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A chloroplast-localized dual-specificity protein phosphatase in Arabidopsis contains a phylogenetically dispersed and ancient carbohydrate-binding domain, which binds the polysaccharide starch

  1. David Kerk1,*,
  2. Terry R. Conley2,
  3. Flor A. Rodriguez1,
  4. Hue T. Tran3,
  5. Mhairi Nimick3,
  6. Douglas G. Muench3,
  7. Greg B. G. Moorhead3

Article first published online: 3 APR 2006

DOI: 10.1111/j.1365-313X.2006.02704.x

Issue

The Plant Journal

The Plant Journal

Volume 46, Issue 3, pages 400–413, May 2006

Additional Information

How to Cite

Kerk, D., Conley, T. R., Rodriguez, F. A., Tran, H. T., Nimick, M., Muench, D. G. and Moorhead, G. B. G. (2006), A chloroplast-localized dual-specificity protein phosphatase in Arabidopsis contains a phylogenetically dispersed and ancient carbohydrate-binding domain, which binds the polysaccharide starch. The Plant Journal, 46: 400–413. doi: 10.1111/j.1365-313X.2006.02704.x

Author Information

  1. 1

    Department of Biology, Point Loma Nazarene University, 3900 Lomaland Drive, San Diego, CA 92106, USA,

  2. 2

    Department of Biology, Oklahoma City University, 2501 North Blackwelder, Oklahoma City, OK 73106-1493, USA, and

  3. 3

    Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada

* *(fax +1 619 849 2598; e-mail dkerk@ptloma.edu).

Publication History

  1. Issue published online: 3 APR 2006
  2. Article first published online: 3 APR 2006
  3. Received 30 November 2005; accepted 15 December 2005.

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References

  • Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402.
  • Bailey, T.L. and Elkan, C. (1995) Unsupervised learning of multiple motifs in biopolymers using EM. Mach. Learn. 21, 51–80.
  • Bailey, T.L. and Gribskov, M. (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics, 14, 48–54.
  • Bannai, H., Tamada, Y., Maruyama, O., Nakai, K. and Miyano, S. (2002) Extensive feature detection of N terminal protein sorting signals. Bioinformatics, 18, 298–305.
  • Bateman, A., Birney, E., Durbin, R., Eddy, S.R., Howe, K.I. and Sonnhammer, E.L.L. (2000) The Pfam protein families database. Nucleic Acids Res. 28, 263–266.
  • Bridges, D., Fraser, M.E. and Moorhead, G.B.G. (2005) Cyclic nucleotide binding proteins in the Arabidopsis thaliana and Oryza sativa genomes. BMC Bioinformatics, 6, 6 doi:10.1186/1471-2105-6-6.
  • Bucher, P., Karplus, K., Moeri, N. and Hofmann, K. (1996) A flexible search technique based on generalized profiles. Comput. Chem. 20, 3–24.
  • Chan, E.M., Ackerley, C.A., Lohi, H., Ianzano, L., Cortez, M.A., Shannon, P., Scherer, S.W. and Minassian, B.A. (2004) Laforin preferentially binds the neurotoxic starch-like polyglucosans, which form in its absence in progressive myoclonus epilepsy. Hum. Mol. Genet. 13, 1117–1129.
  • Cohen, P.T.W. (2002) Protein phosphatase 1 – targeted in many directions. J. Cell. Sci. 115, 241–256.
  • Emanuelsson, O., Nielsen, H., Brunak, S. and von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005–1016.
  • Felsenstein, J. (1996) Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. Methods Enzymol. 266, 418–426.
  • Fernandez-Sanchez, M.E., Criado-Garcia, O., Heath, K.E., Garcia-Fojeda, B., Medrano-Fernandez, I., Gomez-Garre, P., Sanz, P., Serratosa, J.M. and Rodriguez de Cordoba, S. (2003) Laforin, the dual-phosphatase responsible for Lafora disease, interacts with R5 (PTG), a regulatory subunit of protein phosphatase-1 that enhances glycogen accumulation. Hum. Mol. Genet. 12, 3161–3171.
  • Fordham-Skelton, A.P., Chilley, P., Lumbreras, V., Reignoux, S., Fenton, T.R., Dahm, C.C., Pages, M. and Gatehouse, J.A. (2002) A novel higher plant protein tyrosine phosphatase interacts with SNF1-related protein kinases via a KIS (kinase interaction sequence) domain. Plant J. 29, 705–715.
    Direct Link:
  • Ganesh, S., Tsurutani, N., Suzuki, T., Hoshii, Y., Ishihara, T., Delgado-Escueta, A.V. and Yamakawa, K. (2004) The carbohydrate-binding domain of Lafora disease protein targets Lafora polyglucosan bodies. Biochem. Biophys. Res. Commun. 313, 1101–1109.
  • Gribskov, M. and Veretnik, S. (1996) Identification of sequence patterns with profile analysis. Methods Enzymol. 266, 198–211.
  • Hardie, D.G., Scott, J.W., Pan, D.A. and Hudson, E.R. (2003) Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett. 546, 113–120.
  • Higgins, D.G., Thompson, J.D. and Gibson, T.J. (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 266, 383–401.
  • Hubbard, M.J. and Cohen, P. (1993) On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci. 18, 172–177.
  • Hudson, E.R., Pan, D.A., James, J., Lucocq, J.M., Hawley, S.A., Green, K.A., Baba, O., Terashima, T. and Hardie, D.G. (2003) A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias. Curr. Biol. 13, 861–866.
  • Kerk, D., Bulgrien, J., Smith, D.W., Barsam, B., Veretnik, S. and Gribskov, M. (2002) The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis. Plant Physiol. 129, 908–925.
  • Kleffmann, T., Russenberger, D., von Zychlinski, A., Christopher, W., Sjolander, K., Gruissem, W. and Baginsky, S. (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14, 354–362.
  • Kossmann, J. and Lloyd, J. (2000) Understanding and influencing starch biochemistry. Crit. Rev. Plant Sci. 19, 171–226.
  • Kotting, O., Pusch, K., Tiessen, A., Geigenberger, P., Steup, M. and Ritte, G. (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol. 137, 242–252.
  • Lorberth, R., Ritte, G., Willmitzer, L. and Kossmann, J. (1998) Inhibition of a starch-granule-bound protein leads to modified starch and repression of cold sweetening. Nat. Biotechnol. 16, 473–477.
  • Luan, S. (2003) Protein phosphatases in plants. Annu. Rev. Plant Biol. 54, 63–92.
  • Moorhead, G., MacKintosh, C., Morrice, N. and Cohen, P. (1995) Purification of the hepatic glycogen-associated form of PP1 by Microcystin-Sepharose affinity chromatography. FEBS Lett. 362, 101–105.
  • Moorhead, G., Douglas, P., Cotelle, V. et al. (1999) Plant proteins containing phosphopeptide motifs that bind to 14-3-3 proteins. Plant J. 18, 1–12.
    Direct Link:
  • Notredame, C., Higgins, D.G. and Heringa, J. (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205–217.
  • Pawson, T. and Nash, P. (2003) Assembly of cell regulatory systems through protein interaction domains. Science, 300, 445–452.
  • Polekhina, G., Gupta, A., Michell, B. et al. (2003) AMPK β subunit targets metabolic stress sensing to glycogen. Curr. Biol. 13, 867–871.
  • Polekhina, G., Gupta, A., van Denderen, B.J.W., Feil, S.C., Kemp, B.E., Stapleton, D. and Parker, M.W. (2005) Structural basis for glycogen recognition by AMP-activated protein kinase. Structure, 13, 1453–1462.
  • Richly, E. and Leister, D. (2004) An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene, 329, 11–16.
  • Ritte, G., Eckermann, N., Haebel, S., Lorberth, R. and Steup, M. (2000) Compartmentation of the starch-related R1 protein in higher plants. Starch, 52, 179–185.
    Direct Link:
  • Ritte, G., Lloyd, J.R., Eckermann, N., Rottmann, A., Kossmann, J. and Steup, M. (2002) The starch-related R1 protein is an α-glucan, water dikinase. Proc. Natl Acad. Sci. USA, 99, 7166–7171.
  • Ronquist, F. and Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
  • Rychlewski, L., Jaroszewski, L., Li, W. and Godzik, A. (2000) Comparison of sequence profiles. Strategies for structural predictions using sequence information. Protein Sci. 9, 232–241.
  • Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.
  • Sambrook, J. and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
  • Schein, A.I., Kissinger, J.C. and Ungar, L.H. (2001) Chloroplast transit peptide prediction: a peek inside the black box. Nucleic Acids Res. 29, E82.
  • Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D. and Lohmann, J. (2005) A gene expression map of Arabidopsis development. Nat. Genet. 37, 501–506.
  • Schmidt, H.A., Strimmer, K., Vingron, M. and Von Haeseler, A. (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics, 18, 502–504.
  • Sehnke, P.C., Chung, H.J., Wu, K. and Ferl, R.J. (2001) Regulation of starch accumulation by granule-associated plant 14-3-3 proteins. Proc. Natl Acad. Sci. USA, 98, 765–770.
  • Small, I., Peeters, N., Legeai, F. and Lurin, C. (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics, 4, 1581–1590.
    Direct Link:
  • Smith, C.S., Weljie, A.M. and Moorhead, G.B.G. (2003) Molecular properties of the putative nitrogen sensor, PII, from Arabidopsis thaliana. Plant J. 33, 353–360.
    Direct Link:
  • Smith, C.S., Morrice, N. and Moorhead, G.B.G. (2004a) Lack of evidence for phosphorylation of Arabidopsis thaliana PII: implications for plastid carbon and nitrogen signaling. Biochim. Biophys. Acta, 1699, 145–154.
  • Smith, S.M., Fulton, D.C., Chia, T., Thorneycroft, D., Chapple, A., Dunstan, H., Hylton, C., Zeeman, S.C. and Smith, A.M. (2004b) Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and posttranscriptional regulation of starch metabolism in Arabidopsis leaves. Plant Physiol. 136, 2687–2699.
  • Smith, A.M., Zeeman, S.C. and Smith, S.M. (2005) Starch degradation. Annu. Rev. Plant Biol. 56, 73–98.
  • Tetlow, I.J., Wait, R., Lu, Z., Akkasaeng, R., Bowsher, C.G., Esposito, S., Kosar-Hashemi, B., Morell, M.K. and Emes, M.J. (2004) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein–protein interactions. Plant Cell, 16, 694–708.
  • Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24, 4876–4882.
  • Wang, W. and Roach, P.J. (2004) Glycogen and related polysaccharides inhibit the larforin dual-specificity protein phosphatase. Biochem. Biophys. Res. Commun. 325, 726–730.
  • Wang, J., Stuckey, J.A., Wishart, M.J. and Dixon, J.E. (2002) A unique carbohydrate binding domain targets the lafora disease phosphatase to glycogen. J. Biol. Chem. 277, 2377–2380.
  • Ward, J.M. (2001) Identification of novel families of membrane proteins from the model plant Arabidopsis thaliana. Bioinformatics, 17, 560–563.
  • Wiatrowski, H.A., van Denderen, B.J.W., Berkey, C.D., Kemp, B.E., Stapleton, D. and Carlson, M. (2004) Mutations in the Gal83 glycogen-binding domain activate the Snf1/Gal83 kinase pathway by a glycogen-independent mechanism. Mol. Cell. Biol. 24, 352–361.
  • Yamada, K., Lim, J., Dale, J.M. et al. (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science, 302, 842–846.
  • Yu, T.-S., Kofler, H., Hausler, R.E. et al. (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell, 13, 1907–1918.
  • Zeeman, S.C., Northrop, F., Smith, A.M. and Rees, T. (1998) A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. Plant J. 15, 357–365.
    Direct Link:
  • Zer, H. and Ohad, I. (2003) Light, redox state, thylakoid-protein phosphorylation and signaling gene expression. Trends Biochem. Sci. 28, 467–470.
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