Skip to main content
Log in

Prediction of biological functions of Shewanella-like protein phosphatases (Shelphs) across different domains of life

  • Review
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

PPP protein phosphatases are an important enzyme family involved in a variety of aspects of cellular signalling and metabolism. PPPs are ubiquitous in eukaryotes, and are also present in many bacteria. Canonical eukaryotic PPP phosphotases are represented by five major subfamilies (PP1, PP2A, calcineurin, PP5 and PPEF/PP7). We previously reported that three “bacterial-like” PPP groups span the prokaryote–eukaryote boundary, including “Shewanella-like” phosphatases (Shelphs), which are in the focus of this study. Here we predict possible biological functions and functional partners of Shelphs by examining composition of bacterial operons and expression data for eukaryotes available in public databases. In Arabidopsis thaliana, the predicted possible roles include light-dependent regulation of chloroplast functions, signalling between the nucleus and the chloroplast, and defence responses. In Plasmodium falciparum, Shelphs are predicted to be associated with host cell invasion. One isoform has been located in the apical complex, essential for the interaction with the host cell. This makes P. falciparum Shelphs obvious potential candidates for therapeutic targets. Shelphs are also present in bacteria that constitute a considerable proportion of symbiotic microflora in humans. The predicted involvement of bacterial Shelphs in sensing and import of nutrients and extrusion of toxins may be relevant to the links between physiology of humans and our symbionts. Thus, despite the absence of Shelphs in animals, including humans, they may have a direct relationship to human health. Some predicted biological processes and potential functional partners of Shelphs are common between different bacterial and/or eukaryotic lineages, suggesting evolutionary conservation of some Shelph regulatory modules.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alabadi D, Yanovsky MJ, Mas P, Harmer SL, Kay SA (2002) Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. Curr Biol 12(9):757–761

    Article  PubMed  CAS  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121(2):207–221

    Article  PubMed  CAS  Google Scholar 

  • Andreeva AV, Kutuzov MA (1999) Physcomitrella patens gene/cDNA fragments related to genes encoding protein Ser/Thr phosphatases. J Plant Physiol 155(2):153–158

    Article  CAS  Google Scholar 

  • Andreeva AV, Kutuzov MA (2001) PPP family of protein Ser/Thr phosphatases: two distinct branches? Mol Biol Evol 18(3):448–452

    Article  PubMed  CAS  Google Scholar 

  • Andreeva AV, Kutuzov MA (2004) Widespread presence of “bacterial-like” PPP phosphatases in eukaryotes. BMC Evol Biol 4:47

    Article  PubMed  Google Scholar 

  • Asakura Y, Kikuchi S, Nakai M (2008) Non-identical contributions of two membrane-bound cpSRP components, cpFtsY and Alb3, to thylakoid biogenesis. Plant J 56(6):1007–1017

    Article  PubMed  CAS  Google Scholar 

  • Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M, Magallanes-Lundback M, DellaPenna D, McCarty DR, Klee HJ (2006) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45(6):982–993

    Article  PubMed  CAS  Google Scholar 

  • Baerenfaller K, Grossmann J, Grobei MA, Hull R, Hirsch-Hoffmann M, Yalovsky S, Zimmermann P, Grossniklaus U, Gruissem W, Baginsky S (2008) Genome-scale proteomics reveals Arabidopsis thaliana gene models and proteome dynamics. Science 320(5878):938–941

    Article  PubMed  CAS  Google Scholar 

  • Baginsky S, Gruissem W (2009) The chloroplast kinase network: new insights from large-scale phosphoproteome profiling. Mol Plant 2(6):1141–1153

    Article  PubMed  CAS  Google Scholar 

  • Barta JR, Thompson RCA (2006) What is cryptosporidium? Reappraising its biology and phylogenetic affinities. Trends Parasitol 22(10):463–468

    Article  PubMed  Google Scholar 

  • Bollen M, Peti W, Ragusa MJ, Beullens M (2010) The extended PP1 toolkit: designed to create specificity. Trends Biochem Sci 35(8):450–458

    Article  PubMed  CAS  Google Scholar 

  • Bradshaw N, Walter P (2007) The signal recognition particle (SRP) RNA links conformational changes in the SRP to protein targeting. Mol Biol Cell 18(7):2728–2734

    Article  PubMed  CAS  Google Scholar 

  • Braun S, Matuschewski K, Rape M, Thoms S, Jentsch S (2002) Role of the ubiquitin-selective CDC48(UFD1/NPL4)chaperone (segregase) in ERAD of OLE1 and other substrates. EMBO J 21(4):615–621

    Article  PubMed  CAS  Google Scholar 

  • Brooks BE, Buchanan SK (2008) Signaling mechanisms for activation of extracytoplasmic function (ECF) sigma factors. Biochim Biophys Acta 1778(9):1930–1945

    Article  PubMed  CAS  Google Scholar 

  • Busch W, Wunderlich M, Schoffl F (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 41(1):1–14

    Article  PubMed  CAS  Google Scholar 

  • Campbell EA, Westblade LF, Darst SA (2008) Regulation of bacterial RNA polymerase sigma factor activity: a structural perspective. Curr Opin Microbiol 11(2):121–127

    Article  PubMed  CAS  Google Scholar 

  • Chinkers M (2001) Protein phosphatase 5 in signal transduction. Trends Endocrinol Metabol 12(1):28–32

    Article  CAS  Google Scholar 

  • Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45

    Article  PubMed  CAS  Google Scholar 

  • Clay NK, Nelson T (2005) The recessive epigenetic swellmap mutation affects the expression of two step II splicing factors required for the transcription of the cell proliferation gene STRUWWELPETER and for the timing of cell cycle arrest in the Arabidopsis leaf. Plant Cell 17(7):1994–2008

    Article  PubMed  CAS  Google Scholar 

  • Cline K, Mori H (2001) Thylakoid Delta pH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J Cell Biol 154(4):719–729

    Article  PubMed  CAS  Google Scholar 

  • Coates JC, Laplaze L, Haseloff J (2006) Armadillo-related proteins promote lateral root development in Arabidopsis. Proc Natl Acad Sci U S A 103(5):1621–1626

    Article  PubMed  CAS  Google Scholar 

  • Cohen PT (1997) Novel protein serine/threonine phosphatases: variety is the spice of life. Trends Biochem Sci 22(7):245–251

    Article  PubMed  CAS  Google Scholar 

  • Cohen PT (2002) Protein phosphatase 1–targeted in many directions. J Cell Sci 115(Pt 2):241–256

    PubMed  CAS  Google Scholar 

  • Cowman AF, Crabb BS (2006) Invasion of red blood cells by malaria parasites. Cell 124(4):755–766

    Article  PubMed  CAS  Google Scholar 

  • Date SV, Stoeckert CJ Jr (2006) Computational modeling of the Plasmodium falciparum interactome reveals protein function on a genome-wide scale. Genome Res 16(4):542–549

    Article  PubMed  CAS  Google Scholar 

  • Davidson AL, Dassa E, Orelle C, Chen J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72(2):317–364, table of contents

    Article  PubMed  CAS  Google Scholar 

  • de Carbonnel M, Davis P, Roelfsema MR, Inoue S, Schepens I, Lariguet P, Geisler M, Shimazaki K, Hangarter R, Fankhauser C (2010) The Arabidopsis PHYTOCHROME KINASE SUBSTRATE2 protein is a phototropin signaling element that regulates leaf flattening and leaf positioning. Plant Physiol 152(3):1391–1405

    Article  PubMed  Google Scholar 

  • De Marchis ML, Giorgi A, Schinina ME, Bozzoni I, Fatica A (2005) Rrp15p, a novel component of pre-ribosomal particles required for 60S ribosome subunit maturation. RNA 11(4):495–502

    Article  PubMed  Google Scholar 

  • Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, Roos DS, Cowman AF, McFadden GI (2003) Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299(5607):705–708

    Article  PubMed  CAS  Google Scholar 

  • Fujiwara M, Nagashima A, Kanamaru K, Tanaka K, Takahashi H (2000) Three new nuclear genes, sigD, sigE and sigF, encoding putative plastid RNA polymerase sigma factors in Aarabidopsis thaliana. FEBS Lett 481(1):47–52

    Article  PubMed  CAS  Google Scholar 

  • Fukao Y, Hayashi M, Nishimura M (2002) Proteomic analysis of leaf peroxisomal proteins in greening cotyledons of Arabidopsis thaliana. Plant Cell Physiol 43(7):689–696

    Article  PubMed  CAS  Google Scholar 

  • Galperin MY, Koonin EV (2004) ‘Conserved hypothetical’ proteins: prioritization of targets for experimental study. Nucleic Acids Res 32(18):5452–5463

    Article  PubMed  CAS  Google Scholar 

  • Grennan AK (2006) Genevestigator. Facilitating Web-based gene-expression analysis. Plant Physiol 141(4):1164–1166

    Article  PubMed  CAS  Google Scholar 

  • Haase S, Cabrera A, Langer C, Treeck M, Struck N, Herrmann S, Jansen PW, Bruchhaus I, Bachmann A, Dias S, Cowman AF, Stunnenberg HG, Spielmann T, Gilberger TW (2008) Characterization of a conserved rhoptry-associated leucine zipper-like protein in the malaria parasite Plasmodium falciparum. Infect Immun 76(3):879–887

    Article  PubMed  CAS  Google Scholar 

  • Hazen SP, Schultz TF, Pruneda-Paz JL, Borevitz JO, Ecker JR, Kay SA (2005) LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc Natl Acad Sci U S A 102(29):10387–10392

    Article  PubMed  CAS  Google Scholar 

  • Helmann JD (2006) Deciphering a complex genetic regulatory network: the Bacillus subtilis sigmaW protein and intrinsic resistance to antimicrobial compounds. Sci Prog 89(Pt 3–4):243–266

    Article  PubMed  CAS  Google Scholar 

  • Hu G, Cabrera A, Kono M, Mok S, Chaal BK, Haase S, Engelberg K, Cheemadan S, Spielmann T, Preiser PR, Gilberger TW, Bozdech Z (2010) Transcriptional profiling of growth perturbations of the human malaria parasite Plasmodium falciparum. Nat Biotechnol 28(1):91–98

    Article  PubMed  CAS  Google Scholar 

  • Hughes BT, Espenshade PJ (2008) Oxygen-regulated degradation of fission yeast SREBP by Ofd1, a prolyl hydroxylase family member. EMBO J 27(10):1491–1501

    PubMed  CAS  Google Scholar 

  • Hung NJ, Lo KY, Patel SS, Helmke K, Johnson AW (2008) Arx1 is a nuclear export receptor for the 60S ribosomal subunit in yeast. Mol Biol Cell 19(2):735–744

    Article  PubMed  CAS  Google Scholar 

  • Janssens V, Longin S, Goris J (2008) PP2A holoenzyme assembly: in cauda venenum (the sting is in the tail). Trends Biochem Sci 33(3):113–121

    Article  PubMed  CAS  Google Scholar 

  • Jasinski M, Sudre D, Schansker G, Schellenberg M, Constant S, Martinoia E, Bovet L (2008) AtOSA1, a member of the Abc1-like family, as a new factor in cadmium and oxidative stress response. Plant Physiol 147(2):719–731

    Article  PubMed  CAS  Google Scholar 

  • Jen CH, Manfield IW, Michalopoulos I, Pinney JW, Willats WGT, Gilmartin PM, Westhead DR (2006) The Arabidopsis co-expression tool (ACT): a WWW-based tool and database for microarray-based gene expression analysis. Plant J 46(2):336–348

    Article  PubMed  CAS  Google Scholar 

  • Jiang M, Sullivan SM, Walker AK, Strahler JR, Andrews PC, Maddock JR (2007) Identification of novel Escherichia coli ribosome-associated proteins using isobaric tags and multidimensional protein identification techniques. J Bacteriol 189(9):3434–3444

    Article  PubMed  CAS  Google Scholar 

  • Jing HC, Dijkwel PP (2008) CPR5: A Jack of all trades in plants. Plant Signal Behav 3(8):562–563

    Article  PubMed  Google Scholar 

  • Kapri-Pardes E, Naveh L, Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. Plant Cell 19(3):1039–1047

    Article  PubMed  CAS  Google Scholar 

  • Kapushesky M, Emam I, Holloway E, Kurnosov P, Zorin A, Malone J, Rustici G, Williams E, Parkinson H, Brazma A (2010) Gene expression atlas at the European bioinformatics institute. Nucleic Acids Res 38(Database issue):D690–D698

    Article  PubMed  CAS  Google Scholar 

  • Karimpour-Fard A, Leach SM, Gill RT, Hunter LE (2008) Predicting protein linkages in bacteria: which method is best depends on task. BMC Bioinformatics 9:397

    Article  PubMed  Google Scholar 

  • Kennelly PJ (2001) Protein phosphatases—a phylogenetic perspective. Chem Rev 101(8):2291–2312

    Article  PubMed  CAS  Google Scholar 

  • Keurentjes JJ, Fu J, Terpstra IR, Garcia JM, van den Ackerveken G, Snoek LB, Peeters AJ, Vreugdenhil D, Koornneef M, Jansen RC (2007) Regulatory network construction in Arabidopsis by using genome-wide gene expression quantitative trait loci. Proc Natl Acad Sci U S A 104(5):1708–1713

    Article  PubMed  CAS  Google Scholar 

  • Kohler D, Schmidt-Gattung S, Binder S (2010) The DEAD-box protein PMH2 is required for efficient group II intron splicing in mitochondria of Arabidopsis thaliana. Plant Mol Biol 72(4–5):459–467

    Article  PubMed  Google Scholar 

  • Kovács-Bogdán E, Soll J, Bolter B (2010) Protein import into chloroplasts: the Tic complex and its regulation. Biochim Biophys Acta 1803(6):740–747

    Article  PubMed  Google Scholar 

  • Koyama T, Furutani M, Tasaka M, Ohme-Takagi M (2007) TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary-specific genes in Arabidopsis. Plant Cell 19(2):473–484

    Article  PubMed  CAS  Google Scholar 

  • Kumimoto RW, Adam L, Hymus GJ, Repetti PP, Reuber TL, Marion CM, Hempel FD, Ratcliffe OJ (2008) The nuclear factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis. Planta 228(5):709–723

    Article  PubMed  CAS  Google Scholar 

  • Kutuzov MA, Andreeva AV (2008) Protein Ser/Thr phosphatases of parasitic protozoa. Mol Biochem Parasitol 161(2):81–90

    Article  PubMed  CAS  Google Scholar 

  • LaCount DJ, Vignali M, Chettier R, Phansalkar A, Bell R, Hesselberth JR, Schoenfeld LW, Ota I, Sahasrabudhe S, Kurschner C, Fields S, Hughes RE (2005) A protein interaction network of the malaria parasite Plasmodium falciparum. Nature 438(7064):103–107

    Article  PubMed  CAS  Google Scholar 

  • Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299(5608):902–906

    Article  PubMed  CAS  Google Scholar 

  • Ledger S, Strayer C, Ashton F, Kay SA, Putterill J (2001) Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. Plant J 26(1):15–22

    Article  PubMed  CAS  Google Scholar 

  • Lin R, Wang H (2004) Arabidopsis FHY3/FAR1 gene family and distinct roles of its members in light control of Arabidopsis development. Plant Physiol 136(4):4010–4022

    Article  PubMed  CAS  Google Scholar 

  • Magoulas C, Zatsepina OV, Jordan PWH, Jordan EG, Fried M (1998) The SURF-6 protein is a component of the nucleolar matrix and has a high binding capacity for nucleic acids in vitro. Eur J Cell Biol 75(2):174–183

    Article  PubMed  CAS  Google Scholar 

  • Marri L, Sparla F, Pupillo P, Trost P (2005) Co-ordinated gene expression of photosynthetic glyceraldehyde-3-phosphate dehydrogenase, phosphoribulokinase, and CP12 in Arabidopsis thaliana. J Exp Bot 56(409):73–80

    PubMed  CAS  Google Scholar 

  • Matsuyama A, Arai R, Yashiroda Y, Shirai A, Kamata A, Sekido S, Kobayashi Y, Hashimoto A, Hamamoto M, Hiraoka Y, Horinouchi S, Yoshida M (2006) ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 24(7):841–847

    Article  PubMed  CAS  Google Scholar 

  • Michael TP, Breton G, Hazen SP, Priest H, Mockler TC, Kay SA, Chory J (2008) A morning-specific phytohormone gene expression program underlying rhythmic plant growth. PLoS Biol 6(9):e225

    Article  PubMed  Google Scholar 

  • Miotto G, Tessaro S, Rotta GA, Bonatto D (2007) In silico analyses of Fsf1 sequences, a new group of fungal proteins orthologous to the metazoan sideroblastic anemia-related sideroflexin family. Fungal Genet Biol 44(8):740–753

    Article  PubMed  CAS  Google Scholar 

  • Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song HR, Carre IA, Coupland G (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2(5):629–641

    Article  PubMed  CAS  Google Scholar 

  • Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci U S A 98(4):2053–2058

    Article  PubMed  CAS  Google Scholar 

  • Moorhead GB, De Wever V, Templeton G, Kerk D (2009) Evolution of protein phosphatases in plants and animals. Biochem J 417(2):401–409

    Article  PubMed  CAS  Google Scholar 

  • Nelissen H, Fleury D, Bruno L, Robles P, De Veylder L, Traas J, Micol JL, Van Montagu M, Inze D, Van Lijsebettens M (2005) The elongata mutants identify a functional Elongator complex in plants with a role in cell proliferation during organ growth. Proc Natl Acad Sci U S A 102(21):7754–7759

    Article  PubMed  CAS  Google Scholar 

  • Nguyen PH, Hasek J, Kohlwein SD, Romero C, Choi JH, Vancura A (2005) Interaction of Pik1p and Sjl proteins in membrane trafficking. FEMS Yeast Res 5(4–5):363–371

    Article  PubMed  CAS  Google Scholar 

  • Nixon PJ, Michoux F, Yu JF, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot-London 106(1):1–16

    Article  CAS  Google Scholar 

  • Oeffinger M, Fatica A, Rout MP, Tollervey D (2007) Yeast Rrp14p is required for ribosomal subunit synthesis and for correct positioning of the mitotic spindle during mitosis. Nucleic Acids Res 35(4):1354–1366

    Article  PubMed  CAS  Google Scholar 

  • Pagano A, Letourneur F, Garcia-Estefania D, Carpentier JL, Orci L, Paccaud JP (1999) Sec24 proteins and sorting at the endoplasmic reticulum. J Biol Chem 274(12):7833–7840

    Article  PubMed  CAS  Google Scholar 

  • Pakrasi HB (1995) Genetic analysis of the form and function of photosystem I and photosystem II. Annu Rev Genet 29:755–776

    Article  PubMed  CAS  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425(6955):257–263

    Article  PubMed  CAS  Google Scholar 

  • Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150(3):1541–1555

    Article  PubMed  Google Scholar 

  • Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12(17):1484–1495

    Article  PubMed  CAS  Google Scholar 

  • Pendle AF, Clark GP, Boon R, Lewandowska D, Lam YW, Andersen J, Mann M, Lamond AI, Brown JW, Shaw PJ (2005) Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Mol Biol Cell 16(1):260–269

    Article  PubMed  CAS  Google Scholar 

  • Pesaresi P, Pribil M, Wunder T, Leister D (2010) Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: the roles of STN7, STN8 and TAP38. Biochim Biophys Acta 1807(8):887–896

    PubMed  Google Scholar 

  • Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmuller R (2006) pTAC2, −6, and −12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18(1):176–197

    Article  PubMed  CAS  Google Scholar 

  • Privat I, Hakimi MA, Buhot L, Favory JJ, Mache-Lerbs S (2003) Characterization of Arabidopsis plastid sigma-like transcription factors SIG1, SIG2 and SIG3. Plant Mol Biol 51(3):385–399

    Article  PubMed  CAS  Google Scholar 

  • Proveniers M, Rutjens B, Brand M, Smeekens S (2007) The Arabidopsis TALE homeobox gene ATH1 controls floral competency through positive regulation of FLC. Plant J 52(5):899–913

    Article  PubMed  CAS  Google Scholar 

  • Puthiyaveetil S, Allen JF (2009) Chloroplast two-component systems: evolution of the link between photosynthesis and gene expression. Proc Biol Sci 276(1665):2133–2145

    Article  PubMed  CAS  Google Scholar 

  • Qiu JL, Zhou L, Yun BW, Nielsen HB, Fiil BK, Petersen K, Mackinlay J, Loake GJ, Mundy J, Morris PC (2008) Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol 148(1):212–222

    Article  PubMed  CAS  Google Scholar 

  • Raines CA (2003) The Calvin cycle revisited. Photosynth Res 75(1):1–10

    Article  PubMed  CAS  Google Scholar 

  • Schult K, Meierhoff K, Paradies S, Toller T, Wolff P, Westhoff P (2007) The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell 19(4):1329–1346

    Article  PubMed  CAS  Google Scholar 

  • Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8(4):517–527

    Article  PubMed  CAS  Google Scholar 

  • Schwager KM, Calderon-Villalobos LI, Dohmann EM, Willige BC, Knierer S, Nill C, Schwechheimer C (2007) Characterization of the VIER F-BOX PROTEINE genes from Arabidopsis reveals their importance for plant growth and development. Plant Cell 19(4):1163–1178

    Article  PubMed  CAS  Google Scholar 

  • Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, Finazzi G, Grunwald D, Rappaport F, Vavasseur A, Joyard J, Richaud P, Rolland N (2006) HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J Biol Chem 281(5):2882–2892

    Article  PubMed  CAS  Google Scholar 

  • Shimizu M, Kato H, Ogawa T, Kurachi A, Nakagawa Y, Kobayashi H (2010) Sigma factor phosphorylation in the photosynthetic control of photosystem stoichiometry. Proc Natl Acad Sci U S A 107(23):10760–10764

    Article  PubMed  CAS  Google Scholar 

  • Shpakovskii GV, Lebedenko EN (1997) The first member of a novel family of eukaryotic transcription factors detected by the heterospecific complementation. Bioorg Khim 23(3):234–237

    PubMed  CAS  Google Scholar 

  • Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM (2007) Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development 134(6):1051–1060

    Article  PubMed  CAS  Google Scholar 

  • Skalitzky CA, Martin JR, Harwood JH, Beirne JJ, Adamczyk BJ, Heck GR, Cline K, Fernandez DE (2010) Plastids contain a second sec translocase system with essential functions. Plant Physiol 155(1):354–369

    Article  PubMed  Google Scholar 

  • Sorkin A (2000) The endocytosis machinery. J Cell Sci 113(Pt 24):4375–4376

    PubMed  CAS  Google Scholar 

  • Srinivasasainagendra V, Page GP, Mehta T, Coulibaly I, Loraine AE (2008) CressExpress: a tool for large-scale mining of expression data from Arabidopsis. Plant Physiol 147(3):1004–1016

    Article  PubMed  CAS  Google Scholar 

  • Sterner DE, Grant PA, Roberts SM, Duggan LJ, Belotserkovskaya R, Pacella LA, Winston F, Workman JL, Berger SL (1999) Functional organization of the yeast SAGA complex: distinct components involved in structural integrity, nucleosome acetylation, and TATA-binding protein interaction. Mol Cell Biol 19(1):86–98

    PubMed  CAS  Google Scholar 

  • Stolarczyk EI, Reiling CJ, Paumi CM (2011) Regulation of ABC transporter function via phosphorylation by protein kinases. Curr Pharm Biotechnol 12:621–635

    Article  PubMed  CAS  Google Scholar 

  • Thum KE, Shin MJ, Gutierrez RA, Mukherjee I, Katari MS, Nero D, Shasha D, Coruzzi GM (2008) An integrated genetic, genomic and systems approach defines gene networks regulated by the interaction of light and carbon signaling pathways in Arabidopsis. BMC Syst Biol 2:31

    Article  PubMed  Google Scholar 

  • Tsuruta H, Aizono Y (2003) Catalytic efficiency and some structural properties of cold-active protein-tyrosine-phosphatase. J Biochem 133(2):225–230

    Article  PubMed  CAS  Google Scholar 

  • Tsuruta H, Mikami B, Aizono Y (2005) Crystal structure of cold-active protein-tyrosine phosphatase from a psychrophile, Shewanella sp. J Biochem 137(1):69–77

    Article  PubMed  CAS  Google Scholar 

  • West AH, Stock AM (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26(6):369–376

    Article  PubMed  CAS  Google Scholar 

  • Wilson-Grady JT, Villen J, Gygi SP (2008) Phosphoproteome analysis of fission yeast. J Proteome Res 7(3):1088–1097

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors are indebted to all researchers who have deposited their primary data into open access repositories, and who have made their software freely available. This work would have been impossible without these contributions. We are also grateful to Jonathan Goldberg for critical reading of the manuscript and valuable comments.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Mikhail A. Kutuzov or Alexandra V. Andreeva.

Additional information

This work is dedicated to the memory of Nelly Bennett, our collaborator and friend.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1

(XLS 41 kb)

Supplementary Table 2

(XLS 31 kb)

Supplementary Table 3

(XLS 40 kb)

Supplementary Table 4

(XLS 258 kb)

Supplementary Table 5–10

(XLS 101 kb)

Supplementary Table 11

(XLS 36 kb)

Supplementary Table 12

(XLS 27 kb)

Supplementary Table 13

(XLS 83 kb)

Supplementary Table 14

(XLS 38 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kutuzov, M.A., Andreeva, A.V. Prediction of biological functions of Shewanella-like protein phosphatases (Shelphs) across different domains of life. Funct Integr Genomics 12, 11–23 (2012). https://doi.org/10.1007/s10142-011-0254-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-011-0254-z

Keywords

Navigation