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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.

SUBMITTER: Roth R

PROVIDER: S-EPMC6224560 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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

Roth Ronelle R Chiapello Marco M Montero Héctor H Gehrig Peter P Grossmann Jonas J O'Holleran Kevin K Hartken Denise D Walters Fergus F Yang Shu-Yi SY Hillmer Stefan S Schumacher Karin K Bowden Sarah S Craze Melanie M Wallington Emma J EJ Miyao Akio A Sawers Ruairidh R Martinoia Enrico E Paszkowski Uta U

Nature communications 20181108 1

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 Arbuscul ...[more]

PMID: 30410018

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Project description:How cells control the proper delivery of vesicles and their associated cargo to specific plasma membrane (PM) domains upon internal or external cues is a major question in plant cell biology. A widely held hypothesis is that expansion of plant exocytotic machinery components, such as SNARE proteins, has led to a diversification of exocytotic membrane trafficking pathways to function in specific biological processes. A key biological process that involves the creation of a specialized PM domain is the formation of a host-microbe interface (the peri-arbuscular membrane) in the symbiosis with arbuscular mycorrhizal fungi. We have previously shown that the ability to intracellularly host AM fungi correlates with the evolutionary expansion of both v- (VAMP721d/e) and t-SNARE (SYP132α) proteins, that are essential for arbuscule formation in Medicago truncatula. Here we studied to what extent the symbiotic SNAREs are different from their non-symbiotic family members and whether symbiotic SNAREs define a distinct symbiotic membrane trafficking pathway. We show that all tested SYP1 family proteins, and most of the non-symbiotic VAMP72 members, are able to complement the defect in arbuscule formation upon knock-down/-out of their symbiotic counterparts when expressed at sufficient levels. This functional redundancy is in line with the ability of all tested v- and t-SNARE combinations to form SNARE complexes. Interestingly, the symbiotic t-SNARE SYP132α appeared to occur less in complex with v-SNAREs compared to the non-symbiotic syntaxins in arbuscule-containing cells. This correlated with a preferential localization of SYP132α to functional branches of partially collapsing arbuscules, while non-symbiotic syntaxins accumulate at the degrading parts. Overexpression of VAMP721e caused a shift in SYP132α localization toward the degrading parts, suggesting an influence on its endocytic turn-over. These data indicate that the symbiotic SNAREs do not selectively interact to define a symbiotic vesicle trafficking pathway, but that symbiotic SNARE complexes are more rapidly disassembled resulting in a preferential localization of SYP132α at functional arbuscule branches.

Project description:BackgroundThe arbuscular mycorrhizal (AM) symbiosis consists of a mutualistic relationship between soil fungi and roots of most plant species. This association provides the arbuscular mycorrhizal fungus with sugars while the fungus improves the uptake of water and mineral nutrients in the host plant. Then, the establishment of the arbuscular mycorrhizal (AM) symbiosis requires the fine tuning of host gene expression for recognition and accommodation of the fungal symbiont. In plants, calcium plays a key role as second messenger during developmental processes and responses to environmental stimuli. Even though calcium transients are known to occur in host cells during the AM symbiosis, the decoding of the calcium signal and the molecular events downstream are only poorly understood.ResultsThe expression of seventeen Calcium-dependent Protein Kinase (CPK) genes representative of the four distinct phylogenetic groups of rice CPKs was monitored during the presymbiotic phase of the AM symbiosis. Among them, OsCPK18 and OsCPK4, were found to be transcriptionally activated in response to inoculation with the AM fungus Glomus intraradices. OsCPK18 and OsCPK4 gene expression was also up-regulated by fungal-produced diffusible molecules. Laser microdissection revealed expression of OsCPK18 in cortical cells, and not in epidermal cells of G. intraradices-inoculated rice roots, suggesting a preferential role of this gene in the root cortex. Moreover, a plasma membrane localization of OsCPK18 was observed by transient expression assays of green fluorescent protein-tagged OsCPK18 in onion epidermal cells. We also show that the myristoylation site of the OsCPK18 N-terminus is required for plasma membrane targeting.ConclusionThe rapid activation of OsCPK18 expression in response to AM inoculation, its expression being also induced by fungal-secreted signals, together with the observed plasma membrane localization of OsCPK18, points to a role for OsCPK18 in perception of the AM fungus. The OsCPK18 gene might be considered as a marker for the presymbiotic phase of the symbiotic process. These findings provide a better understanding of the signaling mechanisms operating during the AM symbiosis and will greatly facilitate their molecular dissection.

Project description:Arbuscular mycorrhizal (AM) play an important role in improving plant growth and development. The interaction between phytohormones and AM symbiosis is gradually revealed. Here we examined the effect of Brassinosteroids (BR) on AM symbiosis and discussed the synergistic promotion of plant growth by BR and AM symbiosis. The xylophyta Eucalyptus grandis Hill (E. grandis) was inoculated with AM fungi Rhizoglomus irregularis R197198 (R. irregularis) and treated with different concentrations (0, 1, 10, and 100 nM) of 24-epibrassinolide (24-epiBL) for 6 weeks. With the increase of 24-epiBL concentration, E. grandis growth was firstly promoted and then inhibited, but inoculation with AM fungi alleviated this inhibition. 24-epiBL and R. irregularis colonization significantly improved E. grandis growth and antioxidant system response, and the synergistic effect was the best. Compared with the control group, 24-epiBL treatment significantly increased the mycorrhizal colonization and arbuscular abundance of AM fungi R. irregular in E. grandis roots. The expression of AM symbiosis maker genes was significantly increased by 24-epiBL treatment. Both 24-epiBL treatment and AM colonization upregulated gibberellins (GA) synthesis genes, but no inhibition caused by GA levels was found. 24-epiBL is a kind of synthetic highly active BR. Based on the results of 24-epiBL treatment, we hypothesized that BR actively regulates AM symbiosis regulates AM symbiosis without affecting GA-INSENSITIVE DWARF1 (GID1)-DELLA expression. The synergistic treatment of BR and AM symbiosis can significantly promote the growth and development of plants. IMPORTANCE Brassinosteroids (BR) and Arbuscular mycorrhizas (AM) symbiosis play an important role in improving plant growth and development. Previous studies have shown that there is a complex regulatory network between phytohormones and AM symbiosis. However, the interactions of BR-signaling and AM symbiosis are still poorly understood. Our results suggest that BR actively regulates the colonization and development of AM fungi, and AM fungal colonization can alleviate the inhibition of plant growth caused by excessive BR. In addition, BR actively regulates AM symbiosis, but does not primarily mediate gibberellins-DELLA interaction. The synergistic treatment of BR and AM symbiosis can significantly promote the growth and development of plants. The conclusions of this study provide a reference for phytohormones-AM symbiosis interaction.

Dataset Information

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

Publications

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

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