Lack of cytochrome c in Arabidopsis decreases stability of Complex IV and modifies redox metabolism without affecting Complexes i and III

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Elina Welchen
  • Tatjana M. Hildebrandt
  • Dagmar Lewejohann
  • Daniel H. Gonzalez
  • Hans Peter Braun

External Research Organisations

  • Universidad Nacional del Litoral
View graph of relations

Details

Original languageEnglish
Pages (from-to)990-1001
Number of pages12
JournalBiochimica et Biophysica Acta - Bioenergetics
Volume1817
Issue number7
Publication statusPublished - 18 Apr 2012

Abstract

We studied the role of cytochrome c (CYTc), which mediates electron transfer between Complexes III and IV, in cellular events related with mitochondrial respiration, plant development and redox homeostasis. We analyzed single and double homozygous mutants in both CYTc-encoding genes from Arabidopsis: CYTC-1 and CYTC-2. While individual mutants were similar to wild-type, knock-out of both genes produced an arrest of embryo development, showing that CYTc function is essential at early stages of plant development. Mutants in which CYTc levels were extremely reduced respective to wild-type had smaller rosettes with a pronounced decrease in parenchymatic cell size and an overall delay in development. Mitochondria from these mutants had lower respiration rates and a relative increase in alternative respiration. Furthermore, the decrease in CYTc severely affected the activity and the amount of Complex IV, without affecting Complexes I and III. Reactive oxygen species levels were reduced in these mutants, which showed induction of genes encoding antioxidant enzymes. Ascorbic acid levels were not affected, suggesting that a small amount of CYTc is enough to support its normal synthesis. We postulate that, in addition to its role as an electron carrier between Complexes III and IV, CYTc influences Complex IV levels in plants, probably reflecting a role of this protein in Complex IV stability. This double function of CYTc most likely explains why it is essential for plant survival.

Keywords

    Arabidopsis thaliana, Cytochrome c, Embryo lethal, Mitochondrion, Respiratory chain complex

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Biophysics
  • Biochemistry, Genetics and Molecular Biology(all)
  • Biochemistry
  • Biochemistry, Genetics and Molecular Biology(all)
  • Cell Biology

Cite this

Lack of cytochrome c in Arabidopsis decreases stability of Complex IV and modifies redox metabolism without affecting Complexes i and III. / Welchen, Elina; Hildebrandt, Tatjana M.; Lewejohann, Dagmar et al.
In: Biochimica et Biophysica Acta - Bioenergetics, Vol. 1817, No. 7, 18.04.2012, p. 990-1001.

Research output: Contribution to journalArticleResearchpeer review

Download
@article{39ec1a5460654709a783e0b152d05474,
title = "Lack of cytochrome c in Arabidopsis decreases stability of Complex IV and modifies redox metabolism without affecting Complexes i and III",
abstract = "We studied the role of cytochrome c (CYTc), which mediates electron transfer between Complexes III and IV, in cellular events related with mitochondrial respiration, plant development and redox homeostasis. We analyzed single and double homozygous mutants in both CYTc-encoding genes from Arabidopsis: CYTC-1 and CYTC-2. While individual mutants were similar to wild-type, knock-out of both genes produced an arrest of embryo development, showing that CYTc function is essential at early stages of plant development. Mutants in which CYTc levels were extremely reduced respective to wild-type had smaller rosettes with a pronounced decrease in parenchymatic cell size and an overall delay in development. Mitochondria from these mutants had lower respiration rates and a relative increase in alternative respiration. Furthermore, the decrease in CYTc severely affected the activity and the amount of Complex IV, without affecting Complexes I and III. Reactive oxygen species levels were reduced in these mutants, which showed induction of genes encoding antioxidant enzymes. Ascorbic acid levels were not affected, suggesting that a small amount of CYTc is enough to support its normal synthesis. We postulate that, in addition to its role as an electron carrier between Complexes III and IV, CYTc influences Complex IV levels in plants, probably reflecting a role of this protein in Complex IV stability. This double function of CYTc most likely explains why it is essential for plant survival.",
keywords = "Arabidopsis thaliana, Cytochrome c, Embryo lethal, Mitochondrion, Respiratory chain complex",
author = "Elina Welchen and Hildebrandt, {Tatjana M.} and Dagmar Lewejohann and Gonzalez, {Daniel H.} and Braun, {Hans Peter}",
note = "Funding information: We gratefully acknowledge Dr. G{\'e}raldine Bonnard (IBMP-CNRS, Strasbourg, France) for her collaboration during initial stages of this work under the cooperative project SECYT-ECOS (A03B04). We also acknowledge Dr. Eduardo Zabaleta (IIB, Mar del Plata, Argentina) for the gift of carbonic anhydrase antibodies and Dr. Raul Comelli for the development of COX2 antibodies. This project was supported by grants from CONICET (Consejo Nacional de Investigaciones Cient{\'i}ficas y T{\'e}cnicas) , ANPCyT (Agencia Nacional de Promoci{\'o}n Cient{\'i}fica y Tecnol{\'o}gica) , and UNL (Universidad Nacional del Litoral) . EW and DHG are members of CONICET and UNL. PostDoc stipend to EW to perform a relevant part of this work in the laboratory of HPB at Hannover University, was supported by the Deutsche Akademische Austauschdienst (DAAD) .",
year = "2012",
month = apr,
day = "18",
doi = "10.1016/j.bbabio.2012.04.008",
language = "English",
volume = "1817",
pages = "990--1001",
journal = "Biochimica et Biophysica Acta - Bioenergetics",
issn = "0005-2728",
publisher = "Elsevier",
number = "7",

}

Download

TY - JOUR

T1 - Lack of cytochrome c in Arabidopsis decreases stability of Complex IV and modifies redox metabolism without affecting Complexes i and III

AU - Welchen, Elina

AU - Hildebrandt, Tatjana M.

AU - Lewejohann, Dagmar

AU - Gonzalez, Daniel H.

AU - Braun, Hans Peter

N1 - Funding information: We gratefully acknowledge Dr. Géraldine Bonnard (IBMP-CNRS, Strasbourg, France) for her collaboration during initial stages of this work under the cooperative project SECYT-ECOS (A03B04). We also acknowledge Dr. Eduardo Zabaleta (IIB, Mar del Plata, Argentina) for the gift of carbonic anhydrase antibodies and Dr. Raul Comelli for the development of COX2 antibodies. This project was supported by grants from CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas) , ANPCyT (Agencia Nacional de Promoción Científica y Tecnológica) , and UNL (Universidad Nacional del Litoral) . EW and DHG are members of CONICET and UNL. PostDoc stipend to EW to perform a relevant part of this work in the laboratory of HPB at Hannover University, was supported by the Deutsche Akademische Austauschdienst (DAAD) .

PY - 2012/4/18

Y1 - 2012/4/18

N2 - We studied the role of cytochrome c (CYTc), which mediates electron transfer between Complexes III and IV, in cellular events related with mitochondrial respiration, plant development and redox homeostasis. We analyzed single and double homozygous mutants in both CYTc-encoding genes from Arabidopsis: CYTC-1 and CYTC-2. While individual mutants were similar to wild-type, knock-out of both genes produced an arrest of embryo development, showing that CYTc function is essential at early stages of plant development. Mutants in which CYTc levels were extremely reduced respective to wild-type had smaller rosettes with a pronounced decrease in parenchymatic cell size and an overall delay in development. Mitochondria from these mutants had lower respiration rates and a relative increase in alternative respiration. Furthermore, the decrease in CYTc severely affected the activity and the amount of Complex IV, without affecting Complexes I and III. Reactive oxygen species levels were reduced in these mutants, which showed induction of genes encoding antioxidant enzymes. Ascorbic acid levels were not affected, suggesting that a small amount of CYTc is enough to support its normal synthesis. We postulate that, in addition to its role as an electron carrier between Complexes III and IV, CYTc influences Complex IV levels in plants, probably reflecting a role of this protein in Complex IV stability. This double function of CYTc most likely explains why it is essential for plant survival.

AB - We studied the role of cytochrome c (CYTc), which mediates electron transfer between Complexes III and IV, in cellular events related with mitochondrial respiration, plant development and redox homeostasis. We analyzed single and double homozygous mutants in both CYTc-encoding genes from Arabidopsis: CYTC-1 and CYTC-2. While individual mutants were similar to wild-type, knock-out of both genes produced an arrest of embryo development, showing that CYTc function is essential at early stages of plant development. Mutants in which CYTc levels were extremely reduced respective to wild-type had smaller rosettes with a pronounced decrease in parenchymatic cell size and an overall delay in development. Mitochondria from these mutants had lower respiration rates and a relative increase in alternative respiration. Furthermore, the decrease in CYTc severely affected the activity and the amount of Complex IV, without affecting Complexes I and III. Reactive oxygen species levels were reduced in these mutants, which showed induction of genes encoding antioxidant enzymes. Ascorbic acid levels were not affected, suggesting that a small amount of CYTc is enough to support its normal synthesis. We postulate that, in addition to its role as an electron carrier between Complexes III and IV, CYTc influences Complex IV levels in plants, probably reflecting a role of this protein in Complex IV stability. This double function of CYTc most likely explains why it is essential for plant survival.

KW - Arabidopsis thaliana

KW - Cytochrome c

KW - Embryo lethal

KW - Mitochondrion

KW - Respiratory chain complex

UR - http://www.scopus.com/inward/record.url?scp=84860794562&partnerID=8YFLogxK

U2 - 10.1016/j.bbabio.2012.04.008

DO - 10.1016/j.bbabio.2012.04.008

M3 - Article

C2 - 22551905

AN - SCOPUS:84860794562

VL - 1817

SP - 990

EP - 1001

JO - Biochimica et Biophysica Acta - Bioenergetics

JF - Biochimica et Biophysica Acta - Bioenergetics

SN - 0005-2728

IS - 7

ER -

By the same author(s)