Bryophytes as Strong Aluminum Accumulators in Acidic Soils: Cell-Wall Binding and Physiological Tolerance Mechanisms

Bryophytes are key components of acid–soil ecosystems; however, their capacity for aluminum (Al) accumulation and tolerance remains poorly understood. In this study, bryophytes and a limited number of pteridophyte and lichen species were collected from acidic soils of tea plantations and adjacent forest stands in the Caspian region of northern Iran and analyzed. Nearly all bryophyte specimens exhibited Al concentrations above the critical accumulation threshold (1000 µg g−1 DW), with some reaching values exceeding 28,000 µg g−1 DW, confirming their strong accumulation capacity. After Al, iron was the most abundantly accumulated metal (1430–22,800 µg g−1 DW), followed by manganese (100–3100 µg g−1 DW). The sampled lichen species accumulated Al at concentrations between 1063 and 9154 µg g−1 DW, while Al levels in the aerial parts of pteridophytes rarely exceeded the critical threshold; when they did, accumulation occurred predominantly in old and fertile fronds rather than sterile ones. Three field-collected bryophyte species—Barbula unguiculata, Palamocladium euchloron, and Hypnum cupressiforme—were acclimated to laboratory conditions and treated with two Al levels (without or with 150 µM Al, pH 4.0) for 12 weeks. The leafy shoots were analyzed for their antioxidant response, osmolyte accumulation, phenolic metabolism, callose deposition, and carboxylic-acid profile. Histochemical analyses revealed predominant localization of Al in cell walls, associated with enrichment of pectin and uronic acids. These responses were most pronounced in H. cupressiforme, followed by P. euchloron, and least evident in B. unguiculata. Elevated levels of intracellular detoxification compounds—phenolics, flavonoids, and carboxylic acids (tartaric, oxalic, malic, and citric acids)—were detected, again with species-specific differences. Overall, the results reveal that bryophytes employ multiple physiological strategies to tolerate Al toxicity, with substantial interspecific variation. These findings emphasize their ecological significance and provide a foundation for future research on the physiological and evolutionary mechanisms underlying Al tolerance and accumulation in early land plants.