TY - JOUR

T1 - Life without complex I

T2 - Proteome analyses of an Arabidopsis mutant lacking the mitochondrial NADH dehydrogenase complex

AU - Fromm, Steffanie

AU - Senkler, Jennifer

AU - Eubel, Holger

AU - Peterhänsel, Christoph

AU - Braun, Hans Peter

N1 - Funding information: We gratefully acknowledge the technical assistance of Dagmar Lewejohann and Dr Christin Lorenz. We thank Dr Tatjana Hildebrandt and Dr Ahmed Debez for critically reading the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft (DFG), Forschergruppe 1186 (grant Br1829/10-2)

PY - 2016/4/27

Y1 - 2016/4/27

N2 - The mitochondrial NADH dehydrogenase complex (complex I) is of particular importance for the respiratory chain in mitochondria. It is the major electron entry site for the mitochondrial electron transport chain (mETC) and therefore of great significance for mitochondrial ATP generation. We recently described an Arabidopsis thaliana double-mutant lacking the genes encoding the carbonic anhydrases CA1 and CA2, which both form part of a plant-specific 'carbonic anhydrase domain' of mitochondrial complex I. The mutant lacks complex I completely. Here we report extended analyses for systematically characterizing the proteome of the ca1ca2 mutant. Using various proteomic tools, we show that lack of complex I causes reorganization of the cellular respiration system. Reduced electron entry into the respiratory chain at the first segment of the mETC leads to induction of complexes II and IV as well as alternative oxidase. Increased electron entry at later segments of the mETC requires an increase in oxidation of organic substrates. This is reflected by higher abundance of proteins involved in glycolysis, the tricarboxylic acid cycle and branched-chain amino acid catabolism. Proteins involved in the light reaction of photosynthesis, the Calvin cycle, tetrapyrrole biosynthesis, and photorespiration are clearly reduced, contributing to the significant delay in growth and development of the double-mutant. Finally, enzymes involved in defense against reactive oxygen species and stress symptoms are much induced. These together with previously reported insights into the function of plant complex I, which were obtained by analysing other complex I mutants, are integrated in order to comprehensively describe 'life without complex I'.

AB - The mitochondrial NADH dehydrogenase complex (complex I) is of particular importance for the respiratory chain in mitochondria. It is the major electron entry site for the mitochondrial electron transport chain (mETC) and therefore of great significance for mitochondrial ATP generation. We recently described an Arabidopsis thaliana double-mutant lacking the genes encoding the carbonic anhydrases CA1 and CA2, which both form part of a plant-specific 'carbonic anhydrase domain' of mitochondrial complex I. The mutant lacks complex I completely. Here we report extended analyses for systematically characterizing the proteome of the ca1ca2 mutant. Using various proteomic tools, we show that lack of complex I causes reorganization of the cellular respiration system. Reduced electron entry into the respiratory chain at the first segment of the mETC leads to induction of complexes II and IV as well as alternative oxidase. Increased electron entry at later segments of the mETC requires an increase in oxidation of organic substrates. This is reflected by higher abundance of proteins involved in glycolysis, the tricarboxylic acid cycle and branched-chain amino acid catabolism. Proteins involved in the light reaction of photosynthesis, the Calvin cycle, tetrapyrrole biosynthesis, and photorespiration are clearly reduced, contributing to the significant delay in growth and development of the double-mutant. Finally, enzymes involved in defense against reactive oxygen species and stress symptoms are much induced. These together with previously reported insights into the function of plant complex I, which were obtained by analysing other complex I mutants, are integrated in order to comprehensively describe 'life without complex I'.

KW - Arabidopsis thaliana

KW - Carbonic anhydrase

KW - Complex I

KW - Mitochondrial metabolism

KW - Photosynthesis

KW - Proteomics

KW - Respiratory chain

UR - http://www.scopus.com/inward/record.url?scp=84969972759&partnerID=8YFLogxK

U2 - 10.1093/jxb/erw165

DO - 10.1093/jxb/erw165

M3 - Article

C2 - 27122571

AN - SCOPUS:84969972759

VL - 67

SP - 3079

EP - 3093

JO - Journal of experimental botany

JF - Journal of experimental botany

SN - 0022-0957

IS - 10

ER -