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

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.15479· OSTI ID:1611094

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.

Research Organization:
J. Craig Venter Institute, Inc., Rockville, MD (United States)
Sponsoring Organization:
USDOE Office of Science (SC); European Research Council (ERC); Institut de France; French Government; National Science Foundation (NSF); Gordon and Betty Moore Foundation
Grant/Contract Number:
SC0008593; SC00006719; ANR-10-LABX-54; ANR-1253 11-IDEX-0001-02; ANR-11-BTBR-0008; MCB-1024913; GBMF3828
OSTI ID:
1611094
Journal Information:
New Phytologist, Vol. 221, Issue 3; ISSN 0028-646X
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 24 works
Citation information provided by
Web of Science

References (77)

Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death journal December 2006
Changes in Plant Mitochondrial Electron Transport Alter Cellular Levels of Reactive Oxygen Species and Susceptibility to Cell Death Signaling Molecules journal November 2006
The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells journal July 1999
Plant PA signaling via diacylglycerol kinase journal September 2009
C 3 and C 4 Pathways of Photosynthetic Carbon Assimilation in Marine Diatoms Are under Genetic, Not Environmental, Control journal July 2007
Genomic Footprints of a Cryptic Plastid Endosymbiosis in Diatoms journal June 2009
TagFinder for the quantitative analysis of gas chromatography—mass spectrometry (GC-MS)-based metabolite profiling experiments journal January 2008
Nitric Oxide Mediates Nitrite-Sensing and Acclimation and Triggers a Remodeling of Lipids journal September 2017
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions journal January 2013
clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters journal May 2012
Trimmomatic: a flexible trimmer for Illumina sequence data journal April 2014
Gas chromatography mass spectrometry–based metabolite profiling in plants journal June 2006
The Phaeodactylum genome reveals the evolutionary history of diatom genomes journal October 2008
Perception of Environmental Signals by a Marine Diatom journal June 2000
Alternative oxidase: a target and regulator of stress responses journal December 2009
Integrative analysis of large scale transcriptome data draws a comprehensive landscape of Phaeodactylum tricornutum genome and evolutionary origin of diatoms journal March 2018
An original adaptation of photosynthesis in the marine green alga Ostreococcus journal May 2008
Alternative Oxidase: A Mitochondrial Respiratory Pathway to Maintain Metabolic and Signaling Homeostasis during Abiotic and Biotic Stress in Plants journal March 2013
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences journal February 2016
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks journal March 2012
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research journal August 2005
The water–water cycle as alternative photon and electron sinks journal October 2000
An In Vivo Perspective of the Role(s) of the Alternative Oxidase Pathway journal March 2018
Identification of Diacylglycerol Pyrophosphate as a Novel Metabolic Product of Phosphatidic Acid during G-protein Activation in Plants journal June 1996
Cyclic Electron Transport Around Photosystem I: Genetic Approaches journal June 2007
Alternative Oxidase Isoforms Are Differentially Activated by Tricarboxylic Acid Cycle Intermediates journal December 2017
Contribution of the Alternative Respiratory Pathway to PSII Photoprotection in C3 and C4 Plants journal January 2017
Evolution and metabolic significance of the urea cycle in photosynthetic diatoms journal May 2011
Alternative oxidase respiration maintains both mitochondrial and chloroplast function during drought journal August 2016
Mesoscale Iron Enrichment Experiments 1993-2005: Synthesis and Future Directions journal February 2007
Reactive oxygen signaling and abiotic stress journal July 2008
Analysis of Posttranslational Activation of Alternative Oxidase Isoforms journal June 2017
A Diatom Gene Regulating Nitric-Oxide Signaling and Susceptibility to Diatom-Derived Aldehydes journal June 2008
Expression and signal regulation of the alternative oxidase genes under abiotic stresses journal September 2013
Phospholipid signalling in plant defence journal August 2002
GC-MS libraries for the rapid identification of metabolites in complex biological samples journal January 2005
A discrete role for alternative oxidase under hypoxia to increase nitric oxide and drive energy production journal July 2018
Signals Regulating the Expression of the Nuclear Gene Encoding Alternative Oxidase of Plant Mitochondria journal June 1996
Role of the alternative oxidase in limiting superoxide production by plant mitochondria journal May 1997
The role of C 4 metabolism in the marine diatom Phaeodactylum tricornutum journal October 2012
Dehydroascorbate: a possible surveillance molecule of oxidative stress and programmed cell death in the green alga Chlamydomonas reinhardtii journal December 2013
Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms journal July 2015
Induction of the AOX1D Isoform of Alternative Oxidase in A. thaliana T-DNA Insertion Lines Lacking Isoform AOX1A Is Insufficient to Optimize Photosynthesis when Treated with Antimycin A journal March 2009
Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation journal July 2008
Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria journal November 2003
Insights into global diatom distribution and diversity in the world’s ocean journal February 2016
A Stress Surveillance System Based on Calcium and Nitric Oxide in Marine Diatoms journal February 2006
Recommendations for Reporting Metabolite Data journal July 2011
Thermogenic Respiration in Aroids journal June 1975
Alternative oxidase: a defence against metabolic fluctuations? journal December 2009
Covalent and Noncovalent Dimers of the Cyanide-Resistant Alternative Oxidase Protein in Higher Plant Mitochondria and Their Relationship to Enzyme Activity journal November 1993
Up-Regulation of Mitochondrial Alternative Oxidase Concomitant with Chloroplast Over-Reduction by Excess Light journal April 2007
Paradoxically, prior acquisition of antioxidant activity enhances oxidative stress-induced cell death journal September 2009
Hydrogen peroxide and nitric oxide as signalling molecules in plants journal May 2002
Chloroplast-mitochondria cross-talk in diatoms journal January 2012
Early perturbation in mitochondria redox homeostasis in response to environmental stress predicts cell fate in diatoms journal August 2014
GMD@CSB.DB: the Golm Metabolome Database journal December 2004
Abiotic stress signalling pathways: specificity and cross-talk journal June 2001
In vitro antibacterial activity of some aliphatic aldehydes from Olea europaea L. journal April 2001
The intracellular distribution of inorganic carbon fixing enzymes does not support the presence of a C4 pathway in the diatom Phaeodactylum tricornutum journal March 2018
ALTERNATIVE OXIDASE: From Gene to Function journal June 1997
The Evolution of Modern Eukaryotic Phytoplankton journal July 2004
Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus journal January 2017
A Model for Carbohydrate Metabolism in the Diatom Phaeodactylum tricornutum Deduced from Comparative Whole Genome Analysis journal January 2008
Alternative Oxidase Is Positive for Plant Performance journal July 2018
The life of diatoms in the world's oceans journal May 2009
Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose journal August 1998
Ontologizer 2.0--a multifunctional tool for GO term enrichment analysis and data exploration journal May 2008
Plasticity and robustness of pattern formation in the model diatom Phaeodactylum tricornutum journal February 2009
The Microbial Engines That Drive Earth's Biogeochemical Cycles journal May 2008
Nitric oxide functions as a signal in plant disease resistance journal August 1998
Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum journal December 2007
Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome journal May 2017
Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context journal August 2005
Phosphatidic acid: a multifunctional stress signaling lipid in plants journal August 2005
Role of the alternative oxidase in limiting superoxide production by plant mitochondria journal May 1997
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions text January 2013

Cited By (2)

Swimming, gliding, and rolling toward the mainstream: cell biology of marine protists journal May 2019
Cross‐compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom Phaeodactylum tricornutum journal February 2019