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).