Abstract
Endophytic fungi were isolated from healthy tissues of Lippia sidoides Cham. (Verbenaceae), a medicinal plant used as an antiseptic in the northeast of Brazil. From 480 fragments of leaves (240) and stems (240), a total of 203 endophytic fungi were isolated, representing 14 species belonging to the groups Ascomycota, Coelomycetes and Hyphomycetes. Endophytic colonization was greater in leaves (50.4%) than in stems (35.4%). Colletotrichum gloeosporiodes had the maximum colonization frequency (12.3%), followed by Alternaria alternata (7.08%), Guignardia bidwelli (6.87%) and Phomopsis archeri (5.41%). Some species showed specificity for the host tissue: Curvularia pallescens, Dreschlera dematioidea, G. bidwellii, Microascus desmosporum, Peacilomyces variotti, Periconia byssoides and Ulocladium oudemansii were only isolated from leaves while Fusarium lateritium and Phoma tracheiphila were only isolated from stems. Through a preliminary screening and fermentation assay, 16 isolates where found to produce antimicrobial metabolites against bacterial and fungi. The diversity and role of endophytes in medicinal plants is briefly discussed. In conclusion, endophytic fungi from L. sidoides have pharmaceutical potential and can be seen as an attractive source of biologically active compounds.
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Araújo WL, Maccheroni W Jr, Aguilar-Vildoso CI, Barroso PAV, Saridakis HO, Azevedo JL (2001) Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can J Microbiol 47:229–236
Araújo WL, Marcon J, Maccheroni W Jr, van Elsas JD, van Vuurde JWL, Azevedo JL (2002a) Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl Environ Microbiol 68(10):4906–4914
Araújo WL, Lima SOA, Azevedo JL, Marcon J, Sobral JK, Lavaca PT (2002b) Manual: isolamento de microrganismos endofíticos. CALQ, Piracicaba
Azevedo JL (1999) Botânica: uma ciência básica ou aplicada? Rev bras Bot 22(02):225–229
Azevedo JL, Maccheroni W Jr, Pereira JO, Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. EJB Eletron J Biotecnol 3(1):40–65
Azevedo JL, Serafine LA, Barros NM (2002) Microrganismos endofíticos e seu papel em plantas tropicais. In: Serafine LA, Barros e NM, Azevedo JL (eds) Biotecnologia: avanços na agricultura e na industria. Universidade de Caxias do Sul, Caxias do Sul, pp 233–265, Cap. 08
Bandara WMMS, Seneviratne G, Kulasooriya SA (2006) Interactions among endophytic bacteria and fungi: effects and potentials. J Biosci 31(5):645–650
Barnett HL, Hunter BB (1987) Illustrated genera of imperfect fungi, 4th edn. APS Press. The American Phytopathological Society, St. PaulMinessota, USA
Bauer AM, Kirby WMM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 43:493–496
Bertini LM, Pereira AF, Oliveira CLL, Menezes EA, Morais SM, Cunha FA (2005) Cavalcanti ESB Perfil de sensibilidade de bactérias frente a óleos essenciais de algumas plantas no Nordeste do Brasil. Informa, San Salvador 17(3/4):21–27
Bills GF, Pollishook JD (1992) Recovery of endophytic fungi from Chamaecyparis thyoides. Sydowia 44:1–12
Booth C (1971) The genus Fusarium. Commonwealth Mycological Institute, Kew
Botelho MA, Nogueira NAP, Bastos GM, Fonseca SGC, Lemos TLG, Matos FJA, Montenegro D, Heukelbach J, Rao VS, Brito GAC (2007) Antimicrobial activity of the essential oil from Lippia sidoides, carvacrol and thymol against oral pathogens. Braz J Med Biol Res 40:349–356
Bunkers GF, Kenfield D, Strobel GA (1991) Production of pestasol by Drechslera gigantia in liquid culture. Mycol Res 95:347–351
Button CB (1980) The Coelomycetes Fungi Imperfect with pycnidia, acervuli and stromata. Commonwealth, Survey
Carvalho AFU, Melo VMM, Craveiro AA, Machado MIL, Bantim MB, Rabelo EF (2003) Larvicidal activity of the essential oil from Lippia sidoides Cham. against Aedes aegypti Linn. Mem Inst Oswaldo Cruz, Rio de Janeiro 98(4):569–571
Cavalcanti SCH, Niculau ES, Blank AF, Câmara CAG, Araújo IN, Alves PB (2010) Composition and acaricidal activity of Lippia sidoides essential oil against two-spotted spider mite (Tetranychus urticae Koch). Bioresour Technol 101:829–832
Chareprasert S, Piapukiew J, Thienhirun S, Whalley AJS, Sihanonth P (2006) Endophytic fungi of teak leaves Tectona grandis L. and rain tree leaves Samanea saman Merr. World J Microbiol Biotechnol 22:481–486
Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:99–127
Collado J, Gonzalez A, Platas G, Stchigel AM, Guarro J, Pelaez F (2002) Monosporascus ibericus sp. nov., an endophytic ascomycete from plants on saline soils, with observations on the position of the genus based on sequence analysis of the 18S rDNA. Mycol Res 106:118–127
Costa SMO, Lemos TLG, Pessia DL, Assunção JCC, Braz-Filho R (2002) Constituintes químicos de Lippia sidoides (CHAM) Verbenaceae. Rev Bras Farmacogn 12:66–67
Ellis MB (1971) Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew
Ellis MB (1976) More Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew
Fisher PJ, Anson AE, Petrini O (1986) Fungal endophytes in Ulex europaeus and U. galli. Trans Br Mycol Soc 86:153–156
Fisher PJ, Petrini O (1990) A comparative study of fungal endophytes in xylem and bark of Alnus sp. in England and Switzerland. Mycol Res 94:313–319
Fisher PJ, Petrini O, Petrini LE, Sutton BC (1994) Fungal endophytes from the leaves and twigs of Quercus ilex L from England, Majorca and Switzerland. New Phytol 127:133–137
Fontenelle ROS, Morais SM, Brito EHS, Kerntopf MR, Brilhante RSN, Cordeiro RA, Tomé AR, Queiroz MGR, Nascimento NRF, Sidrim JJC, Rocha MFG (2007) Chemical composition, toxicological aspects and antifungal activity of essential oil from Lippia sidoides Cham. J Antimicrob Chemother 59:934–940
Ganley RJ, Newcombe G (2006) Fungal endophytes in seeds and needles of Pinus monticola. Mycol Res 110:318–327
Gunatilaka AAL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity and applications of their occurrence. J Nat Prod 69:509–526
Hanlin RT (2000) Illustrated genera of Ascomycetes, vol II. APS Press. The American Phytopathological Society, Minessota
Hata K, Atari R, Sone K (2002) Isolation of endophytic fungi from leaves of Pasania edulis and their within-leaf distributions. Mycoscience 43:369–373
Ichikawa T, Date M, Ishikura T, Ozaki A (1971) Improvement of Kasugamycin—producing strain by the agar piece method and the prototroph method. Folia Microbiol 16:218–224
Kim S, Shin D, Lee T, Oh K (2004) Periconicins, two new fusicoccane diterpenes produced by an endophytic fungus Periconia sp. with antibacterial activity. J Nat Prod 67:448–450
Kogel K-H, Franken P, Hückelhoven R (2006) Endophyte or parasite—what decides? Curr Opin Plant Biol 9(4):358–363
Kowalski T, Kehr RD (1995) Two new species of Phialocephala occurring on Picea and Alnus. Can J Bot 73:26–32
Krohn K, Flörke U, John M, Root N, Steingrover K, Aust H-J, Draeger S, Schulz B, Antus S, Simonyi M, Zsila F (2001) Biologically active metabolites from fungi Part 16. New preussomerins J, K and L from an endophytic fungus: structure elucidation, crystal structure analysis and determination of absolute configuration by CD calculations. Tetrahedron 57:4343–4348
Lacoste E, Chaumont JP, Mandin D, Plumel MM, Matos FJ (1996) Antiseptic properties of essential oil of Lippia sidoides Cham. Application to the cutaneous microflora. Ann Pharm Fr 54:228–230
Larran S, Mónaco C, Alippi HE (2001) Endophytic fungi in leaves of Lycopersicon esculentum Mill. World J Microbiol Biotechnol 17:181–184
Larran S, Perelló A, Simón MR, Moreno V (2002) Isolation and analysis of endophytic microorganisms in wheat (Triticum aestivum L.) leaves. World J Microbiol Biotechnol 18:683–686
Lemos TLG, Matos FJA, Alencar JW, Craveiro AA, Clark AM, McChesney JD (1990) Antimicrobial activity of essential oils of brazilian plants. Phytother Res 4(2):82–84
Li JY, Sidhu RS, Ford E, Hess WM, Strobel GA (1998) The induction of taxol production in the edophytic fungus Periconia sp. From Torreya grandifolia. J Ind Microbiol Biotech 20:259–264
Lin X, Lu C, Huang Y, Zheng Z, Su W, Shen Y (2007) Endophytic fungi from a pharmaceutical plant, Camptotheca acuminata: isolation, identification and bioactivity. World J Microbiol Biotechnol 23:1037–1040
Mason EW, Ellis MB (1953) British species of Periconia. Mycol Pap 56(25):1–127
Matos FJA, Oliveira F (1998) Lippia sidoides Cham.: farmacognosia, química e farmacologia. Rev Bras Farmacogn 79:84–87
Morton FJ, Smith G (1963) The genera Scopulariopsis Bainier, Microascus Zukal and Doratomyces Corda. Mycol Pap 8(20):1–94
Osono T (2007) Endophytic and epiphytic phyllosphere fungi of red-osier dogwood (Cornus stolonifera) in British Columbia. Mycoscience 48:47–52
Owen NL, Hundley N (2004) Endophytes—the chemical synthesizers inside plants. Sci Prog 87:79–99
Pascual ME (2001) Lippia: traditional uses, chemistry and pharmacology: a review. J Ethnopharmacol 76(3):201–214
Petrini O, Fisher PJ (1986) Fungal endophytes in Salicornia perennis. Trans Br Mycol Soc 87:647–651
Petrini O (1991) Fungal endophyte of tree leaves. In: Andrews J, Hirano SS (eds) Microbial ecology of leaves. Springer Verlag, New York, pp 179–197
Petrini O, Sieber TN, Toti L, Viret O (1992) Ecology, metabolite production and substrate utilization in endophytic fungi. Nat Toxins 1:185–196
Phongpaichit S, Rungjindamai N, Rukachaisirikul V, Sakayaroj J (2006) Antimicrobial activity in cultures of endophytic fungi isolated from Garcinia species. FEMS Immunol Med Microbiol 48(3):367–372
Rodrigues KF (1994) The foliar fungal endophytes of the Amazonian palm Euterpeoleracea. Mycologia 86:376–385
Roll HF, Roll HH (1979) Ascocoryne species in living stems of Picea spp. Eur J For Pathol 5:275–280
Rudgers JA, Holah J, Orr SP, Clay K (2007) Forest succession suppressed by an introduced plant-fungal symbiosis. Ecology 88:18–25
Saikkonen K, Helander M, Faeth SH (2004) Fungal endophytes: hitchhikers of the green world. In: Gillings M, Holmes A (eds) Plant microbiology. BIOS Scietific Publishers, Oxford, pp 77–95
Santamaría J, Bayman P (2005) Fungal epiphytes and endophytes of coffee leaves (Coffea Arabica). Microb Ecol 50:1–8
Sette LD, Passarini MRZ, Delarmelina C, Salati F, Duarte MCT (2006) Molecular characterization and antimicrobial activity of endophytic fungi from coffee plants. World J Microbiol Biotechnol 22:1185–1195
Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109(06):661–686
Schulz B, Boyle C, Draeger S, Aust HJ, Römmert AK, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106(9):996–1004
Siqueira VM, Souza-Motta C, Braun U (2008) Corynespora subcylindrica sp. nov., a new hyphomycete species from Brazil and a discussion on the taxonomy of corynespora-like genera. Sydowia 60(1):113–122
Souza AQL, Souza ADL, Astolfi-Filho S, Pinheiro MLB, Sarquis MIM, Pereira JO (2004) Antimicrobial activity of endophytic fungi isolated from amazonian toxic plants: Palicourea longiflora (aubl.) rich and Strychnos cogens bentham. Acta Amaz 34:185–195
Stierle A, Strobel GA, Stierle D (1993) Taxol and taxen production by Taxomyces andreanae an endophytic fungus of pacific yew. Science 260:214–216
Stone JK, Polishook JD, White JF Jr (2004) Endophytic fungus. In: Mueller JM, Bills GF, Foster MS (eds) Biodiversity of fungi; inventory and monitoring methods. Elsevier Academic Press, San Diego, pp 241–270
Strobel GA (2002) Rainforest endophytes and bioactive products. Crit Rev Biotechnol 22:315–333
Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502
Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268
Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites, The Royal Society of Chemistry. Nat Prod Rep 18:448–459
Verma VC, Gond SK, Kumar A, Kharwar RN, Strobel G (2007) The Endophytic Mycoflora of Bark, Leaf, and Stem Tissues of Azadirachta indica A. Juss (Neem) from Varanasi (India). Microb Ecol 54:119–125
Weber RWS, Stenger E, Meffert A, Hahn M (2004) Brefeldin A production by Phoma medicaginis in dead precolonized plant tissue: a strategy for habitat conquest? Mycol Res 108:662–671
Wilson BJ, Addy HD, Tsuneda A, Hambleton S, Currah RS (2004) Phialocephala sphaeroides sp. nov., a new species among the dark septate endophytes from a boreal wetland in Canada. Can J Bot 82:607–617
Wiyakrutta S, Sriubolmas N, Panphut W, Thongon N, Danwisetkanjana K, Ruangrungsi N, Meevootisom V (2004) Endophytic fungi with anti-microbial, anti-cancer and anti-malarial activities isolated from Thai medicinal plants. World J Microbiol Biotechnol 20:265–272
Xing X, Guo S, Fu J (2010) Biodiversity and distribution of endophytic fungi associated with Panax quinquefolium L. cultivated in a forest reserve. Symbioses 51:161–166
Zhao K, Ping W, Li Q, Hao S, Zhao L, Gao T, Zhou D (2009) Aspergillus niger var. taxi, a new species variant of taxol-producing fungus isolated from Taxus cuspidate in China. J Appl Microbiol 107:1202–1207
Zhou LH, Sun QS, Qiao LC, Liu J (2000) Preliminary studies on the chemical constituents in the active section of the leaves of Quercus variabilis Blume. J Shenyang Pharm Univ 17:179–181
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de Siqueira, V.M., Conti, R., de Araújo, J.M. et al. Endophytic fungi from the medicinal plant Lippia sidoides Cham. and their antimicrobial activity. Symbiosis 53, 89–95 (2011). https://doi.org/10.1007/s13199-011-0113-7
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DOI: https://doi.org/10.1007/s13199-011-0113-7