Skip to main content
SpringerLink
Log in

Genome-wide analysis of genes encoding FK506-binding proteins in rice

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The FK506-binding proteins (FKBPs) are a class of peptidyl-prolyl cis/trans isomerase enzymes, some of which can also operate as molecular chaperones. FKBPs comprise a large ubiquitous family, found in virtually every part of the cell and involved in diverse processes from protein folding to stress response. Higher plant genomes typically encode about 20 FKBPs, half of these found in the chloroplast thylakoid lumen. Several FKBPs in plants are regulators of hormone signalling pathways, with important roles in seed germination, plant growth and stress response. Some FKBP isoforms exists as homologous duplicates operating in finely tuned mechanisms to cope with abiotic stress. In order to understand the roles of the plant FKBPs, especially in view of the warming environment, we have identified and analysed the gene families encoding these proteins in rice using computational approaches. The work has led to identification of all FKBPs from the rice genome, including novel high molecular weight forms. The rice FKBP family appears to have evolved by duplications of FKBP genes, which may be a strategy for increased stress tolerance.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

FKBP:

FK506- and rapamycin-binding protein

FKBd:

FK506- and rapamycin-binding domain

CYP:

Cyclophilin

PPIase:

Peptidyl prolyl cis/trans isomerase

TPR:

Tetratricopeptide repeat

CaMBd:

Calmodulin-binding domain

References

  • Agredano-Moreno LT, Cruz HRdl, Martınez-Castilla LP, Jimenez ESd (2007) Distinctive expression and functional regulation of the maize (Zea mays L.) TOR kinase ortholog. Mol Biosyst 3:794–802

    Article  CAS  PubMed  Google Scholar 

  • Alnemri ES, Fernandes-Alnemri T, Pomerenken K, Robertson NM, Dudley K, DuBois GC, Litwack G (1994) FKBP46, a novel Sf9 insect cell nuclear immunophilin that forms a protein-kinase complex. J Biol Chem 269:30828–30834

    CAS  PubMed  Google Scholar 

  • Aster JC, Robertson ES, Hasserjian RP, Turner JR, Kieff E, Sklar J (1997) Oncogenic forms of NOTCH1 lacking either the primary binding site for RBP-Jkappa or nuclear localization sequences retain the ability to associate with RBP-Jkappa and activate transcription. J Biol Chem 272:11336–11343

    Article  CAS  PubMed  Google Scholar 

  • Aviezer-Hagai K, Skovorodnikova J, Galigniana M, Farchi-Pisanty O, Maayan E, Bocovza S, Efrat Y, Koskull-Doring Pv, Ohad N, Breiman A (2007) Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Mol Biol 63:237–255

    Article  CAS  PubMed  Google Scholar 

  • Bailly A, Sovero V, Vincenzetti V, Santelia D, Bartnik D, Koenig BW, Mancuso S, Martinoia E, Geisler M (2008) Modulation of p-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J Biol Chem 283:21817–21826

    Article  CAS  PubMed  Google Scholar 

  • Bates PA, Kelley LA, MacCallum RM, Sternberg MJE (2001) Enhancement of protein modeling by human intervention in applying the automatic programs 3d-jigsaw and 3d-pssm. Proteins Struc Func Bioinf 45:39–46

    Article  CAS  Google Scholar 

  • Bierer BE, Patricia KS, Thomas JW, Burakoff SJ, Schreiber SL (1990) Probing immunosuppressant action with a nonnatural immunophilin ligand. Science 250:556–559

    Article  CAS  PubMed  Google Scholar 

  • Blomqvist LA, Ryberg M, Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals their significance in chloroplast development. Photosynth Res 96:37–50

    Article  CAS  PubMed  Google Scholar 

  • Bouchard R, Bailly A, Blakeslee JJ, Oehring SC, Vincenzetti V, Lee OR, Paponov I, Palme K, Mancuso S, Murphy AS, Schulz B, Geisler M (2006) Immunophilin-like Twisted Dwarf1 modulates auxin efflux activities of Arabidopsis p-glycoproteins. J Biol Chem 281:30603–30612

    Article  CAS  PubMed  Google Scholar 

  • Breiman A, Fawcett TW, Ghirardi ML, Mattoo AK (1992) Plant organelles contain distinct peptidylprolyl cis/trans-isomerases. J Biol Chem 267:21293–21296

    CAS  PubMed  Google Scholar 

  • Buchanan BB, Luan S (2005) Redox regulation in the chloroplast thylakoid lumen: a new frontier in photosynthesis research. J Exp Bot 56:1439–1447

    Article  CAS  PubMed  Google Scholar 

  • Callebaut I, Renoir J, Lebeau M, Massol N, Burny A, Baulieu E, Mornon J (1992) An immunophilin that binds MR 90,000 heat shock protein: main structural features of a mammalian p59 protein. Proc Natl Acad Sci 89:6270–6274

    Article  CAS  PubMed  Google Scholar 

  • Carol R, Breiman A, Erel N, Vittorioso P, Bellini C (2001) Pasticcino1 (AtFKBP70) is a nuclear-localised immunophilin required during Arabidopsis thaliana embryogenesis. Plant Sci 161:527–535

    Article  CAS  Google Scholar 

  • Cline K, Theg SM (2007) The sec and tat protein translocation pathways in chloroplasts. In: Dalbey RE, Koehler CM, Tamanhoi F (eds) The enzymes. Academic Press, London, pp 463–492

    Google Scholar 

  • Crespo JL, Díaz-Troya S, Florencio FJ (2005) Inhibition of target of rapamycin signaling by rapamycin in the unicellular green alga Chlamydomonas reinhardtii. Plant Physiol 139:1736–1749

    Article  CAS  PubMed  Google Scholar 

  • Davies TH, Ning Y-M, Sanchez ER (2005) Differential control of glucocorticoid receptor hormone-binding function by tetratricopeptide repeat (TPR) proteins and the immunosuppressive ligand FK506. Biochemistry 44:2030–2038

    Article  CAS  PubMed  Google Scholar 

  • DeCenzo MT, Park ST, Jarrett BP, Aldape RA, Futer O, Murcko MA, Livingston DJ (1996) FK506-binding protein mutational analysis: defining the active-site residue contributions to catalysis and the stability of ligand complexes. Prot Eng 9:173–180

    Article  CAS  Google Scholar 

  • Denny WB, Prapapanich V, Smith DF, Scammell JG (2005) Structure–function analysis of squirrel monkey FK506-binding protein 51, a potent inhibitor of glucocorticoid receptor activity. Endocrinology 146:3194–3201

    Article  CAS  PubMed  Google Scholar 

  • Dolinski K, Muir S, Cardenas M, Heitman J (1997) All cyclophilins and FK506 binding proteins are, individually and collectively, dispensable for viability in Saccharomyces cerevisiae. Proc Natl Acad Sci 94:13093–13098

    Article  CAS  PubMed  Google Scholar 

  • Dwivedi RS, Breiman A, Herman EM (2003) Differential distribution of the cognate and heat-stress induced isoforms of high MR cis–trans prolyl peptidyl isomerase (FKBP) in the cytoplasm and nucleoplasm. J Exp Bot 54:2679–2689

    Article  CAS  PubMed  Google Scholar 

  • Edlich F, Weiwad M, Erdmann F, Fanghanel J, Jarczowski F, Rahfeld J, Fischer G (2005) Bcl- 2 regulator FKBP38 is activated by Ca2 +/calmodulin. EMBO J 24:2688–2699

    Article  CAS  PubMed  Google Scholar 

  • Edvardsson A, Shapiguzov A, Petersson UA, Schroder WP, Vener AV (2007) Immunophilin AtFKBP13 sustains all peptidyl-prolyl isomerase activity in the thylakoid lumen from Arabidopsis thaliana deficient in AtCYP20–2. Biochemistry 46:9432–9442

    Article  CAS  PubMed  Google Scholar 

  • Faure J-D, Gingerich D, Howell SH (1998a) An Arabidopsis immunophilin, AtFKBP12, binds to AtFIP37 (FKBP interacting protein) in an interaction that is disrupted by FK506. Plant J 15:783–789

    Article  CAS  PubMed  Google Scholar 

  • Faure J-D, Vittorioso P, Santoni V, Fraisier V, Prinsen E, Barlier I, Onckelen HV, Caboche M, Bellini C (1998b) The PASTICCINO genes of Arabidopsis thaliana are involved in the control of cell division and differentiation. Development 125:909–918

    CAS  PubMed  Google Scholar 

  • Fischer G, Wittmann-Liebold B, Lang K, Kiefhaber T, Schmid FX (1989) Cyclophilin and peptidyl-prolyl cis–trans isomerase are probably identical proteins. Nature 337:476–478

    Article  CAS  PubMed  Google Scholar 

  • Friso G, Giacomelli L, Ytterberg A, Peltier J-B, Rudella A, Sun Q, van Wijk KJ (2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions and a plastid proteome database. The Plant Cell 16:478–499

    Article  CAS  PubMed  Google Scholar 

  • Galat A (2000) Sequence diversification of the FK506-binding proteins in several different genomes. Eur J Biochem 267:4945–4959

    Article  CAS  PubMed  Google Scholar 

  • Galat A (2003) Peptidylprolyl cis/trans isomerases (immunophilins): biological diversity—targets—functions. Curr Topics Medic Chem 3:1315–1347

    Article  CAS  Google Scholar 

  • Galat A (2004) A note on clustering the functionally-related paralogues and orthologues of proteins: a case of the FK506-binding proteins (FKBPs). Comp Biol Chem 28:129–140

    Article  CAS  Google Scholar 

  • Galat A (2008) Functional drift of sequence attributes in the FK506-binding proteins (FKBPs). J Chem Inf Model 48:1118–1130

    Article  CAS  PubMed  Google Scholar 

  • Galigniana MD, Radanyi C, Renoir J-M, Housley PR, Pratt WB (2001) Evidence that the peptidylprolyl isomerase domain of the HSP90-binding immunophilin FKBP52 is involved in both dynein interaction and glucocorticoid receptor movement to the nucleus. J Biol Chem 276:14884–14889

    Article  CAS  PubMed  Google Scholar 

  • Galigniana MD, Harrell JM, O’Hagen HM, Ljungman M, Pratt WB (2004) HSP90-binding immunophilins link p53 to dynein during p53 transport to the nucleus. J Biol Chem 279:22483–22489

    Article  CAS  PubMed  Google Scholar 

  • Geisler M, Bailly A (2007) Tete-a-tete: the function of FKBPs in plant development. Trends Plant Sci 12:1360–1385

    Google Scholar 

  • Geisler M, Kolukisaoglu HU, Bouchard R, Billion K, Berger J, Saal B, Frangne N, Koncz-Kalman Z, Koncz C, Dudler R, Blakeslee JJ, Murphy AS, Martinoia E, Schulz B (2003) TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Mol Biol Cell 14:4238–4249

    Article  CAS  PubMed  Google Scholar 

  • Geisler M, Girin M, Brandt S, Vincenzetti V, Plaza S, Paris N, Kobae Y, Maeshima M, Billion K, Kolukisaoglu UH, Schulz B, Martinoia E (2004) Arabidopsis immunophilin-like TWD1 functionally interacts with vacuolar ABC transporters. Mol Biol Cell 15:3393–3405

    Article  CAS  PubMed  Google Scholar 

  • Goebl M, Yanagida M (1991) The TPR snap helix: a novel protein repeat motif from mitosis to transcription. Trends Biochem Sci 16:173–177

    Article  CAS  PubMed  Google Scholar 

  • Goodyear N, Murthy JN, Soldin SJ (1997) The 37 kDa immunophilin has uracil DNA glycosylase but not rotamase activity. Clin Biochem 30:497–499

    Article  CAS  PubMed  Google Scholar 

  • Gopalan G, He Z, Balmer Y, Romano P, Gupta R, Heroux A, Buchanan BB, Swaminathan K, Luan S (2004) Structural analysis uncovers a role for redox in regulating FKBP13, an immunophilin of the chloroplast thylakoid lumen. Proc Natl Acad Sci 101:13945–13950

    Article  CAS  PubMed  Google Scholar 

  • Gopalan G, He Z, Battaile KP, Luan S, Swaminathan K (2006) Structural comparison of oxidized and reduced FKBP13 from Arabidopsis thaliana. Proteins Struc Func Bioinf 65:789–795

    Article  CAS  Google Scholar 

  • Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardestro P, Schroder W, Hurry V (2006) The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. Plant J 47:720–734

    Google Scholar 

  • Griffith JP, Kim JL, Kim EE, Sintchak MD, Thomson JA, Fitzgibbon MJ, Fleming MA, Caron PR, Hsiao K, Navia MA (1995) X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12-FK506 complex. Cell 82:507–522

    Article  CAS  PubMed  Google Scholar 

  • Gupta R, Mould RM, He Z, Luan S (2002) A chloroplast FKBP interacts with and affects the accumulation of Rieske subunit of cytochrome bf complex. Proc Natl Acad Sci 99:15806–15811

    Article  CAS  PubMed  Google Scholar 

  • Harding MW, Galat A, Uehling DE, Schreiber SL (1989) A receptor for the immunosuppressant FK506 is a cis–trans peptidyl-prolyl isomerase. Nature 341:758–760

    Article  CAS  PubMed  Google Scholar 

  • Harrell JM, Kurek I, Breiman A, Radanyi C, Renoir J-M, Pratt WB, Galigniana MD (2002) All of the protein interactions that link steroid receptor HSP90 immunophilin heterocomplexes to cytoplasmic dynein are common to plant and animal cells. Biochemistry 41:5581–5587

    Article  CAS  PubMed  Google Scholar 

  • Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858

    Article  CAS  PubMed  Google Scholar 

  • He Z, Li L, Luan S (2004) Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis. Plant Physiol 134:1248–1267

    Article  CAS  PubMed  Google Scholar 

  • Heitman J, Movva NR, Hiestandt PC, Hall MN (1991) FK506-binding protein proline rotamase is a target for the immunosuppressive agent FK506 in Saccharomyces cerevisiae. Proc Natl Acad Sci 88:1948–1952

    Article  CAS  PubMed  Google Scholar 

  • Hueros G, Rahfeld J, Salamini F, Thompson R (1998) A maize FK506-sensitive immunophilin, MzFKBP-66, is a peptidylproline cis–trans-isomerase that interacts with calmodulin and a 36-kDa cytoplasmic protein. Planta 205:121–131

    Article  CAS  PubMed  Google Scholar 

  • Imamura A, Yoshino Y, Mizuno T (2001) Cellular localization of the signaling components of Arabidopsis His-to-Asp phosphorelay. Biosci Biotech Biochem 65:2113–2117

    Article  CAS  Google Scholar 

  • Ivery MTG, Weiler L (1997) Modeling the interaction between FK506 and FKBP12: a mechanism for formation of the calcineurin inhibitory complex. Bioorg Med Chem 5:217–232

    Article  CAS  PubMed  Google Scholar 

  • Jewett AI, Baumketner A, Shea J-E (2004) Accelerated folding in the weak hydrophobic environment of a chaperonin cavity: creation of an alternate fast folding pathway. Proc Natl Acad Sci 101:13192–13197

    Article  CAS  PubMed  Google Scholar 

  • Kamphausen T, Fanghanel J, Neumann D, Schulz B, Rahfeld J-U (2002) Characterization of Arabidopsis thaliana AtFKBP42 that is membrane-bound and interacts with HSP90. Plant J 32:263–276

    Article  CAS  PubMed  Google Scholar 

  • Kang CB, Ye H, Dhe-Paganon S, Yoon HS (2008) FKBP family proteins: Immunophilins with versatile biological functions. Neurosignals 16:318–325

    Article  CAS  PubMed  Google Scholar 

  • Kay JE (1996) Structure–function relationships in the FK506-binding protein (FKBP) family of peptidylprolyl cis–trans isomerases. Biochem J 314:361–385

    CAS  PubMed  Google Scholar 

  • Koussevitzky S, Neeman E, Peleg S, Harel E (2008) Polyphenol oxidase can cross thylakoids by both the Tat and the Sec-dependent pathways: a putative role for the stromal processing sites. Physiol Plant 133:266–277

    Article  CAS  PubMed  Google Scholar 

  • Kurek I, Aviezer K, Erel N, Herman E, Breiman A (1999) The wheat peptidyl prolyl cis–trans-isomerase FKBP77 is heat induced and developmentally regulated. Plant Physiol 119:693–703

    Article  CAS  PubMed  Google Scholar 

  • Kurek I, Pirkl F, Fischer E, Buchner J, Breiman A (2002) Wheat FKBP73 functions in vitro as a molecular chaperone independently of its peptidyl prolyl cis–trans isomerase activity. Planta 215:119–126

    Article  CAS  PubMed  Google Scholar 

  • Kuzuhara T, Horikoshi M (2004) A nuclear FK506-binding protein is a histone chaperone regulating rDNA silencing. Nature Struct Mol Biol 11:275–283

    Article  CAS  Google Scholar 

  • Lima A, Lima S, Wong JH, Phillips RS, Buchanan BB, Luan S (2006) A redox-active FKBP-type immunophilin functions in accumulation of the photosystem II supercomplex in Arabidopsis thaliana. Proc Natl Acad Sci 103:12631–12636

    Article  CAS  PubMed  Google Scholar 

  • Luan S, Albers MW, Schreiber SL (1994) Light-regulated, tissue-specific immunophilins in a higher plant. Proc Natl Acad Sci 91:984–988

    Article  CAS  PubMed  Google Scholar 

  • Luan S, Kulda J, Gruissem W, Schreiber SL (1996) Molecular characterization of a FKBP-type immunophilin from higher plants. Proc Natl Acad Sci 93:6964–6969

    Article  CAS  PubMed  Google Scholar 

  • Magiri EN, Farchi-Pisanty O, Avni A, Breiman A (2006) The expression of the large rice FK506 binding proteins (FKBPs) demonstrate tissue specificity and heat stress responsiveness. Plant Sci 170:695–704

    Article  CAS  Google Scholar 

  • Mahfouz MM, Kim S, Delauney AJ, Verma DPS (2006) Arabidopsis target of rapamycin interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18:477–490

    Article  CAS  PubMed  Google Scholar 

  • Marchand C, Maréchal PL, Meyer Y, Miginiac-Maslow M, Issakidis-Bourguet E, Decottignies P (2004) New targets of Arabidopsis thioredoxins revealed by proteomic analysis. Proteomics 4:2696–2706

    Article  CAS  PubMed  Google Scholar 

  • Meiri D, Breiman A (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J 59:387–399

    Google Scholar 

  • Menand B, Desnos T, Nussaume L, Berger F, Bouchez D, Meyer C, Robaglia C (2002) Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci 99:6422–6427

    Article  CAS  PubMed  Google Scholar 

  • Merz F, Boehringer D, Schaffitzel C, Preissler S, Hoffmann A, Maier T, Rutkowska A, Lozza J, Ban N, Bukau B, Deuerling E (2008) Molecular mechanism and structure of trigger factor bound to the translating ribosome. EMBO J 27:1622–1632

    Article  CAS  PubMed  Google Scholar 

  • Michelet L, Zaffagnini M, Vanacker H, Marechal PL, Marchand C, Schroda M, Lemaire SD, Decottignies P (2008) In vivo targets of S-thiolation in Chlamydomonas reinhardtii. J Biol Chem 283:21571–21578

    Article  CAS  PubMed  Google Scholar 

  • Molik S, Karnauchov I, Weidlich C, Herrmann RG, Klosgen RB (2001) The Rieske Fe/S protein of the cytochrome b6/f complex in chloroplasts missing link in the evolution of protein transport pathways in chloroplasts? J Biol Chem 276:42761–42766

    Article  CAS  PubMed  Google Scholar 

  • Nigam N, Singh A, Sahi C, Chandramouli A, Grover A (2008) SUMO-conjugating enzyme (Sce) and FK506-binding protein (FKBP) encoding rice (Oryza sativa L.) genes: genome-wide analysis, expression studies and evidence for their involvement in abiotic stress response. Mol Genet Genom 279:371–383

    Article  CAS  Google Scholar 

  • Pahl A, Keller U (1994) Streptomyces chrysomallus FKBP-33 is a novel immunophilin consisting of two FK506 binding domains; its gene is transcriptionally coupled to the FKBP-12 gene. EMBO J 13:3472–3480

    CAS  PubMed  Google Scholar 

  • Patterson CE, Gao J, Rooney AP, Davis EC (2002) Genomic organization of mouse and human 65 kDa FK506-binding protein genes and evolution of the FKBP multigene family. Genomics 79:881–889

    Article  CAS  PubMed  Google Scholar 

  • Peltier J-B, Emanuelsson O, Kalume DE, Ytterberg J, Friso G, Rudella A, Liberles DA, Söderberg L, Roepstorff P, Heijne Gv, Wijk KJv (2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant J 14:211–236

    CAS  Google Scholar 

  • Perez-Perez JM, Ponce MR, Micol JL (2004) The ULTRACURVATA2 gene of Arabidopsis encodes an FK506-binding protein involved in auxin and brassinosteroid signaling. Plant Physiol 134:101–117

    Article  CAS  PubMed  Google Scholar 

  • Pinto D, Duarte M, Soares S, Tropschug M, Videira A (2008) Identification of all FK506-binding proteins from Neurospora crassa. Fungal Genet Biol 45:1600–1607

    Article  CAS  PubMed  Google Scholar 

  • Pratt WB, Galigniana MD, Harrell JM, DeFranco DB (2004) Role of HSP90 and the HSP90-binding immunophilins in signalling protein movement. Cell Signal 16:857–872

    Article  CAS  PubMed  Google Scholar 

  • Radanyi C, Chambraud B, Baulieu E-E (1994) The ability of the immunophilin FKBP59-HBI to interact with the 90-kDa heat shock protein is encoded by its tetratricopeptide repeat domain. Proc Natl Acad Sci 91:11197–11201

    Article  CAS  PubMed  Google Scholar 

  • Rahfeld J, Schierhorn A, Mann K, Fischer G (1994) A novel peptidyl-prolyl cis/trans isomerase from Escherichia coli. FEBS Lett 343:65–69

    Article  CAS  PubMed  Google Scholar 

  • Reddy RK, Kurek I, Silverstein AM, Chinkers M, Breiman A, Krishna P (1998) High-mol-weight FK506-binding proteins are components of heat-shock protein 90 heterocomplexes in wheat germ lysate. Plant Physiol 118:1395–1401

    Article  CAS  PubMed  Google Scholar 

  • Riggs DL, Cox MB, Tardif HL, Hessling M, Buchner J, Smith DF (2007) Noncatalytic role of the FKBP52 peptidyl-prolyl isomerase domain in the regulation of steroid hormone signaling. Mol Cell Biol 27:8658–8669

    Article  CAS  PubMed  Google Scholar 

  • Romano P, Gray J, Horton P, Luan S (2005) Plant immunophilins: functional versatility beyond protein maturation. New Phytol 166:753–769

    Article  CAS  PubMed  Google Scholar 

  • Rulten SL, Kinloch RA, Tateossian H, Robinson C, Gettins L, Kay JE (2006) The human FK506-binding proteins: characterization of human FKBP19. Mammal Genome 17:322–331

    Article  CAS  Google Scholar 

  • Samso M, Shen X, Allen PD (2006) Structural characterization of the RyR1–FKBP12 interaction. J Mol Biol 356:917–927

    Article  CAS  PubMed  Google Scholar 

  • Santiago MJ, Alejandre-Durán E, Ruiz-Rubi M (2009) Alternative splicing of two translesion synthesis DNA polymerases from Arabidopsis thaliana. Plant Sci 176:591–596

    Article  CAS  Google Scholar 

  • Scheidt HA, Vogel A, Eckho A, Koenig BW, Huster D (2007) Solid-state NMR characterization of the putative membrane anchor of TWD1 from Arabidopsis thaliana. Eur Biophys J 36:393–404

    Article  CAS  PubMed  Google Scholar 

  • Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365

    Article  CAS  PubMed  Google Scholar 

  • Shapiguzov A, Edvardsson A, Vener AV (2006) Profound redox sensitivity of peptidyl-prolyl isomerase activity in Arabidopsis thylakoid lumen. FEBS Lett 580:3671–3676

    Article  CAS  PubMed  Google Scholar 

  • Siekierka JJ, Staruch MJ, Hung SH, Sigal NH (1989) FK-506, a potent novel immunosuppressive agent, binds to a cytosolic protein which is distinct from the cyclosporin A-binding protein, cyclophilin. J Immunol 143:1580–1583

    CAS  PubMed  Google Scholar 

  • Siekierka JJ, Wiederrecht G, Greulichn H, Boulton D, Hung SHY, Cryan J, Hodges PJ, Sigal NH (1990) The cytosolic-binding protein for the immunosuppressant FK-506 is both a ubiquitous and highly conserved peptidyl-prolyl cis–trans isomerase. J Biol Chem 265:21011–21015

    CAS  PubMed  Google Scholar 

  • Silverstein AM, Galigniana MD, Kanelakis KC, Radanyi C, Renoir J-M, Pratt WB (1999) Different regions of the immunophilin FKBP52 determine its association with the glucocorticoid receptor, HSP90, and cytoplasmic dynein. J Biol Chem 274:36980–36986

    Article  CAS  PubMed  Google Scholar 

  • Sinars CR, Cheung-Flynn J, Rimerman RA, Scammell JG, Smith DF, Clardy J (2003) Structure of the large FK506-binding protein FKBP51, an HSP90-binding protein and a component of steroid receptor complexes. Proc Natl Acad Sci 100:868–873

    Article  CAS  PubMed  Google Scholar 

  • Smyczynski C, Roudier F, Gissot L, Vaillant E, Grandjean O, Morin H, Masson T, Bellec Y, Geelen D, Faure J-D (2006) The C terminus of the immunophilin PASTICCINO1 is required for plant development and for interaction with a NAC-like transcription factor. J Biol Chem 281:25475–25484

    Article  CAS  PubMed  Google Scholar 

  • Somarelli JA, Herrera RJ (2007) Evolution of the 12 kDa FK506-binding protein gene. Biol Cell 99:311–321

    Article  CAS  PubMed  Google Scholar 

  • Somarelli JA, Lee SY, Skolnick J, Herrera RJ (2008) Structure-based classification of 45 FK506-binding proteins. Proteins Struc Func Bioinf 72:197–208

    Article  CAS  Google Scholar 

  • Standaert RF, Galat A, Verdine GL, Schreiber SL (1990) Molecular cloning and overexpression of the human FK506-binding protein FKBP. Nature 346:671–674

    Google Scholar 

  • Stoller G, Rucknagel KP, Nierhaus KH, Schmid FX, Fischer G, Rahfeld J-U (1995) A ribosome-associated peptidyl-prolyl cis/trans isomerase identified as the trigger factor. EMBO J 14:4939–4948

    CAS  PubMed  Google Scholar 

  • Tai P-KK, Albers MW, Chang H, Faber LE, Schreiber SL (1992) Association of a 59-kiloDalton immunophilin with the glucocorticoid receptor complex. Science 256:1315–1318

    Article  CAS  PubMed  Google Scholar 

  • Takahashi N, Hayano T, Suzuki M (1989) Peptidyl-prolyl cis–trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature 337:473–475

    Article  CAS  PubMed  Google Scholar 

  • Timerman A, Ogunbumni E, Freund E, Wiederrecht G, Marks A, Fleischer S (1993) The calcium release channel of sarcoplasmic reticulum is modulated by FK-506-binding protein. Dissociation and reconstitution of FKBP-12 to the calcium release channel of skeletal muscle sarcoplasmic reticulum. J Biol Chem 268:22992–22999

    CAS  PubMed  Google Scholar 

  • Tradler T, Stoller G, Ruëcknagel KP, Schierhorn A, Rahfeld J-U, Fischer G (1997) Comparative mutational analysis of peptidyl prolyl cis/trans isomerases: active sites of Escherichia coli trigger factor and human FKBP12. FEBS Lett 407:184–190

    Article  CAS  PubMed  Google Scholar 

  • Tullman-Ercek D, DeLisa MP, Kawarasaki Y, Iranpour P, Ribnicky B, Palmer T, Georgiou G (2007) Export pathway selectivity of Escherichia coli twin arginine translocation signal peptides. J Biol Chem 282:8309–8316

    Article  CAS  PubMed  Google Scholar 

  • Vallon O (2005) Chlamydomonas immunophilins and parvulins: survey and critical assessment of gene models. Euk Cell 4:230–241

    Article  CAS  Google Scholar 

  • Van Duyne GD, Standaert RF, Karplus A, Schreiber S, Clardy J (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J Mol Biol 229:105–124

    Article  PubMed  Google Scholar 

  • Vespa L, Vachon G, Berger Fdr, Perazza D, Faure J-D, Herzog M (2004) The immunophilin-interacting protein AtFIP37 from Arabidopsis is essential for plant development and is involved in trichome endoreduplication. Plant Physiol 134:1283–1292

    Article  CAS  PubMed  Google Scholar 

  • Vittorioso P, Cowling R, Faure J-D, Caboche M, Bellini C (1998) Mutation in the Arabidopsis PASTICCINO1 gene, which encodes a new FK506-binding protein-like protein, has a dramatic effect on plant development. Mol Cell Biol 18:3034–3043

    CAS  PubMed  Google Scholar 

  • von Heijne G (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14:4683–4690

    Google Scholar 

  • Vucich VA, Gasser CS (1996) Novel structure of a high mol weight FK506 binding protein from Arabidopsis thaliana. Mol Gen Genet 252:510–517

    CAS  PubMed  Google Scholar 

  • Wang T, Donahoe PK, Zervos AS (1994) Specific interaction of type 1 receptors of the TGF-beta family with the immunophilin FKBP-12. Science 265:674–676

    Article  CAS  PubMed  Google Scholar 

  • Wilson KP, Yamashita MM, Sintchak MD, Rotstein SH, Murcko MA, Boger J, Thomson JA, Fitzgibbon MJ, Black JR, Navia MA (1995) Comparative X-ray structures of the major binding protein for the immunosuppressant FK506 (tacrolimus) in unliganded form and in complex with FK506 and rapamycin. Acta Cryst D51:511–521

    CAS  Google Scholar 

  • Wochnik GM, Ruegg J, Abel GA, Schmidt U, Holsboer F, Rein T (2005) FK506-binding proteins 51 and 52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells. J Biol Chem 280:4609–4616

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Kurata N, Tanoue H, Shimokawa T, Umehara Y, Yano M, Sasaki T (1998) Physical mapping of duplicated genomic regions of two chromosome ends in rice. Genetics 150:1595–1603

    CAS  PubMed  Google Scholar 

  • Wu B, Li P, Liu Y, Lou Z, Ding Y, Shu C, Ye S, Bartlam M, Shen B, Rao Z (2004) 3D structure of human FK506-binding protein 52: implications for the assembly of the glucocorticoid receptor HSP90-immunophilin heterocomplex. Proc Natl Acad Sci 101:8348–8353

    Article  CAS  PubMed  Google Scholar 

  • Xiao H, Jackson V, Lei M (2006) The FK506-binding protein, FPR4, is an acidic histone chaperone. FEBS Lett 580:4357–4364

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Liang S, Kudla J, Luan S (1998) Molecular characterization of a plant FKBP12 that does not mediate action of FK506 and rapamycin. Plant J 15:511–519

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

PG gratefully acknowledges a Ph.D. scholarship awarded by the Grains Research and Development Corporation (GRDC), Australia.

Author information

Authors and Affiliations

  1. Environment and Biotechnology Centre, Faculty of Life and Social Sciences, Swinburne University of Technology, PO Box 218, Hawthorn, VIC, 3122, Australia

    Peter J. Gollan & Mrinal Bhave

Authors
  1. Peter J. Gollan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mrinal Bhave
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mrinal Bhave.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 208 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gollan, P.J., Bhave, M. Genome-wide analysis of genes encoding FK506-binding proteins in rice. Plant Mol Biol 72, 1–16 (2010). https://doi.org/10.1007/s11103-009-9547-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-009-9547-1

Keywords

Search

Navigation