Advertisement

Elicitors derived from endophytic fungi Chaetomium globosum and Paraconiothyrium brasiliense enhance paclitaxel production in Corylus avellana cell suspension culture

  • Mina Salehi
  • Ahmad Moieni
  • Naser Safaie
  • Siamak Farhadi
Original Article
First Online:

Abstract

Paclitaxel is an impressive chemotherapeutic agent that shows biological activity against a wide range of cancers. Cell suspension culture of Corylus avellana has been reported as an alternative source for production of the valuable secondary metabolite, paclitaxel. The fungal elicitors have been considered as the most impressive strategy for enhancement of secondary metabolites in plant cell culture. In this study, two endophytic fungal strains YEF20 and HEF114 were isolated from Taxus baccata and C. avellana, respectively. The isolates YEF20 and HEF114 were identified as Chaetomium globosum and Paraconiothyrium brasiliense, respectively by sequencing of ITS1-5.8S-ITS2 rDNA region. This is the first report of P. brasiliense on C. avellana tree. Also, this study presents the positive effect of fungal elicitors on paclitaxel production in C. avellana for the first time. The effect of fungal elicitors on paclitaxel production was dependent on fungal species, and also type, concentration and adding time of elicitors to cell culture. The highest total yield of paclitaxel in cell culture treated with cell extract (CE) of C. globosum (291.5 µg L−1) was obtained by using 10% (v/v) of this fungal elicitor on 17th day of cell culture cycle (late log-phase), which was about 4.1 times obtained in the control culture. The cell culture treated with C. globosum CE had an average growth rate of 0.491 g L−1 day−1, i.e. 12.3% lower than that in the control. Among the fungal elicitors, 10% (v/v) CE of C. globosum on 17th day of culture cycle showed the best results with respect to extracellular paclitaxel portion (44.0%). Paclitaxel secretion to culture medium is essential for large-scale steady production of paclitaxel.

Keywords

Endophytic fungi Taxus baccata Anticancer Secondary metabolite 

Abbreviations

CSC

Cell suspension cultures

CE

Cell extract

CF

Culture filtrate

DW

Dry weight

FW

Fresh weight

HPLC

High performance liquid chromatography

MS

Murashige and Skoog (1962)

PDA

Potato Dextrose Agar

PDB

Potato Dextrose Broth (PDB)

ITS

Internal transcribed spacer

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

Notes

Acknowledgements

Authors gratefully acknowledge Research Deputy of Tarbiat Modares University, Tehran for financial support of this research project.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval and informed consent

All authors approve ethics and consent for participation and publication.

Supplementary material

11240_2018_1503_MOESM1_ESM.docx (705 kb)
Supplementary material 1 (DOCX 704 KB)

References

  1. Amini SA, Shabani L, Afghani L, Jalalpour Z, Sharifi-Tehrani M (2014) Squalestatininduced production of taxol and baccatin in cell suspension culture of yew (Taxus baccata L.). Turk J Biol 38:528–536.  https://doi.org/10.3906/biy-1401-47 CrossRefGoogle Scholar
  2. Awad V, Kuvalekar A, Harsulkar A (2014) Microbial elicitation in root cultures of Taverniera cuneifolia (Roth) Arn. for elevated glycyrrhizic acid production. Ind Crops Prod 54:13–16.  https://doi.org/10.1016/j.indcrop.2013.12.036 CrossRefGoogle Scholar
  3. Badi HN, Abdoosi V, Farzin N (2015) New approach to improve taxol biosynthetic. Trakia J Sci 2:115–124.  https://doi.org/10.15547/tjs.2015.02.002 CrossRefGoogle Scholar
  4. Baldi A, Srivastava AK, Bisaria VS (2009) Fungal elicitors for enhanced production of secondary metabolites in plant cell suspension cultures, vol. 18. In: Varma A, Kharkwal AC (eds) Symbiotic fungi, soil biology. Springer, Berlin, pp. 373–380.  https://doi.org/10.1007/978-3-540-95894-9_23 CrossRefGoogle Scholar
  5. Barrett LG, Heil M (2012) Unifying concepts and mechanisms in the specificity of plant-enemy interactions. Trends Plant Sci 17:282–292.  https://doi.org/10.1016/j.tplants.2012.02.009 CrossRefPubMedGoogle Scholar
  6. Belchí-Navarro S, Almagro L, Lijavetzky D, Bru R, Pedreño MA (2012) Enhanced extracellular production of trans-resveratrol in Vitis vinifera suspension cultured cells by using cyclodextrins and methyljasmonate. Plant Cell Rep 31:81–89.  https://doi.org/10.1007/s00299-011-1141-8 CrossRefGoogle Scholar
  7. Bestoso F, Ottaggio L, Armirotti A, Balbi A, Damonte G, Degan P, Mazzei M, Cavalli F, Ledda B, Miele M (2006) In vitro cell cultures obtained from different explants of Corylus avellana produce Taxol and taxanes. BMC Biotechnol 6:45–56.  https://doi.org/10.1186/1472-6750-6-45 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Carbone I, Kohn LM (1999) A method for designing primersets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556CrossRefGoogle Scholar
  9. Chen F, Ren CG, Zhou T, Wei YJ, Dai CC (2016) A novel exopolysaccharide elicitor from endophytic fungus Gilmaniella sp. AL12 on volatile oils accumulation in Atractylodes lancea. Sci Rep 6:34735.  https://doi.org/10.1038/srep34735 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Christen AA, Gibson DM, Bland T (1991) Production of taxol or taxol-like compounds in cell culture. U.S. Patent 5019504. https://www.google.com/patents/US5019504
  11. Cragg GM, Schepartz SA, Suffness M, Grever MR (1993) The taxol supply crisis. New NCI policies for handling the large-scale production of novel natural product anticancer and anti-HIV agents. J Nat Prod 56(10):1657–1668CrossRefGoogle Scholar
  12. Cutler HG, Crumley FG, Cox RH, Cole RJ, Dorner JW, Springer JP, Latterell FM, Thean JE, Rossi AE (1980) Chaetoglobosin K: a new plant growth inhibitor and toxin from Diplodia macrospora. J Agric Food Chem 28:139–142.  https://doi.org/10.1021/jf60227a011 CrossRefPubMedGoogle Scholar
  13. DiCosmo F, Quesnel A, Misawa M, Tallevi SG (1987) Increased synthesis of ajmalicine and catharanthine by cell suspension cultures of Catharanthus roseus in response to fungal culture-filtrates. Appl Biochem Biotechnol 14:101–106CrossRefGoogle Scholar
  14. Ding CH, Wang QB, Guo S, Wang ZY (2018) The improvement of bioactive secondary metabolites accumulation in Rumex gmelini Turcz through co-culture with endophytic fungi. Braz J Microbiol 49(2):362–369CrossRefGoogle Scholar
  15. Esmaeilzadeh Bahabadi SE, Sharifi M, Safaie N, Murata J, Yamagaki T, Satake H (2011) Increased lignan biosynthesis in the suspension cultures of Linum album by fungal extracts. Plant Biotechnol Rep 5:367–373.  https://doi.org/10.1007/s11816-011-0190-3 CrossRefGoogle Scholar
  16. Esmaeilzadeh Bahabadi S, Sharifi M, Behmanesh M, Safaie N, Murata J, Araki R, Yamagaki T, Satake H (2014) Time-course changes in fungal elicitor-induced lignan synthesis and expression of the relevant genes in cell cultures of Linum album. J Plant Physiol 169 (2012):487–491.  https://doi.org/10.1016/j.jplph.2011.12.006 CrossRefGoogle Scholar
  17. Espinosa-Leal CA, Puente-Garza CA, García-Lara S (2018) In vitro plant tissue culture: means for production of biological active compounds. Planta 247:1–18.  https://doi.org/10.1007/s00425-018-2910-1 CrossRefGoogle Scholar
  18. Gallego A, Imseng N, Bonfill M, Cusido RM, Palazon J, Eibl R, Moyano E (2015) Development of a hazel cell culture-based paclitaxel and baccatin III production process on a benchtop scale. J Biotechnol 195:93–102.  https://doi.org/10.1016/j.jbiotec.2014.12.023 CrossRefPubMedGoogle Scholar
  19. Gallego A, Malik S, Yousefzadi M, Makhzoum A, Tremouillaux-Guiller J, Bonfill M (2017) Taxol from Corylus avellana: paving the way for a new source of this anti-cancer drug. Plant Cell Tissue Organ Cult 129:1–16.  https://doi.org/10.1007/s11240-016-1164-5 CrossRefGoogle Scholar
  20. GraphPad Prism 5 (2005) GraphPad Prism 5. GraphPad Software Inc., San DiegoGoogle Scholar
  21. Hoffman A, Khan W, Worapong J, Strobel G, Griffin D, Arbogast B, Barofsky D, Boone RB, Ning L, Zheng P, Daley L (1998) Bioprospecting for Taxol in angiosperm plant extracts-Using high performance liquid chromatography thermospray mass spectrometry to detect the anticancer agent and its related metabolites in Filbert trees. Spectroscopy 13(6):22–32Google Scholar
  22. Jordan MA, Wilson L (2004) Microtubules as a target for anticancer drugs. Nat Rev Cancer 4(4):253–265.  https://doi.org/10.1038/nrc1317 CrossRefPubMedGoogle Scholar
  23. Kanokmedhakul S, Kanokmedhakul K, Phonkerd N, Soytong K, Kongsaeree P, Suksamrarn A (2002) Antimycobacterial anthraquinone–chromanone compound and diketopiperazine alkaloid from the fungus Chaetomium globosum KMITL-N0802. Planta Med 68:834–836.  https://doi.org/10.1055/s-2002-34415 CrossRefPubMedGoogle Scholar
  24. Kusari S, Singh S, Jayabaskaran C (2014) Rethinking production of Taxol® (paclitaxel) using endophyte biotechnology. Trends Biotechnol 32(6):304–311.  https://doi.org/10.1016/j.tibtech.2014.03.011 CrossRefPubMedGoogle Scholar
  25. Lan WZ, Yu LJ, Li MY, Qin WM (2003) Cell death unlikely contributes to taxol production in fungal elicitor-induced cell suspension cultures of Taxus chinensis. Biotechnol Lett 25(1):47–49.  https://doi.org/10.1023/A:1021726030724 CrossRefPubMedGoogle Scholar
  26. Larkin MA, Blackshields G, Brown NP, Chenna R, Mc Gettigan PA, Mc William H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG, Clustal W (2007) Clustal Xversion 2.0. Bioinformatics 23:2947–2948.  https://doi.org/10.1093/bioinformatics/btm404 CrossRefGoogle Scholar
  27. Li YC, Tao WY (2009) Interactions of Taxol-producing endophytic fungus with its host (Taxus spp.) during Taxol accumulation. Cell Biol Int 33:106–112.  https://doi.org/10.1016/j.cellbi.2008.10.007 CrossRefPubMedGoogle Scholar
  28. Liu K, Ding X, Deng B, Chen W (2009) Isolation and characterization of endophytic taxol-producing fungi from Taxus chinensis. J Ind Microbiol Biotechnol 36:1171–1177.  https://doi.org/10.1007/s10295-009-0598-8 CrossRefPubMedGoogle Scholar
  29. Ludwig-Müller J (2015) Plants and endophytes: equal partners in secondary metabolite production? Biotechnol lett 37(7):1325–1334.  https://doi.org/10.1007/s10529-015-1814-4 CrossRefPubMedGoogle Scholar
  30. Luo J, Liu L, Wu CD (2001) Enhancement of paclitaxel production by abscisic acid in cell suspension cultures of Taxus chinensis. Biotechnol Lett 23(16):1345–1348.  https://doi.org/10.1023/A:1010597802741 CrossRefGoogle Scholar
  31. Ming Q, Su C, Zheng C, Jia M, Zhang Q, Zhang H, Qin L (2013) Elicitors from the endophytic fungus Trichoderma atroviride promote Salvia miltiorrhiza hairy root growth and tanshinone biosynthesis. J Exp Bot 64(18):5687–5694.  https://doi.org/10.1093/jxb/ert342 CrossRefPubMedGoogle Scholar
  32. Naik PM, Al-Khayri JM (2016) Impact of abiotic elicitors on in vitro production of plant secondary metabolites: a review. J Adv Res Biotech 1(2):7.  https://doi.org/10.15226/2475-4714/1/2/00102 CrossRefGoogle Scholar
  33. Nielsen KF, Gravesen S, Nielsen PA, Andersen B, Thrane U, Frisvad JC (1999) Production of mycotoxins on artificially and naturally infested building materials. Mycopathologia 145:43–56.  https://doi.org/10.1023/A:1007038211176 CrossRefPubMedGoogle Scholar
  34. Park JH, Choi GJ, Jang KS, Lim HK, Kim HT, Cho KY, Kim JC (2005) Antifungal activity against plant pathogenic fungi of chaetoviridins isolated from Chaetomium globosum. FEMS Microbiol Lett 252:309–313.  https://doi.org/10.1016/j.femsle.2005.09.013 CrossRefPubMedGoogle Scholar
  35. Qin WM, Lan WZ (2004) Fungal elicitorinduced cell death in Taxus chinensis suspension cells is mediated by ethylene and polyamines. Plant Sci 166:989–995.  https://doi.org/10.1016/j.plantsci.2003.12.013 CrossRefGoogle Scholar
  36. Rahpeyma SA, Moieni A, Jalali Javaran M (2015) Paclitaxel production is enhanced in suspension-cultured hazel (Corylus avellana L.) cells by using a combination of sugar, precursor, and elicitor. Eng Life Sci 15(2):234–242.  https://doi.org/10.1002/elsc.201400115 CrossRefGoogle Scholar
  37. Rahpeyma SA, Moieni A, Jalali-Javaran M (2017) Enhancement of paclitaxel content in induced tetraploid Corylus avellana L. cell suspension culture with regulating the expression of genes in paclitaxel biosynthetic pathway. Acta Physiol Plant 39:241.  https://doi.org/10.1007/s11738-017-2531-5 CrossRefGoogle Scholar
  38. Rakotoniriana EF, Munaut F, Decock C, Randriamampionona D, Andriambololoniaina M, Rakotomalala T, Rakotonirina EJ, Rabemanantsoa C, Cheuk K, Ratsimamanga SU, Mahillon J, El-Jaziri M, Quetin-Leclercq J, Corbisier AM (2008) Endophytic fungi from leaves of Centella asiatica: occurrence and potential interactions within leaves. Antonie Van Leeuwenhoek 93:27–36.  https://doi.org/10.1007/s10482-007-9176-0 CrossRefGoogle Scholar
  39. Ramirez-Estrada K, Vidal-Limon H, Hidalgo D, Moyano E, Golenioswki M, Cusidó RM, Palazon J (2016) Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 21(2):182‏.  https://doi.org/10.3390/molecules21020182 CrossRefPubMedGoogle Scholar
  40. Rebecca AIN, Hemamalini V, Kumar DM, Srimathi S, Muthumary J, Kalaichelvan PT (2012) Endophytic Chaetomium sp. from Michelia champaca L. and its taxol production. J Acad Ind Res 1(68):72Google Scholar
  41. Safaie N, Alizadeh A, Saidi A, Rahimian H, Adam G (2005) Molecular characterization and genetic diversity among Iranian populations of Fusarium graminearum, the causal agent of wheat head blight. Iran J Plant Pathol 41:171–189Google Scholar
  42. Salehi M, Moieni A, Safaie N (2017) A novel medium for enhancing callus growth of hazel (Corylus avellana L.). Sci Rep 7(1):15598.  https://doi.org/10.1038/s41598-017-15703-z CrossRefPubMedPubMedCentralGoogle Scholar
  43. Salehi M, Moieni A, Safaie N (2018) Elicitors derived from hazel (Corylus avellana L.) cell suspension culture enhance growth and paclitaxel production of Epicoccum nigrum. Sci Rep 8(1):12053.  https://doi.org/10.1038/s41598-018-29762-3 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Salma U, Kundu S, Ali MN, Mandal N (2018) Elicitor mediated enhancement of wedelolactone in cell suspension culture of Eclipta alba (L.) Hassk. Plant Cell Tissue Organ Cult.‏  https://doi.org/10.1007/s11240-018-1431-8 CrossRefGoogle Scholar
  45. Schiff PB, Fant J, Horwitz SB (1979) Promotion of microtubule assembly in vitro by taxol. Nature 277(5698):665.  https://doi.org/10.1038/277665a0 CrossRefGoogle Scholar
  46. Service RF (2000) Hazel trees offer new source of cancer drug. Science 288:27–28.  https://doi.org/10.1126/science.288.5463.27a CrossRefPubMedGoogle Scholar
  47. Simic SG, Tusevski O, Maury S, Hano C, Delaunay A, Chabbert B, Lamblin F, Laine E, Joseph C, Hagège D (2015) Fungal elicitor-mediated enhancement in phenylpropanoid and naphtodianthrone contents of Hypericum perforatum L. cell cultures. Plant Cell Tissue Organ Cult 122(1):213–226.  https://doi.org/10.1007/s11240-015-0762-y CrossRefGoogle Scholar
  48. Smetanska I (2008) Production of secondary metabolites using plant cell cultures. Adv Biochem Eng Biotechnol 111:187–228.  https://doi.org/10.1007/10_2008_103 CrossRefGoogle Scholar
  49. Soca-Chafre G, Rivera-Orduña FN, Hidalgo-Lara ME, Hernandez-Rodriguez C, Marsch R, Flores-Cotera LB (2011) Molecular phylogeny and paclitaxel screening of fungal endophytes from Taxus globosa. Fungal Boil 115(2):143–156.  https://doi.org/10.1016/j.funbio.2010.11.004 CrossRefGoogle Scholar
  50. Somssich IE, Hahlbrok K (1998) Pathogen defence in plant—a paradigm of biological complexity. Trends Plant Sci 3:86–90.  https://doi.org/10.1016/S1360-1385(98)01199-6 CrossRefGoogle Scholar
  51. Strobel GA, Hess WM (1997) Glucosylation of the peptide leucinostatin A, produced by an endophytic fungus of European yew, may protect the host from leucinostatin toxicity. Chem Biol 4:529–536CrossRefGoogle Scholar
  52. Strobel G, Stierle A, van Kujik F (1992) Factors influencing the in vitro production of radiolabeled taxol by Pacific yew, Taxus brevifolia. Plant Sci 84:65–74.  https://doi.org/10.1016/0168-9452(92)90209-5 CrossRefGoogle Scholar
  53. Strobel G, Yang X, Sears J, Kramer R, Sidhu RS, Hess WM (1996) Taxol from Pestalotiopsis microspora, an endophytic fungus of Taxus wallachiana. Microbiology 142:435–440.  https://doi.org/10.1099/13500872-142-2-435 CrossRefPubMedGoogle Scholar
  54. Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268.  https://doi.org/10.1021/np030397v CrossRefPubMedGoogle Scholar
  55. Takeuchi C, Nagatani K, Sato Y (2013) Chitosan and a fungal elicitor inhibit tracheary element differentiation and promote accumulation of stress lignin-like substance in Zinnia elegans xylogenic culture. J Plant Res 126:811–821.  https://doi.org/10.1007/s10265-013-0568-0 CrossRefPubMedGoogle Scholar
  56. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599.  https://doi.org/10.1093/molbev/msm092 CrossRefGoogle Scholar
  57. Tashackori H, Sharifi M, Chashmi NA, Behmanesh M, Safaie N (2018) Piriformospora indica cell wall modulates gene expression and metabolite profile in Linum album hairy roots. Planta 2018:1–18.  https://doi.org/10.1007/s00425-018-2973-z CrossRefGoogle Scholar
  58. Wang C, Wu J, Mei X (2001) Enhancement of taxol production and excretion in Taxus chinensis cell culture by fungal elicitation and medium renewal. Appl Microb Biotechnol 55(4):404–410.  https://doi.org/10.1016/j.cellbi.2008.10.007 CrossRefGoogle Scholar
  59. Wang Y, Dai C, Zhao Y, Peng Y (2011) Fungal endophyte-induced volatile oil accumulation in Atractylodes lancea plantlets is mediated by nitric oxide, salicylic acid and hydrogen peroxide. Process Biochem 46:730–735.  https://doi.org/10.1016/j.procbio.2010.11.020 CrossRefGoogle Scholar
  60. Wang Y, Dai CC, Cao JL (2012) Comparison of the effects of fungal endophyte Gilmaniella sp. and its elicitor on Atractylodes lancea plantlets. World J Microbiol Biotechnol 28:575–584.  https://doi.org/10.1007/s11274-011-0850-z CrossRefPubMedGoogle Scholar
  61. Wani MC, Taylor HL, Wall ME, Coggon P, Mc Phail AT (1971) Plant antitumor agents. VI. The isolation and structure of taxol. A novel antileukemic and antitumor agent from Taxus brevifolia. J Am Chem Soc 93:2325–2327CrossRefGoogle Scholar
  62. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322.  https://doi.org/10.1016/B978-0-12-372180-8.50042-1 CrossRefGoogle Scholar
  63. Wu ZL, Yuan YJ, Liu JX, Xuan HY, Hu ZD, Sun AC, Hu CX (1999) Study on enhanced production of Taxol from Taxus chinensis var. mairei in biphasic-liquid culture. Acta Bot Sin 41:1108–1113Google Scholar
  64. Yuan YJ, Li C, Hu ZD, Wu JC, Zeng AP (2002) Fungal elicitor-induced cell apoptosis in suspension cultures of Taxus chinensis var. mairei for taxol production. Process Biochem 38(2):193–198.  https://doi.org/10.1016/S0032-9592(02)00071-7 CrossRefGoogle Scholar
  65. Zhai X, Jia M, Chen L, Zheng CJ, Rahman K, Han T, Qin LP (2016) The regulatory mechanism of fungal elicitor-induced secondary metabolite biosynthesis in medical plants. Crit Rev Microbiol 43(2):238–261.  https://doi.org/10.1080/1040841X.2016.1201041 CrossRefPubMedGoogle Scholar
  66. Zhang JF, Gong S, Guo ZG (2011) Effects of different elicitors on 10-deacetylbaccatin III-10-O-acetyltransferase activity and cytochrome P450 monooxygenase content in suspension cultures of Taxus cuspidata cells. Cell Boil Int Rep 18(1):7–13.  https://doi.org/10.1042/CBR20110001&%23x200F; CrossRefGoogle Scholar
  67. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333.  https://doi.org/10.1016/j.biotechadv.2005.01.003 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Mina Salehi
    • 1
  • Ahmad Moieni
    • 1
  • Naser Safaie
    • 2
  • Siamak Farhadi
    • 1
  1. 1.Department of Plant Breeding and Biotechnology, Faculty of AgricultureTarbiat Modares UniversityTehranIran
  2. 2.Department of Plant Pathology, Faculty of AgricultureTarbiat Modares UniversityTehranIran

Personalised recommendations

Cite article

Buy options