Systematic Trans-Genomic Comparison of Protein Kinases between Arabidopsis and Saccharomyces cerevisiae1

The genome of the budding yeast (Saccharomyces cerevisiae) provides an important paradigm for transgenomic comparisons with other eukaryotic species. Here, we report a systematic comparison of the protein kinases of yeast (119 kinases) and a reference plant Arabidopsis (1,019 kinases). Using a whole-protein-based, hierarchical clustering approach, the complete set of protein kinases from both species were clustered. We validated our clustering by three observations: (a) clustering pattern of functional orthologs proven in genetic complementation experiments, (b) consistency with reported classifications of yeast kinases, and (c) consistency with the biochemical properties of those Arabidopsis kinases already experimentally characterized. The clustering pattern identified no overlap between yeast kinases and the receptor-like kinases (RLKs) of Arabidopsis. Ten more kinase families were found to be specific for one of the two species. Among them, the calcium-dependent protein kinase and phosphoenolpyruvate carboxylase kinase families are specific for plants, whereas the Ca2+/calmodulin-dependent protein kinase and provirus insertion in mouse-like kinase families were found only in yeast and animals. Three yeast kinase families, nitrogen permease reactivator/halotolerance-5), polyamine transport kinase, and negative regulator of sexual conjugation and meiosis, are absent in both plants and animals. The majority of yeast kinase families (21 of 26) display Arabidopsis counterparts, and all are mapped into Arabidopsis families of intracellular kinases that are not related to RLKs. Representatives from 11 of the common families (54 kinases from Arabidopsis and 17 from yeast) share an extremely high degree of similarity (blast E value < 10-80), suggesting the likelihood of orthologous functions. Selective expansion of yeast kinase families was observed in Arabidopsis. This is most evident for yeast genes CBK1, HRR25, and SNF1 and the kinase family S6K. Reduction of kinase families was also observed, as in the case of the NEK-like family. The distinguishing features between the two sets of kinases are the selective expansion of yeast families and the generation of a limited number of new kinase families for new functionality in Arabidopsis, most notably, the Arabidopsis RLKs that constitute important components of plant intercellular communication apparatus.

[1]  K. Shinozaki,et al.  Cloning and characterization of two cDNAs encoding casein kinase II catalytic subunits in Arabidopsis thaliana , 2004, Plant Molecular Biology.

[2]  Jonathan A. Cooper,et al.  Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. , 1995, Current opinion in cell biology.

[3]  C. Fankhauser,et al.  The Phytochromes, a Family of Red/Far-red Absorbing Photoreceptors* , 2001, The Journal of Biological Chemistry.

[4]  D. Hirata,et al.  GSK‐3 kinase Mck1 and calcineurin coordinately mediate Hsl1 down‐regulation by Ca2+ in budding yeast , 2001, The EMBO journal.

[5]  Marek S. Skrzypek,et al.  YPDTM, PombePDTM and WormPDTM: model organism volumes of the BioKnowledgeTM Library, an integrated resource for protein information , 2001, Nucleic Acids Res..

[6]  S. Karlin,et al.  Applications and statistics for multiple high-scoring segments in molecular sequences. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. R. Adams,et al.  Comparative genomics of the eukaryotes. , 2000, Science.

[8]  Michael Gribskov,et al.  PlantsP: a functional genomics database for plant phosphorylation , 2001, Nucleic Acids Res..

[9]  J. M. Seguí-Simarro,et al.  The protein kinases AtMAP3Kepsilon1 and BnMAP3Kepsilon1 are functional homologues of S. pombe cdc7p and may be involved in cell division. , 2001, The Plant journal : for cell and molecular biology.

[10]  Paulo,et al.  The Arabidopsís Functional Homolog of the p 34 Protein Kinase , 2002 .

[11]  M. Ishitani,et al.  The Arabidopsis SOS 2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS 3 , 2000 .

[12]  B. Barrell,et al.  Life with 6000 Genes , 1996, Science.

[13]  P. Shewry,et al.  Complementation of snf1, a mutation affecting global regulation of carbon metabolism in yeast, by a plant protein kinase cDNA. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[14]  R. Bhalerao,et al.  Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  K. Irie,et al.  Possible involvement of differential splicing in regulation of the activity of Arabidopsis ANP1 that is related to mitogen-activated protein kinase kinase kinases (MAPKKKs). , 1997, The Plant journal : for cell and molecular biology.

[16]  D. Sterner,et al.  The yeast carboxyl-terminal repeat domain kinase CTDK-I is a divergent cyclin-cyclin-dependent kinase complex , 1995, Molecular and cellular biology.

[17]  S. Kim,et al.  An Arabidopsis GSK3/shaggy-like gene that complements yeast salt stress-sensitive mutants is induced by NaCl and abscisic acid. , 1999, Plant physiology.

[18]  G. Tena,et al.  Plant mitogen-activated protein kinase signaling cascades. , 2001, Current opinion in plant biology.

[19]  G. Schaller Histidine kinases and the role of two-component systems in plants , 2000 .

[20]  N Linial,et al.  ProtoMap: Automatic classification of protein sequences, a hierarchy of protein families, and local maps of the protein space , 1999, Proteins.

[21]  Kara Dolinski,et al.  Saccharomyces Genome Database (SGD) provides biochemical and structural information for budding yeast proteins , 2003, Nucleic Acids Res..

[22]  Sudhir Kumar,et al.  Comparative Genomics in Eukaryotes , 2005 .

[23]  K. Irie,et al.  A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[24]  T. Petes,et al.  Protein kinase activity of Tel1p and Mec1p, two Saccharomyces cerevisiae proteins related to the human ATM protein kinase. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[25]  B. Rost Enzyme function less conserved than anticipated. , 2002, Journal of molecular biology.

[26]  Y. Kimata,et al.  Molecular characterization of two Arabidopsis Ire1 homologs, endoplasmic reticulum-located transmembrane protein kinases. , 2001, Plant physiology.

[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]  W. McCombie,et al.  The First Plant Genome , 2001, Cell.

[29]  D. Inzé,et al.  CDK-related protein kinases in plants , 2000, Plant Molecular Biology.

[30]  R. Lew,et al.  Arabidopsis thaliana cDNA isolated by functional complementation shows homology to serine/threonine protein kinases. , 1996, Biochimica et biophysica acta.

[31]  J. E. Kranz,et al.  YPD, PombePD and WormPD: model organism volumes of the BioKnowledge library, an integrated resource for protein information. , 2001, Nucleic acids research.

[32]  Gareth W. Price,et al.  Complete nucleotide sequence, expression, and chromosomal localisation of human mixed-lineage kinase 2. , 1995, European journal of biochemistry.

[33]  S. Tabata,et al.  ARR1, a Transcription Factor for Genes Immediately Responsive to Cytokinins , 2001, Science.

[34]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[35]  H. Sano,et al.  An Arabidopsis SNF1-related protein kinase, AtSR1, interacts with a calcium-binding protein, AtCBL2, of which transcripts respond to light. , 2001, Plant & cell physiology.

[36]  K. Shinozaki,et al.  A Transmembrane Hybrid-Type Histidine Kinase in Arabidopsis Functions as an Osmosensor , 1999, Plant Cell.

[37]  J. Tregear,et al.  Plant MAP kinase kinase kinases structure, classification and evolution. , 1999, Gene.

[38]  T. Hunter,et al.  The protein kinases of budding yeast: six score and more. , 1997, Trends in biochemical sciences.

[39]  J. Tregear,et al.  An unusual protein kinase displaying characteristics of both the serine/threonine and tyrosine families is encoded by the Arabidopsis thaliana gene ATN1 , 1996 .

[40]  M. Ishitani,et al.  The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  K. Irie,et al.  Identification of a possible MAP kinase cascade in Arabidopsis thaliana based on pairwise yeast two‐hybrid analysis and functional complementation tests of yeast mutants , 1998, FEBS letters.

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

[43]  Temple F. Smith,et al.  Comparison of the complete protein sets of worm and yeast: orthology and divergence. , 1998, Science.

[44]  Joseph R. Ecker,et al.  CTR1, a negative regulator of the ethylene response pathway in arabidopsis, encodes a member of the Raf family of protein kinases , 1993, Cell.

[45]  Robert R. Sokal,et al.  A statistical method for evaluating systematic relationships , 1958 .

[46]  K. Shinozaki,et al.  ATMRK1, an Arabidopsis protein kinase related to mammal mixed-lineage kinases and Raf protein kinases , 1997 .

[47]  Y. Zhao,et al.  Cloning and characterization of a novel member of protein kinase family from soybean. , 1993, Biochimica et biophysica acta.

[48]  G. N. Lance,et al.  A General Theory of Classificatory Sorting Strategies: 1. Hierarchical Systems , 1967, Comput. J..

[49]  M. Gribskov,et al.  CDPKs - a kinase for every Ca2+ signal? , 2000, Trends in plant science.