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

Wang, Yan; Lyu, Wenhui; Berkowitz, Oliver; Radomiljac, Jordan D; Law, Simon R; Murcha, Monika W; Carrie, Chris; Teixeira, Pedro F; Kmiec, Beata and Duncan, Owen, et al. (2016) In Molecular Plant 9(5). p.696-710
Abstract

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... (More)

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.

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publication status
published
subject
keywords
mitochondria, complex I, retrograde signaling, chloroplast, cytosol
in
Molecular Plant
volume
9
issue
5
pages
15 pages
publisher
Oxford University Press
external identifiers
  • scopus:84966662480
ISSN
1752-9867
DOI
10.1016/j.molp.2016.01.009
language
English
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no
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499aa330-9fbf-4d8d-8976-a49be06db98d
date added to LUP
2017-05-08 10:46:11
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2017-06-26 10:53:52
@article{499aa330-9fbf-4d8d-8976-a49be06db98d,
  abstract     = {<p>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.</p>},
  author       = {Wang, Yan and Lyu, Wenhui and Berkowitz, Oliver and Radomiljac, Jordan D and Law, Simon R and Murcha, Monika W and Carrie, Chris and Teixeira, Pedro F and Kmiec, Beata and Duncan, Owen and Van Aken, Olivier and Narsai, Reena and Glaser, Elzbieta and Huang, Shaobai and Roessner, Ute and Millar, A. Harvey and Whelan, James},
  issn         = {1752-9867},
  keyword      = {mitochondria,complex I,retrograde signaling,chloroplast,cytosol},
  language     = {eng},
  month        = {05},
  number       = {5},
  pages        = {696--710},
  publisher    = {Oxford University Press},
  series       = {Molecular Plant},
  title        = {Inactivation of Mitochondrial Complex I Induces the Expression of a Twin Cysteine Protein that Targets and Affects Cytosolic, Chloroplastidic and Mitochondrial Function},
  url          = {http://dx.doi.org/10.1016/j.molp.2016.01.009},
  volume       = {9},
  year         = {2016},
}