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First published online August 4, 2006; 10.1104/pp.106.085886 Plant Physiology 142:574-585 (2006) © 2006 American Society of Plant Biologists IMMUTANS Does Not Act as a Stress-Induced Safety Valve in the Protection of the Photosynthetic Apparatus of Arabidopsis during Steady-State Photosynthesis1Department of Biology and The Biotron, University of Western Ontario, London, Ontario, Canada, N6A 5B7 (D.R., A.G.I., J.G.-L., L.H., M.G., G.S., M.K., D.P.M., N.P.A.H.); Department of Genetics, Development and Cell Biology, Iowa State University, Ames, Iowa 50011 (A.F., S.R.R.); and Umea Plant Science Centre, Department of Plant Physiology, Umea University, Umea S–901 87, Sweden (L.H., V.H.)
IMMUTANS (IM) encodes a thylakoid membrane protein that has been hypothesized to act as a terminal oxidase that couples the reduction of O2 to the oxidation of the plastoquinone (PQ) pool of the photosynthetic electron transport chain. Because IM shares sequence similarity to the stress-induced mitochondrial alternative oxidase (AOX), it has been suggested that the protein encoded by IM acts as a safety valve during the generation of excess photosynthetically generated electrons. We combined in vivo chlorophyll fluorescence quenching analyses with measurements of the redox state of P700 to assess the capacity of IM to compete with photosystem I for intersystem electrons during steady-state photosynthesis in Arabidopsis (Arabidopsis thaliana). Comparisons were made between wild-type plants, im mutant plants, as well as transgenics in which IM protein levels had been overexpressed six (OE-6x) and 16 (OE-16x) times. Immunoblots indicated that IM abundance was the only major variant that we could detect between these genotypes. Overexpression of IM did not result in increased capacity to keep the PQ pool oxidized compared to either the wild type or im grown under control conditions (25°C and photosynthetic photon flux density of 150 µmol photons m–2 s–1). Similar results were observed either after 3-d cold stress at 5°C or after full-leaf expansion at 5°C and photosynthetic photon flux density of 150 µmol photons m–2 s–1. Furthermore, IM abundance did not enhance protection of either photosystem II or photosystem I from photoinhibition at either 25°C or 5°C. Our in vivo data indicate that modulation of IM expression and polypeptide accumulation does not alter the flux of intersystem electrons to P700+ during steady-state photosynthesis and does not provide any significant photoprotection. In contrast to AOX1a, meta-analyses of published Arabidopsis microarray data indicated that IM expression exhibited minimal modulation in response to myriad abiotic stresses, which is consistent with our functional data. However, IM exhibited significant modulation in response to development in concert with changes in AOX1a expression. Thus, neither our functional analyses of the IM knockout and overexpression lines nor meta-analyses of gene expression support the model that IM acts as a safety valve to regulate the redox state of the PQ pool during stress and acclimation. Rather, IM appears to be strongly regulated by developmental stage of Arabidopsis.
1 This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC; grant to D.P.M., and N.P.A.H.) and by the U.S. Department of Energy (Energy Biosciences; grant no. DF–FG02–94ER20147 to S.R.R.). D.R. is the recipient of an NSERC postgraduate scholarship. 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: Norman P.A. Hüner (nhuner{at}uwo.ca). www.plantphysiol.org/cgi/doi/10.1104/pp.106.085886 * Corresponding author; e-mail nhuner{at}uwo.ca; fax 519–661–3935. Received June 28, 2006; accepted July 27, 2006; published August 4, 2006. Related articles in Plant Physiol.:
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