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Origin, Evolution, and Metabolic Role of a Novel Glycolytic GAPDH Enzyme Recruited by Land Plant Plastids

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Abstract

NAD-specific glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is a cytosolic marker enzyme of eukaryotes (GapC; EC 1.2.1.12). Land plants possess an additional NADP+-dependent enzyme (EC 1.2.1.13) within their chloroplasts which is composed of two subunits, GapA and GapB. Another plastid GAPDH enzyme (GapCp) was recently discovered in gymnosperms and ferns. This novel GapCp is closely related to cytosolic GapC and displays glycolytic NAD+ cosubstrate specificity. Here we show that this new gene GapCp is also present and actively expressed in angiosperms, mosses, and liverworts. Phylogenetic analyses of the available GapC and GapCp sequences suggest that the gene duplication giving rise to GapCp occurred in ancestral charophyte algae. The data are also consistent with a monophyletic origin of charophytes and land plants and further support the view that land plants arose from a Coleochaete-like green alga. Northern hybridizations were employed to study the expression of the genes GapCp, GapC, GapA, and GapB in green and nongreen tissues from pepper (Capsicum annuum). The results demonstrate that GapCp mRNAs are mainly expressed in red pepper fruit and roots, in which the transcript levels of photosynthetic GapA and GapB are downregulated. This suggests that in flowering plants GapCp plays a specific role in glycolytic energy production of nongreen plastids such as chromoplasts and leukoplasts and that angiosperms may be the only land plants where glycolysis is absent in green chloroplasts.

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Acknowledgements

We thank William Martin (Düsseldorf) for the cDNA library from Physcomitrella patens, Steph Seufert (DSMZ, Braunschweig) for the sterile culture from Marchantia polymorpha, and Walter Wimmer (Salzgitter) for provision and identification Chara vulgaris and Sphagnum cuspidatum. Major financial support, including a Ph.D. stipend for J.P., was received from the Deutsche Forschungsgemeinschaft (priority program “The Molecular Basis of Plant Evolution”).

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Authors and Affiliations

  1. Institute of Genetics, University of Braunschweig, D-38106 Braunschweig, Germany

    Jörn Petersen & Rüdiger Cerff

  2. Institute of Evolutionary Biology, University of Konstanz, D-78457 Konstanz, Germany

    Henner Brinkmann

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  1. Jörn Petersen
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  2. Henner Brinkmann
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Correspondence to Rüdiger Cerff.

Additional information

The nucleotide sequence data will appear in the DDBJ/EMBL/GenBank International Nucleotide Sequence Database under the following accession numbers. PCR clones: AJ246008, AJ246009, AJ246010, AJ246011, and AJ246012 (GapA1, GapA2, GapB, GapC1, and GapC2 of Capsicum annuum); AJ246021 and AJ246022 (GapC and GapCp of Sphagnum cuspidatum); AJ246019 (GapC of Coleochaete scutata); AJ246015 and AJ246016 (GapC1 and GapC2 of Chara vulgaris); AJ246020 (GapC of Klebsormidium flaccidum). cDNA clones: AJ246013, AJ246024, and AJ246025 (GapCp of Capsicum annuum, Marchantia polymorpha, and Physcomitrella patens); AJ236023 (GapC of Marchantia polymorpha). Genomic clones: AJ272042 and AJ272043 (GapCp of Capsicum annuum).

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Petersen, J., Brinkmann, H. & Cerff, R. Origin, Evolution, and Metabolic Role of a Novel Glycolytic GAPDH Enzyme Recruited by Land Plant Plastids . J Mol Evol 57, 16–26 (2003). https://doi.org/10.1007/s00239-002-2441-y

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