Pattern of aluminum-induced secretion of organic acids differs between rye and wheat

Abstract

Al-Induced secretion of organic acids from the roots has been considered as a mechanism of Al tolerance, but the processes leading to the secretion of organic acids are still unknown. In this study, the secretion pattern and alteration in the metabolism of organic acids under Al stress were examined in rye (Secale cereale L. cv King) and wheat (Triticum aestivum L. cv Atlas 66). Al induced rapid secretion of malate in the wheat, but a lag (6 and 10 h for malic and citric acids, respectively) between the exposure to Al and the secretion of organic acids was observed in the rye. The activities of isocitrate dehydrogenase, phosphoenolpyruvate carboxylase, and malate dehydrogenase were not affected by Al in either plant. The activity of citrate synthase was increased by the exposure to Al in the rye, but not in the wheat. The secretion of malate was not suppressed at low temperature in the wheat, but that of citrate was stopped in the rye. The Al-induced secretion of citrate from roots of the rye was inhibited by the inhibitors of a citrate carrier, which transports citrate from the mitochondria to the cytoplasm. All of these results suggest that alteration in the metabolism of organic acids is involved in the Al-induced secretion of organic acids in rye, but only activation of an anion channel seems to be responsible for the rapid secretion of malate in the wheat.

Figure 1

Effect of Al on the root elongation in the rye (cv King) and the wheat (cv Atlas 66). The roots were exposed to 0.5 mm CaCl₂ solution (pH 4.5) containing 0, 10, 30, or 50 μm Al for 24 h. Vertical bars represent sd (n = 12).

Figure 2

Organic acids secreted from rye (A) and wheat (B) at different times in the presence of Al. Both rye (cv King) and wheat (cv Atlas 66) were exposed to 0.5 mm CaCl₂ solution (pH 4.5) containing 50 μm Al. Root exudates were collected every 2 h after initiation of Al treatment. Organic acids were analyzed by HPLC. Vertical bars represent sd (n = 3).

Figure 3

Effect of external Al concentration on the secretion of organic acids in the rye (A) and the wheat (B). Seedlings of the rye (cv King) and the wheat (cv Atlas 66) were exposed to 0.5 mm CaCl₂ solution (pH 4.5) containing 0, 10, 30, or 50 μm Al. After a 24-h exposure, the root exudates were collected and organic acids were analyzed by HPLC. Vertical bars represent sd (n = 3).

Figure 4

Effect of Al on the activity of CS in root apexes of the rye (A) and the wheat (B). The roots were exposed to 0.5 mm CaCl₂ solution with (+Al) or without (−Al) 50 μm Al for 0, 2, 4, 6, 8, and 12 h, respectively, then the root apices (1 cm) were excised. CS activity was assayed as described in “Materials and Methods.” Bar represents sd (n = 3).

Figure 5

Effect of citrate-carrier inhibitor on the Al-induced secretion of citric acid in rye. Seedlings were exposed to 0.5 mm CaCl₂ solution (pH 4.5) containing 25 μm of PP and PI in the presence of 50 μm Al. After a 12-h exposure, the root exudates were collected and citric acid was analyzed by HPLC. Bar represents sd (n = 3).