Skip to main content
SpringerLink
Log in

A reporter gene system used to study developmental expressionof alternative oxidase and isolate mitochondrial retrograde regulationmutants in Arabidopsis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Perturbation of mitochondrial function causes altered nuclear gene expression in plants. To study this response, called mitochondrial retrograde regulation, and developmental gene expression, a transgenic Arabidopsis thaliana (Col-0) line containing a firefly luciferase gene controlled by a promoter region of the Arabidopsis alternative oxidase 1a gene (AtAOX1a) was created. The transgene and the endogenous gene were developmentally induced in young cotyledons to a level higher than in older cotyledons and leaves. Analysis of transgene expression suggests that this is true for emerging leaves as well. Antimycin A (AA), a mitochondrial electron transport chain inhibitor, and monofluroacetate (MFA), a TCA cycle inhibitor, induced expression of the transgene and the endogenous gene in parallel. The following comparative responses of the transgene to inhibitors were observed: (a) the response in cotyledons to AA treatment differed greatly in magnitude from the response in leaves; (b) the induction kinetics in cotyledons following MFA treatment differed greatly from the kinetics in leaves; and (c) the induction kinetics following MFA treatment differed from the kinetics of AA in both leaves and cotyledons. The transgenic line was used in a genetic screen to isolate mutants with greatly decreased transgene and AtAOX1a induction in response to AA. Some of these mutant lines showed greatly decreased induction by MFA, but one did not. Taken altogether, the data provide genetic evidence that suggests that induction of the AtAOX1a gene by distinct mitochondrial perturbations are via distinct, but overlapping signaling pathways that are tissue specific.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AA:

antimycin A

AOX:

alternative oxidase

AP:

alternative respiratory pathway

CP:

cytochrome respiratory pathway

COX:

cytochrome oxidase

luc + :

enhanced firefly luciferase gene

MFA:

monofluoroacetate

mrrd:

mitochondrial retrograde regulation deficient

mtETC:

mitochondrial electron transport chain

ROS:

reactive oxygen species

TCA:

tricarboxylic acid

UQ:

ubiquinone/ubiquinol

References

  • H. Aguilaniu L. Gustafsson M. Rigoulet T Nystrom (2001) ArticleTitleProtein oxidation in G0 cells of Saccharomyces cerevisiae depends on the state rather than rate of respiration and is enhanced in pos9 but not yap1 mutants J. Biol. Chem. 276 35396–35404 Occurrence Handle10.1074/jbc.M101796200 Occurrence Handle1:CAS:528:DC%2BD3MXntFaiu7g%3D Occurrence Handle11431467

    Article  CAS  PubMed  Google Scholar 

  • T. Arnould S. Vankoningsloo P. Renard A. Houbion N. Ninane C. Demazy J. Remacle M Raes (2002) ArticleTitleCREB activation induced by mitochondrial dysfunction is a new signaling pathway that impairs cell proliferation EMBO J. 21 53–63 Occurrence Handle10.1093/emboj/21.1.53 Occurrence Handle1:CAS:528:DC%2BD38XpsFCjtw%3D%3D Occurrence Handle11782425

    Article  CAS  PubMed  Google Scholar 

  • G. Biswas O.A. Adebanjo B.D. Freedman H.K. Anandatheerthavarada C. Vijayasarathy M. Zaidi M. Kotlikoff N.G Avadhani (1999) ArticleTitleRetrograde Ca2+ signaling in C2C12 skeletal myocytes in response to mitochondrial genetic and metabolic stress: a novel mode of inter-organelle crosstalk EMBO J. 18 522–533 Occurrence Handle10.1093/emboj/18.3.522 Occurrence Handle1:CAS:528:DyaK1MXhslaisr0%3D Occurrence Handle9927412

    Article  CAS  PubMed  Google Scholar 

  • A. Boveris E Cadenas (1982) ArticleTitleProduction of superoxide radicals and hydrogen peroxide in mitochondria In Superoxide Dismutase L.W. Oberley, ed (Boca Raton, FL CRC–Press), pp 15–30

    Google Scholar 

  • S.A Bustin (2002) ArticleTitleQuantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems J. Mol. Endocrinol. 29 23–39 Occurrence Handle10.1677/jme.0.0290023 Occurrence Handle1:CAS:528:DC%2BD38XmvFOhu7s%3D Occurrence Handle12200227

    Article  CAS  PubMed  Google Scholar 

  • N.S. Chandel D.S. McClintock C.E. Feliciano T.M. Wood J.A. Melendez A.M. Rodriguez P.T Schumacker (2000) ArticleTitleReactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1 alpha during hypoxia- A mechanism of O-2 sensing J. Biol. Chem. 275 25130–25138 Occurrence Handle1:CAS:528:DC%2BD3cXmtVeiur4%3D Occurrence Handle10833514

    CAS  PubMed  Google Scholar 

  • S.J. Clough A.F Bent (1998) ArticleTitleFloral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Plant J. 16 735–743

    Google Scholar 

  • I. Djajanegara P.M. Finnegan C. Mathieu T. McCabe J. Whelan D.A Day (2002) ArticleTitleRegulation of alternative oxidase gene expression in soybean Plant Mol. Biol. 50 735–742 Occurrence Handle1:CAS:528:DC%2BD38Xms1ekt70%3D Occurrence Handle12374304

    CAS  PubMed  Google Scholar 

  • C. Dutilleul M. Garmier G. Noctor C. Mathieu P Chetrit C.H. Foyer R Paepe (2003) ArticleTitleLeaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation Plant Cell 15 1212–1226 Occurrence Handle1:CAS:528:DC%2BD3sXjvV2htbs%3D Occurrence Handle12724545

    CAS  PubMed  Google Scholar 

  • T.E. Elthon R.L. Nickels L Mcintosh (1989) ArticleTitleMitochondrial Events During Development of Thermogenesis in Sauromatum-guttatum (Schott) Planta 180 82–89 Occurrence Handle1:CAS:528:DyaK3cXlt1GhtQ%3D%3D

    CAS  Google Scholar 

  • D.F. Gómez-Casati M.V. Busi N. Gonzalez-Schain A. Mouras E.J. Zabaleta A Araya (2002) ArticleTitleA mitochondrial dysfunction induces the expression of nuclear-encoded complex I genes in engineered male sterile Arabidopsis thaliana FEBS Let. 532 70–74

    Google Scholar 

  • G.R. Gray D.P. Maxwell A.R. Villarimo L McIntosh (2004) ArticleTitleMitochondria/nuclear signaling of alternative oxidase gene expression occurs through distinct pathways involving organic acids and reactive oxygen species Plant Cell Rep. 23 497–503 Occurrence Handle1:CAS:528:DC%2BD2cXhtVagtr%2FI

    CAS  Google Scholar 

  • K. Gregg B. Hamdorf K. Henderson J. Kopecny C Wong (1998) ArticleTitleGenetically modified ruminal bacteria protect sheep from fluoroacetate poisoning Appl. Environ. Microbiol. 64 3496–3498 Occurrence Handle1:CAS:528:DyaK1cXmtVajtb4%3D Occurrence Handle9726903

    CAS  PubMed  Google Scholar 

  • M. Gülden S. Morchel H Seibert (2001) ArticleTitleFactors influencing nominal effective concentrations of chemical compounds in vitro: cell concentration Toxicol. In Vitro 15 233–243 Occurrence Handle11377096

    PubMed  Google Scholar 

  • P. Hajdukiewicz Z. Svab P Maliga (1994) ArticleTitleThe small, versatile pPZP family of Agrobacterium binary vectors for plant transformation Plant Mol. Biol. 25 989–994 Occurrence Handle1:CAS:528:DyaK2MXhsVWksLk%3D Occurrence Handle7919218

    CAS  PubMed  Google Scholar 

  • M. Hernould S. Suharsono E. Zabaleta J.P. Carde S. Litvak A. Araya A Mouras (1998) ArticleTitleImpairment of tapetum and mitochondria in engineered male-sterile tobacco plants Plant Mol. Biol. 36 499–508 Occurrence Handle1:CAS:528:DyaK1cXht1eltL8%3D Occurrence Handle9484445

    CAS  PubMed  Google Scholar 

  • J.I. Jeong Y.W. Lee Y.K Kim (2003) ArticleTitleChemical hypoxia-induced cell death in human glioma cells: role of reactive oxygen species, ATP depletion, mitochondrial damage and Ca2+ Neurochem. Res. 28 1201–1211 Occurrence Handle1:CAS:528:DC%2BD3sXks1OrtLo%3D Occurrence Handle12834260

    CAS  PubMed  Google Scholar 

  • O.V. Karpova E.V. Kuzmin T.E. Elthon K.J Newton (2002) ArticleTitleDifferential expression of alternative oxidase genes in maize mitochondrial mutants Plant Cell 14 3271–3284 Occurrence Handle1:CAS:528:DC%2BD3sXhtFCksA%3D%3D Occurrence Handle12468742

    CAS  PubMed  Google Scholar 

  • J.A. Kreps Y.J. Wu H.S. Chang T. Zhu X. Wang J.F Harper (2002) ArticleTitleTranscriptome changes for Arabidopsis in response to salt, osmotic, and cold stress Plant Physiol. 130 2129–2141 Occurrence Handle1:CAS:528:DC%2BD3sXktlym Occurrence Handle12481097

    CAS  PubMed  Google Scholar 

  • A.M. Kumar D Soll (1992) ArticleTitleArabidopsis alternative oxidase sustains Escherichia coli respiration Proc. Natl. Acad. Sci. USA 89 10842–10846 Occurrence Handle1:CAS:528:DyaK3sXkvFWitL4%3D Occurrence Handle1438286

    CAS  PubMed  Google Scholar 

  • S. Kushnir E. Babiychuk S. Storozhenko M.W. Davey J. Papenbrock R. Rycke ParticleDe G. Engler U.W. Stephan H. Lange G. Kispal R. Lill M Montagu ParticleVan (2001) ArticleTitleA mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik Plant Cell 13 89–100 Occurrence Handle1:CAS:528:DC%2BD3MXjslCrtrs%3D Occurrence Handle11158531

    CAS  PubMed  Google Scholar 

  • E.V. Kuzmin O.V. Karpova T.E.K.J Elthon Newton (2004) ArticleTitleMitochondrial respiratory deficiencies signal up-regulation of genes for heat shock proteins J. Biol. Chem. 279 20672–20677 Occurrence Handle1:CAS:528:DC%2BD2cXjvV2nsr0%3D Occurrence Handle15016808

    CAS  PubMed  Google Scholar 

  • B.H. Lee H.J. Lee L.M. Xiong J.K Zhu (2002) ArticleTitleA mitochondrial complex I defect impairs cold-regulated nuclear gene expression Plant Cell 14 1235–1251 Occurrence Handle1:CAS:528:DC%2BD38Xlt1amu7c%3D Occurrence Handle12084824

    CAS  PubMed  Google Scholar 

  • X.S. Liao W.C. Small P.A. Srere R.A Butow (1991) ArticleTitleIntramitochondrial functions regulate non-mitochondrial citrate synthase (CIT2) expression in Saccharomyces cerevisiae Mol. Cell. Biol. 11 38–46 Occurrence Handle1:CAS:528:DyaK3MXns1Wnug%3D%3D Occurrence Handle1986232

    CAS  PubMed  Google Scholar 

  • X.S. Liao R.A Butow (1993) ArticleTitleRtg1 and Rtg2 – 2 Yeast Genes Required for a Novel Path of Communication from Mitochondria to the Nucleus Cell 72 61–71 Occurrence Handle1:CAS:528:DyaK3sXltlamu7s%3D Occurrence Handle8422683

    CAS  PubMed  Google Scholar 

  • J. Lightner T. Caspar (1998) Seed mutagenesis in Arabidopsis J. Martínez-Zapater J. Salinas (Eds) Methods in Molecular Biology Arabidopsis Protocols Humana Press Totowa, NJ 91–103

    Google Scholar 

  • D.P. Maxwell Y. Wang L McIntosh (1999) ArticleTitleThe alternative oxidase lowers mitochondrial reactive oxygen production in plant cells Proc. Natl. Acad. Sci. USA. 96 8271–8276 Occurrence Handle1:CAS:528:DyaK1MXltVOrtr8%3D Occurrence Handle10393984

    CAS  PubMed  Google Scholar 

  • D.P. Maxwell R. Nickels L McIntosh (2002) ArticleTitleEvidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence Plant J. 29 269–279 Occurrence Handle1:CAS:528:DC%2BD38XhvFOit7Y%3D Occurrence Handle11844105

    CAS  PubMed  Google Scholar 

  • T.C. McCabe P.M. Finnegan A.H. Millar D.A. Day J Whelan (1998) ArticleTitleDifferential expression of alternative oxidase genes in soybean cotyledons during postgerminative development Plant Physiol. 118 675–682 Occurrence Handle1:CAS:528:DyaK1cXmslyqtbg%3D Occurrence Handle9765553

    CAS  PubMed  Google Scholar 

  • N. Minagawa S. Koga M. Nakano S. Sakajo A Yoshimoto (1992) ArticleTitlePossible involvement of superoxide anion in the induction of cyanide-resistant respiration in Hansenula anomala FEBS Let. 302 217–219 Occurrence Handle1:CAS:528:DyaK38Xkt1ejtLc%3D

    CAS  Google Scholar 

  • I.M Møller (2001) ArticleTitlePlant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species Annu. Rev. Plant Physiol. Plant Mol. Biol. 52 561–591 Occurrence Handle11337409

    PubMed  Google Scholar 

  • M.G. Murray W.F Thompson (1980) ArticleTitleRapid isolation of high molecular weight plant DNA Nucl. Acids Res. 8 4321–4325 Occurrence Handle1:CAS:528:DyaL3cXmtVSmtL8%3D Occurrence Handle7433111

    CAS  PubMed  Google Scholar 

  • S. Neill R. Desikan J Hancock (2002) ArticleTitleHydrogen peroxide signalling Curr. Opin. Plant Biol. 5 388–395 Occurrence Handle1:CAS:528:DC%2BD38XmtlGjtL8%3D Occurrence Handle12183176

    CAS  PubMed  Google Scholar 

  • N.E. Owen P.T. Chaure I.F Connerton (1992) ArticleTitleIsolation and characterization of new fluoroacetate resistant/acetate non-utilizing mutants of Neurospora crassa J. Gen. Microbiol. 138 2599–2608 Occurrence Handle1:CAS:528:DyaK3sXns1yhsg%3D%3D Occurrence Handle1362582

    CAS  PubMed  Google Scholar 

  • K. Padmasree A.S Raghavendra (2001) ArticleTitleConsequence of restricted mitochondrial oxidative metabolism on photosynthetic carbon assimilation in mesophyll protoplasts: Decrease in light activation of four chloroplastic enzymes Physiol. Plant. 112 582–588 Occurrence Handle1:CAS:528:DC%2BD3MXlslShuro%3D Occurrence Handle11473720

    CAS  PubMed  Google Scholar 

  • L. Padmavathi A.S Raghavendra (2001) ArticleTitleImportance of the cytochrome pathway of mitochondrial electron transport over the alternative pathway during the Kok effect in leaf discs of pea (Pisum sativum) Physiol. Plant. 113 430–434 Occurrence Handle1:CAS:528:DC%2BD3MXosFymsr4%3D Occurrence Handle12060290

    CAS  PubMed  Google Scholar 

  • R.O. Poyton J.E McEwen (1996) ArticleTitleCrosstalk between nuclear and mitochondrial genomes Annu. Rev. Biochem. 65 563–607 Occurrence Handle1:CAS:528:DyaK28XktFamur4%3D Occurrence Handle8811190

    CAS  PubMed  Google Scholar 

  • A.C Purvis (1997) ArticleTitleRole of the alternative oxidase in limiting superoxide production by plant mitochondria Physiol. Plant 100 165–170 Occurrence Handle1:CAS:528:DyaK2sXkvFejs7Y%3D

    CAS  Google Scholar 

  • D.M. Rhoads L McIntosh (1992) ArticleTitleSalicylic-acid regulation of respiration in higher-plants: alternative oxidase expression Plant Cell 4 1131–1139 Occurrence Handle1:CAS:528:DyaK3sXjvFSl Occurrence Handle12297672

    CAS  PubMed  Google Scholar 

  • B.A. Rothermel J.L. Thornton R.A Butow (1997) ArticleTitleRtg3p, a basic helix-loop-helix/leucine zipper protein that functions in mitochondrial-induced changes in gene expression, contains independent activation domains J. Biol. Chem. 272 19801–19807 Occurrence Handle1:CAS:528:DyaK2sXltlGksL0%3D Occurrence Handle9242640

    CAS  PubMed  Google Scholar 

  • D. Saisho E. Nambara S. Naito N. Tsutsumi A. Hirai M Nakazono (1997) ArticleTitleCharacterization of the gene family for alternative oxidase from Arabidopsis thaliana Plant Mol. Biol. 35 585–596 Occurrence Handle1:CAS:528:DyaK2sXmvVers7s%3D Occurrence Handle9349280

    CAS  PubMed  Google Scholar 

  • D. Saisho M. Nakazono N. Tsutsumi A Hirai (2001) ArticleTitleATP synthesis inhibitors as well as respiratory inhibitors increase steady-state level of alternative oxidase mRNA in Arabidopsis thaliana J. Plant Physiol. 158 241–245 Occurrence Handle1:CAS:528:DC%2BD3MXitlSnsbc%3D

    CAS  Google Scholar 

  • J. Sambrook E.F. Fritsch T. Maniatis (1989) Molecular Cloning: A Laboratory Manual, 2nd ed Cold Spring Harbor Press Cold Spring Harbor, NY

    Google Scholar 

  • R. Scholl L. Rivero-Lepinckas D. Crist (1998) Growth of plants and preservation of seeds J. Martínez-Zapater J. Salinas (Eds) Arabidopsis Protocols Humana Press Totowa, NJ 1–12

    Google Scholar 

  • B.A. Sherf K.V Wood (1994) ArticleTitleFirefly luciferase engineered for improved genetic reporting Promega Notes 49 14–21

    Google Scholar 

  • J.N. Siedow A.L Umbach (1995) ArticleTitlePlant Mitochondrial Electron-Transfer and Molecular Biology Plant Cell 7 821–831 Occurrence Handle1:CAS:528:DyaK2MXnt1Sgsbk%3D Occurrence Handle12242388

    CAS  PubMed  Google Scholar 

  • I. Sipos L. Tretter V Adam-Vizi (2003) ArticleTitleQuantitative relationship between inhibition of respiratory complexes and formation of reactive oxygen species in isolated nerve terminals J. Neurochem. 84 112–118 Occurrence Handle1:CAS:528:DC%2BD3sXhtF2iug%3D%3D Occurrence Handle12485407

    CAS  PubMed  Google Scholar 

  • C.C. Subbaiah D.S. Bush M.M Sachs (1994) ArticleTitleElevation of cytosolic calcium precedes anoxic gene-expression in maize suspension-cultured cells Plant Cell 6 1747–1762 Occurrence Handle1:CAS:528:DyaK2MXivVWkt7k%3D Occurrence Handle7866021

    CAS  PubMed  Google Scholar 

  • C.C. Subbaiah D.S. Bush M.M Sachs (1998) ArticleTitleMitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells Plant Physiol. 118 759–771 Occurrence Handle1:CAS:528:DyaK1cXnsFektrs%3D Occurrence Handle9808720

    CAS  PubMed  Google Scholar 

  • N.L. Taylor D.A. Day A.H Millar (2002) ArticleTitleEnvironmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxylase J. Biol. Chem. 277 42663–42668 Occurrence Handle1:CAS:528:DC%2BD38Xos1entr8%3D Occurrence Handle12213810

    CAS  PubMed  Google Scholar 

  • D. Thirkettle-Watts T.C. McCabe R. Clifton C. Moore P.M. Finnegan D. Day J Whelan (2003) ArticleTitleAnalysis of the alternative oxidase promoters from soybean Plant Physiol. 133 1158–1169 Occurrence Handle1:CAS:528:DC%2BD3sXptFGit7c%3D Occurrence Handle14551329

    CAS  PubMed  Google Scholar 

  • F. Breusegem ParticleVan E. Vranova J.F. Dat D Inze (2001) ArticleTitleThe role of active oxygen species in plant signal transduction Plant Sci. 161 405–414

    Google Scholar 

  • J. Vandesompele K. Preter ParticleDe F. Pattyn B. Poppe N. Roy ParticleVan A. Paepe F Speleman ParticleDe (2002) ArticleTitleAccurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes Genome Biol. 3 00341–003411

    Google Scholar 

  • G.C. Vanlerberghe L McIntosh (1992) ArticleTitleLower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco Plant Physiol. 100 115–119 Occurrence Handle1:CAS:528:DyaK38XmsVylsL8%3D

    CAS  Google Scholar 

  • G.C. Vanlerberghe L McIntosh (1994) ArticleTitleMitochondrial electron-transport regulation of nuclear gene-expression – Studies with the alternative oxidase gene of tobacco Plant Physiol. 105 867–874 Occurrence Handle1:CAS:528:DyaK2cXlsFSgtbk%3D Occurrence Handle8058837

    CAS  PubMed  Google Scholar 

  • G.C. Vanlerberghe D.A. Day J.T. Wiskich A.E. Vanlerberghe L McIntosh (1995) ArticleTitleAlternative oxidase activity in tobacco leaf mitochondria: dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation Plant Physiol. 109 353–361 Occurrence Handle1:CAS:528:DyaK2MXoslOqsLk%3D Occurrence Handle12228600

    CAS  PubMed  Google Scholar 

  • G.C. Vanlerberghe L McIntosh (1996) ArticleTitleSignals regulating the expression of the nuclear gene encoding alternative oxidase of plant mitochondria Plant Physiol. 111 589–595 Occurrence Handle1:CAS:528:DyaK28Xjs1Cgsb0%3D Occurrence Handle12226312

    CAS  PubMed  Google Scholar 

  • G.C. Vanlerberghe L McIntosh (1997) ArticleTitleAlternative oxidase: from gene to function Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 703–734 Occurrence Handle1:CAS:528:DyaK2sXjs1eku70%3D Occurrence Handle15012279

    CAS  PubMed  Google Scholar 

  • G.C. Vanlerberghe C.A. Robson J.Y.H Yip (2002) ArticleTitleInduction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death Plant Physiol. 129 1829–1842 Occurrence Handle1:CAS:528:DC%2BD38Xmtl2gtLo%3D Occurrence Handle12177496

    CAS  PubMed  Google Scholar 

  • A. Veiga J.D. Arrabaca M.C Loureiro-Dias (2003) ArticleTitleStress situations induce cyanide-resistant respiration in spoilage yeasts J. Appl. Microbiol. 95 364–371 Occurrence Handle1:CAS:528:DC%2BD3sXntFOrurg%3D Occurrence Handle12859770

    CAS  PubMed  Google Scholar 

  • A.M Wagner (1995) ArticleTitleA role for active oxygen species as 2nd messengers in the induction of alternative oxidase gene-expression in petunia-hybrida cells FEBS Let. 368 339–342 Occurrence Handle1:CAS:528:DyaK2MXntFCrs7o%3D

    CAS  Google Scholar 

  • D. Weigel J. Glazebrook (2002) Arabidopsis: a laboratory manual Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY

    Google Scholar 

  • N. Yao Y. Tada M. Sakamoto H. Nakayashiki P. Park Y. Tosa S Mayama (2002) ArticleTitleMitochondrial oxidative burst involved in apoptotic response in oats Plant J. 30 567–579 Occurrence Handle1:CAS:528:DC%2BD38XlsFyktLg%3D Occurrence Handle12047631

    CAS  PubMed  Google Scholar 

  • J.L. Zhou F.C. Kauffman C.H. Ballow R.G Thurman (1984) ArticleTitleInhibition of mixed-function oxidation in perfused rat liver by fluoroacetate treatment Biochem. Pharmacol. 33 319–323 Occurrence Handle1:CAS:528:DyaL2cXhs12nu78%3D Occurrence Handle6704153

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Life Sciences Arizona, State University, Box 874501, Tempe, AZ , 85287, USA

    Jelena Zarkovic & David M. Rhoads

  2. DuPont Qualicon, 3531 Silverside Road, Wilmington, DE, 19810, USA

    Shawn L. Anderson

Authors
  1. Jelena Zarkovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shawn L. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David M. Rhoads
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David M. Rhoads.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zarkovic, J., Anderson, S.L. & Rhoads, D.M. A reporter gene system used to study developmental expressionof alternative oxidase and isolate mitochondrial retrograde regulationmutants in Arabidopsis. Plant Mol Biol 57, 871–888 (2005). https://doi.org/10.1007/s11103-005-3249-0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-005-3249-0

Keywords

Search

Navigation