Skip to main content
Log in

Genetic diversity of endophytic fungi from Coffea arabica cv. IAPAR-59 in organic crops

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Endophytes are microorganisms that live inside plant tissues throughout its life cycle and during certain phases of development. The endophyte–host relationships can provide benefits to the host, protecting it against attack by insects and diseases. Several studies have demonstrated the diversity of endophytes from Coffea arabica, but few studies in varieties of organic crops. Thus, the objective in this study was to corroborate these reports with knowledge of the endophytic fungi communities in an organic variety of C. arabica L. cultivar IAPAR-59. We identified the endophytic fungi by molecular methods using the ITS1-5.8S-ITS2 region of rDNA and phylogenetic analyses. In the antagonist activity tests, the endophytes were tested against phytopathogens with the evaluation of the kind of interactions between them. Analyses demonstrated a diversity of genera, including: Colletotrichum, Trichoderma, Schizophyllum, Mycosphaerella, Cladosporium, and Cercospora, as well as the first record of the genus Ophiognomonia in C. arabica. The antagonist activity showed reduced growth of the phytopathogenic fungi Glomerella sp., Colletotrichum sp. and Sclerotinia sclerotiorum. The results obtained in this work, with the identification for the first time, of a highly diverse isolated endophytic of the species Ophiognomonia sp. in the coffee plants, is the second report of the detection of these fungi in Brazil. Also, the detection of different isolates with the ability to antagonise pathogens, emphasises the importance of further research, involving the isolation, identification and exploration of endophytes of other genetic varieties of coffee, obtained by breeding programs of this important crop in Brazil.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Almeida TT, Orlandelli RC, Azevedo JL, Pamphile JA (2015) 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 14(2):4920–4931

    Article  CAS  PubMed  Google Scholar 

  • Azevedo JL, Maccheroni W Jr, Pereira JO, Araújo WL (2000) Endophytic microrganisms: a review on insect control and recent advances on tropical plants. EJB Eletronic J Biotechnol 3:40–65

    Google Scholar 

  • Badalyan SM, Innocenti G, Garibyan NG (2002) Antagonistic activity of xylotrophic mushrooms against pathogenic fungi of cereals in dual culture. Phytopathol Mediterr 41:200–225

    Google Scholar 

  • Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288(7):4502–4512

  • Bernardi-Wenzel J, Garcia A, Filho CJR, Prioli AJ, Pamphile JA (2010) Evaluation of foliar fungal endophyte diversity and colonization of medicinal plant Luehea divaricata (Martius et Zuccarini). Biol Res 43:375–384

    Article  PubMed  Google Scholar 

  • Cai L, Hyde KD, Taylor PWJ, Weir BS, Waller J, Abang MM, Zhang JZ, Yang YL, Phoulivong S, Liu ZY, Prihastut H, Shivas RG, McKenzie EHC, Johnston PR (2009) A polyphasic approach for studying Colletotrichum. Fungal Divers 39:183–204

    Google Scholar 

  • Camatti-Sartori V, Silva-Ribeiro RT, Valdebenito-Sanhueza RM, Pagnocca FC, Echeverrigaray S, Azevedo LL (2005) Endophytic yeasts and filamentous fungi associated with southern Brazilian apple (Malus domestica) orchards subjected to conventional, integrated or organic cultivation. J Basic Microbiol 45:397–402

    Article  PubMed  Google Scholar 

  • Campanile G, Ruscelli A, Luisi N (2007) Antagonistic activity of endophytic fungi towards Diplodia corticola assessed by in vitro and in planta tests. Eur J Plant Pathol 117:237–246

    Article  Google Scholar 

  • Carvalho DC, Brigagão MRPL, Santos MH, Paula FBA, Giusti-Paiva A, Azevedo L (2011) Organic and conventional Coffea arabica L.: a comparative study of the chemical composition and physiological, biochemical and toxicological effects in wistar rats. Plant Foods Hum Nutr 66(2):114–21

    Article  Google Scholar 

  • Chen CA, Chang C-C, Wei NV, Chen C-H, Lein Y-T, Lin Ho-E, Dai C-F, Wallace CC (2004) Secondary structure and phylogenetic utility of the Ribosomal Internal Transcribed Spacer 2 (ITS2) in Scleractinian corals. Zool Stud 1021–5506

  • Ferreira DF (2011) Sisvar: a computer analysis system. Ciênc Agrotec 35:1039–1042

    Google Scholar 

  • Gangadevi V, Muthumary J (2008) Isolation of Colletotrichum gloeosporioides, a novel endophytic taxol-producing fungus from the leaves of a medicinal plant, Justicia gendarussa. Mycol Balc 5:1–4

    Google Scholar 

  • Garcia A, Rhoden AS, Rubin Filho CJ, Nakamura CV, Pamphile JA (2012) Diversity of foliar endophytic fungi from the medicinal plant Sapindus saponaria L. and their localization by scanning electron microscopy. Biol Res 45:149–158

    Article  Google Scholar 

  • Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agric Ecosyst Environ 113(1):17–35

  • Gottel NR, Castro HF, Kerley M, Yang Z, Pelletier DA, Podar M et al (2011) Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl Environ Microbiol 77(17):5934–5944

  • Harman GE (2000) Myths and dogmas of biocontrol: changes in perception derived from research on Trichoderma harzianum T-22. Plant Dis 84:377–393

    Article  Google Scholar 

  • Kamalakannan A, Mohan L, Harish S, Radjacommare R, Amutha G, Chiara K, Karuppiah R, Mareeswari P, Rajinimala N, Angayarkanni T (2004) Biocontrol agents induce disease resistance in Phyllanthus niruri Linn against camping-off disease caused by Rhizoctonia solani. Phytopathol Mediterr 43:187–194

    Google Scholar 

  • Kogel KH, Franken P, Huckelhoven R (2006) Endophyte or parasite-what decides? Curr Opin Plant Biol 9:358–363

    Article  PubMed  Google Scholar 

  • Koulman A, Lane GA, Christensen MJ, Fraser K, Tapper BA (2007) Peramine and other fungal alkaloids are exuded in the guttation fluid of endophyte-infected grasses. Phytochemistry 68:355–360

    Article  CAS  PubMed  Google Scholar 

  • Leite TS, Cnossen-Fassoni A, Pereira OL, Mizubuti ESG, Araújo EF, Queiroz MV (2013) Novel and highly diverse fungal endophytes in soybean revealed by the consortium of two different techniques. J Microbiol 51(1):56–69

    Article  CAS  Google Scholar 

  • Lima JS, Figueiredo JG, Gomes RG, Stringari D, Goulin EH, Adamoski D, Kava-Cordeiro V, Galli-Terasawa V, Glienke C (2012) Genetic diversity of Colletotrichum spp. an endophytic fungi in a medicinal plant, Brazilian pepper tree. ISRN Microbiol 2012:1–7

    Article  Google Scholar 

  • McGinnis S, Madden TL (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32:20–25

    Article  Google Scholar 

  • Mónaco C, Sisterna M, Perelló A, Dal Bello G (2004) Preliminary studies on biological control of the blackpoint complex of wheat in Argentina. World J Microbio Biotechnol 20(3):285–290

  • Moreno E, Varughese T, Spadafora C, Arnold AE, Coley PD, Kursar TA, Gerwick WH, Cubilla-Rios L (2011) Chemical constituents of the new endophytic fungus Mycosphaerella sp. nov. and their anti-parasitic activity. Nat Prod Commun 6(6):835–840

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira RJV, Souza RG, Lima TEF, Cavalcanti MAQ (2014) Endophytic fungal diversity in coffee leaves (Coffea Arabica) cultivated using organic and conventional crop management systems. Mycosphere 5(4):523–530

    Google Scholar 

  • Orlandelli RC, Alberto RN, Rubin Filho CJ, Pamphile JA (2012) Diversity of endophytic fungal community associated with Piper hispidum (Piperaceae) leaves. Genet Mol Res 11:1575–1585

    Article  CAS  PubMed  Google Scholar 

  • Pamphile JA, Azevedo JL (2002) Molecular characterization of endophytic strains of Fusarium verticillioides (Fusarium moniliforme) from maize (Zea mays L). World J Microb Biotechnol 18:391–96

    Article  CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Rhoden SA, Garcia A, Rubin Filho CJ, Azevedo JL, Pamphile JA (2012) Phylogenetic diversity of endophytic leaf fungus isolates from the medicinal tree Trichilia elegans (Meliaceae). Genet Mol Res 11:2513–2522

    Article  CAS  PubMed  Google Scholar 

  • Rhoden SA, Garcia A, Azevedo JL, Pamphile JA (2013) In silico analysis of diverse endophytic fungi by using ITS1-5.8S-ITS2 sequences with isolates from various plant families in Brazil. Genet Mol Res 12:935–950

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Salgado SML, Resende MLV, Campos VP (2005) Reprodução de Meloidogyne exigua em cultivares de cafeeiros resistentes e suscetíveis. Fitopatol Bras 30(4):413–415

    Article  Google Scholar 

  • Santamaría J, Bayman P (2005) Fungal epiphytes and endophytes of coffee leaves (Coffea arabica). Microb Ecol 50:1–8

    Article  PubMed  Google Scholar 

  • Schubert K, Braun U (2004) Taxonomic revision of the genus Cladosporium s. lat. 2. Cladosporium species occurring on hosts of the families Bignoniaceae and Orchidaceae. Sydowia 56:296–317

    Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  • Sera GH, Sera T, Fonseca ICB, Ito DS (2010) Resistance to leaf rust in coffee cultivars. Coffee Sci 5:59–66

  • 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

    Article  CAS  Google Scholar 

  • Shiomi HF, Melo IS, Minhoni MTA (2008) Selection of endophytic bacteria with antagonic action against plant pathogens. Sci Agrár 9:535–538

    Google Scholar 

  • Silva JL, Souza PE, Monteiro FP, Freitas MLO, Júnior S, Belan LL (2014) Antifungal activity using medicinal plant extracts against pathogens of coffee tree. Revista Brasileira de Plantas Medicinais 16(3):539–544

    Article  Google Scholar 

  • Souza AO, Pamphile JA, Rocha CLMSC, Azevedo JL (2004) Plant-microbe interactions between maize (Zea mays L.) and endophytic microorganisms observed by scanning electron microscopy. Acta Sci Biol Sci 26(3):357–359

    Google Scholar 

  • Teles HDF, Pires LL, Cunha MGD, Santos FPD, Ameloti Neto F (2013) Incidence of Sclerotinia sclerotiorum and the physical and physiological quality of soybean seeds based on processing stages. J Seed Sci 35(4):409–418

    Article  Google Scholar 

  • Tommerup IC, Briggs GG (1981) Influence of agricultural chemicals on germination of vesicular-arbuscular endophyte spores. Trans Br Mycol Soc 76(2):326–328

  • Vega FE, Posada F, Aime MC, Pava-Ripoll M, Infante F, Rehner AS (2008) Entomopathogenic fungal endophytes. Biol Control 46:72–78

    Article  Google Scholar 

  • Vega FE, Simpkins A, Aime MC, Posada F, Peterson SW, Rehner SA, Infante F, Castillo A, Arnold AE (2010) Fungal endophyte diversity in coffee plants from Colombia, Hawaii, Mexico and Puerto Rico. Fungal Ecol 3:122–138

    Article  Google Scholar 

  • Walker DW, Castlebury LA, Rossman AY, Mejía LC, White JF (2012) Phylogeny and taxonomy of Ophiognomonia (Gnomoniaceae, Diaporthales), including twenty-five new species in this highly diverse genus. Fungal Divers. doi:10.1007/s13225-012-0200-y

    Google Scholar 

  • Waller JM, Bridge PD, Black R, Hakiza G (1993) Characterization of the coffee berry disease pathogen, Colletotrichum kahawae sp. nov. Mycol Res 97(8):989–994

    Article  Google Scholar 

  • Xia Y, DeBolt S, Dreyer J, Scott D, Williams MA (2015) Characterization of culturable bacterial endophytes and their capacity to promote plant growth from plants grown using organic or conventional practices. Front Plant Sci 6:1–10

    Article  CAS  Google Scholar 

  • Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links?. Ecol 84(8):2042–2050

  • Zervakis GI, Moncalvo J-M, Vilgalys R (2004) Molecular phylogeny, biogeography and speciation of the mushroom species Pleurotus cystidiosus and allied taxa. Microbiology 150:715–726

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Complex Research Support Centres (COMCAP-UEM), Laboratory of Molecular Biology and Structural for the facilities provided in the sequencing of ITS1-5.8S-ITS2 regions, and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for granting the scholarship. Additional acknowledgments are given to CNPq (311534/2014-7; 447265/2014-8) and Fundação Araucária – FA (276/2014) for financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to João Alencar Pamphile.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bongiorno, V.A., Rhoden, S.A., Garcia, A. et al. Genetic diversity of endophytic fungi from Coffea arabica cv. IAPAR-59 in organic crops. Ann Microbiol 66, 855–865 (2016). https://doi.org/10.1007/s13213-015-1168-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-015-1168-0

Keywords

Navigation