Identification of a Hydrolyzable Tannin, Oenothein B, as an Aluminum-Detoxifying Ligand in a Highly Aluminum-Resistant Tree, Eucalyptus camaldulensis

Abstract

Eucalyptus camaldulensis is a tree species in the Myrtaceae that exhibits extremely high resistance to aluminum (Al). To explore a novel mechanism of Al resistance in plants, we examined the Al-binding ligands in roots and their role in Al resistance of E. camaldulensis. We identified a novel type of Al-binding ligand, oenothein B, which is a dimeric hydrolyzable tannin with many adjacent phenolic hydroxyl groups. Oenothein B was isolated from root extracts of E. camaldulensis by reverse-phase high-performance liquid chromatography and identified by nuclear magnetic resonance and mass spectrometry analyses. Oenothein B formed water-soluble or -insoluble complexes with Al depending on the ratio of oenothein B to Al and could bind at least four Al ions per molecule. In a bioassay using Arabidopsis (Arabidopsis thaliana), Al-induced inhibition of root elongation was completely alleviated by treatment with exogenous oenothein B, which indicated the capability of oenothein B to detoxify Al. In roots of E. camaldulensis, Al exposure enhanced the accumulation of oenothein B, especially in EDTA-extractable forms, which likely formed complexes with Al. Oenothein B was localized mostly in the root symplast, in which a considerable amount of Al accumulated. In contrast, oenothein B was not detected in three Al-sensitive species, comprising the Myrtaceae tree Melaleuca bracteata, Populus nigra, and Arabidopsis. Oenothein B content in roots of five tree species was correlated with their Al resistance. Taken together, these results suggest that internal detoxification of Al by the formation of complexes with oenothein B in roots likely contributes to the high Al resistance of E. camaldulensis.Aluminum (Al) toxicity is a major factor that limits plant growth in acid soils and affects approximately 30% of the total ice-free land area of the world (von Uexküll and Mutert, 1995). Although Al in soils exist in nonphytotoxic silicate or oxide forms at neutral pH, it is solubilized into a phytotoxic form, mainly as Al 3+

TRICHOME BIREFRINGENCE-LIKE27 Affects Aluminum Sensitivity by Modulating the O-Acetylation of Xyloglucan and Aluminum-Binding Capacity in Arabidopsis

“…Once the threshold of 67% XyG O-acetylation is reached, Al-binding capacity is exhausted. Recently, Tahara et al (2014) reported that a tannin compound in the roots of Eucalyptus camaldulensis, oenothein B, can efficiently bind Al by forming complexes with the adjacent phenolic hydroxyl groups. Therefore, it is reasonable to assume that the hydroxyl groups in XyG may bind Al, and the amount of the nonacetylated hydroxyl groups and their spatial distribution might be important to decide the amount of Al that XyG can bind.…”

Plant Adaptation to Acid Soils: The Molecular Basis for Crop Aluminum Resistance

“…Tahara et al (122) found that, in response to Al stress, the roots of highly Al-resistant camphor (Cinnamomum camphora) and Eucalyptus camaldulensis trees synthesize oenothein B, a dimeric hydrolyzable tannin containing several adjacent phenolic hydroxyl groups, which they showed was an effective Al-binding ligand. The higher levels of oenothein B content in roots were positively correlated with the degree of Al resistance displayed among five tree species.…”

Contribution of constitutive characteristics of lipids and phenolics in roots of tree species in Myrtales to aluminum tolerance

“…27 Al NMR analysis indicated that most Al in tea leaves forms complexes mostly with catechin (Nagata et al ). Tahara et al () reported that oenothein B binds to Al in M . cajuputi .…”

“…Ofei‐manu et al () reported that woody plants with higher concentrations of phenolics in their roots showed higher Al tolerance. Eucalyptus camaldulensis , an Al‐resistant tree, contains oenothein B in its root, a compound having the ability to detoxify Al and possibly contributing to the Al tolerance of this species (Tahara et al ). Furthermore, it has been suggested that some phenolics could detoxify Al in leaves in some Al‐tolerant plants such as Rumex acetosa and Camellia sinensis (Nagata et al , Tolrà et al , ).…”