The plasma membrane strength of the root-tip cells and root phenolic compounds are correiated with Al tolerance in several common woody plants

Abstract

Ten species including one cultivar of common woody plants, i.e., Picea abies Karst. (Norway spruce), Gleditsia triacanthos L. (honey locust), Robinia pseudoacacia L. (black locust), Populus tremuloides Michx. (quaking aspen), Eucalyptus viminalis Labill. (eucalyptus), Cryptomeria japonica (Japanese cedar), Camellia sinensis L., cv. Yabukita (tea), Rhus succedanea L. (sumac), Pinus densiflora (Japanese red pine), and Pinus thunbergii Parl., cv. Sanshu (Sanshu black pine), and 2 species of marker crop plants, i.e., Oryza sativa L., cv. Sasanishiki (rice) and Hordeum vulgare L., cv. Manriki (barley), were cultured for 38 d at pH 4.3 in full nutrient solutions under three different stress conditions; 1) high AI, low P and low pH (combined stress), 2) low P and low pH, and 3) control. Soluble ionic Al and P concentrations in the media were maintained at almost 55 and 7 µM, respectively. P. thunbergii cv. Sanshu, C. sinensis, G. triacanthos, R. pseudoacacia, P. abies, and C. japonica were more tolerant to the combined stress than Oryza sativa known to be one of the most tolerant crop plants. Al tolerance obtained after the short-term stress for 24 h in CaCl₂ solution at pH 4.7 was positively correlated with that obtained after the long-term combined stress, suggesting that a short-term screening technique can be used for the estimation of tolerance in acid soils. Under the combined stress conditions, low P stress was not expressed in any plant parts, Al stress was expressed primarily in roots and low pH stress was highly expressed in shoots. The roots of the AI-tolerant plants contained a significantly lower amount of Al with a higher K accumulation ratio. The plasma membrane strength (PMS), corresponding to the intactness of the PM permeability of root-tip cells during the re-elongation period without Al after temporary treatment with AI, was correlated with Al tolerance. Positive correlation between low pH tolerance and Al tolerance at pH 4.7 without H⁺ toxicity in both short-term experiments suggested that the PM of the root-tip cells was a common target for both stresses. Al tolerance of woody plants was positively correlated with the concentration of soluble phenolic compounds in roots irrespective of the treatment, but not with exuded phenolic compounds. In contrast to acidic conditions, in vitro binding affinity to Al ions at pH 7.0 was significantly higher at equimolar concentrations of quercetin, catechin, and chlorogenic acid but lower in the case of rutin, citric, oxalic, and malic acids. To our knowledge, this is the first report in which phenolic compounds in roots were quantitatively related to Al tolerance in woody plants. It was eventually suggested that AI-tolerant woody plants constitutively adopted a dual strategy involving a superior PMS and a higher amount of root phenolic compounds which can bind strongly with and detoxify Al ions in the cytoplasm.