Isolation of genes conferring salt tolerance from Piriformospora indica by random overexpression in Escherichia coli

World Journal of Microbiology and Biotechnology

Volumn 31, Issue 8, 2015, Pages 1195-1209

  Gahlot, Sunayna ^a   Joshi, Amita ^a   Singh, Pratap ^b   Tuteja, Renu ^a   Dua, Meenakshi ^b   Jogawat, Abhimanyu ^b   Kumar, Manoj ^b   Raj, Sumit ^b   Dayaman, Vikram ^b   Johri, Atul Kumar ^b   Tuteja, Narendra ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

Escherichia coli; Functional screening; Piriformospora indica; Root endophytic fungus; Salt tolerance conferring genes

Indexed keywords

ESCHERICHIA COLI; FUNGI; GENES; MOBILE SECURITY; POLYMERASE CHAIN REACTION;

ENDOPHYTIC FUNGI; FUNCTIONAL SCREENING; MOLECULAR ANALYSIS; PIRIFORMOSPORA INDICA; QUANTITATIVE RT-PCR; SALINITY TOLERANCE; SALT STRESS TOLERANCE; SALT TOLERANCE;

GENE EXPRESSION;

ESCHERICHIA COLI; FUNGI; PIRIFORMOSPORA INDICA;

FUNGAL PROTEIN; SODIUM CHLORIDE;

BASIDIOMYCETES; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SALT TOLERANCE;

BASIDIOMYCOTA; ESCHERICHIA COLI; FUNGAL PROTEINS; GENE EXPRESSION; MOLECULAR SEQUENCE DATA; SALT-TOLERANCE; SODIUM CHLORIDE;

EID: 84933672416     PISSN: 09593993     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11274-015-1867-5     Document Type: Article

References (43)

1. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48. doi:10.1038/ncomms1046
2. Breuninger M, Requena N (2004) Recognition events in AM symbiosis: analysis of fungal gene expression at the early appressorium stage. Fungal Genet Biol 41:794–804. doi:10.1016/j.fgb.2004.04.002
3. Bücking H, Heyser W (2003) Uptake and transfer of nutrients in ectomycorrhizal associations: interactions between photosynthesis and phosphate nutrition. Mycorrhiza 13:59–68. doi:10.1007/s00572-002-0196-3
4. Doukhanina EV, Chen S, Van Der Zalm E, Godzik A, Reed J, Dickman MB (2006) Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J Biol Chem 281:18793–18801. doi:10.1074/jbc.M511794200
5. Forment J, Naranjo MA, Roldan M, Serrano R, Vicente O (2002) Expression of Arabidopsis SR-like splicing proteins confers salt tolerance to yeast and transgenic plants. Plant J 30:511–519
6. Harrison MJ (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 50:361–389. doi:10.1146/annurev.arplant.50.1.361
7. Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429. doi:10.1105/tpc.004861
8. Hill TW, Käfer E (2001) Improved protocols for aspergillus medium: trace elements and minimum medium salt stock solutions. Fungal Genet Newsl 48:20–21
9. Jogawat A, Saha S, Bakshi M, Dayaman V, Kumar M, Dua M, Varma A, Oelmüller R, Tuteja N, Johri AK (2013) Piriformospora indica rescues growth diminution of rice seedlings during high salt stress. Plant Signal Behav 8:e26891. doi:10.4161/psb.26891
10. Joseph JD, Heitman J, Means AR (1999) Molecular cloning and characterization of Aspergillus nidulans cyclophilin B. Fungal Genet Biol 27(1):55–66. doi:10.1006/fgbi.1999.1131
11. Joshi A, Dang HQ, Vaid N, Tuteja N (2009) Isolation of high salinity stress tolerant genes from Pisum sativum by random overexpression in Escherichia coli and their functional validation. Plant Signal Behav 4:400–412. doi:10.4161/psb.4.5.8387
12. Kanhonou R, Serrano R, Palau RR (2001) A catalytic subunit of the sugar beet protein kinase CK2 is induced by salt stress and increases NaCl tolerance in Saccharomyces cerevisiae. Plant Mol Biol 47:571–579
13. Karandashov V, Nagy R, Wegmuller S, Amrhein N, Bucher M (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 101:6285–6290. doi:10.1073/pnas.0306074101
14. Kizawa H, Tomura D, Odat M, Fukamizu A, Hoshino T, Gotohll O, Yasui T, Shoun H (1991) Nucleotide sequence of the unique nitrate/nitrite-inducible cytochrome P-450 cDNA from Fusarium oxysporum. J Biol Chem 266:10632–10637
15. Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155:780–790. doi:10.1099/mic.0.019869-0
16. Li W, Liu X, Qiao H, Sun J, Duan D (2005) Two phase tillage: quick method for crop production in saline soils. Agrifood Res Rep 68:66–72
17. Limpens E, Bisseling T (2003) Signaling in symbiosis. Curr Opin Plant Biol 6:343–350. doi:10.1016/S1369-5266(03)00068-2
18. Maas E, Bisswanger H (1990) Localization of the alpha-oxoacid dehydrogenase multienzyme complexes within the mitochondrion. FEBS Lett 17:189–190. doi:10.1016/0014-5793(90)80840-F
19. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158. doi:10.1016/j.abb.2005.10.018
20. Marx J (2004) The roots of plant-microbe collaborations. Science 304:234–236. doi:10.1126/science.304.5668.234
21. Matouschek A, Rospert S, Schmid K, Glick BS, Schatz G (1995) Cyclophilin catalyzes protein folding in yeast mitochondria. Proc Natl Acad Sci USA 92:6319–6323. doi:10.4161/psb.22734
22. Mundree SG, Whittaker A, Thomson JA, Farrant JM (2000) An aldose reductase homolog from the resurrection plant Xerophyta viscosa. Planta 211:693–700
23. Nakashima S, Zhao Y, Nozawa Y (1996) Molecular cloning of delta 9 fatty acid desaturase from the protozoan Tetrahymena thermophila and its mRNA expression during thermal membrane adaptation. J Biochem 317:29–34. doi:10.1016/S1567-1356(02)00088-0
24. Newman EI, Reddell P (1987) The distribution of mycorrhizas among families of vascular plants. New Phytol 106:745–751. doi:10.1111/j.1469-8137.1987.tb00175.x
25. Nikolaou E, Agrafioti I, Stumpf M, Quinn J, Stansfield I, Brown AJ (2009) Phylogenetic diversity of stress signalling pathways in fungi. BMC Evol Biol 9:44. doi:10.1186/1471-2148-9-44
26. Nomura M (1999) Regulation of ribosome biosynthesis in Escherichia coli and Saccharomyces cerevisiae: diversity and common principles. J Bacteriol 181:6857–6864
27. Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414–421. doi:10.1016/j.pbi.2004.05.011
28. Pascale M, Rosati A, Festa M, Basile A, d’Avenia M, Falco A, Torino G, Turco MC (2010) BAG3 protein: role in some neoplastic cell types and Identification as a candidate target for therapy. Apoptosome. doi:10.1007/978-90-481-3415-1_7
29. Peskan-Berghofer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanke V, Kost G, Varma A, Oelmuller R (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol Plant 122:465–477. doi:10.1111/j.1399-3054.2004.00424.x
30. Pham GH, Kumari R, Singh AN, Sachdev M, Prasad R, Kaldorf M, Buscot F, Oelmüller R, Peskan T, Weiss M, Hampp R, Varma A (2004) Axenic culture of symbiotic fungus Piriformospora indica. Plant Surf Microbiol. doi:10.1007/978-3-540-74051-3_30
31. Rausell A, Kanhonou R, Yenush L, Serrano R, Ros R (2003) The translation initiation factor eIF1A is an important determinant in the tolerance to NaCl stress in yeast and plants. Plant J 34:257–267
32. Selosse MA, Setaro S, Glatard F, Richard F, Urcelay C, Weiss M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878. doi:10.1111/j.1469-8137.2007.02064.x
33. Shannon MC (1997) Adaptation of plants to salinity. Adv Agron 60:75–120
34. Takayama S, Sato T, Krajewski S, Kochel K, Irie S, Millan JA, Reed JC (1995) Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell 80:279–284. doi:10.1016/0092-8674(95)90410-7
35. Varma A, Savita V, Sudha Sahay N, Butehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744. doi:10.1128/AEM.05225-11
36. Viaud MC, Balhadere PV, Talbot NJ (2002) A Magnaporthe grisea cyclophilin acts as a virulence determinant during plant infection. Plant Cell 14:917–930. doi:10.1105/tpc.010389
37. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391. doi:10.1073/pnas.0504423102
38. Wang P, Cardenas ME, Cox GM, Perfect JR, Heitman J (2001) Two cyclophilin A homologs with shared and distinct functions important for growth and virulence of Cryptococcus neoformans. EMBO Rep 2:511–518. doi:10.1093/embo-reports/kve109
39. Weiss M, Selosse MA, Rexer KH, Urban A, Oberwinkler F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1003–1010. doi:10.1111/j.1469-8137.1967.tb05434.x
40. Yadav V, Kumar M, Kumar H, Deep DK, Tripathi T, Sharma R, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from root endophytic fungus Piriformospora indica plays a role in the phosphate transport to the host plant. J Biol Chem 285:26532–26544. doi:10.1074/jbc.M110.111021
41. Yamada A, Saitoh T, Mimura T, Ozeki Y (2002) Expression of mangrove allene oxide cyclise enhances salt tolerance in Escherichia coli, yeast and tobacco cells. Plant Cell Physiol 4:903–910
42. Yamada A, Tsutsumi K, Tanimoto S, Ozeki Y (2003) Plant RelA/SpoT homolog confers salt tolerance in Escherichia coli and Saccharomyces cerevisiae. Plant Cell Physiol 44:3–9
43. Zuccaro A, Lahrmann U, Güldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M, Murat C, Martin F, Kogel KH (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7:e1002290. doi:10.1371/journal.ppat.1002290