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Plant Cell, Vol. 11, 1277-1292, July 1999, Copyright © 1999, American Society of Plant Physiologists

Elevated Glutathione Biosynthetic Capacity in the Chloroplasts of Transgenic Tobacco Plants Paradoxically Causes Increased Oxidative Stress

Gary Creissena, John Firmina, Michael Fryerb, Baldeep Kulara, Nicola Leylanda, Helen Reynoldsa, Gabriela Pastoria, Florence Wellburnc, Neil Bakerb, Alan Wellburnc, and Philip Mullineauxa
a John Innes Centre, Norwich Research Park, Colney, Norwich NR4 7UH, United Kingdom
b Department of Biological and Chemical Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom
c Institute of Environmental and Biological Sciences, University of Lancaster, Bailrigg, Lancaster LA1 4YQ, United Kingdom

Correspondence to: Gary Creissen, creissen{at}bbsrc.ac.uk (E-mail), 44-1603-456844 (fax)

Glutathione (GSH), a major antioxidant in most aerobic organisms, is perceived to be particularly important in plant chloroplasts because it helps to protect the photosynthetic apparatus from oxidative damage. In transgenic tobacco plants overexpressing a chloroplast-targeted {gamma}-glutamylcysteine synthetase ({gamma}-ECS), foliar levels of GSH were raised threefold. Paradoxically, increased GSH biosynthetic capacity in the chloroplast resulted in greatly enhanced oxidative stress, which was manifested as light intensity–dependent chlorosis or necrosis. This phenotype was associated with foliar pools of both GSH and {gamma}-glutamylcysteine (the immediate precursor to GSH) being in a more oxidized state. Further manipulations of both the content and redox state of the foliar thiol pools were achieved using hybrid transgenic plants with enhanced glutathione synthetase or glutathione reductase activity in addition to elevated levels of {gamma}-ECS. Given the results of these experiments, we suggest that {gamma}-ECS–transformed plants suffered continuous oxidative damage caused by a failure of the redox-sensing process in the chloroplast.




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