Evolutionary implications of the family of 14-3-3 brain protein homologs in Arabidopsis thaliana

The GF14 family of proteins in Arabidopsis thaliana consists of a homologous group of polypeptides ranging in size from ∼27 kDa to ∼32 kDa. As a group, GF14 proteins are also homologous to a family of mammalian proteins most commonly referred to as 14-3-3 proteins. Several distinct and different biochemical activities have been historically attributed to the various isoforms of the mammalian 14-3-3 proteins. These data present the possibility that the various activities are performed by functionally distinct lineages of the gene family. Here we present phylogenetic analyses based on the derived amino acid sequences of five GF14 isoforms expressed in Arabidopsis suspension-cultured cells. A high degree of sequence integrity is apparent in the various Arabidopsis isoforms, and the overall structures of the plant forms are quite conserved with regard to the structures of the known mammalian forms. These gene phylogenies indicate no evolutionary conservation of specific isoform lineages within both plants and animals. Rather, the evolutionary history of this protein appears to be characterized by a separate radiation of plant and animal forms from a common ancestral sequence. Even though the plant and animal forms have evolved independently since that ancestral split, large domains are conserved in both major lineages.

[1]  P. Nielsen.  Primary structure of a human protein kinase regulator protein. , 1991, Biochimica et biophysica acta.

[2]  A. Aitken,et al.  14-3-3 proteins : a highly conserved widespread family of eukaryotic proteins , 2003 .

[3]  T. Isobe,et al.  Brain 14‐3‐3 protein is an activator protein that activates tryptophan 5‐monooxygenase and tyrosine 3‐monooxygenase in the presence of Ca2+,calmodulin‐dependent protein kinase II , 1987, FEBS letters.

[4]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[5]  R. Kuwano,et al.  Widespread Distribution of the 14‐3‐3 Protein in Vertebrate Brains and Bovine Tissues: Correlation with the Distributions of Calcium‐Dependent Protein Kinases , 1991, Journal of neurochemistry.

[6]  M. Nei,et al.  The neighbor-joining method , 1987 .

[7]  E. Lagendijk,et al.  Characterization of the yeast BMH1 gene encoding a putative protein homologous to mammalian protein kinase II activators and protein kinase C inhibitors , 1992, FEBS letters.

[8]  H. Thordal-Christensen,et al.  A pathogen-induced gene of barley encodes a protein showing high similarity to a protein kinase regulator. , 1992, The Plant journal : for cell and molecular biology.

[9]  Masahiko Watanabe,et al.  Molecular cloning of cDNA to rat 14-3-3 η chain polypeptide and the neuronal expression of the mRNA in the central nervous system , 1991 .

[10]  K. Swanson,et al.  Characterization of a Drosophila melanogaster gene similar to the mammalian genes encoding the tyrosine/tryptophan hydroxylase activator and protein kinase C inhibitor proteins. , 1992, Gene.

[11]  R. Burgoyne,et al.  Exol and Exo2 proteins stimulate calcium-dependent exocytosis in permeabilized adrenal chromaff in cells , 1992, Nature.

[12]  A. Toker,et al.  Multiple isoforms of a protein kinase C inhibitor (KCIP-1/14-3-3) from sheep brain. Amino acid sequence of phosphorylated forms. , 1992, European journal of biochemistry.

[13]  A. Toker,et al.  Kinase and neurotransmitters , 1990, Nature.

[14]  A. Aitken,et al.  A plant homologue to mammalian brain 14‐3‐3 protein and protein kinase C inhibitor , 1992, FEBS letters.

[15]  G. Martens,et al.  Evolutionary conservation of the 14-3-3 protein. , 1992, Biochemical and biophysical research communications.

[16]  A. Toker,et al.  Protein kinase C inhibitor proteins. Purification from sheep brain and sequence similarity to lipocortins and 14-3-3 protein. , 1990, European journal of biochemistry.

[17]  A. Kato,et al.  Isolation and characterization of a rice cDNA similar to the bovine brain-specific 14-3-3 protein gene , 2004, Plant Molecular Biology.

[18]  N. de Vetten,et al.  A maize protein associated with the G-box binding complex has homology to brain regulatory proteins. , 1992, The Plant cell.

[19]  T. Isobe,et al.  Activation of protein kinase C by the 14‐3‐3 proteins homologous with Exol protein that stimulates calcium‐dependent exocytosis , 1992, FEBS letters.

[20]  R. Ferl,et al.  Brain proteins in plants: an Arabidopsis homolog to neurotransmitter pathway activators is part of a DNA binding complex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[21]  F. D. Carlson.  Physiological and Biochemical Aspects of Nervous Integration , 1968 .

[22]  R. Kuwano,et al.  Distinct forms of the protein kinase-dependent activator of tyrosine and tryptophan hydroxylases. , 1991, Journal of molecular biology.

[23]  R. Burgoyne,et al.  Interaction between protein kinase C and Exo1 (14-3-3 protein) and its relevance to exocytosis in permeabilized adrenal chromaffin cells. , 1992, The Biochemical journal.

[24]  R. Gross,et al.  Cloning and expression of a human 14-3-3 protein mediating phospholipolysis. Identification of an arachidonoyl-enzyme intermediate during catalysis. , 1992, The Journal of biological chemistry.