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Title: Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom

Abstract

Diatom dominance in contemporary aquatic environments indicates that they have developed unique and effective mechanisms to cope with the rapid and considerable fluctuations that characterize these environments. In view of their evolutionary history from a secondary endosymbiosis, inter-organellar regulation of biochemical activities may be of particular relevance. Diatom mitochondrial alternative oxidase (AOX) is believed to play a significant role in supplying chloroplasts with ATP produced in the mitochondria. Using the model diatom Phaeodactylum tricornutum we generated AOX knockdown lines, and followed sensitivity to stressors, photosynthesis and transcriptome and metabolome profiles of wild-type and knockdown lines. We show here that expression of the AOX gene is upregulated by various stresses including H2O2, heat, high light illumination, and iron or nitrogen limitation. AOX knockdown results in hypersensitivity to stress. Knockdown lines also show significantly reduced photosynthetic rates and their chloroplasts are more oxidized. Comparisons of transcriptome and metabolome profiles suggest a strong impact of AOX activity on gene expression, which is carried through to the level of the metabolome. Our data provide evidence for the involvement of mitochondrial AOX in processes central to the cell biology of diatoms, revealing that cross-talk between mitochondria and chloroplasts is crucial for maintaining sensitivity to changingmore » environments.« less

Authors:
 [1];  [1];  [1];  [1];  [2]; ORCiD logo [3];  [2]; ORCiD logo [1]
  1. Paris Sciences et Lettres University (PSL) (France)
  2. Max Planck Inst. for Molecular Plant Physiology, Potsdam (Germany)
  3. J. Craig Venter Institute, La Jolla, CA (United States); Univ. of California, San Diego, CA (United States)
Publication Date:
Research Org.:
J. Craig Venter Institute, Inc., Rockville, MD (United States)
Sponsoring Org.:
USDOE Office of Science (SC); European Research Council (ERC); Institut de France; French Government; National Science Foundation (NSF); Gordon and Betty Moore Foundation
OSTI Identifier:
1611094
Grant/Contract Number:  
SC0008593; SC00006719; ANR-10-LABX-54; ANR-1253 11-IDEX-0001-02; ANR-11-BTBR-0008; MCB-1024913; GBMF3828
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 221; Journal Issue: 3; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; plant sciences; alternative oxidase (AOX); diatoms; metabolite profiling; mitochondria; oxidative stress; photosynthesis; transcriptome

Citation Formats

Murik, Omer, Tirichine, Leila, Prihoda, Judit, Thomas, Yann, Araújo, Wagner L., Allen, Andrew E., Fernie, Alisdair R., and Bowler, Chris. Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom. United States: N. p., 2018. Web. doi:10.1111/nph.15479.
Murik, Omer, Tirichine, Leila, Prihoda, Judit, Thomas, Yann, Araújo, Wagner L., Allen, Andrew E., Fernie, Alisdair R., & Bowler, Chris. Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom. United States. https://doi.org/10.1111/nph.15479
Murik, Omer, Tirichine, Leila, Prihoda, Judit, Thomas, Yann, Araújo, Wagner L., Allen, Andrew E., Fernie, Alisdair R., and Bowler, Chris. Fri . "Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom". United States. https://doi.org/10.1111/nph.15479. https://www.osti.gov/servlets/purl/1611094.
@article{osti_1611094,
title = {Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom},
author = {Murik, Omer and Tirichine, Leila and Prihoda, Judit and Thomas, Yann and Araújo, Wagner L. and Allen, Andrew E. and Fernie, Alisdair R. and Bowler, Chris},
abstractNote = {Diatom dominance in contemporary aquatic environments indicates that they have developed unique and effective mechanisms to cope with the rapid and considerable fluctuations that characterize these environments. In view of their evolutionary history from a secondary endosymbiosis, inter-organellar regulation of biochemical activities may be of particular relevance. Diatom mitochondrial alternative oxidase (AOX) is believed to play a significant role in supplying chloroplasts with ATP produced in the mitochondria. Using the model diatom Phaeodactylum tricornutum we generated AOX knockdown lines, and followed sensitivity to stressors, photosynthesis and transcriptome and metabolome profiles of wild-type and knockdown lines. We show here that expression of the AOX gene is upregulated by various stresses including H2O2, heat, high light illumination, and iron or nitrogen limitation. AOX knockdown results in hypersensitivity to stress. Knockdown lines also show significantly reduced photosynthetic rates and their chloroplasts are more oxidized. Comparisons of transcriptome and metabolome profiles suggest a strong impact of AOX activity on gene expression, which is carried through to the level of the metabolome. Our data provide evidence for the involvement of mitochondrial AOX in processes central to the cell biology of diatoms, revealing that cross-talk between mitochondria and chloroplasts is crucial for maintaining sensitivity to changing environments.},
doi = {10.1111/nph.15479},
journal = {New Phytologist},
number = 3,
volume = 221,
place = {United States},
year = {Fri Sep 14 00:00:00 EDT 2018},
month = {Fri Sep 14 00:00:00 EDT 2018}
}

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