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WHOLE PLANT AND ECOPHYSIOLOGY

The Shoot-Specific Expression of -Glutamylcysteine Synthetase Directs the Long-Distance Transport of Thiol-Peptides to Roots Conferring Tolerance to Mercury and Arsenic¹

Department of Genetics, University of Georgia, Athens, Georgia 30602–7223 (Y.L., O.P.D., A.P.S., R.B.M.); and Applied PhytoGenetics, Athens, Georgia 30602 (L.C.)

Thiol-peptides synthesized as intermediates in phytochelatin (PC) biosynthesis confer cellular tolerance to toxic elements like arsenic, mercury, and cadmium, but little is known about their long-distance transport between plant organs. A modified bacterial -glutamylcysteine synthetase (ECS) gene, S1pt::ECS, was expressed in the shoots of the ECS-deficient, heavy-metal-sensitive cad2-1 mutant of Arabidopsis (Arabidopsis thaliana). S1pt::ECS directed strong ECS protein expression in the shoots, but no ECS was detected in the roots of transgenic plant lines. The S1pt::ECS gene restored full mercury tolerance and partial cadmium tolerance to the mutant and enhanced arsenate tolerance significantly beyond wild-type levels. After arsenic treatment, the root concentrations of -glutamylcysteine (EC), PC₂, and PC₃ peptides in a S1pt::ECS-complemented cad2-1 line increased 6- to 100-fold over the mutant levels and were equivalent to wild-type concentrations. The shoot and root levels of glutathione were 2- to 5-fold above those in wild-type plants, with or without treatment with toxicants. Thus, EC and perhaps glutathione are efficiently transported from shoots to roots. The possibility that EC or other PC pathway intermediates may act as carriers for the long-distance phloem transport and subsequent redistribution of thiol-reactive toxins and nutrients in plants is discussed.

² Present address: Emory School of Medicine, Department of Human Genetics, Emory University, Atlanta, GA 30345.

³ Present address: Department of Plant, Soil, and Insect Sciences, University of Massachusetts, Amherst, MA 01002.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Richard B. Meagher (meagher{at}uga.edu).

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.074815.

^* Corresponding author; e-mail meagher{at}uga.edu; fax 706–542–1387.

Received November 29, 2005; returned for revision February 25, 2006; accepted March 6, 2006.