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.

Cellulose is the strongest cell wall polymer defining plant cell shape and growth, and the most abundant biopolymer on the Earth. Its synthesis by the plasma membrane (PM)-localized cellulose synthase complexes (CSCs) depends on surrounding lipids that establish the membrane microenvironment in which CSCs work and form vesicles delivering and removing CSCs to and from the PM by exo- and endocytosis. The role of exact lipid molecular species in these processes is poorly understood. In the present work we used hypocotyls of etiolated wild-type Col-0 and mutant ixr1-1 Arabidopsis thaliana seedlings grown with or without isoxaben, a specific cellulose synthesis inhibitor, as a model to reveal lipid molecular species associated with cellulose biosynthesis. Different lipid classes were separated by thin-layer chromatography (TLC) and their molecular species were analyzed by liquid chromatography–triple quadrupole tandem mass spectrometry (LC-QqQ-MS/MS). A total of 250 lipid molecular species were identified. Col-0 plants maintained stable levels of membrane glycerophospholipids but displayed significant remodeling of their acyl chains. In the presence of isoxaben, they accumulated three times more phosphatidic acids, a hallmark of a stress response. The isoxaben-resistant mutant ixr1-1 was characterized by a higher relative content of phosphatidylethanolamines, potentially rendering membranes more labile, as well as plastid galactolipids, which accumulated under isoxaben treatment. The multifaceted effects of isoxaben, including its impact on endomembrane lipids, suggest that it has additional binding sites beyond CSC.

Epiphytic lichens are naturally subjected to highly fluctuating light and must protect their algal symbionts from harmful short wavelengths while facilitating efficient photosynthesis. Confocal microscopy confirmed that the upper cortices of Hypogymnia physodes and H. bitteri thalli contained colorless secondary metabolites atranorin and chloroatranorin, which were able to protect lichens against excessive UV and blue–violet radiation in two ways. The first way screens algae through visible light reflection; the second way is realized through the absorption of UV-A and blue–violet radiation and fluorescence emission in the yellow–green spectrum. Acetone rinsing removed atranorin and chloroatranorin crystals from the cortical surface, thus reducing the reflectance of both H. physodes and H. bitteri. Nevertheless, fluorescence in H. physodes remained largely unaffected due to the deep-layer localization of atranorin within the upper cortex. However, melanized H. bitteri exhibited weak fluorescence either before or after acetone rinsing, despite containing atranorin and chloroatranorin at levels comparable to H. physodes. Within the heavily melanized lower cortical layer of H. bitteri, young areas contained significant amounts of atranorin and chloroatranorin. A reduction in their content resulted in a compensatory enhancement of non-photochemical quenching in algae. This phenomenon suggests that atranorin and chloroatranorin contribute to the photoprotection of lichens in yet another way through light reflectance and through fluorescence in a photosynthetically safe manner.