucleotide gated channel 15). The
calcium-bound form of calmodulin 2 (holo-CaM2) is required to sustain
prolonged CNGC15-dependent calcium oscillations. An engineered holo-CaM2
enhanced root nodule symbiosis but not arbuscular mycorrhization,
indicating that the holo-CaM2-CNGC15s module is specific to Rhizobial
symbiosis (Del Cerro et al., 2022). Calcium-phytohormone crosstalk
functions alongside bi-directional nutrient exchange to establish
rhizobia/AMF symbioses.
The light-induced GmSTF3/4 (soybean TGACG-motif binding factor 3/4) and
FLOWERING LOCUS T (GmFTs) proteins function as mobile shoot-to-root
signals. CCaMK (calcium- and calmodulin-dependent protein kinase)
mediated phosphorylation of GmSTF3 triggers the formation of a
GmSTF3–GmFT2a complex, which activates the expression of nodule
inception (NIN) and nuclear factor Y (NF-YA1 and NF-YB1) that together
regulate nodule organogenesis. The CCaMK–STF–FT module ensures a
sustained shoot carbon supply (T. Wang et al., 2021). Rhizobial
colonization, which is impaired in della mutants, is tightly
controlled by host-derived GA signals. DELLA proteins promote the
formation of the CCaMK–IPD3 complex. They also interact with NSP2
(Nodulation Signaling Pathway2), enhancing the expression of
Nod-factor-inducible genes that are required for NSP1 binding to the NIN
promoter. In this way, DELLA integration of the IPD3 and NSP1/2 pathways
provides the transcriptional framework for successful root nodulation
(Jin et al., 2016).
While our knowledge of inter-organism ROS signal communication remains
rudimentary, it is evident that the cell-to-cell transmission of ROS
waves and its crosstalk with hormones is a central feature of
communication between the cells of a single organism and between
different organisms (Fichman, Zandalinas, Peck, Luan, & Mittler, 2022).
For example, ROS-dependent auxin production in tomato shoots triggers
systemic signaling that enhances root strigolactone biosynthesis,
promoting AMF symbiosis, and thus increasing orthophosphate (Pi) uptake
and utilization (Zhou et al., 2019). Such studies provide new insights
into potential targets for the manipulation of symbiosis for high
nutrient utilization, particularly under future climate change
scenarios, where plant nutrient accumulation will be increasingly
challenged (Dong, Gruda, Lam, Li, & Duan, 2018; Loladze, 2014).