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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Manganese Deficiency in Chlamydomonas Results in Loss of Photosystem II and MnSOD Function, Sensitivity to Peroxides, and Secondary Phosphorus and Iron Deficiency^1,[W],[OA]

Department of Chemistry and Biochemistry, University of California, Los Angeles, California 90095–1569

For photoheterotrophic growth, a Chlamydomonas reinhardtii cell requires at least 1.7 x 10⁷ manganese ions in the medium. At lower manganese ion concentrations (typically <0.5 µM), cells divide more slowly, accumulate less chlorophyll, and the culture reaches stationary phase at lower cell density. Below 0.1 µM supplemental manganese ion in the medium, the cells are photosynthetically defective. This is accompanied by decreased abundance of D1, which binds the Mn₄Ca cluster, and release of the OEE proteins from the membrane. Assay of Mn superoxide dismutase (MnSOD) indicates loss of activity of two isozymes in proportion to the Mn deficiency. The expression of MSD3 through MSD5, encoding various isoforms of the MnSODs, is up-regulated severalfold in Mn-deficient cells, but neither expression nor activity of the plastid Fe-containing superoxide dismutase is changed, which contrasts with the dramatically increased MSD3 expression and plastid MnSOD activity in Fe-deficient cells. Mn-deficient cells are selectively sensitive to peroxide but not methyl viologen or Rose Bengal, and GPXs, APX, and MSRA2 genes (encoding glutathione peroxidase, ascorbate peroxidase, and methionine sulfoxide reductase 2) are slightly up-regulated. Elemental analysis indicates that the Mn, Fe, and P contents of cells in the Mn-deficient cultures were reduced in proportion to the deficiency. A natural resistance-associated macrophage protein homolog and one of five metal tolerance proteins were induced in Mn-deficient cells but not in Fe-deficient cells, suggesting that the corresponding gene products may be components of a Mn²⁺-selective assimilation pathway.

² Present address: Institute for Cell and Molecular Biosciences, Medical School, University of Newcastle upon Tyne, Newcastle upon Tyne NE2 4HH, UK.

³ Present address: Instituto de Bioquímica Vegetal y Fotosíntesis (Univ. de Sevilla-CSIC), Centro de Investigaciones Científicas Isla de la Cartuja, Avda. Americo Vespucio s/n 41092 Sevilla, Spain.

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: Sabeeha S. Merchant (merchant{at}chem.ucla.edu).

^[W] The online version of this article contains Web-only data.

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.106.088609

^* Corresponding author; e-mail merchant{at}chem.ucla.edu; fax 1–310–206–1035.

Received August 21, 2006; accepted October 28, 2006; published November 3, 2006.

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