An evolutionary conserved group of plant GSK-3/shaggy-like protein kinase genes preferentially expressed in developing pollen.

Genes and cDNAs encoding plant protein kinases highly homologous to the animal GSK-3/shaggy subfamily were isolated from Arabidopsis thaliana, Brassica napus, Petunia hybrida and Nicotiana tabacum using the P. hybrida PSK6 GSK-3/shaggy related cDNA as a probe. All the derived protein sequences contained the characteristic catalytic domain of GSK-3/shaggy protein kinases. Sequence comparisons within the catalytic domain with other plant GSK-3/shaggy like kinases clearly indicate that the novel sequences form an isolated group of genes termed the PSK6 group. All the proteins within this group possess an amino-terminal extension which contains short amino acid motifs highly conserved between species and possibly implicated in mitochondrial targeting. Northern hybridisation experiments and reverse transcriptase PCR analysis demonstrated that these novel cDNAs are predominantly expressed in developing pollen. The three genes isolated from P. hybrida and A. thaliana show the same genomic organisation into 12 introns and 13 exons. Although the size of the introns varies, their positions are conserved between genes and species. The comparison of these gene structures and the analysis of deduced protein sequences belonging to different plants hold important information to understand the function of individual members. They suggest that some of the characterised sequences represent most likely true orthologues whereas others must be paralogues. They also allow us to discuss the evolution of the plant GSK-3/shaggy like gene family with regard to plant speciation.

[1]  Philip R. Cohen,et al.  Multisite phosphorylation of glycogen synthase. Molecular basis for the substrate specificity of glycogen synthase kinase-3 and casein kinase-II (glycogen synthase kinase-5). , 1984, Biochimica et biophysica acta.

[2]  H. Hirt,et al.  The MsK family of alfalfa protein kinase genes encodes homologues of shaggy/glycogen synthase kinase-3 and shows differential expression patterns in plant organs and development. , 1993, The Plant journal : for cell and molecular biology.

[3]  G von Heijne,et al.  Cleavage-site motifs in mitochondrial targeting peptides. , 1990, Protein engineering.

[4]  E. Heberle‐Bors,et al.  Isolation and expression during pollen development of a tobacco cDNA clone encoding a protein kinase homologous to shaggy/glycogen synthase kinase-3. , 1995, Biochimica et biophysica acta.

[5]  B. Neel,et al.  Specific modulation of ectodermal cell fates in Xenopus embryos by glycogen synthase kinase. , 1995, Development.

[6]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[7]  J. Woodgett,et al.  Molecular cloning and expression of glycogen synthase kinase‐3/factor A. , 1990, The EMBO journal.

[8]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[9]  S. McCormick,et al.  Male Gametophyte Development. , 1993, The Plant cell.

[10]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[11]  K. Imahori,et al.  Regulation of mitochondrial pyruvate dehydrogenase activity by tau protein kinase I/glycogen synthase kinase 3beta in brain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[12]  M. Kanehisa,et al.  A knowledge base for predicting protein localization sites in eukaryotic cells , 1992, Genomics.

[13]  A. Depaoli-Roach,et al.  Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. , 1994, The Journal of biological chemistry.

[14]  R. Moon,et al.  WNTs modulate cell fate and behavior during vertebrate development. , 1997, Trends in genetics : TIG.

[15]  R. Insall Glycogen synthase kinase and Dictyostelium development: old pathways pointing in new directions? , 1995, Trends in genetics : TIG.

[16]  P. Cohen,et al.  The α‐isoform of glycogen synthase kinase‐3 from rabbit skeletal muscle is inactivated by p70 S6 kinase or MAP kinase‐activated protein kinase‐1 in vitro , 1994, FEBS letters.

[17]  Norbert Perrimon,et al.  Components of wingless signalling in Drosophila , 1994, Nature.

[18]  T. Hunter,et al.  The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification 1 , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[19]  Peter G. Korning,et al.  Splice Site Prediction in Arabidopsis Thaliana Pre-mRNA by Combining Local and Global Sequence Information , 1996 .

[20]  Harold E. Varmus,et al.  Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos , 1995, Nature.

[21]  L. Hood,et al.  Gene families: the taxonomy of protein paralogs and chimeras. , 1997, Science.

[22]  V. Pantesco,et al.  Drosophila shaggy kinase and rat glycogen synthase kinase-3 have conserved activities and act downstream of Notch , 1993, Nature.

[23]  S. Pierce,et al.  Regulation of Spemann organizer formation by the intracellular kinase Xgsk-3. , 1995, Development.

[24]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[25]  V. Pantesco,et al.  Functional significance of a family of protein kinases encoded at the shaggy locus in Drosophila. , 1993, The EMBO journal.

[26]  W. Gilbert Why genes in pieces? , 1978, Nature.

[27]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[28]  J. P. Mascarenhas Gene Activity During Pollen Development , 1990 .

[29]  T. Hunter,et al.  The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. , 1988, Science.

[30]  M. Kreis,et al.  Petunia hybrida homologues of shaggy/zeste-white 3 expressed in female and male reproductive organs. , 1995, The Plant journal : for cell and molecular biology.

[31]  D. Twell Molecular and Cellular Aspects of Plant Reproduction: The diversity and regulation of gene expression in the pathway of male gametophyte development , 1994 .

[32]  J. Woodgett,et al.  Modulation of the glycogen synthase kinase‐3 family by tyrosine phosphorylation. , 1993, The EMBO journal.

[33]  S. Somerville,et al.  Signalling pathways: A common theme in plants and animals? , 1997, Current Biology.

[34]  H. Strutt,et al.  Glycogen synthase kinase 3 regulates cell fate in dictyostelium , 1995, Cell.

[35]  C. Proud,et al.  GSK3: a SHAGGY frog story. , 1996, Trends in cell biology.