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Gamma carbonic anhydrases in plant mitochondria

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Abstract

Three genes from Arabidopsis thaliana with high sequence similarity to gamma carbonic anhydrase (γCA), a Zn containing enzyme from Methanosarcina thermophila(CAM), were identified and characterized. Evolutionary and structural analyses predict that these genes code for active forms of γCA. Phylogenetic analyses reveal that these Arabidopsis gene products cluster together with CAM and related sequences from α and γ proteobacteria, organisms proposed as the mitochondrial endosymbiont ancestor. Indeed, in vitro and in vivo experiments indicate that these gene products are transported into the mitochondria as occurs with several mitochondrial protein genes transferred, during evolution, from the endosymbiotic bacteria to the host genome. Moreover, putative CAM orthologous genes are detected in other plants and green algae and were predicted to be imported to mitochondria. Structural modeling and sequence analysis performed in more than a hundred homologous sequences show a high conservation of functionally important active site residues. Thus, the three histidine residues involved in Zn coordination (His 81, 117 and 122), Arg 59, Asp 61, Gin 75, and Asp 76 of CAM are conserved and properly arranged in the active site cavity of the models. Two other functionally important residues (Glu 62 and Glu 84 of CAM) are lacking, but alternative amino acids that might serve to their roles are postulated. Accordingly, we propose that photosynthetic eukaryotic organisms (green algae and plants) contain γCAs and that these enzymes codified by nuclear genes are imported into mitochondria to accomplish their biological function.

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Authors and Affiliations

  1. IB-INTECH (CONICET/UNSAM), IC.C. 164, Instituto de Investigaciones Biotecnologicas, C.C.164, 7130, Chascomus, Argentina

    Gustavo Parisi, María Fornasari, Alejandro Colaneri, Nahuel Schain, Diego Casati & Eduardo Zabaleta

  2. Centro de Estudios de Investigaciones, Universidad Nacional de Quilmes, Roque Sáenz Peña, 180, Argentina

    Mariano Perales & Julián Echave

  3. Department of Biochemistry and Molecular Biology, Eberly College of Science, Pennsylvania State University, University Park, Pennsylvania, United States of America

    Sabrina Zimmermann & James Ferry

  4. Abteilung Molekulare Botanik, Universität Ulm, Albert Einstein Allee, Germany

    Axel Brennicke

  5. UMR 5097 R.E.G.E.R., CNRS-Université, Victor Segalen Bordeaux 2, 146 rue Léo, Saignat, France

    Alejandro Araya

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  1. Gustavo Parisi
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Parisi, G., Perales, M., Fornasari, M. et al. Gamma carbonic anhydrases in plant mitochondria. Plant Mol Biol 55, 193–207 (2004). https://doi.org/10.1007/s11103-004-0149-7

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