The Allelopathic Effect of the Epiphytic Lichen Physcia alnophila on Biochemical and Growth Processes in the Tissues of Larix gmelinii in the Cryolithozone

Epiphytic lichens are integral to boreal forest ecosystems, yet their allelopathic interactions with host trees, particularly in cryolithozone regions, remain poorly understood. This study elucidates the physiological and biochemical impacts of the epiphytic lichen Physcia alnophila on Larix gmelinii (Gmelin larch), a keystone species in Siberian permafrost forests. By combining dendrochronology, GC–MS metabolomic analysis, and HPLC–ESI–MS/MS analysis, we demonstrate that the lichen’s primary metabolite, atranorin (ATR), systemically migrates from thalli into the host’s cambium, roots, and needles, with root accumulation reaching 36.3 µg g−1 DW. Lichen-colonized trees exhibited severe radial growth inhibition (27%–51% reduction over five years) and suppressed apical growth, despite comparable heights to controls, indicating chronic phytotoxicity. Metabolomic profiling revealed lichen-specific polyols (e.g., arabitol, mannitol) in larch tissues, alongside elevated stress biomarkers (terpenes, sterols, phenolic acids), and significant disruptions to the tricarboxylic acid cycle and oxidative phosphorylation. These metabolic perturbations correlate with reduced monosaccharide availability and impaired energy production, directly linking ATR translocation to growth suppression. L. gmelinii exhibited compensatory responses, including increased fatty acids and arabinogalactan synthesis, suggesting adaptive mechanisms to mitigate lichen-induced stress. Our findings suggest P. alnophila as a biotic stressor that affects tree physiology in extreme climates, with implications for boreal forest resilience. This work provides an insight to the rarely pointed out species interactions, which, when combined with climate change, may alter carbon cycling and forest dynamics in permafrost ecosystems.