Diversity and Biological Activities of Endophytic Fungi Associated with Micropropagated Medicinal Plant <i>Echinacea purpurea</i> (L.) Moench — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Diversity and Biological Activities of Endophytic Fungi Associated with Micropropagated Medicinal Plant <i>Echinacea purpurea</i> (L.) Moench
Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Minas Gerais, Brazil
,
National Center for Natural Products Research, Research Institute of Pharmaceutical Sciences, School of Pharmacy, University of Mississippi, Oxford, USA
,
National Center for Natural Products Research, Research Institute of Pharmaceutical Sciences, School of Pharmacy, University of Mississippi, Oxford, USA
,
USDA-ARS, Natural Products Utilization Research Unit (NPURU), University of Mississippi, Oxford, USA
,
USDA-ARS, Natural Products Utilization Research Unit (NPURU), University of Mississippi, Oxford, USA
,
USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), Gainesville, USA
,
USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), Gainesville, USA
,
USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), Gainesville, USA
,
National Center for Natural Products Research, Research Institute of Pharmaceutical Sciences, School of Pharmacy, University of Mississippi, Oxford, USA
,
Center for Water and Wetland Resources, The University of Mississippi Field Station, Abbeville, USA
1 Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Minas Gerais, Brazil
2 National Center for Natural Products Research, Research Institute of Pharmaceutical Sciences, School of Pharmacy, University of Mississippi, Oxford, USA
3 National Center for Natural Products Research, Research Institute of Pharmaceutical Sciences, School of Pharmacy, University of Mississippi, Oxford, USA
4 USDA-ARS, Natural Products Utilization Research Unit (NPURU), University of Mississippi, Oxford, USA
5 USDA-ARS, Natural Products Utilization Research Unit (NPURU), University of Mississippi, Oxford, USA
6 USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), Gainesville, USA
7 USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), Gainesville, USA
8 USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), Gainesville, USA
9 National Center for Natural Products Research, Research Institute of Pharmaceutical Sciences, School of Pharmacy, University of Mississippi, Oxford, USA
10 Center for Water and Wetland Resources, The University of Mississippi Field Station, Abbeville, USA
Echinacea is one of the top ten selling medicinal herbs in Europe and United States. Commercially available formulations may contain different plant parts of three species ( Echinacea purpurea , E. pallida , and E. angustifolia ). Our study evaluates the diversity of microbial community associated with healthy E. purpurea clones and their ability to produce defense compounds. We recovered and identified thirty-nine fungal endophytes through the molecular methods in 15 distinct phylotypes, which were closely related to species of the following genera Ceratobasidium , Cladosporium Colletotrichum , Fusarium , Glomerella , and Mycoleptodiscus . These taxa were previously reported as decomposer and phytopathogenic fungi. The fungal community associated with two E. purpurea clones showed high richness and dominance indices with different distribution among plant organs. Crude extracts of fungal isolates were tested for antifungal and insecticidal biological activities. A total of 16 extracts (41%) showed antifungal properties; while just the extract of M. indicus exhibited larvicidal activity against A. aegypti . These results suggest that the symbiosis between the endophytic fungal community and micropropagated clones of E. purpurea was re-established after acclimatization to soil and the endophytic fungi produced compounds against phytopathogenic fungi.
D. S. Heckman, D. M. Geiser, B. R. Eidell, R. L. Stauffer, N. L. Kardos and S. B. Hedges, “Molecular Evidence for the Early Colonization of Land by Fungi and Plants,” Science, Vol. 293, No. 5532, 2001, pp. 1129-1133. doi:10.1126/science.1061457
K. Clay and J. Holah, “Fungal Endophyte Symbiosis and Plant Diversity in Successional Fields,” Science, Vol. 285, No. 5434, 1999, pp. 1742-1744. doi:10.1126/science.285.5434.1742
J. E. Taylor, K. D. Hyde and E. B. G. Jones, “Endophytic Fungi Associated with Temperate Palm, Trachycarpus fortunei, within and outside Its Natural Geographic Range,” New Phytologist, Vol. 142, No. 2, 1999, pp. 335-346. doi:10.1046/j.1469-8137.1999.00391.x
S. Phongpaichit, N. Rungjindamai, V. Rukachaisirikul and J. Sakayaroj, “Antimicrobial Activity in Cultures of Endophytic Fungi Isolated from Garcinia Species,” FEMS Immunology & Medical Microbiology, Vol. 48, No. 3, 2006, 367-372. doi:10.1111/j.1574-695X.2006.00155.x
L. H. Rosa, V. N. Gon?alves, R. B. Caligiorne, T. M. A. Alves, A. Rabello, P. A. Sales, A. J. Romanha, M. E. G. Sobral, C. A. Rosa and C. L. Zani, “Leishmanicidal, Trypanocidal, and Cytotoxic Activities of Endophytic Fungi Associated with Bioactive Plants in Brazil,” Brazilian Journal of Microbiology, Vol. 41, No. 2, 2010, pp. 420-430. doi:10.1590/S1517-83822010000200024
M. L. V. Vieira, A. F. S. Hughes, V. B. Gil, A. B. M. Vaz, T. M. A. Alves, C. L. Zani, C. A. Rosa and L. H. Rosa, “Diversity and Antimicrobial Activities of the Fungal Endophyte Community Associated with the Traditional Brazilian Medicinal Plant Solanum cernuum Vell. (Solanaceae),” Canadian Journal of Microbiology, Vol. 58, No. 1, 2012, pp. 54-66. doi:10.1139/w11-105
N. D. Pugh, P. Balachandran, H. Lata, F. E. Dayan, V. Joshi, E. Bedir, T. Makino, R. Moraes, I. Khan and D. S. Pasco, “Melanin: Dietary Mucosal Immune Modulator from Echinacea and Other Botanical Supplements,” International Immunopharmacology, Vol. 5, No. 4, 2005, pp. 637-647. doi:10.1016/j.intimp.2004.12.011
R. M. Moraes, H. Lata, J. Sumyanto, A. M. S. Pereira, B. W. Bertoni, V. C. Joshi, N. D. Pugh, I. A. Khan and D. S. Pasco, “Characterization and Pharmacological Properties of in Vitro Propagated Clones of Echinacea tennesseensis (Beadle) Small,” Plant Cell, Tissue and Organ Culture, Vol. 106, No. 2, 2011, pp. 309-315. doi:10.1007/s11240-011-9922-x
H. Lata, Z. De Andrade, B. Schaneberg, E. Bedir, I. Khan and R. Moraes, “Arbuscular Mycorrhizal Inoculation Enhances Survival Rates and Growth of Micropropagated Plantlets of Echinacea pallid,” Planta Medica, Vol. 69, No. 7, 2003, pp. 679-682.
T. Murashige and F. Skoog, “A Revised Medium for Rapid Growth and Bioassays with Tobacco Tissue Cultures,” Physiologia Plantarum, Vol. 15, No. 3, 1962, pp. 473-497. doi:10.1111/j.1399-3054.1962.tb08052.x
H. Lata, E. Bedir, I. Khan and R. M. Moraes, “Mass Propagation of Echinacea angustifolia: A Protocol Refinement Using Shoot Encapsulation and Temporary Immersion Bioreactor,” Acta Horticulturae, Vol. 629, 2004, pp. 409-414.
T. J. White, T. D. Bruns, S. B. Lee and J. W. Taylor, “Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics,” In: N. A. Innis, J. Gelfand and J. Sninsky, Eds., PCR Protocols: A Guide to Methods and Applications, Academic Press, San Diego, 1990, pp. 315-322.
R. Gazis, S. Rehner and P. Chaverri, “Species Delimitation in Fungal Endophyte Diversity Studies and Its Implications in Ecological and Biogeographic Inferences,” Molecular Ecology, Vol. 20, No. 14, 2011, pp. 3001-3013. doi:10.1111/j.1365-294X.2011.05110.x
L. H. Rosa, M. de L. A. Vieira, I. F. Santiago and C. A. Rosa, “Endophytic Fungi Community Associated with the Dicotyledonous Plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica,” FEMS Microbiology Ecology, Vol. 73, No. 1, 2010, pp. 178-189.
K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei and S. Kumar, “MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods,” Molecular Biology and Evolution, Vol. 28, No. 10, 2011, pp. 2731-2739. doi:10.1093/molbev/msr121
G. S. Ryan, D. A. T. Harper and J. S. Whalley, “PALSTAT, Statistics for Palaeontologist,” Chapman & Hall, London, 1995.
I. F. Santiago, T. M. A. Alves, A. Rabello, P. A. Sales Jr, A. J. Romanha, C. L. Zani, C. A. Rosa and L. H. Rosa, “Leishmanicidal and Antitumoral Activities of Endophytic Fungi Associated with the Antarctic Angiosperms Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth) Bartl.,” Extremophiles, Vol. 16, No. 1, 2012, pp. 95-103. doi:10.1007/s00792-011-0409-9
D. E. Wedge and J. M. Kuhajek, “A Microbioassay for Fungicide Discovery,” Southern Association of Agricultural Scientists Bulletin, Biochemistry and Biotechnology, Vol. 11, 1998, pp. 1-7.
D. E. Wedge, J. A. Klun, N. Tabanca, et al., “Bioactivity-Guided Fractionation and GC/MS Fingerprinting of Angelica sinensis and Angelica archangelica Root Components for Antifungal and Mosquito Deterrent Activity,” Journal of Agriculture and Food Chemistry, Vol. 57, No. 2, 2009, pp. 464-470.
N. Tabanca, U. R. Bernier, M. Tsikola, et al., “Eupatorium capillifolium Essential Oil: Chemical Composition, Antifungal Activity, and Insecticidal Activity,” Natural Products Communication, Vol. 5, No. 9, 2010, pp. 1409-1415.
P. Zalar, G. S. de Hoog, H.-J. Schroers, P. W. Crous, J. Z. Groenewald and N. Gunde-Cimerman, “Phylogeny and Ecology of the Ubiquitous Saprobe Cladosporium sphaerospermum, with Descriptions of Seven New Species from Hypersaline Environments,” Studies in Mycology, Vol. 58, No. 1, 2007, pp. 157-183. doi:10.3114/sim.2007.58.06
D. S. S. Kumar, H. Y. Cheung, C. S. Lau, F. Chen and K. D. Hyde, “In Vitro Studies of Endophytic Fungi from Tripterygium wilfordii with Anti-Proliferative Activity on Human Peripheral Blood Mononuclear Cells,” Journal of Ethnopharmacology, Vol. 94, No. 2-3, 2004, pp. 295-300. doi:10.1016/j.jep.2004.05.019
A. B. M. Vaz, M. C. Mota, M. R. Q. Bomfim, et al., “Antimicrobial Activity of Endophytic Fungi Associated with Orchidaceae in Brazil,” Canadian Journal of Microbiology, Vol. 55, No. 12, 2009, pp. 1381-1391. doi:10.1139/W09-101
B. C. Sutton, “Pucciniopsis, Mycoleptodiscus and Amerodiscosiella,” Transactions of the British Mycological Society, Vol. 60, No. 3, 1973, pp. 525-536. doi:10.1016/S0007-1536(73)80036-1
C. L. Dewar and L. Sigler, “Fungal Arthritis of the Knee Caused by Mycoleptodiscus indicus,” Clinical Rheumatology, Vol. 29, No. 9, 2010, pp. 1061-1065. doi:10.1007/s10067-010-1448-9
C. A. Metry, P. S. Hoien-Dalen, C. W. Maddox, et al., “Subcutaneous Mycoleptodiscus indicus Infection in an Immunosuppressed Dog,” Journal of Clinical Microbiology, Vol. 48, No. 8, 2010, pp. 3008-3011. doi:10.1128/JCM.02368-09
L. D. Guo, K. D. Hyde and E. C. Y. Liew, “Detection and Taxonomic Placement of Endophytic Fungi within Frond Tissues of Livistona chinensis Based on rDNA Sequences,” Molecular Phylogenetics and Evolution, Vol. 20, No. 1, 2001, pp. 1-13. doi:10.1006/mpev.2001.0942
E. F. Rakotoniriana, F. Munaut, C. Decock, et al., “Endophytic Fungi from Leaves of Centella asiatica: Occurrence and Potential Interactions within Leaves,” Antonie van Leeuwenhoek, Vol. 93, No. 1-2, 2008, pp. 27-36. doi:10.1007/s10482-007-9176-0
Y. Zhang, C. L. Schoch, J. Fournier, et al., “Multi-Locus Phylogeny of Pleosporales: A Taxonomic, Ecological and Evolutionary Re-Evaluation,” Studies in Mycology, Vol. 64, No. 1, 2009, pp. 85-102. doi:10.3114/sim.2009.64.04
O. Petrini, L. E. Petrini and K. Rodrigues, “Xylariaceaous Endophytes: An Exercise in Biodiversity,” Fitopatologia Brasileira, Vol. 20, 1995, pp. 531-539.
B. A. Summerell and J. F. Leslie, “Fifty Years of Fusarium: How Could Nine Species Have Ever Been Enough?” Fungal Diversity, Vol. 50, No. 1, 2011, pp. 135-144. doi:10.1007/s13225-011-0132-y
H. W. Zhang, Y. C. Song and R. X. Tan, “Biology and Chemistry of Endophytes,” Natural Products Reports, Vol. 27, No. 5, 2006, pp. 753-771. doi:10.1039/b609472b
F. F. Campos, S. Johann, B. B. Cota, T. M. A. Alves, L. H. Rosa, R. B. Caligiorne, P. S. Cisalpino, C. A. Rosa and C. L. Zani, “Antifungal Activity of Trichothecenes from Fusarium sp. against Clinical Isolates of Paracoccidioides brasiliensis,” Mycoses, Vol. 54, No. 4, 2011, pp. e122-e129. doi:10.1111/j.1439-0507.2009.01854.x
L. H. Rosa, M. L. A. Vieira, B. B. Cota, S. Johann, T. M. A. Alves, C. L. Zani and C. A. Rosa, “Endophytic Fungi of Tropical Forests: A Promising Source of Bioactive Prototype Molecules for the Treatment of Neglected Diseases,” In: D. Ekinci, Ed., Drug Development—A Case Study Based Insight into Modern Strategies, Intech, Croatia, 2011, pp. 1-18.