Evolution of the Phosphoenolpyruvate Carboxylase Protein Kinase Family in C3 and C4 Flaveria spp.
The key enzyme for C4photosynthesis, Phosphoenolpyruvate Carboxylase (PEPC), evolved from nonphotosynthetic PEPC found in C3ancestors. In all plants, PEPC is phosphorylated by Phosphoenolpyruvate Carboxylase Protein Kinase (PPCK). However, differences in the phosphorylation pattern exist among plants with these photosynthetic types, and it is still not clear if they are due to interspecies differences or depend on photosynthetic type. The genus Flaveria contains closely related C3, C3-C4intermediate, and C4species, which are evolutionarily young and thus well suited for comparative analysis. To characterize the evolutionary differences in PPCK between plants with C3and C4photosynthesis, transcriptome libraries from nine Flaveria spp. were used, and a two-member PPCK family (PPCKA and PPCKB) was identified. Sequence analysis identified a number of C3- and C4-specific residues with various occurrences in the intermediates. Quantitative analysis of transcriptome data revealed that PPCKA and PPCKB exhibit inverse diel expression patterns and that C3and C4Flaveria spp. differ in the expression levels of these genes. PPCKA has maximal expression levels during the day, whereas PPCKB has maximal expression during the night. Phosphorylation patterns of PEPC varied among C3and C4Flaveria spp. too, with PEPC from the C4species being predominantly phosphorylated throughout the day, while in the C3species the phosphorylation level was maintained during the entire 24 h. Since C4Flaveria spp. evolved from C3ancestors, this work links the evolutionary changes in sequence, PPCK expression, and phosphorylation pattern to an evolutionary phase shift of kinase activity from a C3to a C4mode.
Institut für Entwicklungs- und Molekularbiologie der Pflanzen (S.H.A., J.M., U.G., P.W., B.A.), Molecular Proteomics Laboratory (D.M.W.-L., K.S.), and Biochemische Pflanzenphysiologie (G.G.), Heinrich-Heine-Universität, 40225 Duesseldorf, Germany;Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.E.W., T.D.S.); andCluster of Excellence on Plant Sciences, From Complex Traits towards Synthetic Modules, 40225 Duesseldorf, Germany (K.S., G.G., U.G., P.W., B.A.).
Sophia H
SH
Aldous
Institut für Entwicklungs- und Molekularbiologie der Pflanzen (S.H.A., J.M., U.G., P.W., B.A.), Molecular Proteomics Laboratory (D.M.W.-L., K.S.), and Biochemische Pflanzenphysiologie (G.G.), Heinrich-Heine-Universität, 40225 Duesseldorf, Germany;Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.E.W., T.D.S.); andCluster of Excellence on Plant Sciences, From Complex Traits towards Synthetic Modules, 40225 Duesseldorf, Germany (K.S., G.G., U.G., P.W., B.A.).
Sean E
SE
Weise
Institut für Entwicklungs- und Molekularbiologie der Pflanzen (S.H.A., J.M., U.G., P.W., B.A.), Molecular Proteomics Laboratory (D.M.W.-L., K.S.), and Biochemische Pflanzenphysiologie (G.G.), Heinrich-Heine-Universität, 40225 Duesseldorf, Germany;Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.E.W., T.D.S.); andCluster of Excellence on Plant Sciences, From Complex Traits towards Synthetic Modules, 40225 Duesseldorf, Germany (K.S., G.G., U.G., P.W., B.A.).
Thomas D
TD
Sharkey
Institut für Entwicklungs- und Molekularbiologie der Pflanzen (S.H.A., J.M., U.G., P.W., B.A.), Molecular Proteomics Laboratory (D.M.W.-L., K.S.), and Biochemische Pflanzenphysiologie (G.G.), Heinrich-Heine-Universität, 40225 Duesseldorf, Germany;Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.E.W., T.D.S.); andCluster of Excellence on Plant Sciences, From Complex Traits towards Synthetic Modules, 40225 Duesseldorf, Germany (K.S., G.G., U.G., P.W., B.A.).
Daniel M
DM
Waldera-Lupa
Institut für Entwicklungs- und Molekularbiologie der Pflanzen (S.H.A., J.M., U.G., P.W., B.A.), Molecular Proteomics Laboratory (D.M.W.-L., K.S.), and Biochemische Pflanzenphysiologie (G.G.), Heinrich-Heine-Universität, 40225 Duesseldorf, Germany;Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.E.W., T.D.S.); andCluster of Excellence on Plant Sciences, From Complex Traits towards Synthetic Modules, 40225 Duesseldorf, Germany (K.S., G.G., U.G., P.W., B.A.).
Kai
K
Stühler
Institut für Entwicklungs- und Molekularbiologie der Pflanzen (S.H.A., J.M., U.G., P.W., B.A.), Molecular Proteomics Laboratory (D.M.W.-L., K.S.), and Biochemische Pflanzenphysiologie (G.G.), Heinrich-Heine-Universität, 40225 Duesseldorf, Germany;Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.E.W., T.D.S.); andCluster of Excellence on Plant Sciences, From Complex Traits towards Synthetic Modules, 40225 Duesseldorf, Germany (K.S., G.G., U.G., P.W., B.A.).
Julia
J
Mallmann
Institut für Entwicklungs- und Molekularbiologie der Pflanzen (S.H.A., J.M., U.G., P.W., B.A.), Molecular Proteomics Laboratory (D.M.W.-L., K.S.), and Biochemische Pflanzenphysiologie (G.G.), Heinrich-Heine-Universität, 40225 Duesseldorf, Germany;Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.E.W., T.D.S.); andCluster of Excellence on Plant Sciences, From Complex Traits towards Synthetic Modules, 40225 Duesseldorf, Germany (K.S., G.G., U.G., P.W., B.A.).
Georg
G
Groth
Institut für Entwicklungs- und Molekularbiologie der Pflanzen (S.H.A., J.M., U.G., P.W., B.A.), Molecular Proteomics Laboratory (D.M.W.-L., K.S.), and Biochemische Pflanzenphysiologie (G.G.), Heinrich-Heine-Universität, 40225 Duesseldorf, Germany;Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.E.W., T.D.S.); andCluster of Excellence on Plant Sciences, From Complex Traits towards Synthetic Modules, 40225 Duesseldorf, Germany (K.S., G.G., U.G., P.W., B.A.).
Udo
U
Gowik
Institut für Entwicklungs- und Molekularbiologie der Pflanzen (S.H.A., J.M., U.G., P.W., B.A.), Molecular Proteomics Laboratory (D.M.W.-L., K.S.), and Biochemische Pflanzenphysiologie (G.G.), Heinrich-Heine-Universität, 40225 Duesseldorf, Germany;Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.E.W., T.D.S.); andCluster of Excellence on Plant Sciences, From Complex Traits towards Synthetic Modules, 40225 Duesseldorf, Germany (K.S., G.G., U.G., P.W., B.A.).
Peter
P
Westhoff
Institut für Entwicklungs- und Molekularbiologie der Pflanzen (S.H.A., J.M., U.G., P.W., B.A.), Molecular Proteomics Laboratory (D.M.W.-L., K.S.), and Biochemische Pflanzenphysiologie (G.G.), Heinrich-Heine-Universität, 40225 Duesseldorf, Germany;Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.E.W., T.D.S.); andCluster of Excellence on Plant Sciences, From Complex Traits towards Synthetic Modules, 40225 Duesseldorf, Germany (K.S., G.G., U.G., P.W., B.A.) arsova@hhu.de.
Borjana
B
Arsova