Inactivation of Mitochondrial Complex i Induces the Expression of a Twin Cysteine Protein that Targets and Affects Cytosolic, Chloroplastidic and Mitochondrial Function

Y. Wang, W. Lyu, O. Berkowitz, J.D. Radomiljac, S.R. Law, Monika W. Murcha, C. Carrie, P.F. Teixeira, B. Kmiec, Owen Duncan, Olivier Van Aken, R. Narsai, E. Glaser, Shaobai Huang, U. Roessner, A. Harvey Millar, J. Whelan

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Abstract

© 2016 The Author.
At12Cys-1 (At5g64400) and At12Cys-2 (At5g09570) are two closely related isogenes that encode small, twin cysteine proteins, typically located in mitochondria. At12Cys-2 transcript is induced in a variety of mutants with disrupted mitochondrial proteins, but an increase in At12Cys protein is only detected in mutants with reduced mitochondrial complex I abundance. Induction of At12Cys protein in mutants that lack mitochondrial complex I is accompanied by At12Cys protein located in mitochondria, chloroplasts, and the cytosol. Biochemical analyses revealed that even single gene deletions, i.e., At12cys-1 or At12cys-2, have an effect on mitochondrial and chloroplast functions. However, only double mutants, i.e., At12cys-1:At12cys-2, affect the abundance of protein and mRNA transcripts encoding translation elongation factors as well as rRNA abundance. Blue native PAGE showed that At12Cys co-migrated with mitochondrial supercomplex I + III. Likewise, deletion of both At12cys-1 and At12cys-2 genes, but not single gene deletions, results in enhanced tolerance to drought and light stress and increased anti-oxidant capacity. The induction and multiple localization of At12Cys upon a reduction in complex I abundance provides a mechanism to specifically signal mitochondrial dysfunction to the cytosol and then beyond to other organelles in the cell.
Original languageEnglish
Pages (from-to)696-710
JournalMolecular Plant
Volume9
Issue number5
DOIs
Publication statusPublished - 2 May 2016

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    Wang, Y., Lyu, W., Berkowitz, O., Radomiljac, J. D., Law, S. R., Murcha, M. W., Carrie, C., Teixeira, P. F., Kmiec, B., Duncan, O., Van Aken, O., Narsai, R., Glaser, E., Huang, S., Roessner, U., Millar, A. H., & Whelan, J. (2016). Inactivation of Mitochondrial Complex i Induces the Expression of a Twin Cysteine Protein that Targets and Affects Cytosolic, Chloroplastidic and Mitochondrial Function. Molecular Plant, 9(5), 696-710. https://doi.org/10.1016/j.molp.2016.01.009