Molecular Crosstalk Underlying Pre-Colonization Signaling and Recognition in Ectomycorrhizal Symbiosis

Ectomycorrhizal (ECM) symbiosis is a fundamental mutualism crucial for forest eco-system health. Its establishment is governed by sophisticated molecular dialogue preceding physical colonization. This review synthesizes this pre-colonization crosstalk, beginning with reciprocal signal exchange where root exudates trigger fungal growth, and fungal lipochitooligosaccharides activate host symbiotic programming, often via the common symbiosis pathway. Successful colonization requires fungi to navigate plant immunity. They employ effectors, notably mycorrhiza-induced small secreted proteins (MiSSPs), to suppress defenses, e.g., by stabilizing jasmonate signaling repressors or inhibiting apoplastic proteases, establishing a localized “mycorrhiza-induced resistance.” Concurrent structural adaptations, including fungal hydrophobins, expansins, and cell wall-modifying enzymes like chitin deacetylase, facilitate adhesion and apoplastic penetration. While this sequential model integrates immune suppression with structural remodeling, current understanding is predominantly derived from a limited set of model systems. Significant knowledge gaps persist regarding species-specific determinants in non-model fungi and hosts, the influence of environmental variability and microbiome interactions, and methodological challenges in capturing early signaling in situ. This review’s main contributions are: providing a synthesized sequential model of molecular crosstalk; elucidating the dual fungal strategy of simultaneous immune suppression and structural remodeling; and identifying crucial knowledge gaps regarding non-model systems and species-specific determinants, establishing a research roadmap with implications for forest management and ecosystem sustainability.