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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

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Abstract

We report an in-depth characterization of two major stress proteins namely SUMO-conjugating enzyme (Sce) and peptidyl prolyl cis-trans isomerase (PPIase) in rice (Oryza sativa L.). Sce mediates addition of SUMO group to various cell proteins, through process referred to as SUMOylation. Rice nuclear genome has two putative genes encoding the Sce protein (OsSce1 and OsSce2). PCR-amplified full-length OsSce1 cDNA functionally complemented the growth defect in yeast cells lacking the equivalent Ubc9 protein (ScΔubc9). RT-PCR analysis showed that transcript levels of OsSce1 and OsSce2 in rice seedlings were regulated by temperature stress. OsSce1 protein was localized to the nucleus in onion epidermal cells as evidenced by the transient GFP expression analysis following micro-projectile gun-based shooting of an OsSce1-GFP fusion construct. PPIase proteins assist molecular chaperones in reactions associated with protein folding and protein transport across membrane. There are 23 putative genes encoding for FK506-binding proteins (FKBPs; specific class of PPIase) in rice genome. OsFKBP20 cDNA was isolated as a stress-inducible EST clone. Largest ORF of 561 bases in OsFKBP20 showed characteristic FK506-binding domain at N-terminus and a coiled-coil motif at C-terminus. RNA expression analysis indicated that OsFKBP20 transcript is heat-inducible. OsFKBP20 over-expression in yeast endowed capacity of high temperature tolerance to yeast cells. Yeast two-hybrid analysis showed that OsSce1 protein physically interacts with the OsFKBP20 protein. It is thus proposed that OsSce1 and OsFKBP20 proteins in concert mediate the stress response of rice plants.

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References

  • Agarwal M, Sahi C, Katiyar-Agarwal S, Agarwal S, Young T, Gallie DR, Sharma VM, Ganesan K, Grover A (2003) Molecular characterization of rice hsp101: complementation of yeast hsp104 mutation by disaggregation of protein granules and differential expression in indica and japonica rice types. Plant Mol Biol 51:543–553

    Article  PubMed  CAS  Google Scholar 

  • Aghdasi B, Ye K, Resnick A, Huang A, Ha HC, Guo X, Dawson TM, Dawson VL, Snyder SH (2001) FKBP12, the 12-kDa FK506-binding protein, is a physiologic regulator of the cell cycle. Proc Natl Acad Sci USA 98:2425–2430

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Andreeva L, Heads R, Green CJ (1999) Cyclophilins and their possible role in the stress response. Int J Exp Pathol 80:305–315

    Article  PubMed  CAS  Google Scholar 

  • Asadulghani, Nitta K, Kaneko Y, Kojima K, Fukuzawa H, Kosaka H, Nakamoto H (2004) Comparative analysis of the hspA mutant and wildtype Synechocystis sp. strain PCC6803 under salt stress: evaluation of the role of hspA in salt stress management. Arch Microbiol 182:487–497

    Article  PubMed  CAS  Google Scholar 

  • Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Breiman A, Camus I (2002) The involvement of mammalian and plant FK506-binding proteins (FKBPs) in development. Transgenic Res 11:321–335

    Article  PubMed  CAS  Google Scholar 

  • Buchholz WG, Harris-Haller L, DeRose RT, Hall TC (1994) Cyclophilins are encoded by a small gene family in rice. Plant Mol Biol 25:837–843

    Article  PubMed  CAS  Google Scholar 

  • Castillo AG, Kong LJ, Hanley-Bowdoin L, Bejarano ER (2004) Interaction between a geminivirus replication protein and the plant sumoylation system. J Virol 78:2758–2769

    Article  PubMed  CAS  Google Scholar 

  • Causier B, Davies B (2004) Analyzing protein-protein interactions with the yeast two-hybrid system. Plant Mol Biol 50:855–870

    Article  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  • Dobson CM (2004) Principles of protein folding, misfolding and aggregation. Semin Cell Dev Biol 15:3–16

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Gelinas R, Endlich B, Pfeiffer C, Yagi M, Stamatoyannopoulos G (1985) G-substitution to A-substitution in the distal CCAAT box of the gamma-globin gene in Greek hereditary persistence of fetal hemoglobin. Nature 313:323–325

    Article  PubMed  CAS  Google Scholar 

  • Gill G (2005) Something about SUMO inhibits transcription. Curr Opin Genet Dev 15:536–541

    Article  PubMed  CAS  Google Scholar 

  • Harrar Y, Bellini C, Faure JD (2001) FKBPs: at the crossroads of folding and transduction. Trends Plant Sci 6:426–431

    Article  PubMed  CAS  Google Scholar 

  • Haseloff J, Siemering KR, Prasher DC, Hodges S (1997) Removal of a cryptic intron and sub-cellular localization of GFP are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci 94:2122–2127

    Article  PubMed  CAS  Google Scholar 

  • He Z, Li L, Luan S (2004) Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis. Plant Physiol 134:1–20

    Article  Google Scholar 

  • Hilgarth RS, Murphy LA, O’Connor CM, Clark JA, Park-Sarge OK, Sarge KD (2004) Identification of Xenopus heat shock transcription factor-2: conserved role of sumoylation in regulating deoxyribonucleic acid-binding activity of heat shock transcription factor-2 proteins. Cell Stress Chaperones 9:214–220

    Article  PubMed  CAS  Google Scholar 

  • Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12:343–351

    Article  PubMed  CAS  Google Scholar 

  • Hochstrasser M (2000) All in the ubiquitin family. Science 289:563–564

    Article  PubMed  CAS  Google Scholar 

  • Hong Y, Rogers R, Matunis MJ, Mayhew CN, Goodson ML, Park-Sarge OK, Sarge KD (2001) Regulation of heat shock transcription factor 1 by stress-induced SUMO-1 modification. J Biol Chem 276:40263–40267

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Joanisse DR, Inaguma Y, Tanguay RM (1998) Cloning and developmental expression of a nuclear ubiquitin-conjugating enzyme (DmUbc9) that interacts with small heat shock proteins in Drosophila melanogaster. Biochem Biophys Res Commun 244:102–109

    Article  PubMed  CAS  Google Scholar 

  • Johnson ES (2004) Protein modification by SUMO. Annu Rev Biochem 73:355–382

    Article  PubMed  CAS  Google Scholar 

  • Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159–180

    Article  PubMed  CAS  Google Scholar 

  • Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung DY, Vierstra RD (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J Biol Chem 278:6862–6872

    Article  PubMed  CAS  Google Scholar 

  • Letunic I, Copley RR, Pils B, Pinkert S, Schultz J, Bork P (2006) SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 34:D257–D260

    Article  PubMed  CAS  Google Scholar 

  • Lois LM, Lima CD (2005) Structures of the SUMO E1 provide mechanistic insights into SUMO activation and E2 recruitment to E1. EMBO J 24:439–451

    Article  PubMed  CAS  Google Scholar 

  • Lois LM, Lima CD, Chua NH (2003) Small ubiquitin-like modifier modulates abscisic acid signaling in Arabidopsis. Plant Cell 15:1347–1359

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Melchior F, Schergaut M, Pichler A (2003) SUMO: ligases, isopeptidases and nuclear pores. Trends Biochem Sci 28:612–618

    Article  PubMed  CAS  Google Scholar 

  • Meza-Zepeda LA, Bando MM, Palva ET, Heino P (1998) Isolation and characterization of a cDNA corresponding to a stress activated cyclophilin gene in Solanum commersoni. J Exp Bot 49:1451–1452

    Article  CAS  Google Scholar 

  • Miernyk JA (1999) Protein folding in the plant cell. Plant Physiol 121:695–703

    Article  PubMed  CAS  Google Scholar 

  • Morris DP, Phatnani HP, Greenleaf AL (1999) Phospho-carboxyl-terminal domain binding and the role of a prolyl isomerase in pre-mRNA 3′-end formation. J Biol Chem 274:31583–31587

    Article  PubMed  CAS  Google Scholar 

  • Mueller JW, Kessler D, Neumann D, Stratmann T, Papatheodorou P, Hartmann-Fatu C, Bayer P (2006) Characterization of novel elongated Parvulin isoforms that are ubiquitously expressed in human tissues and originate from alternative transcription initiation. BMC Mol Biol 7:9

    Article  PubMed  Google Scholar 

  • Nacerddine K, Lehembre F, Bhaumik M, Artus J, Cohen-Tannoudji M, Babinet C, pandolfi PP, Dejean A (2005) The SUMO pathway is essential for nuclear integrity and chromosome segregation on mice. Dev Cell 9:769–779

    Article  PubMed  CAS  Google Scholar 

  • Olive MR, Peacock WJ, Dennis ES (1991) The anaerobic responsive element contains two GC-rich sequences essential for binding a nuclear protein and hypoxic activation of the maize Adh1 promoter. Nucleic Acids Res 19:7053–7060

    Article  PubMed  CAS  Google Scholar 

  • Owens-Grillo JK, Stancato LF, Hoffmann K, Pratt WB, Krishna P (1996) Binding of immunophilins to the 90 kDa heat shock protein (hsp90) via a tetratricopeptide repeat domain is a conserved protein interaction in plants. Biochem 35:15249–15255

    Article  CAS  Google Scholar 

  • Paterson AH (2006) Leafing through the genomes of our major crop plants: strategies for capturing unique information. Nat Rev Genet 7:174–184

    Article  PubMed  CAS  Google Scholar 

  • Pichler A, Melchoir F (2002) Ubiquitin-related modifier SUMO1 and nucleocytoplasmic transport. Traffic 3:381–387

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sahi C, Agarwal M, Reddy MK, Sopory SK, Grover A (2003) Isolation and expression analysis of salt stress-associated ESTs from contrasting rice cultivars using a PCR-based subtraction method. Theor Appl Genet 106:620–628

    PubMed  CAS  Google Scholar 

  • Sahi C, Singh A, Kumar K, Blumwald E, Grover A (2006) Salt stress response in rice: genetics, molecular biology, and comparative genomics. Funct Integr Genomics 6:263–284

    Article  PubMed  CAS  Google Scholar 

  • Sakaguchi K, Koshiyama A, Iwabata K (2007) Meiosis and ubiquitin-related modifier (SUMO)-conjugating enzyme, Ubc9. FEBS J 274:3519–3531

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Saracco SA, Miller MJ, Kurepa J, Vierstra RD (2008) Genetic analysis of sumoylation in Arabidopsis: heat-induced conjugation of SUMO1 and 2 is essential. Plant Physiol (in press). doi:10.1104/pp.107.102285

  • Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95:5857–5864

    Article  PubMed  CAS  Google Scholar 

  • Seki M, Umezawa T, Urano K, Shinzoaki K (2007) Regulatory metabolic networks in drought stress responses, Curr Opin Plant Biol 10:296–302

    Article  PubMed  CAS  Google Scholar 

  • Seufert W, Futcher B, Jentsch S (1995) Role of a ubiquitin-conjugating enzyme in degradation of S- and N-phase cyclins. Nature 373:78–81

    Article  PubMed  CAS  Google Scholar 

  • Shaw PE (2007) Peptidyl-prolyl cis/trans isomerases and transcription: is there a twist in the tail? EMBO Rep 8:40–45

    Article  PubMed  CAS  Google Scholar 

  • Smyczynski C, Roudier F, Gissot L, Vaillant E, Grandjean O, Morin H, Masson T, Bellec Y, Geelen D, Faure JD (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  PubMed  CAS  Google Scholar 

  • Stade K, Vogel F, Schwienhorst J, Meusser B, Volkwein C, Nentwig Bm Dihmen RJ, Sommer J (2002) A lack of SUMO conjugation affects cNLS-dependent nuclear protein import in yeast. J Biol Chem 277:49554–49561

    Article  PubMed  CAS  Google Scholar 

  • The Rice Chromosomes 11, 12 Sequencing Consortia (2005) The sequence of rice chromosome 11 and 12, rich in disease resistance genes and recent gene duplications. BMC Biol 3:20

    Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Article  PubMed  CAS  Google Scholar 

  • Vespa L, Vachon G, Berger F, Perazza D, Faure JD, 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  PubMed  CAS  Google Scholar 

  • Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620

    Article  CAS  Google Scholar 

  • Yasugi T, Howley PM (1996) Identification of the structural and functional human homolog of the yeast conjugating enzyme UBC9. Nucleic Acids Res 24:2005–2010

    Article  PubMed  CAS  Google Scholar 

  • Zhou W, Ryan JJ, Zhou H (2004) Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J Biol Chem 279:32262–32268

    Article  PubMed  CAS  Google Scholar 

  • Zivy M, Thiellement H, deVienne D, Hofmann JP (1983) Study on nuclear and cytoplasmic genome expression in wheat by two-dimensional gel electrophoresis. Theor Appl Genet 66:1–7

    Article  CAS  Google Scholar 

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Acknowledgments

AG thanks Department of Biotechnology, Government of India for the Bioscience Career Award Project grant. We thank Prof. Robert Tanguay for providing the anti-DmUBC9 antibodies and Prof. Stefan Jentsch for the yeast wild type and Δubc9 mutant strain. NN acknowledges Monsanto (India) and Rotary Club of India while CS and AS acknowledge the Council of Scientific and Industrial Research, New Delhi for the fellowship awards.

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  1. Department of Plant Molecular Biology, University of Delhi South Campus, Benito Juarez Road, New Delhi, 110021, India

    Neha Nigam, Amanjot Singh, Chandan Sahi, Anupama Chandramouli & Anil Grover

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  1. Neha Nigam
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  2. Amanjot Singh
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  3. Chandan Sahi
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  4. Anupama Chandramouli
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Correspondence to Anil Grover.

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Communicated by J.-K. Zhu.

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Nigam, N., Singh, A., Sahi, C. et al. 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 Genomics 279, 371–383 (2008). https://doi.org/10.1007/s00438-008-0318-5

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