TY - JOUR

T1 - Mitochondrial gamma carbonic anhydrases are required for complex I assembly and plant reproductive development

AU - Fromm, Steffanie

AU - Braun, Hans Peter

AU - Peterhansel, Christoph

N1 - This work was supported by the Deutsche Forschungsgemeinschaft (DFG), Forschergruppe 1186 (grant Br1829/10-2). We gratefully acknowledge Professor Dr Traud Winkelmann for her support with DIC microscopy and the embryo rescue technique and Dr Etienne Meyer for providing the ndufs4 mutant.

PY - 2016/5/31

Y1 - 2016/5/31

N2 - Complex I of the mitochondrial electron transport chain (mETC) in plants contains an extra domain that is made up from proteins homologous to prokaryotic gamma-carbonic anhydrases (γCA). This domain has been suggested to participate in complex I assembly or to support transport of mitochondrial CO2 to the chloroplast. Here, we generated mutants lacking CA1 and CA2 - two out of three CA proteins in Arabidopsis thaliana. Double mutants were characterized at the developmental and physiological levels. Furthermore, the composition and activity of the mETC were determined, and mutated CA versions were used for complementation assays. Embryo development of double mutants was strongly delayed and seed development stopped before maturation. Mutant plants could only be rescued on sucrose media, showed severe stress symptoms and never produced viable seeds. By contrast, callus cultures were only slightly affected in growth. Complex I was undetectable in the double mutants, but complex II and complex IV were upregulated concomitant with increased oxygen consumption in mitochondrial respiration. Ectopic expression of inactive CA variants was sufficient to complement the mutant phenotype. Data indicate that CA proteins are structurally required for complex I assembly and that reproductive development is dependent on the presence of complex I.

AB - Complex I of the mitochondrial electron transport chain (mETC) in plants contains an extra domain that is made up from proteins homologous to prokaryotic gamma-carbonic anhydrases (γCA). This domain has been suggested to participate in complex I assembly or to support transport of mitochondrial CO2 to the chloroplast. Here, we generated mutants lacking CA1 and CA2 - two out of three CA proteins in Arabidopsis thaliana. Double mutants were characterized at the developmental and physiological levels. Furthermore, the composition and activity of the mETC were determined, and mutated CA versions were used for complementation assays. Embryo development of double mutants was strongly delayed and seed development stopped before maturation. Mutant plants could only be rescued on sucrose media, showed severe stress symptoms and never produced viable seeds. By contrast, callus cultures were only slightly affected in growth. Complex I was undetectable in the double mutants, but complex II and complex IV were upregulated concomitant with increased oxygen consumption in mitochondrial respiration. Ectopic expression of inactive CA variants was sufficient to complement the mutant phenotype. Data indicate that CA proteins are structurally required for complex I assembly and that reproductive development is dependent on the presence of complex I.

KW - NADH

KW - Arabidopsis thaliana

KW - Carbonic anhydrase (γCA)

KW - Complex I

KW - Mitochondrial metabolism

KW - Respiratory chain

KW - Ubiquinone oxidoreductase

UR - http://www.scopus.com/inward/record.url?scp=84959122278&partnerID=8YFLogxK

U2 - 10.1111/nph.13886

DO - 10.1111/nph.13886

M3 - Article

C2 - 26889912

AN - SCOPUS:84959122278

VL - 211

SP - 194

EP - 207

JO - New Phytologist

JF - New Phytologist

SN - 0028-646X

IS - 1

ER -