A rice Serine/Threonine receptor-like kinase regulates arbuscular mycorrhizal symbiosis at the peri-arbuscular membrane

Abstract

In terrestrial ecosystems most plant species live in mutualistic symbioses with nutrient-delivering arbuscular mycorrhizal (AM) fungi. Establishment of AM symbioses includes transient, intracellular formation of fungal feeding structures, the arbuscules. A plant-derived peri-arbuscular membrane (PAM) surrounds the arbuscules, mediating reciprocal nutrient exchange. Signaling at the PAM must be well coordinated to achieve this dynamic cellular intimacy. Here, we identify the PAM-specific Arbuscular Receptor-like Kinase 1 (ARK1) from maize and rice to condition sustained AM symbiosis. Mutation of rice ARK1 causes a significant reduction in vesicles, the fungal storage structures, and a concomitant reduction in overall root colonization by the AM fungus Rhizophagus irregularis. Arbuscules, although less frequent in the ark1 mutant, are morphologically normal. Co-cultivation with wild-type plants restores vesicle and spore formation, suggesting ARK1 function is required for the completion of the fungal life-cycle, thereby defining a functional stage, post arbuscule development.

Receptor-Like Kinases Sustain Symbiotic Scrutiny

“…Beyond RNS, the role of EPR3-type LysM-RLKs remains enigmatic, as recent phylogenetic and phylogenomic surveys of LysM-RLKs identified LjEPR3/MtLYK10 clade to be conserved in plant species capable of engaging in AMS, suggesting a possible function during AMS (Bravo et al, 2016;Buendia et al, 2018). The likely rice orthologue, OsLYK1, is induced by AMF and expressed in arbusculated cells, but oslyk1 mutants showed no defects in AMS (Roth et al, 2018). Thus, whether the various mechanisms of symbiotic scrutiny that are described for RNS also exist in AMS remain unknown.…”

“…Apart from vesicle trafficking and nutrient exchange in sustaining AM symbiosis development (as reviewed in Harrison and Ivanov, 2017; Chiu and Paszkowski, 2019), we now also appreciate the existence of RLK-mediated signalling in symbiosis maintenance via novel and unknown signalling cascades at the peri-arbuscular membrane (PAM). Rice ARBUSCLE RLK1 (OsARK1)/ Medicago KINASE3 (KIN3) encodes a serine/threonine RLK present in AM host species (Bravo et al, 2016;Roth et al, 2018). Localised to the PAM, OsARK1 controls processes post arbuscule development, and is required for sustaining fungal fitness during progressing symbiosis as reflected by the compromised vesicle formation in Osark1 mutants (Roth et al, 2018).…”

“…Rice ARBUSCLE RLK1 (OsARK1)/ Medicago KINASE3 (KIN3) encodes a serine/threonine RLK present in AM host species (Bravo et al, 2016;Roth et al, 2018). Localised to the PAM, OsARK1 controls processes post arbuscule development, and is required for sustaining fungal fitness during progressing symbiosis as reflected by the compromised vesicle formation in Osark1 mutants (Roth et al, 2018). Vesicles emerge as lipid storage bodies and could be crucial for subsequent rounds of infection affected in Osark1 mutants.…”

“…Vesicles emerge as lipid storage bodies and could be crucial for subsequent rounds of infection affected in Osark1 mutants. Interestingly, the Osark1 phenotype is rescued in the presence of a common mycorrhizal network where AMF are supported by wild-type plants, suggesting that OsARK1 is required for fungal vigour (Roth et al, 2018). The OsARK1 signalling mechanisms are still unknown.…”

A Flexible, Low-Cost Hydroponic Co-Cultivation System for Studying Arbuscular Mycorrhiza Symbiosis

“…Under nonaerated conditions, root length colonization was lower and reached about 20% ( Figures 6B, C). We also examined whether the AM-marker genes PT11 and ARK (Gutjahr et al, 2008;Yang et al, 2012;Roth et al, 2018) are normally expressed in hydroponics. Their transcripts accumulated to high levels in colonized roots as compared to non-colonized roots and their transcript accumulation was slightly affected by aeration ( Figure 6C).…”