Abstract
The diversity and biological activities of the endophytic fungi associated with the Brazilian medicinal plant Stryphnodendron adstringens were studied. A total of 320 fungal isolates were obtained, and 66 phylotypes comprising 25 genera were identified. The fungal community of S. adstringens displayed high richness, diversity and low dominance indices. The most abundant phylotypes were closely related to Diaporthe phaseolorum, Guignardia camelliae, and Preussia pseudominima. Sixteen fungal extracts displayed biological activities when screened against bacteria, fungi, cancer cell lines, and amastigote forms of Leishmania amazonensis. The extract of phylotype Nigrospora cf. oryzae exhibited a selective antifungal activity and inhibited the growth of Candida albicans and Cladosporium sphaerospermum. The extracts of Diaporthe cf. phaseolorum and Xylaria sp. phylotypes displayed anticancer activities. Our results indicate that the endophytes associate with this medicinal plant may be a source for novel drugs.
Similar content being viewed by others
References
Agusta A, Ohashi K, Shibuya H (2006) Bisanthraquinone metabolites produced by the endophytic fungus Diaporthe sp. Chem Pharm Bull 54:579–582
Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Anazetti MC, Melo PS, Duran N, Haun M (2003) Comparative cytotoxicity of dimethylamide-crotonin in the promyelocytic leukemia cell line (HL-60) and human peripheral blood mononuclear cells. Toxicology 188:261–274
Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66
Bettucci L, Alonso R, Tiscornia S (1999) Endophytic mycobiota of healthy twigs and the assemblage of species associated with twig lesions of Eucalyptus globulus and E. grandis in Uruguay. Mycol Res 103:468–472
Butler MS, Buss AD (2006) Natural products—the future scaffolds for novel antibiotics? Biochem Pharmacol 71:919–929
Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717–2727
da Silva JMC, Bates JM (2002) Biogeographic patterns and conservation in the South American Cerrado: a tropical Savanna hotspot. Bioscience 52:225–233
de Hoog GS, Guarro J, Gené J, Figueras MA (2000) Atlas of Clinical Fungi, 2nd edn. Centraalbureau voor Schimmelcultures, Utrecht/Universitat Rovira i Virgili, Reus
Eriksson OE, Vue JZ (1998) Bambusicolous pyrenomycetes, an annotated check-list. Myconet I:25–78
Espinel-Ingroff A, Kerkering TM (1991) Spectrophotometric method of inoculum preparation for the in vitro susceptibility testing of filamentous fungi. J Clin Microbiol 29:393–394
Gabler IG, Barbosa AC, Vilela RR, Lyon S, Rosa CA (2008) Incidence and anatomic localization of oral candidiasis in patients with AIDS hospitalized in a public hospital in Belo Horizonte, MG, Brasil. J Appl Oral Sci 16:247–250
Gallo MBC, Chagas FO, Almeida MO, Macedo CC, Cavalcanti BC, Barros FWA, Moraes MO, Costa-Lotufo LV, Pessoa C, Bastos JK, Pupo MT (2009) Endophytic fungi found in association with Smallanthus sonchifolius (Asteraceae) as resourceful producers of cytotoxic bioactive natural products. J Bas Microbiol 49:142–151
Gazis R, Rehner S, Chaverri P (2011) Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences. Mol Ecol 20:3001–3013
Guo LD, Hyde KD, Liew ECY (2000) Identification of endophytic fungi from Livistona chinensis based on morphology and rDNA sequences. New Phytol 147:617–630
Herzog-Soares JDA, Alves R, Isac E, Bezerra JC, Gomes MH, Santos SC, Ferri PH (2002) Atividade tripanocida in vivo de Stryphnodendron adstringens (barbatimão verdadeiro) e Caryocar brasiliensis (pequi). Rev Bras Farmacol 12:1–2
Hoffman M, Arnold AE (2008) Geographic locality and host identity shape fungal endophyte communities in cupressaceous trees. Mycol Res 112:331–44
Huang WY, Cai YZ, Hyde KD, Corke H, Sun M (2008) Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Div 33:61–75
Ishida K, Mello JCP, Cortez DAG, Filho BPD, Ueda-Nakamura T, Nakamura CV (2006) Influence of tannins from Stryphnodendron adstringens on growth and virulence factors of Candida albicans. J Antimicrob Chem 58:942–949
Johnson JH, Meyers E, O’Sullivan J, Phillipson DW, Robinson G, Trejo WH, Wells JS (1989) Culpin, a novel hydroquinone antibiotic of fungal origin. J Antibiot 42:1515–1517
Kim JC, Choi GJ, Park JH, Kim HT, Cho KY (2001) Activity against plant pathogenic fungi of phomalactone isolated from Nigrospora sphaerica. J Pest Sci 57:554–559
Ko TWK, Stephenson SL, Bahkali AH, Hyde KD (2011) From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Div 50:113–120
Larran S, Mónaco C, Alippi HE (2001) Endophytic fungi in leaves of Lycopersicon esculentum Mill. World J Microbiol Biotechnol 17:181–84
Lin X, Lu C, Huang Y, Zheng Z, Su W, Shen Y (2007) Endophytic fungi from a pharmaceutical plant, Camptotheca acuminate: isolation, identification and bioactivity. World J Microbiol Biotechnol 23:1037–1040
Liu X, Dong M, Chen X, Jiang M, Lv X, Guijun Yan G (2007) Antioxidant activity and phenolics of an endophytic Xylaria sp. from Ginkgo biloba. Food Chem 105:548–554
Liu K, Ding X, Deng B, Chen W (2009) Isolation and characterization of endophytic taxol-producting fungi Taxus chinensis. J Ind Microbiol 36:1171–1177
Lodge DJ, Fisher PJ, Sutton BC (1996) Endophytic fungi of Manilkara bidentata leaves in Puerto Rico. Mycologia 88:733–738
Lorenzi H, Matos FJA (2002a) Plantas medicinais no Brasil: nativas e exóticas. Instituto Plantarum, Brasil, Nova Odessa
Lorenzi H, Matos FJA (2002b) Plantas Medicinais no Brasil: nativas e exóticas cultivadas. Instituto Plantarum, Nova Odessa
Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton
Monks A, Scudiero D, Skehan P, Shoemaker R, Paull K, Vistica D, Hose C, Langley J, Cronise P, Vaigro-Wolff A, Gray-Goodrich M, Campbell H, Mayo J, Boyd M (1991) Feasibility of a high- flux anticancer drug screen using a diverse panel of cultured human tumor cell lines. J Nat Cancer Inst 83:757–766
Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Naik BS, Shashikala J, Krishnamurthy YL (2008) Diversity of fungal endophytes in shrubby medicinal plants of Malnad region, Western Ghats, Southern India. Fungal Ecol 1:89–93
National Committee for Clinical Laboratory Standards (2003) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. NCCLS, 940 Pennsylvania, USA
Norrby SR, Nord CE, Finch R (2005) Lack of development of new antimicrobial drugs: a potential serious threat to public health. Lancet Infect Dis 5:115–119
Osono T, To-Anun C, Hagiwara Y, Hirose D (2011) Decomposition of wood, petiole and leaf litter by Xylaria species from northern Thailand. Fungal Ecol 4:210–218
Perello A, Simon MR, Arambarri AM (2002) Interactions between foliar pathogens and the saprophytic microflora of the wheat (Triticum aestivum L.) phylloplane. J Phytopathol 150:232–243
Petrini O (1991) Fungal endophyte of tree leaves. In: Andrews J, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 179–197
Phongpaichit S, Rungjindamai N, Rukachaisirikul V, Sakayaroj J (2008) Antimicrobial activity in cultures of endophytic fungi isolated from Garcinia species. FEMS Immunol Med Microbiol 48:367–372
Rodrigues KF (1994) The foliar fungal endophytes of the Amazonian palm Euterpe oleracea. Mycologia 86:376–385
Rodrigues KF, Sieber TN, Grünig CR, Holdenrieder O (2004) Characterization of Guignardia mangiferae isolated from tropical plants based on morphology, ISSR-PCR amplifications and ITS1-5.8S-ITS2 sequences. Mycol Res 108:45–52
Rodríguez-Tudela JL, Barchiesi F, Bille J, Chryssanthou E, Cenca-Estrella M, Denning D, Donnelly JP, Dupont B, Fegeler W, Moore C, Richardson M, Verweij PE (2003) Method for determination of minimal inhibitory concentration (MIC) by broth dilution of fermentative yeasts. Eucast Discussion Document 7.1. Clinical Microbiology and Infectious 9:1–8
Rosa LH, Vaz ABM, Caligiorne RLB, Campolina SA, Rosa CA (2009) Endophytic fungi associated with the Antarctic grass Deschampsia antarctica Desv. (Poaceae). Polar Biol 32:161–167
Rosa LH, Gonçalves VN, Caligiorne RB, Alves TMA, Rabello A, Sales PA, Romanha AJ, Sobral MEG, Rosa CA, Zani CL (2010a) Leishmanicidal, trypanocidal, and cytotoxic activities of endophytic fungi associated with bioactive plants in Brazil. Braz J Microbiol 41:114–122
Rosa LH, Vieira MLA, Santiago IF, Rosa CA (2010b) Endophytic fungi community associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica. FEMS Microbiol Ecol 73:178–189
Ryan GS, Harper DAT, Whalley JS (1995) PALSTAT, Statistics for palaeontologist. Champman & Hall, London
Sakalidis ML, Hardy GESJ, Burgess TI (2001) Endophytes as potential pathogens of the baobab species Adansonia gregorii: a focus on the Botryosphaeriaceae. Fungal Ecol 4:1–14
Santiago IF, Alves TMA, Rabello A, Sales-Júnior PA, Romanha AJ, Zani CL, Rosa CA, Rosa LH (2012) Leishmanicidal and antitumoral activities of endophytic fungi associated with the Antartic angiosperms Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth) Bartl. Extremophiles 16:95–103
Santos JM, Correia VG, Phillips AJL (2010) Primers for mating-type diagnosis in Diaporthe and Phomopsis: their use in teleomorph induction in vitro and biological species definition. Fungal Biol 14:255–270
Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686
Silva GH, Oliveira CM, Teles HL, Pauletti PM, Castro-Gamboa IC, Silva DHS, Bolzani VS, Young MCM, Costa-Neto CM, Pfenning LH, Berlinck RGS, Araujo AR (2010) Sesquiterpenes from Xylaria sp., an endophytic fungus associated with Piper aduncum (Piperaceae). Phytochemistry Lett 3:164–167
Siqueira VM, Conti R, Araújo JM, Souza-Motta CM (2011) Endophytic fungi from the medicinal plant Lippia sidoides Cham. and their antimicrobial activity. Symbiosis 53:89–95
Slippers B, Wingfield MJ (2007) Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and impact. Fungal Biol Rev 21:90–106
Soca-chafre G, Rivera-Orduna 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 Biol 111:143–156
Stierle A, Strobel G, Stierle D, Grothaus P, Bignami G (1995) The search for a taxol-producing microorganism among the endophytic fungi of the pacific yew, Taxus brevifolia. J Nat Prod 58:1315–1324
Teixeira MC, Jesus SR, Sampaio RB, Pontes CL, Santos WL (2002) A simple and reproducible method to obtain large numbers of axenic amastigotes of different Leishmania species. Parasitol Res 88:963–968
van der Aa HA (1973) Studies in Phyllosticta. Studies in Mycol 5:1–110
Van Niekerk JM, Groenewald JZ, Farr DF, Fourie PH, Halleer F, Crous PW (2005) Reassessment of Phomopsis species on grapevines. Australasian Plant Pathol 34:27–39
Vieira MLA, Hughes AFS, Gil VB, Vaz ABM, Alves TMA, Zani CL, Rosa CA, Rosa LH (2012) Diversity and antimicrobial activities of the fungal endophyte community associated with the traditional Brazilian medicinal plant Solanum cernuum Vell. (Solanaceae). Can J Microbiol 58:1–13
Vaz ABM, Mota MC, Bomfim MRQ, Vieira MLA, Zani CL, Rosa CA, Rosa LH (2009) Antimicrobial activity of endophytic fungi associated with Orchidaceae in Brazil. Can J Microbiol 55:1381–1391
Wang J, Li G, Lu H, Zheng Z, Huang Y, Su W (2000) Taxol from Tubercularia sp. strain TF5, an endophytic fungus of Taxus mairei. FEMS Microbiol Lett 193:249–253
Wedge DE, Kuhajek JM (1998) A microbioassay for fungicide discovery. SAAS Bull Biochem Biotechnol 11:1–7
White IR, Backhouse D (2007) Comparison of fungal endophyte communities in the invasive panicoid Grass Hyparrhenia hirta and the native grass Bothriochloa macra. Australian J Bot 55:178–185
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, San Diego, pp 315–322
Wilson D (2000) Ecology of woody plant endophytes. In: Bacon CW, White JF Jr (eds) Microbial endophytes. Marcel Dekker Inc, New York, pp 389–420
Yu BZ, Zhang GH, Du ZZ, Zheng YT, Xu JC, Luo XD (2008) Phomoeuphorbins A-D, azaphilones from the fungus Phomopsis euphorbiae. Phytochemistry 69:2523–2526
Acknowledgements
This work received support from the Fundação of Amparo the Pesquisa of Minas Gerais (FAPEMIG), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). The authors would also like to thank Dr. L. H. Pfenning for suggestions and Daniela N.B. Maia, Luciana F. Soares, and Fernanda L.M. Francisco for performing the biological assays.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Carvalho, C.R., Gonçalves, V.N., Pereira, C.B. et al. The diversity, antimicrobial and anticancer activity of endophytic fungi associated with the medicinal plant Stryphnodendron adstringens (Mart.) Coville (Fabaceae) from the Brazilian savannah. Symbiosis 57, 95–107 (2012). https://doi.org/10.1007/s13199-012-0182-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-012-0182-2