Fungal endophytes of Catharanthus roseus enhance vindoline content by modulating structural and regulatory genes related to terpenoid indole alkaloid biosynthesis

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Pandey, Shiv S ^a   Singh, Sucheta ^a   Babu, C S Vivek ^a   Shanker, Karuna ^a   Srivastava, N K ^a   Shukla, Ashutosh K ^a   Kalra, Alok ^a  

^a CSIR CENTRAL INSTITUTE OF MEDICINAL AND AROMATIC PLANTS   (India)

Author keywords

[No Author keywords available]

Indexed keywords

VINBLASTINE; VINDOLINE;

ANALOGS AND DERIVATIVES; CATHARANTHUS; ENDOPHYTE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MUCORALES; PLANT LEAF;

CATHARANTHUS; ENDOPHYTES; GENE EXPRESSION REGULATION, PLANT; MUCORALES; PLANT LEAVES; VINBLASTINE;

EID: 84971276137     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep26583     Document Type: Article

References (60)

1. Kusari, S., Hertweck, C., & Spiteller, M. Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem. Biol. 19, 792-798 (2012
2. Ryan, R. P., Germaine, K., Franks, A., Ryan, D. J., & Dowling, D. N. Bacterial endophytes: recent developments and applications. FEMS Microbiol. Lett. 278, 1-9 (2008
3. Lodewyckx, C., et al. Endophytic bacteria and their potential applications. Crit. Rev. Plant Sci. 21, 583-606 (2002
4. Bernardi-Wenzel, J. B., et al. Evaluation of foliar fungal endophyte diversity and colonization of medicinal plant Luehea divaricata (Martius et Zuccarini). Biol. Res. 43, 375-384 (2010
5. Knoth, J. L., Kim, S. H., Ettl, G. J., & Doty, S. L. Biological nitrogen fixation and biomass accumulation within poplar clones as a result of inoculations with diazotrophic endophyte consortia. New Phytol. 201, 599-609 (2014
6. Rodriguez, R., & Redman, R. More than 400 million years of evolution and some plants still can?t make it on their own: Plant stress tolerance via fungal symbiosis. J. Exp. Bot. 59, 1109-1114 (2008
7. Schulz, B., & Boyle, C. The endophytic continuum. Mycol. Res. 109, 661-686 (2005
8. Rodriguez, R. J., Redman, R. S., & Henson, J. M. In The Fungal Community: its Organization and Role in the Ecosystem 3rd edn, (eds Dighton, J., et al.) Ch. 34, 683-695 (CRC Press, Boca Raton, 2005
9. Mousa, W. K., & Raizada, M. N. The diversity of anti-microbial secondary metabolites produced by fungal endophytes: an interdisciplinary perspective. Front. Microbiol. 4, 65 (2013
10. Kumar, A., Patil, D., Rajamohanan, P. R., & Ahmad, A. Isolation, purification and characterization of vinblastine and vincristine from endophytic fungus Fusarium oxysporum isolated from Catharanthus roseus. PLoS One 8, e71805 (2013
11. Soliman, S. S. M., Tsao, R., & Raizada, M. N. Chemical inhibitors suggest endophytic fungal paclitaxel is derived from both mevalonate and non-mevalonate-like pathways. J. Nat. Prod. 74, 2497-2504 (2011
12. Kusari, S., Verma, V. C., Lamshoeft, M., & Spiteller, M. An endophytic fungus from Azadirachta indica A. Juss. that produces azadirachtin. World J. Microbiol. Biotechnol. 28, 1287-1294 (2012
13. Eyberger, A. L., Dondapati, R., & Porter, J. R. Endophyte fungal isolates from Podophyllum peltatum produce podophyllotoxin. J. Nat. Prod. 69, 1121-1124 (2006
14. Kusari, S., Lamshöft, M., & Spiteller, M. Aspergillus fumigatus Fresenius, an endophytic fungus from Juniperus communis L. Horstmann as a novel source of the anticancer pro-drug deoxypodophyllotoxin. J. Appl. Microbiol. 107, 1019-1030 (2009
15. Puri, S. C., Verma, V., Amna, T., Qazi, G. N., & Spiteller, M. An endophytic fungus from Nothapodytes foetida that produces camptothecin. J. Nat. Prod. 68, 1717-1719 (2005
16. Kusari, S., Lamshöft, M., Zühlke, S., & Spiteller, M. An endophytic fungus from Hypericum perforatum that produces hypericin. J. Nat. Prod. 71, 159-162 (2008
17. Kusari, S., Singh, S., & Jayabaskaran, C. Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends Biotechnol. 32, 297-303 (2014
18. Li, J., et al. An endophytic Pseudonocardia species induces the production of artemisinin in Artemisia annua. PloS one 7, e51410 (2012
19. Ming, Q., et al. Elicitors from the endophytic fungus Trichoderma atroviride promote Salvia miltiorrhiza hairy root growth and tanshinone biosynthesis. J. Exp. Bot. 64, 5687-5694 (2013
20. Shukla, A. K., & Khanuja, S. P. S. In OMICS Applications in Crop Science, (ed Barh, D.) Ch. 10, 325-384 (CRC Press, Boca Raton, 2013
21. Torres, A. R., et al. Colonization of Madagascar periwinkle (Catharanthus roseus), by endophytes encoding gfp marker. Arch. Microbiol. 195, 483-489 (2013
22. Ferreira Filho, A. S., et al. Endophytic Methylobacterium extorquens expresses a heterologous β -1, 4-endoglucanase A (EglA) in Catharanthus roseus seedlings, a model host plant for Xylella fastidiosa. World J. Microbiol. Biotechnol. 28, 1475-1481 (2012
23. Lacava, P. T., Araújo, W. L., & Azevedo, J. L. Evaluation of endophytic colonization of Citrus sinensis and Catharanthus roseus seedlings by endophytic bacteria. J. Microbiol. 45, 11-14 (2007
24. Monteiro, P. B., et al. Catharanthus roseus, an experimental host plant for the citrus strain of Xylella fastidiosa. Plant Dis. 85, 246-251 (2001
25. Van Der Heijden, R., Jacobs, D. I., Snoeijer, W., Hallard, D., & Verpoorte, R. The Catharanthus alkaloids: pharmacognosy and biotechnology. Curr. Med. Chem. 11, 607-628 (2004
26. O?Keefe, B. R., Mahady, G. B., Gills, J. J., Beecher, C. W., & Schilling, A. B. Stable vindoline production in transformed cell cultures of Catharanthus roseus. J. Nat. Prod. 60, 261-264 (1997
27. Suttipanta, N., et al. The transcription factor CrWRKY1 positively regulates the terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiol. 157, 2081-2093 (2011
28. Zhang, H., et al. The basic helix-loop-helix transcription factor CrMYC2 controls the jasmonate-responsive expression of the ORCA genes that regulate alkaloid biosynthesis in Catharanthus roseus. Plant J. 67, 61-71 (2011
29. Zhou, M. L., et al. Molecular regulation of terpenoid indole alkaloids pathway in the medicinal plant, Catharanthus roseus. J. Med. Plants Res. 4, 2760-2772 (2010
30. Liu, D. H., et al. Terpenoid indole alkaloids biosynthesis and metabolic engineering in Catharanthus roseus. J. Integr. Plant Biol. 49, 961-974 (2007
31. Memelink, J., & Gantet, P. Transcription factors involved in terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Phytochem. Rev. 6, 353-362 (2007
32. Tiwari, R., et al. Bacterial endophyte-mediated enhancement of in planta content of key terpenoid indole alkaloids and growth parameters of Catharanthus roseus. Ind. Crop. Prod. 43, 306-310 (2013
33. Papageorgiou, G. C., & Govindjee. (Ed.). In Chlorophyll a fluorescence: a signature of photosynthesis, Vol. 19 (Springer, 2004
34. Kharwar, R. N., Verma, V. C., Strobel, G., & Ezra, D. The endophytic fungal complex of Catharanthus roseus (L.) G. Don. Curr. Sci. 95, 228-233 (2008
35. Adams III, W. W., & Demmig-Adams, B. In Chlorophyll a fluorescence: a signature of photosynthesis, Vol. 19 (eds Papageorgiou, G. C., & Govindjee) Ch. 22, 583-604 (Springer, 2004
36. Li, W. D., Duan, W., Fan, P. G., Yan, S. T., & Li, S. H. Photosynthesis in response to sink-source activity and in relation to end products and activities of metabolic enzymes in peach trees. Tree Physiol. 27, 1307-1318 (2007
37. Mucciarelli, M., Scannerini, S., Bertea, C., & Maffei, M. In vitro and in vivo peppermint (Mentha piperita) growth promotion by nonmycorrhizal fungal colonization. New Phytol. 158, 579-591 (2003
38. Varma, A., et al. Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl. Environ. Microbiol. 65, 2741-2744 (1999
39. Costa, M. M., et al. Molecular cloning and characterization of a vacuolar class III peroxidase involved in the metabolism of anticancer alkaloids in Catharanthus roseus. Plant Physiol. 146, 403-417 (2008
40. Ferreres, F., et al. Identification of phenolic compounds in isolated vacuoles of the medicinal plant Catharanthus roseus and their interaction with vacuolar class III peroxidase: an H2O2 affair? J. Exp. Bot. 62, 2841-2854 (2011
41. Christhudas, I. N., Kumar, P. P., & Agastian, P. In Vitro α -Glucosidase inhibition and antioxidative potential of an endophyte species (Streptomyces sp. Loyola UGC) isolated from Datura stramonium L. Curr. Microbiol. 67, 69-76 (2013
42. Wan, Y., et al. Effect of endophyte-infection on growth parameters and Cd-induced phytotoxicity of Cd-hyperaccumulator Solanum nigrum L. Chemosphere 89, 743-750 (2012
43. Pauw, B., et al. Zinc finger proteins act as transcriptional repressors of alkaloid biosynthesis genes in Catharanthus roseus. J. Biol. Chem. 279, 52940-52948 (2004
44. Li, C. Y., et al. The ORCA2 transcription factor plays a key role in regulation of the terpenoid indole alkaloid pathway. BMC Plant Biol. 13, 155 (2013
45. Van Der Fits, L., & Memelink, J. ORCA3, a jasmonate responsive transcriptional regulator of plant primary and secondary metabolism. Science 289, 295-297 (2000
46. Pan, Q., et al. Overexpression of ORCA3 and G10H in Catharanthus roseus plants regulated alkaloid biosynthesis and metabolism revealed by NMR-metabolomics. PloS one 7, e43038 (2012
47. Sibéril, Y., et al. Catharanthus roseus G-box binding factors 1 and 2 act as repressors of strictosidine synthase gene expression in cell cultures. Plant Mol. Biol. 45, 477-488 (2001
48. Raina, S. K., et al. CrMPK3, a mitogen activated protein kinase from Catharanthus roseus and its possible role in stress induced biosynthesis of monoterpenoid indole alkaloids. BMC Plant Biol. 12, 134 (2012
49. Sambrook, J., Fritsch, E. F., & Maniatis, T. In Molecular cloning: a laboratory manual 2nd edn (Cold Spring Harbor Laboratory Press, 1989
50. White, T. J., Bruns, T., Lee, S., & Taylor, J. In PCR protocols A guide to methods and applications (eds Innis, M. A., et al.) Ch. 38, 315-322 (Academic Press, 1990
51. Spiering, M. J., Greer, D. H., & Schmid, J. Effects of the fungal endophyte, Neotyphodium lolii, on net photosynthesis and growth rates of perennial ryegrass (Lolium perenne) are independent of in planta endophyte concentration. Ann. Bot. 98, 379-387 (2006
52. Singh, D. V., Maithy, A., Verma, R. K., Gupta, M. M., & Kumar, S. Simultaneous determination of Catharanthus alkaloids using reversed phase high performance liquid chromatography. J. Liq. Chrom., & Rel. Technol. 23, 601-607 (2000
53. Peebles, C. A. M., Hong, S. B., Gibson, S. I., Shanks, J. V., & San, K. Y. Transient effects of overexpressing anthranilate synthase α and β subunits in Catharanthus roseus hairy roots. Biotechnol. Prog. 21, 1572-1576 (2005
54. Lichtenthaler, H. K., & Buschmann, C. In Current protocols in food analytical chemistry (eds Wrolstad, R. E., et al.) F4.3.1-F4.3.8 (New York: John Wiley, & Sons, 2001
55. Biswal, A. K., et al. Light Intensity-dependent modulation of chlorophyll b biosynthesis and photosynthesis by overexpression of Chlorophyllide a Oxygenase in tobacco. Plant Physiol. 159, 433-449 (2012
56. Pérez-Ruiz, J. M., et al. Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage. Plant Cell 18, 2356-2368 (2006
57. Asada, K., et al. A 7-Deoxyloganetic acid Glucosyltransferase contributes a key step in secologanin biosynthesis in Madagascar Periwinkle. Plant Cell 25, 4123-4134 (2013
58. Besseau, S., et al. A pair of Tabersonine 16-hydroxylases initiates the synthesis of vindoline in an organ-dependent manner in Catharanthus roseus. Plant Physiol. 163, 1792-1803 (2013
59. Schmittgen, T. D., & Livak, K. J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101-1108 (2008
60. Livak, K. J., & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2δδCt method. Methods 25, 402-408 (2001