The Arabidopsis-related halophyte Thellungiella halophila: Boron tolerance via boron complexation with metabolites?

Abstract

Tolerance to boron (B) is still not completely understood. We tested here the hypothesis that Thellungiella halophila, an Arabidopsis thaliana-related 'extremophile' plant, with abundance of B in its natural environment, is tolerant to B, and examined the potential mechanisms of this tolerance. With 1-10mm B applied ([B]ext) to Thellungiella and Arabidopsis grown in hydroponics, the steady-state accumulated B concentration ([B]int) in the root was below [B]ext, and was similar in both, suggesting both extrude B actively. Whether grown in soil or hydroponically, the shoot [B]int was higher in Arabidopsis than in Thellungiella, suggesting more effective net B exclusion by Thellungiella root. Arabidopsis exhibited toxicity symptoms including reduced shoot fresh weight (FW), but Thellungiella was not affected, even at similar levels of shoot-accumulated [B]int (about 10 to 40mm B in 'shoot water'), suggesting additional B tolerance mechanism in Thellungiella shoot. At [B]ext=5mm, the summed shoot concentration of the potentially B-binding polyhydroxyl metabolites (malic acid, fructose, glucose, sucrose and citric acid) in Arabidopsis was below [B]int, but in Thellungiella it was over twofold higher than [B]int, and therefore likely to allow appreciable 1:2 boron-metabolite complexation in the shoot. This, we suggest, is an important component of Thellungiella B tolerance mechanism. In addition to naturally occurring boron-laden land areas, agricultural soils, particularly in semi-arid areas, are progressively contaminated by boron through irrigation by treated wastewater or desalinated sea water, as its removal from these water sources is very costly and thus often impractical. Boron is toxic to plants already at low concentrations and boron-tolerant crops are continuouslysought after to avoid yield losses. The mechanisms underlying toxicity, as well as those underlying boron tolerance are still not well understood. Here, we characterized a hitherto undefined "shoot boron tolerance" in Thellungiella halofila, a close relative of the boron-sensitive Arabidopsis, positioning Thellungiella as an attractive model plant in which to study these mechanisms. © 2011 Blackwell Publishing Ltd.