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FKBP-type peptidyl-prolyl cis-trans isomerase from thermophilic microalga, Scenedesmus sp.: molecular characterisation and demonstration of acquired salinity and thermotolerance in E. coli by recombinant expression

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Abstract

A novel complementary DNA (cDNA) encoding temperature and salt stress-responsive FK506-binding protein 12 (FKBP12), a chaperone with peptidyl-prolyl cis-trans isomerase (PPIase) activity was isolated using suppression subtractive hybridization (SSH) technique from a thermophilic chlorophycean microalga, Scenedesmus sp., isolated from the Manikaran hot springs at Himachal Pradesh, India. To our best knowledge, this is the first report of temperature and salt-responsive FKBP12 isolated from a microalgae. The Scenedesmus FKBP12 (Sce.FKBP12) nucleotide sequence revealed the presence of an open reading frame of 327 bp, encoding 108 amino acid protein containing a single FKBP-like domain with a predicted molecular weight of 12 KDa. Amino acid sequence comparison of Sce.FKBP12 with its ortholog from other eukaryotic organisms showed structural conservation among each other. Expression profile of Sce.FKBP12 gene using quantitative real-time PCR showed significant up-regulated expression under temperature and salinity stress. The recombinant Sce.FKBP12 was over-expressed in Escherichia coli using pET28b expression vector. The recombinant expression of Sce.FKBP12 in E. coli cells imparted temperature and salinity tolerance to the host cells, implying a significant role of Sce.FKBP12 in stress tolerance mechanisms. Sce.FKBP12 could be a promising transgene candidate for imparting abiotic stress tolerance in crop plants, and they need to be further evaluated using plant models like Arabidopsis or Tobacco for confirming its potential as a transgene candidate in development of temperature and salinity-tolerant transgenic crops for improved and sustained productions in adverse agro-climatic conditions.

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References

  • Adams RM, Hurd BH, Lenhart S, Leary N (1998) Effects of global climate change on agriculture: an interpretative review. Climate Res 11:19–30

    Article  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahn J, Kim DW, You Y, Seok M, Park J, Hwang H, Kim BG, Luan S, Park HS, Cho HS (2010) Classification of rice (Oryza sativa L. japonica Nipponbare) immunophilins (FKBPs, CYPs) and expression patterns under water stress. BMC Plant Biol 10:253–275

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Blecher O, Erel N, Callebaut I, Aviezer K, Breiman A (1996) A novel plant peptidyl prolyl- cis-trans-isomerase (PPIase): cDNA cloning, structural analysis, enzymatic activity and expression. Plant Mol Biol 32:493–504

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

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Brillantes AB, Ondrias K, Scott A, Kobrinsky E, Ondriasova E, Moschella MC, Jayaraman T, Landers M, Ehrlich BE, Marks AR (1994) Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77:513–523

    Article  CAS  PubMed  Google Scholar 

  • Chandrasekharam D, Alam MA, Minissale A (2005) Thermal discharges at Manikaran, Himachal Pradesh, India. Proceedings World Geothermal Congress, Antalya, Turkey

  • Chandrasekharam D, Chandrasekhar V (2008) Geothermal resources in India: possibilities for direct use in the Himalayas, Workshop for Decision Makers on Direct Heating Use of Geothermal Resources in Asia, organized by UNU-GTP, TBLRREM and TBGMED, in Tianjin, China

    Google Scholar 

  • Chen A, Wang GL, Qu ZL, Lu CX, Liu N, Wang F, Xia GX (2007) Ectopic expression of ThCYP1, a stress-responsive cyclophilin gene from Thellungiella halophila, confers salt tolerance in fission yeast. Plant Cell Rep 26:237–245

    Article  CAS  PubMed  Google Scholar 

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

  • Desai BN, Myers BR, Schreiber SL (2002) FKBP12-rapamycin-associated protein associates with mitochondria and senses osmotic stress via mitochondrial dysfunction. PNAS 99:4319–4324

    Article  CAS  PubMed  PubMed Central  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

  • Edvardsson A, Eshaghi S, Vener AV, Andersson B (2003) The major peptidyl-prolyl isomerase activity in thylakoid lumen of plant chloroplasts belongs to a novel cyclophilin TLP20. FEBS Lett 542:137–141

    Article  CAS  PubMed  Google Scholar 

  • Faure JD, Gingerich D, Howell SH (1998) 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 

  • Galat A (2003) Peptidyl prolyl cis/trans isomerases (immunophilins): biological diversity –targets– functions. Curr Top Med Chem 3:1315–1347

  • Godoy AV, Lazzaro AS, Casalongue CA, San SB (2000) Expression of a Solanum tuberosum cyclophilin gene is regulated by fungal infection and abiotic stress conditions. Plant Sci 152:123–134

    Article  CAS  Google Scholar 

  • Gollan PJ, Bhave M (2010) Genome-wide analysis of genes encoding FK506-binding proteins in rice. Plant Mol Biol 72:1–16

    Article  CAS  PubMed  Google Scholar 

  • Gornall J, Betts R, Burke E, Clark R, Camp J, Willett K, Wiltshire A (2010) Implications of climate change for agricultural productivity in the early twenty first century. Phil Trans R Soc B 365:2973–2989

    Article  PubMed  PubMed Central  Google Scholar 

  • Hagai KA, Skovorodnikova J, Galigniana M, Farchi PO, Maayan E, Bocovza S, Efrat Y, Doring PK, 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  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

  • Hemantaranjan A, Nishant BA, Singh MN, Yadav DK, Patel PK (2014) Heat stress responses and thermotolerance. Adv Plants Agric Res 1(3):00012

    Google Scholar 

  • Jackson JE, Castenholz RW (1975) Fidelity of thermophilic blue-green algae to hot spring habitats. Limnol Oceanogr 20:305–322

    Article  Google Scholar 

  • Jewell MC, Campbell BC, Godwin ID (2010) Transgenic plants for abiotic stress resistance. Transgenic Crop Plants. doi:10.1007/978-3-642-04812-82

    Google Scholar 

  • Jia Z, Niu J, Huan L, Wu X, Wang G, Hou Z (2013) Cyclophilin participates in responding to stress situations in Porphyra haitanensis (Bangiales, Rhodophyta). J Phycol 49:194–201

    Article  CAS  PubMed  Google Scholar 

  • Kang CB, Ye H, Dhe-Paganon S, Yoon HS (2008) FKBP family proteins: immunophilins with versatile biological functions. Neurosignals doi. doi:10.1159/000123041

    Google Scholar 

  • Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6:238–246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurek I, Stoger E, Dulberger R, Christou P, Breiman A (2002) Over expression of the wheat FK506-binding protein 73 (FKBP73) and the heat-induced wheat FKBP77 in transgenic wheat reveals different functions of the two isoforms. Transgenic Res 11:373–379

    Article  CAS  PubMed  Google Scholar 

  • Lobell DB, Gourdji SM (2012) The influence of climate change on global crop productivity. J Plant Physiol 160:1686–1697

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mierny K (1999) Protein folding in the plant cell. J Plant Physiology 121:695–703

    Article  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  PubMed Central  Google Scholar 

  • Naqvi SMK, Sejian V (2011) Global climate change: role of livestock. Asian J Agric Sci 3:19–25

    Google Scholar 

  • Nath AIV, Bharathi LPA (2011) Diversity in transcripts and translational pattern of stress proteins in marine extremophiles. Extremophiles 15:129–153

    Article  Google Scholar 

  • Ponmani T, Guo R, Ki JS (2015) A novel cyclophilin gene from the dinoflagellate Prorocentrum minimum and its possible role in the environmental stress response. Chemosphere 139:260–267

    Article  CAS  PubMed  Google Scholar 

  • Reddy RK, Kurek I, Silverstein AM, Chinkers M, Breiman A, Krishna P (1998) High-molecular-weight FK506-binding proteins are components of heat-shock protein 90 hetero complexes in wheat germ lysate. J Plant Physiol 118:1395–140

    Article  CAS  Google Scholar 

  • Reed CJ, Lewis H, Trejo E, Winston V, Evilia C (2013) Protein adaptations in archaeal extremophiles. Archaea. doi:10.1155/2013/373275

  • Romano PGN, Edvardsson A, Ruban AV, Andersson B, Vener AV, Gray JE, Horton P (2004) Arabidopsis AtCYP20-2 is a light-regulated cyclophilin-type peptidyl-prolyl cis-trans isomerase associated with the photosynthetic membranes. J Plant Physiol 134:1244–1247

  • Roy S, Nongpiur R, Singla-Pareek SL, Pareek A (2015) Raising stress tolerant rice through genetic manipulation of cyclophilins. J Rice Res 3:3. doi:10.4172/2375-4338.1000e118

    Google Scholar 

  • Ruan SL, Ma HS, Wang SH, Fu YP, Xin Y, Liu WZ, Wang F, Tong JX, Wang SZ, Chen HZ (2011) Proteomic identification of OsCYP2, a rice cyclophilin that confers salt tolerance in rice (Oryza sativa L.) seedlings when over expressed. BMC Plant Biol 11:34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scholze C, Peterson A, Diettrich B, Luckner M (1999) Cyclophilin isoforms from Digitalis lanata. Sequences and expression during embryogenesis and stress. J Plant Physiol 155:212–219

    Article  CAS  Google Scholar 

  • Sekhar K, Priyanka B, Reddy RD, Rao KV (2010) Isolation and characterization of a pigeonpea cyclophilin (CcCYP) gene, and its over expression in Arabidopsis confers multiple abiotic stress tolerance. Plant Cell Environ 33:1324–1338

    CAS  PubMed  Google Scholar 

  • Sharma AD, Kaur P (2009) Combined effect of drought stress and heat shock on cyclophilin protein expression in Triticum aestivum. Gen Appl Plant Physiol 35:88–92

    CAS  Google Scholar 

  • Sharma AD, Singh P (2003) Comparative studies on drought-induced changes in peptidyl prolyl cis–trans isomerase activity in drought- tolerant and susceptible cultivars of Sorghum bicolour. Current Sci 84:911–918

  • Sirohi S, Michaelowa A (2007) Sufferer and cause: Indian livestock and climate change. Climatic Change 85:285–298

    Article  CAS  Google Scholar 

  • Smit B, Ludlow L, Brklacich M (1988) Implications of a global climatic warming for agriculture: a review and appraisal. J Env Qual 17:519–27

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molec Biol Evol 30:725–2729

    Article  Google Scholar 

  • Trivedi DK, Ansari MW, Dutta T, Singh P, Tuteja N (2013) Molecular characterization of cyclophilin A-like protein from Piriformospora indica for its potential role to abiotic stress tolerance in E. coli. BMC Res Notes 6:555

    Article  PubMed  PubMed Central  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 endore duplication. J Plant Physiol 134:1283–1292

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wang T, Donahoe PK (2004) The immunophilin FKBP12: a molecular guardian of the TGF-family type I receptors. Front Biosci 9:619–631

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–52

    Article  CAS  PubMed  Google Scholar 

  • Yazdi SK, Shakouri B (2010) The effects of climate change on aquaculture. Int J Env Sci Develop 1:378–382

    Article  Google Scholar 

  • Yu Y, Zhang H, Li W, Mu C, Zhang F, Wang L, Meng Z (2012) Genome-wide analysis and environmental response profiling of the FK506-binding protein gene family in maize (Zea mays L.). Gene 498:212–222

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thankfully acknowledge The Director, CMFRI, Cochin, for providing the facilities for undertaking this work.

Funding

The study was funded by World Bank-funded National Agricultural Innovation Project, Indian Council of Agricultural Research (project name: Bioprospecting of genes and allele mining for abiotic stress tolerance; project code 2000035105).

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Authors and Affiliations

  1. Marine Biotechnology Division, Central Marine Fisheries Research Institute, Post Box No. 1603, Ernakulam North P.O, Kochi, 682018, Kerala, India

    C. S. Subin & M. A. Pradeep

  2. Central Institute of Brackish Water Aquaculture, Chennai, Tamil Nadu, 600028, India

    K. K. Vijayan

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  1. C. S. Subin
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Correspondence to M. A. Pradeep.

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Subin, C.S., Pradeep, M.A. & Vijayan, K.K. FKBP-type peptidyl-prolyl cis-trans isomerase from thermophilic microalga, Scenedesmus sp.: molecular characterisation and demonstration of acquired salinity and thermotolerance in E. coli by recombinant expression. J Appl Phycol 28, 3307–3315 (2016). https://doi.org/10.1007/s10811-016-0854-z

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