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.
Highlights
In terrestrial ecosystems most plant species live in mutualistic symbioses with nutrientdelivering arbuscular mycorrhizal (AM) fungi
The iron-phytosiderophore transporter yellow stripe 1 (YS1) localizes to the plasmamembrane (PM) of rhizodermal cells (Supplementary Fig. 1a)[26], whereas the Mn and Cd transporter NRAMP-type metal cation transporter 5 (NRAMP5) polarly resides within the distal membrane (EDPM, Supplementary Fig. 1b) and CASP1 within the Casparian Strip subdomain (CSD, Supplementary Fig. 1b) of endo- and exodermal cells, respectively[27,28]
Maize PT629 belongs to the group of conserved symbiotic phosphate transporters that reside within the peri-arbuscular membrane (PAM) surrounding arbuscular fine branches but are absent from other membranes (Supplementary Fig. 1c)[7,9] and serves as an excellent marker for the PAM subdomain[30]
Summary
In terrestrial ecosystems most plant species live in mutualistic symbioses with nutrientdelivering arbuscular mycorrhizal (AM) fungi. 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. Arbuscule formation is accompanied by massive de novo synthesis of the plant peri-arbuscular membrane (PAM) that envelops the fungal structure throughout its life span. At the whole root level, arbuscule development occurs nonsynchronously, with the simultaneous presence of all different stages from initiation to collapse Storage bodies such as vesicles and spores increase over time as the fungus assimilates C and reaches the completion of the fungal life cycle[13,14]. To identify putative PAM-specific signaling proteins from Rhizophagus irregularis colonized roots, we performed an innovative membrane proteome analysis combined with characterization of the transcriptome of laser-dissected arbusculated cells. Our results suggest a role for ARK1 in signaling at the PAM and propose ARK1 function to be essential for the support of fungal fitness
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