Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana

Plant mitochondria contain non-phosphorylating bypasses of the respiratory chain, catalysed by the alternative oxidase (AOX) and alternative NADH dehydrogenases (NDH), as well as uncoupling (UCP) protein. Each of these components either circumvents or short-circuits proton translocation pathways, and each is encoded by a small gene family in Arabidopsis. Whole genome microarray experiments were performed with suspension cell cultures to examine the effects of various 3 h treatments designed to induce abiotic stress. The expression of over 60 genes encoding components of the classical, phosphorylating respiratory chain and tricarboxylic acid cycle remained largely constant when cells were subjected to a broad range of abiotic stresses, but expression of the alternative components responded differentially to the various treatments. In detailed time-course quantitative PCR analysis, specific members of both AOX and NDH gene families displayed coordinated responses to treatments. In particular, the co-expression of AOX1a and NDB2 observed under a number of treatments suggested co-regulation that may be directed by common sequence elements arranged hierarchically in the upstream promoter regions of these genes. A series of treatment sets were identified, representing the response of specific AOX and NDH genes to mitochondrial inhibition, plastid inhibition and abiotic stresses. These treatment sets emphasise the multiplicity of pathways affecting alternative electron transport components in plants.

[1]  Kathleen Marchal,et al.  Computational Approaches to Identify Promoters and cis-Regulatory Elements in Plant Genomes1 , 2003, Plant Physiology.

[2]  Michael Ruogu Zhang,et al.  Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. , 1998, Molecular biology of the cell.

[3]  M. Hodges,et al.  The growing family of mitochondrial carriers in Arabidopsis. , 2004, Trends in plant science.

[4]  Paul G Crichton,et al.  Function of the alternative oxidase: is it still a scavenger? , 2002, Trends in plant science.

[5]  J. Chory,et al.  Signal Transduction between the Chloroplast and the Nucleus Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010446. , 2002, The Plant Cell Online.

[6]  A. Brennicke,et al.  The response regulator ARR2: a pollen-specific transcription factor involved in the expression of nuclear genes for components of mitochondrial Complex I in Arabidopsis , 2001, Molecular Genetics and Genomics.

[7]  Z. Weng,et al.  Detection of functional DNA motifs via statistical over-representation. , 2004, Nucleic acids research.

[8]  M. Ribas-Carbó,et al.  The effect of growth and measurement temperature on the activity of the alternative respiratory pathway , 1999, Plant physiology.

[9]  A. Zachowski,et al.  The plant uncoupling protein homologues: a new family of energy-dissipating proteins in plant mitochondria. , 2004, Plant physiology and biochemistry : PPB.

[10]  D A Day,et al.  The impact of oxidative stress on Arabidopsis mitochondria. , 2002, The Plant journal : for cell and molecular biology.

[11]  J. P. Gustafson,et al.  Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. , 2003, The Plant journal : for cell and molecular biology.

[12]  J. Mesirov,et al.  Interpreting patterns of gene expression with self-organizing maps: methods and application to hematopoietic differentiation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[13]  J. Whelan,et al.  Analysis of the Alternative Oxidase Promoters from Soybean1 , 2003, Plant Physiology.

[14]  G. Vanlerberghe,et al.  Induction of Mitochondrial Alternative Oxidase in Response to a Cell Signal Pathway Down-Regulating the Cytochrome Pathway Prevents Programmed Cell Death1 , 2002, Plant Physiology.

[15]  S. Rodermel,et al.  Pathways of intracellular communication: tetrapyrroles and plastid-to-nucleus signaling. , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[16]  R. Lister,et al.  A Transcriptomic and Proteomic Characterization of the Arabidopsis Mitochondrial Protein Import Apparatus and Its Response to Mitochondrial Dysfunction1[w] , 2004, Plant Physiology.

[17]  K. Newton,et al.  The maize NCS2 abnormal growth mutant has a chimeric nad4-nad7 mitochondrial gene and is associated with reduced complex I function. , 1994, Genetics.

[18]  A. Rasmusson,et al.  Alternative NAD(P)H dehydrogenases of plant mitochondria. , 2004, Annual review of plant biology.

[19]  R. Lister,et al.  Identification, Expression, and Import of Components 17 and 23 of the Inner Mitochondrial Membrane Translocase from Arabidopsis1,212 , 2003, Plant Physiology.

[20]  A. Rasmusson,et al.  Antimycin A treatment decreases respiratory internal rotenone-insensitive NADH oxidation capacity in potato leaves , 2004, BMC Plant Biology.

[21]  J. Kangasjärvi,et al.  Reactive oxygen species and hormonal control of cell death. , 2003, Trends in plant science.

[22]  A. Millar,et al.  Differential Expression of the Multigene Family Encoding the Soybean Mitochondrial Alternative Oxidase , 1997, Plant physiology.

[23]  V. Madeira,et al.  Differential sensitivities of plant and animal mitochondria to the herbicide paraquat , 2001, Journal of biochemical and molecular toxicology.

[24]  Charles Elkan,et al.  Fitting a Mixture Model By Expectation Maximization To Discover Motifs In Biopolymer , 1994, ISMB.

[25]  Stephen M. Hewitt,et al.  Post-analysis follow-up and validation of microarray experiments , 2002, Nature Genetics.

[26]  A I Saeed,et al.  TM4: a free, open-source system for microarray data management and analysis. , 2003, BioTechniques.

[27]  V. Madeira,et al.  A comparative study of plant and animal mitochondria exposed to paraquat reveals that hydrogen peroxide is not related to the observed toxicity. , 2004, Toxicology in vitro : an international journal published in association with BIBRA.

[28]  James Whelan,et al.  Molecular Distinction between Alternative Oxidase from Monocots and Dicots1 , 2002, Plant Physiology.

[29]  S. Naito,et al.  Characterization of the gene family for alternative oxidase from Arabidopsis thaliana , 1997, Plant Molecular Biology.

[30]  J. Mesirov,et al.  Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. , 1999, Science.

[31]  Peter J. Park,et al.  Comparing expression profiles of genes with similar promoter regions , 2002, Bioinform..

[32]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[33]  I. Møller A new dawn for plant mitochondrial NAD(P)H dehydrogenases. , 2002, Trends in plant science.

[34]  L. Sweetlove,et al.  Activation and Function of Mitochondrial Uncoupling Protein in Plants* , 2004, Journal of Biological Chemistry.

[35]  W. Sakamoto Leaf-variegated mutations and their responsible genes in Arabidopsis thaliana. , 2003, Genes & genetic systems.

[36]  F. Ausubel,et al.  Signal transduction mutants of arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development , 1993, Cell.

[37]  Zhiping Weng,et al.  Computational inference of transcriptional regulatory networks from expression profiling and transcription factor binding site identification. , 2004, Nucleic acids research.

[38]  R. Kornberg,et al.  Chromatin and transcription: where do we go from here. , 2002, Current opinion in genetics & development.

[39]  Daniel MacLean,et al.  Coordination of plastid and nuclear gene expression. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  Jerry Li,et al.  Within the fold: assessing differential expression measures and reproducibility in microarray assays , 2002, Genome Biology.

[41]  J. Whelan,et al.  Regulation of alternative oxidase gene expression in soybean , 2002, Plant Molecular Biology.

[42]  L. Mcintosh,et al.  Higher Plant Mitochondria , 1999, Plant Cell.

[43]  H. Heldt,et al.  Plant biochemistry and molecular biology , 1997 .

[44]  B. Haas,et al.  Transcriptional divergence of the duplicated oxidative stress-responsive genes in the Arabidopsis genome. , 2004, The Plant journal : for cell and molecular biology.

[45]  W. Hess,et al.  Inter-organellar crosstalk in higher plants: impaired chloroplast development affects mitochondrial gene and transcript levels. , 1999, The Plant journal : for cell and molecular biology.

[46]  L. Mcintosh,et al.  Mitochondria/nuclear signaling of alternative oxidase gene expression occurs through distinct pathways involving organic acids and reactive oxygen species , 2004, Plant Cell Reports.

[47]  K. Newton,et al.  The NCS3 mutation: genetic evidence for the expression of ribosomal protein genes in Zea mays mitochondria. , 1991, The EMBO journal.

[48]  R. Nuttall,et al.  An evaluation of the performance of cDNA microarrays for detecting changes in global mRNA expression. , 2001, Nucleic acids research.

[49]  P. Brown,et al.  Exploring the metabolic and genetic control of gene expression on a genomic scale. , 1997, Science.

[50]  L. Sweetlove,et al.  A proteomic analysis of plant programmed cell death. , 2004, Phytochemistry.

[51]  I. Jonassen,et al.  Predicting gene regulatory elements in silico on a genomic scale. , 1998, Genome research.

[52]  Hur-Song Chang,et al.  Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress1,212 , 2002, Plant Physiology.

[53]  Hirokazu Handa,et al.  Isolation and characterization of cDNAs encoding mitochondrial uncoupling proteins in wheat: wheat UCP genes are not regulated by low temperature , 2000, Molecular and General Genetics MGG.

[54]  A. Brennicke,et al.  Arabidopsis Genes Encoding Mitochondrial Type II NAD(P)H Dehydrogenases Have Different Evolutionary Origin and Show Distinct Responses to Light1 , 2003, Plant Physiology.

[55]  V. Walbot,et al.  Maize mitochondria synthesize organ-specific polypeptides. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Ashverya Laxmi,et al.  Global Transcription Profiling Reveals Multiple Sugar Signal Transduction Mechanisms in Arabidopsis , 2004, The Plant Cell Online.

[57]  Roger E Bumgarner,et al.  From co-expression to co-regulation: how many microarray experiments do we need? , 2004, Genome Biology.

[58]  L. Mcintosh,et al.  The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[59]  G. Vanlerberghe,et al.  Signals Regulating the Expression of the Nuclear Gene Encoding Alternative Oxidase of Plant Mitochondria , 1996, Plant physiology.

[60]  E. Davidson,et al.  Genomic cis-regulatory logic: experimental and computational analysis of a sea urchin gene. , 1998, Science.

[61]  J. Siedow,et al.  The mitochondrial cyanide-resistant oxidase: structural conservation amid regulatory diversity. , 2000, Biochimica et biophysica acta.

[62]  William C Reinhold,et al.  MatchMiner: a tool for batch navigation among gene and gene product identifiers , 2003, Genome Biology.

[63]  J. Riesmeier,et al.  A plant cold-induced uncoupling protein , 1997, Nature.

[64]  A. Atteia,et al.  Control of Mitochondrial Function via Photosynthetic Redox Signals , 2004, Photosynthesis Research.

[65]  A. Rasmusson,et al.  Light Regulation of the Arabidopsis Respiratory Chain. Multiple Discrete Photoreceptor Responses Contribute to Induction of Type II NAD(P)H Dehydrogenase Genes1 , 2004, Plant Physiology.

[66]  Kathleen Marchal,et al.  PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences , 2002, Nucleic Acids Res..

[67]  O. Karpova,et al.  Differential Expression of Alternative Oxidase Genes in Maize Mitochondrial Mutants Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.005603. , 2002, The Plant Cell Online.

[68]  J. Riechmann,et al.  Transcriptional Regulation: a Genomic Overview , 2002, The arabidopsis book.

[69]  S. R. Turcinelli,et al.  AtPUMP: an Arabidopsis gene encoding a plant uncoupling mitochondrial protein , 1998, FEBS letters.

[70]  T. Werner,et al.  Computer modeling of promoter organization as a tool to study transcriptional coregulation , 2003, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[71]  J. Sullivan,et al.  Plastid Translation Is Required for the Expression of Nuclear Photosynthesis Genes in the Dark and in Roots of the Pea lip1 Mutant , 1999, Plant Cell.

[72]  G. Vanlerberghe,et al.  Mitochondria-Nucleus Interactions: Evidence for Mitochondrial Retrograde Communication in Plant Cells , 2004 .

[73]  Molecular Localization of a Redox-Modulated Process Regulating Plant Mitochondrial Electron Transport , 1998, Plant Cell.

[74]  N. Avadhani,et al.  Mitochondrial signaling: the retrograde response. , 2004, Molecular cell.

[75]  P. Jarvis Intracellular Signalling: The Language of the Chloroplast , 2003, Current Biology.

[76]  T. Werner,et al.  Regulatory context is a crucial part of gene function. , 2002, Trends in genetics : TIG.

[77]  R. Oelmüller,et al.  A Novel Mechanism of Nuclear Photosynthesis Gene Regulation by Redox Signals from the Chloroplast during Photosystem Stoichiometry Adjustment* , 2001, The Journal of Biological Chemistry.

[78]  E. Boekema,et al.  Structure of a mitochondrial supercomplex formed by respiratory-chain complexes I and III. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[79]  A. Vercesi,et al.  Low temperature and aging‐promoted expression of PUMP in potato tuber mitochondria , 1999, FEBS letters.

[80]  G. Church,et al.  Identifying regulatory networks by combinatorial analysis of promoter elements , 2001, Nature Genetics.

[81]  Jürg Bähler,et al.  Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data , 2003, BMC Genomics.

[82]  Naohiro Kato,et al.  Programmed cell death, mitochondria and the plant hypersensitive response , 2001, Nature.

[83]  L. Mcintosh,et al.  Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. , 2002, The Plant journal : for cell and molecular biology.

[84]  A. McDonald,et al.  Methods and approaches to study plant mitochondrial alternative oxidase. , 2002, Physiologia plantarum.

[85]  Jyoti Shah,et al.  The salicylic acid loop in plant defense. , 2003, Current opinion in plant biology.

[86]  Yoshihiro Ugawa,et al.  Plant cis-acting regulatory DNA elements (PLACE) database: 1999 , 1999, Nucleic Acids Res..

[87]  F Vedel,et al.  Lack of mitochondrial and nuclear-encoded subunits of complex I and alteration of the respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[88]  Day,et al.  Differential expression of alternative oxidase genes in soybean cotyledons during postgerminative development , 1998, Plant physiology.

[89]  A. Millar,et al.  Changes in the Mitochondrial Proteome during the Anoxia to Air Transition in Rice Focus around Cytochrome-containing Respiratory Complexes* , 2004, Journal of Biological Chemistry.

[90]  John M. Hancock,et al.  PlantProm: a database of plant promoter sequences , 2003, Nucleic Acids Res..

[91]  D. Leister,et al.  Retrograde Plastid Redox Signals in the Expression of Nuclear Genes for Chloroplast Proteins of Arabidopsis thaliana* , 2005, Journal of Biological Chemistry.

[92]  Parsons,et al.  In Organello and in Vivo Evidence of the Importance of the Regulatory Sulfhydryl/Disulfide System and Pyruvate for Alternative Oxidase Activity in Tobacco. , 1999, Plant physiology.

[93]  L. Sweetlove,et al.  Superoxide Stimulates a Proton Leak in Potato Mitochondria That Is Related to the Activity of Uncoupling Protein* , 2003, Journal of Biological Chemistry.

[94]  Leif E. Peterson Factor analysis of cluster-specific gene expression levels from cDNA microarrays , 2002, Comput. Methods Programs Biomed..

[95]  J. Stuart,et al.  Superoxide activates mitochondrial uncoupling proteins , 2002, Nature.