Extensin-enriched host cell wall specialization restricts fungal invasion while sustaining symbiosis in the mycoheterotrophic orchid, Gastrodia elata.
TL;DR
The results reveal a structural mechanism enabling a fully mycoheterotrophic orchid to accommodate an invasive fungal symbiont, indicating that spatial compartmentalization of host-fungus interactions represents an important mechanism contributing to symbiotic stability.
Abstract
Background
Fully mycoheterotrophic orchids depend entirely on fungal partners for carbon and mineral nutrition, yet the structural mechanisms that regulate fungal accommodation within host tissues remain poorly understood. This question is particularly relevant in the Gastrodia elata-Armillaria symbiosis, where the fungal partner is a wood-decaying basidiomycete capable of aggressive host colonization and responsible for root rot disease in many tree species. Here, we examined whether host cell wall remodeling and extensin deposition contribute to the establishment and regulation of the host-fungus interface in G. elata tubers.
Results
Ultrastructural analyses revealed extensive host-derived cell wall remodeling during fungal colonization of G. elata tubers, including localized wall thickening and the formation of hypha-encasing wall domains within fungal-colonized cells and adjacent boundary cells. Comprehensive Microarray Polymer Profiling identified extensin epitopes recognized by JIM20 as the most strongly enriched hydroxyproline-rich glycoproteins component following colonization. Immunogold labeling localized extensin-enriched HRGPs specifically to modified host cell walls and interfacial matrices surrounding intracellular hyphae. Quantitative comparison demonstrated that the interfacial matrix surrounding intracellular hyphae was substantially thicker than that reported for arbuscular or typical orchid mycorrhizal associations. Chemical inhibition of HRGPs deposition using 3,4-DHP disrupted interfacial wall formation, resulting in uncontrolled fungal spread into normally restricted tissues, cortical necrosis, and reduced tuber growth.
Conclusions
Our findings demonstrate that extensin-enriched host cell wall remodeling establishes a reinforced symbiotic interface that spatially restricts fungal invasion while maintaining potential routes for nutrient exchange. Our results reveal a structural mechanism enabling a fully mycoheterotrophic orchid to accommodate an invasive fungal symbiont, indicating that spatial compartmentalization of host-fungus interactions represents an important mechanism contributing to symbiotic stability.