Brazilian Plants: An Unexplored Source of Endophytes as Producers of Active Metabolites

Abstract

Brazil has an extraordinary biodiversity, and for many years, has been classified as the first of 17 countries with a mega diversity, with 22% of the total plants in the world (more than 55 000 species). Considering that some endophytes are host-specific, the incomparable plant diversity found in Brazil encompasses an immeasurable variety of habitats and may represent a repository of unexplored species. As a result of the endophyte-host interaction, plant-associated microorganisms have an enormous biosynthetic potential to produce compounds with novelties in structure and bioactivity. Numerous studies have been published over the years describing the endophytic species isolated in Brazil. Identification of these species is generally performed via DNA sequencing. However, many of the genera to which the described taxa belong were reviewed phylogenetically and many species were reclassified. Thus, there is a gap in the real biodiversity of endophytes isolated in Brazil in the last decade. In this scenario, the present study reviewed the biodiversity of endophytes isolated from plants found in different Brazilian biomes from 2012 to 2017, including the following topics: (i) species diversity, (ii) species identification challenges, (iii) biotechnological aspects, and (iv) identified metabolites. Endophytes of 54 species of plants were studied from 2012 to 2017, resulting in the identification of 300 genera, with Diaporthe and Bacillus being the most frequent fungal and bacterial genera, respectively.

Key words

Brazilian biodiversity - medicinal plants - endophytes - secondary metabolites

• References

• 1 Siddiqui AA, Iram F, Siddiqui S, Sahu K. Role of natural products in drug discovery process. Int J Drug Dev Res 2014; 6: 172-204
• 2 Chapla VM, Zeraik ML, Ximenes VF, Zanardi LM, Lopes MN, Cavalheiro AJ, Silva DHS, Young MCM, Fonseca LM, Bolzani VS, Araújo AR. Bioactive secondary metabolites from Phomopsis sp., an endophytic fungus from Senna spectabilis . Molecules 2014; 19: 6597-6608
• 3 Gouda S, Das G, Sen SK, Shin HS, Patra JK. Endophytes: a treasure house of bioactive compounds of medicinal importance. Front Microbiol 2016; 7: 1538
• 4 Deepika VB, Murali TS, Satyamoorthy K. Modulation of genetic clusters for synthesis of bioactive molecules in fungal endophytes: A review. Microbiol Res 2016; 182: 125-140
• 5 Stierle AA, Stierle DB. Bioactive secondary metabolites produced by the fungal endophytes of conifers. Nat Prod Commun 2015; 10: 1671-1682
• 6 Brader G, Compat S, Vescio K, Mitter B, Trognitz F, Ma LJ, Sessitsch A. Insights into plant-pathogenic and plant-nonpathogenic endophytes. Annu Rev Phytopathol 2017; 55: 61-83
• 7 Brazil Flora Group (BFG). Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia 2015; 66: 1085-1113
• 8 De Bary A. Morphologie und Physiologie der Pilze, Flechten und Myxomyceten. Handbuch der physiologischen Botanik. 2. Band. Leipzig: Wilhelm Engelmann; 1866: 1831-1888
• 9 Petrini O. Fungal Endophytes of Tree Leaves. In: Andrews J, Hirano S. eds. Microbial Ecology of Leaves. New York: Springer; 1991
• 10 Hardoin PR, van Overbeek LS, Berg G, Pirttila AM, Compant S, Campisano A, Doring M, Sessitsch A. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbil Mol Biol Rev 2015; 79: 293-320
• 11 Kandel SL, Joubert PM, Doty S. Bacterial endophytes colonization and distribution within plants. Microorganisms 2017; 5: E77
• 12 Venieraki A, Dimou M, Katinakis P. Endophytic fungi residing in medicinal plants have the ability to produce the same or similar pharmacologically active secondary metabolites as their hosts. Hellenic Plant Prot J 2017; 10: 51-66
• 13 Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda MDC, Glick B. Plant growth-promoting bacterial endophytes. Microbiol Res 2016; 183: 92-99
• 14 Pusztahelyi T, Holb IJ, Pócsi I. Secondary metabolites in fungus-plant interactions. Front Plant Sci 2015; 6: 573
• 15 Ghini R, Hamada E, Bettiol W. Climate change and plant diseases. Sci Agric 2008; 65: 98-107
• 16 Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J. Biodiversity hotspots for conservation priorities. Nature 2000; 403: 853-858
• 17 Martinez-Klimova E, Rodríguez-Peña K, Sánchez S. Endophytes as sources of antibiotics. Biochem Pharmacol 2017; 134: 1-17
• 18 El-Deeb B, Fayeza K, Gherbawya Y. Isolation and characterization of endophytic bacteria from Plectranthus tenuiflorus medicinal plant in Saudi Arabia desert and their antimicrobial activities. J Plant Interact 2013; 8: 56-64
• 19 Ferreira MC, Vieira MLA, Zani CL, Alves TMA, Junior PAS, Murta SMF, Romanha AJ, Gil LHVG, Carvalho AGO, Zilli JE, Vital MJS, Rosa CA, Rosa LH. Molecular phylogeny, diversity, symbiosis and discover of bioactive compounds of endophytic fungi associated with the medicinal Amazonian plant Carapa guianensis Aublet (Meliaceae). Biochm Syst Ecol 2015; 59: 36-44
• 20 Santos PJC, Savi DC, Gomes RR, Goulin EH, Senkiv CC, Tanaka FAO, Almeida AMR, Galli-Terasawa L, Kava V, Glienke C. Diaporthe endophytica and D. terebinthifolii from medicinal plants for biological control of Phyllosticta citricarpa . Microbiol Res 2016; 186: 153-160
• 21 Nicoletti R, Fiorentino A. Plant bioactive metabolites and drug produced by endophytic fungi of Spermatophyta. Agriculture 2015; 5: 918-970
• 22 Tahir HAS, Gu Q, Wu H, Niu Y, Huo R, Gao X. Bacillus volatiles adversely affect the physiology and ultra-structure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt. Sci Rep 2017; 7: 40481
• 23 Raja HA, Miller NA, Pearce CJ, Oberlies NH. Fungal identification using molecular tools: a primer for the natural products research community. J Nat Prod 2017; 80: 756-770
• 24 Selim KA, El-Beih AA, Abdel-Rahman TM, El-Diwany AI. Biology of endophytic fungi. Cur Res Env App Myc 2012; 2: 31-82
• 25 Gomes RR, Glienke C, Videira SIR, Lombard L, Groenewald JZ, Crous PW. Diaporthe: a genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 2013; 31: 1-41
• 26 Chitrampalam P, Nelson jr. B. Multilocus phylogeny reveals an association of agriculturally important Fusarium solani species complex (FSSC) 11, and clinically important FSSC 5 and FSSC 3 + 4 soybean roots in the north central United States. Antonie Van Leeuwenhoek 2016; 109: 335-347
• 27 Savi DC, Aluizio R, Galli-Terasawa L, Kava V, Glienke C. 16S-gyrB-rpoB multilocus sequence analysis for species identification in the genus Microbispora . Antonie Van Leeuwenhoek 2016; 109: 801-815
• 28 Guo Y, Zheng W, Rong X, Huang Y. A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: use of multilocus sequence analysis for streptomycete systematics. Int J Syst Evol Microbiol 2008; 58: 149-159
• 29 Pereira CB, Oliveira DM, Hughes AFS, Kohlhoff M, Vieira MLA, Vaz ABM, Ferreira MC, Carvalho CR, Rosa LH, Rosa CA, Alves TMA, Zani CL, Johann S, Cota BB. Endophytic fungal compounds active against Cryptococcus neoformans and C. gattii . J Antiob 2015; 1: 1-9
• 30 Crous PW. Mycosphaerella spp. and their anamorphs associated with leaf spot diseases of Eucalyptus. Mycol Memoir 1998; 21: 1-170
• 31 Crous PW, Hong L, Wingfield BD, Wingfield MJ. ITS rDNA phylogeny of selected Mycosphaerella species and their anamorphs occurring on Myrtaceae . Mycol Res 2001; 105: 425-431
• 32 Vieira MLA, Hughes AFS, Gil VB, Vaz ABM, Alves TMA, Zani CL, Rosa CA, Rosa LH. Diversity and antimicrobial activities of the fungal endophyte community associated with the traditional Brazilian medicinal plant Solanum cernuum Vell. (Solanaceae). Can J Microbiol 2012; 58: 54-66
• 33 Conti R, Chagas FO, Caraballo-Rodriguez AM, Melo WGP, Nascimento AM, Cavalcanti BC, Moraes MO, Pessoa C, Costa-Lotufo LV, Krogh R, Adricopulo AD, Lopes NP, Pupo MT. Endophytic actinobacteria from the Brazilian medicinal plant Lychnophora ericoides Mart. and the biological potential of their secondary metabolites. Chem Biodiversity 2016; 13: 727-736
• 34 Wellington EM, Stackebrandt E, Sanders D, Wolstrup J, Jorgenses NO. Taxonomic status of Kitasatospora, and proposed unification with Streptomyces on the basis of phenotypic and 16S rRNA analysis and emendation of Streptomyces . Int J Syst Bacteriol 1992; 42: 156-160
• 35 Chagas FO, Caraballo-Rodrígues AM, Dorrestein PC, Pupo MT. Expanding the chemical repertoire of the endophyte Streptomyces albospinus RLe7 reveals amphotericin B as an inducer of a fungal phenotype. J Nat Prod 2017; 80: 1302-1309
• 36 Silva IP, Brissow E, Kellner Filho LC, Senabio J, da Siqueira KA, Vandresen Filho S, Damasceno JL, Mendes AS, Tavares DC, Magalhães LG, Junior PA, Januário AH, Soares MA. Bioactive compounds of Aspergillus terreus-F7, an endophytic fungus from Hyptis suaveolens (L.) Poit. World J Microbiol Biotechnol 2017; 33: 62-67
• 37 Polonio JC, Ribeiro MAS, Rhoden AS, Sarragiotto MH, Azevedo JL, Pamphile JA. 3-Nitropropionic acid production by the endophytic Diaporthe citri: molecular taxonomy, chemical characterization, and quantification under pH variation. Fungal Biol 2016; 120: 1600-1608
• 38 Orlandelli RC, Almeida TT, Alberto RN, Polonio JC, Azevedo JL, Pamphile JA. Antifungal and proteolytic activities of endophytic fungi isolated from Piper hispium Sw. Braz J Microbiol 2015; 46: 359-366
• 39 Souza A, Cruz JC, Sousa NR, Procópio ARL, Silva GF. Endophytic bacteria from banana cultivars and their antifungal activity. Genet Mol Res 2014; 13: 8661-8670
• 40 Falcão LL, Silva-Werneck JO, Vilarinho BR, Silva JP, Pomella AWV, Marcellino LH. Antimicrobial and plant growth-promoting properties of the cacao endophyte Bacillus subtilis ALB629. App Microbiol 2014; 116: 1584-1592
• 41 Guarnaccia V, Groenewald JZ, Li H, Glienke C, Carstens E, Hattingh V, Fourie PH, Crous PW. First report of Phyllosticta citricarpa and description of two new species, P. paracapitalensis and P. paracitricarpa, from citrus in Europe. Stud Mycol 2017; 87: 161-185
• 42 Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CHW, Perrone G, Seifert KA, Susca A, Tanney JB, Varga J, Kocsub S, Szigeti G, Yaguchi T, Frisvad JC. Phylogeny, identification and nomenclature of the genus Aspergillus . Stud Mycol 2014; 78: 141-173
• 43 Bhandari V, Ahmod NZ, Shah HN, Gupta RS. Molecular signatures for Bacillus species: demarcation of the Bacillus subtilis and Bacillus cereus clades in molecular terms and proposal to limit the placement of new species into the genus Bacillus . Int J Syst Evol Microbiol 2013; 63: 2712-2726
• 44 Labeda DP, Doroghazi JR, Ju KS, Metcaf WW. Taxonomic evaluation of Streptomyces albus and related species using multilocus sequence analysis and proposals to emend the description of Streptomyces albus and describe Streptomyces pathocidini sp. nov. Int J Syst Evol Microbiol 2014; 64: 894-900
• 45 Zhan XY, Zhu QY. Molecular typing of Legionella pneumophila isolates from environmental water samples and clinical samples using a five-gene sequence typing and standard sequence-based typing. PLoS One 2018; 13: e0190986
• 46 Xie T, Song S, Li S, Ouyang L, Xia L, Huang J. Review of natural products databases. Cell Prolif 2015; 48: 398-404
• 47 Hong J. Natural product diversity and its role in chemical biology and drug discovery. Curr Opin Chem Biol 2011; 15: 350-354
• 48 Tonial F, Maia BHLNS, Gomes-Figueiredo JA, Sobottka AM, Bertol CD, Nepel A, Savi DC, Vicente VA, Gomes RR, Glienke C. Influence of culturing conditions on bioprospecting and the antimicrobial potential of endophytic fungi from Schinus terebinthifolius . Curr Microbiol 2015; 72: 173-183
• 49 Bulla LMC, Polonio JC, Portela-Castro ALB, Kava V, Azevedo JL, Pamphile JA. Activity of the endophytic fungi Phlebia sp. and Paecilomyces formosus in decolourisation and the reduction of reactive dyesʼ cytotoxicity in fish erythrocytes. Environ Monit Assess 2017; 88: 1-10
• 50 Silva KJ, Armas RD, Soares CR, Ogliari JB. Communities of endophytic microorganisms in different developmental stages from a local variety as well as transgenic and conventional isogenic hybrids of maize. World J Microbiol Biotechnol 2016; 32: 189
• 51 Santos TT, Leite TS, Queiroz CB, Araujo EF, Pereira OL, Queiroz MV. High genetic variability in endophytic fungi from the genus Diaporthe isolated from common bean (Phaseolus vulgaris L.) in Brazil. J App Microbiol 2016; 120: 388-401
• 52 dos Santos SG, da Silva PRA, Garcia AC, Zilli JE, Berbara RLL. Dark septate endophyte decreases stress on rice plants. Braz J Microbiol 2017; 48: 333-341
• 53 Silva MCS, Polonio JC, Quecine MC, Almeida TT, Bogas AC, Pamphile JA, Pereira JO, Astolfi-Filho S, Azevedo JL. Endophytic cultivable bacterial community obtained from the Paullinia cupana seed in Amazonas and Bahia regions and its antagonistic effects against Colletotrichum gloeosporioides . Microb Pathog 2016; 98: 16-22
• 54 Gos FMR, Savi DC, Shaaban KA, Thorson JS, Aluizio R, Possiede YM, Rohr J, Glienke C. Antibacterial activity of endophytic actinomycetes isolated from the medicinal plant Vochysia divergens (Pantanal, Brazil). Front Microbiol 2017; 8: 1642
• 55 Casella TM, Eparvier V, Mandavid H, Bendelac A, Odonne G, Dayan L, Duplais C, Espndola LS, Stien D. Antimicrobial and cytotoxic secondary metabolites from tropical leaf endophytes. Phytochem 2013; 96: 370-377
• 56 Andrioli WJ, Conti R, Araújo MJ, Zanasi R, Cavalcanti BC, Manfrim V, Toledo JS, Tedesco D, Moraes MO, Pessoa C, Cruz AK, Bertucci C, Sabino J, Nanayakkara DNP, Pupo MT, Bastos JK. Mycoleptones A–C and polyketides from the endophyte Mycoleptodiscus indicus . J Nat Prod 2013; 77: 70-78
• 57 Mandavid H, Rodrigues AMS, Espindola LS, Eparvier V, Stien D. Secondary metabolites isolated from the Amazonian endophytic fungus Diaporthe sp. SNB-GSS10. J Nat Prod 2015; 78: 1735-1739
• 58 Orlandelli RC, da Silva MLC, Vasconcelos AFD, Almeida IV, Vicentini VEP, Prieto A, Hernandez MDD, Azevedo JL, Pamphile JA. β-(1-3,1-6)-D-glucans produced by Diaporthe sp. endophytes: purification, chemical characterization and antiproliferative activity against MCF-7 and HepG2-C3A cells. Int J Biol Macromol 2017; 94: 431-437
• 59 Flores AC, Pamphile JA, Sarragiotto MH, Clemente E. Production of 3-nitropropionic acid by endophytic fungus Phomopsis longicolla isolated from Trichilia elegans A. JUSS ssp. elegans and evaluation of biological activity. World J Microbiol Biotechnol 2013; 29: 923-932
• 60 Sebastianes FLS, Cabedo N, El Aouad N, Valente AM, Lacava PT, Azevedo JL, Pizzirani-Kleiner AA, Cortes D. 3-Hydroxypropionic acid as an antibacterial agent from endophytic fungi Diaporthe phaseolorum . Curr Microbiol 2012; 65: 622-632
• 61 Koolen HHF, Soares ER, Silva FMA, Souza AQL, Medeiros LS, Filho ER, Almeida RA, Ribeiro IA, Pessoa CO, Morais MO, Costa PM, Souza ADL. An antimicrobial diketopiperazine alkaloid and co-metabolites from an endophytic strain of Gliocladium isolated from Strychnos cf. toxifera . Nat Prod Res 2012; 26: 2013-2019
• 62 Netz N, Opatz T. Marine indole alkaloids. Mar Drug 2015; 13: 4814-4914
• 63 Andrioli WJ, Silva TM, Silva VB, Damásio ARL, Maller A, Conti R, Jorge JA, Araújo JM, Silva CHTP, Pupo MT, Polizeli MLTM, Bastos JK. The fungal metabolite eugenitin as additive for Aspergillus niveus glucoamylase activation. J Mol Cat 2012; 74: 156-161
• 64 Tanimura A, Kikukawa M, Yamaguchi S, Kishino S, Ogawa J, Shima J. Direct ethanol production from starch using a natural isolate, Scheffersomyces shehatae: toward consolidated bioprocessing. Sci Rep 2015; 5: 9593
• 65 Gallo MBC, Falso MJS, Balem F, Menezes D, Rocha N, Balachandran R, Sturgeon TS, Pupo MT, Day BW. The anti-promyelocytic leukemia mode of action of two endophytic secondary metabolites unveiled by a proteomic approach. Planta Med 2014; 80: 473-481
• 66 Pacheco SJB, Araujo-Melo MH, Valete-Rosalino CM, Pimentel MIF, Conceição-Silva F, Schubach AO, Marzochi MCA. Endemic tegumentary Leishmaniasis in Brazil: correlation between level of endemicity and number of cases of mucosal disease. Ann J Trop Med Hyg 2012; 84: 901-905
• 67 Pinto EG, Santos IO, Schmidt TJ, Borborema SET, Ferreira VF, Rocha DR, Tempone AG. Potential of 2-hydroxy-3-phenylsulfanylmethyl-[1,4]-naphthoquinones against Leishmania (L.) infantum: biological activity and structure-activity relationships. PLoS One 2014; 9: e105127
• 68 do Nascimento AM, Soares MG, da Silva Torchelsen FK, de Araujo JA, Lage PS, Duarte MC, Andrade PH, Ribeiro TG, Coelho EA, do Nascimento AM. Antileishmanial activity of compounds produced by endophytic fungi derived from medicinal plant Vernonia polyanthes and their potential as source of bioactive substances. World J Microbiol Biotechnol 2015; 31: 1793-1800
• 69 Davies J, Ryan KS. Introducing the parvome: bioactive compounds in the microbial world. Chem Biol 2012; 7: 252-259
• 70 Osmanova N, Schultze W, Ayoub N. Azaphilones: a class of fungal metabolites with diverse biological activities. Phytochem Rev 2010; 9: 315-342
• 71 Oliveira SF, Bocayuva MF, Veloso TGR, Bazzolli DMS, Cynthia CS, Pereira OL, Kasuya MCM. Endophytic and mycorrhizal fungi associated with roots of endangered native orchids from the Atlantic Forest, Brazil. Mycorrhiza 2013; 24: 55-64
• 72 Almeida Trapp M, De Souza GD, Rodrigues-Filho E, Boland W, Mithofer A. Validated method for phytohormone quantification in plants. Front Plant Sci 2014; 5: 417
• 73 Eposito-Polesi NP, de Abreu-Tarazi MF, de Almeida CV, Tsai SM, de Almeida M. Investigation of endophytitic bacterial community in supposedly axenic cultures of pineapple and orchids with evidence on abundant intracellular bacteria. Curr Microbiol 2016; 74: 103-113
• 74 Corrado M, Rodrigues KF. Antimicrobial evaluation of fungal extracts produced by endophytic strains of Phomopsis sp. J Basic Microbiol 2004; 44: 157-160
• 75 Castro RA, Quecine MC, Lacava PT, Batista BD, Luvizotto DM, Marcn J, Ferreira A, Melo IS, Azevedo JL. Isolation and enzyme bioprospection of endophytic bacteria associated with plants of Brazilian mangrove ecosystem. Springerplus 2014; 3: 382
• 76 Vieira MLA, Johann S, Hughes FM, Rosa CA, Rosa LH. The diversity and antimicrobial activity of endophytic fungi associated with medicinal plant Baccharis trimera (Asteraceae) from the Brazilian savannah. Can J Microbiol 2014; 60: 847-856
• 77 Bezerra JDP, Santos MGS, Svedese VM, Lima DMM, Fernandes MJS, Paiva LM, Souza-Motta CM. Richness of endophytic fungi isolated from Opuntia fícus-indica Mill (Cactaceae) and preliminary screening for enzyme production. World J Microbiol Biotechnol 2012; 28: 1989-1995
• 78 Feitosa AO, Dias ACS, Ramos G, Bithencourt HR, Siqueira JES. Lethality of cytochalasin B and other compounds isolated from fungus Aspergillus sp. (Trichocomoceae) endophyte of Bauhinia guianensis (Fabaceae). Rev Argent Microbiol 2016; 48: 259-263
• 79 Azevedo JL, Araujo WL, Lacava PT. The diversity of citrus endophytic bacteria and their interactions with Xylella fastidiosa and host plants. Gen Mol Biol 2016; 39: 476-491
• 80 Oliveira MNV, Santos TMA, Vale HMM, Delvaux JC, Cordero AP, Ferreira AB, Migues PSB, Totola MR, Costa MD, Moraes CA, Borges AC. Endophytic microbial diversity in coffee cherries of Coffea arabica from southeastern Brazil. Can J Microbiol 2013; 59: 221-230
• 81 Almeida TT, Orlandelli RC, Azevedo JL, Pamphile JA. Molecular characterization of the endophytic fungal community associated with Eichhornia azurea (Kunth) and Eichhornia crassipes (Mart.) (Pontederiaceae) native to the upper Paraná river floodplain, Brazil. Genet Mol Res 2015; 14: 4920-4931
• 82 Sposito-Polesi NP, Andrade PAM, Almeida CV, Andreote FD, Almeida M. Endophytic bacterial communities associated with two explant sources of Eucalyptus benthamii Maiden & Cambage. World J Microbiol Biotechnol 2015; 31: 1737-1746
• 83 Miguel PSB, Oliveira MNV, Delvaux JC, Jesus GL, Borges AC, Tótola MR, Neves JCL, Costa MD. Diversity and distribution of the endophytic bacterial community at different stages of Eucalyptus growth. Antonie van Leeuwenhock 2016; 109: 755-771
• 84 Pereira GVM, Magalhães KT, Lorenzetii ER, Souza TP, Schwan RF. A multiphasic approach for the identification of endophytic bacterial in strawberry fruit and their potential for plant growth promotion. Microb Ecol 2012; 63: 405-417
• 85 Fernandes EG, Pereira OL, Silva CC, Bento CBP, Queiroz MV. Diversity of endophytic fungi in Glycine max . Microbiol Res 2015; 181: 84-92
• 86 de Lacerda JRM, Silva TF, Vollú RE, Marques JM, Seldin L. Generally recognized as safe (GRAS) Lactococcus lactis strains associated with Lippia sidoides Cham. are able to solubilize/mineralize phosphate. Springerplus 2016; 5: 828
• 87 Bernrdi-Wenzel J, García A, Filho CJ, Prioli AJ, Pamphile JA. Evaluation of foliar fungal endophyte diversity and colonization of medicinal plant Luehea divaricate (Martius et Zuccarini). Biol Res 2010; 43: 375-384
• 88 Banhos EF, Souza AQL, Andrade JC, Souza ADL, Koolen HHF, Albuquerque PM. Endophytic fungi from Myrcia guianensis at the Brazilian Amazon: distribution and bioactivity. Braz J Microbiol 2014; 45: 153-161
• 89 Lopes RBM, Costa LEO, Vanetti MCD, Araújo EF, Queiroz MV. Endophytic bacteria isolated from common bean (Phaseolus vulgaris) exhibiting high variability showed antimicrobial activity and quorum sensing inhibition. Curr Microbiol 2015; 71: 509-516
• 90 Oliveira ACD, Fernandes ML, Mariano AB. Production and characterization of an extracellular lipase from Candida guilliermondii . Braz J Microbiol 2014; 45: 1503-1511
• 91 dos Santos CM, de Souza DG, Balsanelli E, Cruz LM, de Souza EM, Baldani JI, Schwab S. A culture-independent approach to enrich endophytic bacterial cells from sugarcane stems for community characterization. Microb Ecol 2017; 74: 453-465
• 92 Rosa LH, Tabanca N, Techen N, Pan Z, Wedge DE, Moraes RM. Antifungal activity of extracts from endophytic fungi associated with Smallanthus maintained in vitro as autotrophic cultures and as pot plants in the greenhouse. Can J Microbiol 2012; 58: 1202-1211
• 93 Rhoden AS, Garcia A, Santos e Silva MC, Azevedo JL, Pamphile JA. Phylogenetic analysis of endophytic bacterial isolates from leaves of the medicinal plant Trichilia elegans A. Juss. (Meliaceae). Genet Mol Res 2015; 14: 1515-1525
• 94 Lopes MR, Ferreira MC, Carvalho TFC, Pagnocca FC, Chagas RA, Morais PB, Rosa LH, Lachance MA, Rosa CA. Yamadazyma riverae sp. nov., a yeast species isolated from plant materials. Int J Syst Evol Microbiol 2015; 65: 4469-4473
• 95 Leite J, Fischer D, Rouws LFM, Fernandes-Júnior PI, Hofmann A, Kublik S, Schloter M, Xavier GR, Radl V. Cowpea nodules harbor non-rhizobial bacterial communities that are shaped by soil type rather than plant genotype. Front Plant Sci 2017; 7: 2064
• 96 Brum MCP, Araújo WL, Maki CS, Azevedo JL. Endophytic fungi from Vitis labrusca L. (‘Niagara Rosada’) and its potential for the biological control of Fusarium oxysporum . Genet Mol Res 2012; 11: 4187-4197
• 97 Savi DC, Shaaban KA, Vargas N, Ponomareva LV, Possiede YM, Thorson JS, Glienke C, Rohr J. Microbispora sp. LGMB259 endophytic actinomycete isolated from Vochysia divergens (Pantanal, Brazil) producing B-carbolines and indoles with biological activity. Curr Microbiol 2015; 70: 345-354