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Fungal Endophyte Communities in Begonia Species from the Brazilian Atlantic Rainforest

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Abstract

Tropical plants represent hotspots of endophytic fungal species diversity. Based on culture-dependent methods, we evaluated the endophytic fungal communities in leaves of three plant species found in the Brazilian Atlantic Rainforest: Begonia fischeri, Begonia olsoniae, and Begonia venosa. These species are found in two distant sites: a continental region and an insular area. A total of 426 fungal endophytes in 19 genera were isolated in pure culture including Colletotrichum (51.6% of isolates) and Diaporthe (22.5%) as the most abundant, followed by Phyllosticta (3.5%), Neopestalotiopsis (1.8%), Stagonospora (1.8%), and Nigrospora (1.6%) among the genera found in minor abundance. The diversity and composition of fungal taxa differed across plant hosts. Richness and diversity of fungi were higher in B. fischeri in comparison to B. olsoniae and B. venosa. Discriminatory analysis revealed that fungal communities are structured according to hosts, which means that each plant species had its distinct endophytic communities, but dominated by common fungal taxa. This is the first study to report fungal endophytes in begonia leaves and characterize their communities.

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References

  1. Araújo WL, Lacava PT, Marcon J, Lima AOS, Sobral JK, Azevedo JL, Pizzirani-Kleiner AA (2010) Guia prático: isolamento e caracterização de microrganismos endofíticos. CALO, Piracicaba

    Google Scholar 

  2. Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274

    Article  Google Scholar 

  3. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549

    Article  PubMed  Google Scholar 

  4. Botella L, Diez JJ (2011) Phylogenic diversity of fungal endophytes in Spanish stands of Pinus halepensis. Fungal Divers 47:9–18

    Article  Google Scholar 

  5. Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum—current status and future directions. Stud Mycol 73:181–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  7. Clarke KR, Gorley RN (2001) PRIMER v.5: user manual/tutorial Primer-E, Plymouth

  8. Colwell RK (2013) Estimates: statistical estimation of species richness and shared species from samples. Version 9. User’s Guide and application published at http://purl.oclc.org/estimates

  9. Davis EC, Shaw AJ (2008) Biogeographic and phylogenetic patterns in diversity of liverwort-associated endophytes. Am J Bot 95:914–924

    Article  PubMed  Google Scholar 

  10. Dewitte A, Leus L, Eeckhaut T, Vanstechelman I, Van Huylenbroeck J, Van Bockstaele E (2009) Genome size variation in Begonia. Genome 52:829–838

    Article  CAS  PubMed  Google Scholar 

  11. Dewitte A, Twyford AD, Thomas DC, Kidner CA, Van Huylenbroeck J (2011) The origin of diversity in Begonia: genome dynamism, population processes and phylogenetic patterns. In: Grillo O, Venora G (eds) The dynamical processes of biodiversity: case studies of evolution and spatial distribution. Rijeka, InTech, Croatia, pp 27–52

    Google Scholar 

  12. Dodd SL, Lieckfeldt E, Samuels GJ (2003) Hypocrea atroviridis sp. nov., the teleomorph of Trichoderma atroviride. Mycologia 95:27–40

    Article  PubMed  Google Scholar 

  13. Druzhinina I, Kopchinskiy AG, Komon M, Bissett J, Szakacs G, Kubicek CP (2005) An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genet Biol 42:813–828

    Article  CAS  Google Scholar 

  14. Ellis MB (1971) Dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew, Surrey

    Google Scholar 

  15. Ellis MB (1976) More dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew, Surrey

    Google Scholar 

  16. Fávaro LCL, Melo FL, Aguilar-Vildoso CI, Araújo WL (2011) Polyphasic analysis of intraspecific diversity in Epicoccum nigrum warrants reclassification into separate species. PLoS ONE 6:e14828

    Article  Google Scholar 

  17. Ferreira MC, Vieira MLA, Zani CL, Alves TMA, Sales-Junior PA, Murta SMF, Romanha AJ, Gil LHVG, Carvalho AGO, Zilli JE, Vital MJS, Rosa CA, Rosa LH (2015) Molecular phylogeny, diversity, symbiosis and discover of bioactive compounds of endophytic fungi associated with the medicinal Amazonian plant Carapa guianensis Aublet (Meliaceae). Biochem Syst Ecol 59:36–44

    Article  CAS  Google Scholar 

  18. Goodall-Copestake WP, Pérez-Espona S, Harris DJ, Hollingsworth PM (2010) The early evolution of the mega-diverse genus Begonia (Begoniaceae) inferred from organelle DNA phylogenies. Biol J Linn Soc 101:243–250

    Article  Google Scholar 

  19. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  20. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  21. 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

    Article  Google Scholar 

  22. Higginbotham SJ, Arnold AE, Ibañez A, Spadafora C, Coley PD, Kursar TA (2013) Bioactivity of fungal endophytes as a function of endophyte taxonomy and the taxonomy and distribution of their host plants. PLoS ONE 8:e73192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hughes M, Hollingsworth PM (2008) Population genetic divergence corresponds with species-level biodiversity patterns in the large genus Begonia. Mol Ecol 17:2643–2651

    Article  CAS  PubMed  Google Scholar 

  24. Inderbitzin P, Mehta YR, Berbee ML (2009) Pleospora species with Stemphylium anamorphs: a four locus phylogeny resolves new lineages yet does not distinguish among species in the Pleospora herbarum clade. Mycologia 101:329–339

    Article  CAS  PubMed  Google Scholar 

  25. Jacques EL, Mamede MCH (2005) Notas nomenclaturais em Begonia L. (Begoniaceae). Rev Bras Bot 28:579–588

    Article  Google Scholar 

  26. Jacques EL (2015) Begoniaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. http://reflora.jbrj.gov.br/jabot/floradobrasil/FB5616. Accessed 04 March 2017

  27. Katoh K, Standley DM (2013) Mafft multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  29. Kumaresan V, Suryanarayanan TS (2002) Endophyte assemblages in young, mature and senescent leaves of Rhizophora apiculata: evidence for the role of endophytes in mangrove litter degradation. Fungal Divers 9:81–91

    Google Scholar 

  30. Lau KM, Arnold AE, Johnson NC (2013) Factors influencing communities of foliar fungal endophytes in riparian woody plants. Fungal Ecol 6:365–378

    Article  Google Scholar 

  31. Magurran AE (2004) Measuring biological diversity. Blackwell Science, Oxford

    Google Scholar 

  32. Montoya QV, Meirelles LA, Chaverri P, Rodrigues A (2016) Unraveling Trichoderma species in the attine ant environment: description of three new taxa. Antonie Van Leeuwenhoek 109:633–651

    Article  PubMed  Google Scholar 

  33. Moonlight PW, Richardson JE, Tebbitt MC, Thomas DC, Hollands R, Peng CI, Hughes M (2015) Continental-scale diversification patterns in a megadiverse genus: the biogeography of Neotropical Begonia. J Biogeogr 42:1137–1149

    Article  Google Scholar 

  34. Mousa WK, Raizada MN (2013) The diversity of anti-microbial secondary metabolites produced by fungal endophytes: an interdisciplinary perspective. Front Microbiol 4:65

    Article  Google Scholar 

  35. Nalini MS, Sunayana N, Prakash HS (2014) Endophytic fungal diversity in medicinal plants of western ghats, India. Inter J Biodiver 2014:ID494213

    Article  Google Scholar 

  36. Pandikumar P, Babu NP, Ignacimuthu S (2009) Hypoglycemic and antihyperglycemic effect of Begonia malabarica Lam. in normal and streptozotocin induced diabetic rats. J Ethnopharmacol 124:111–115

    Article  CAS  Google Scholar 

  37. Peršoh D (2013) Factors shaping community structure of endophytic fungi–evidence from the Pinus-Viscum-system. Fungal Divers 60:55–69

    Article  Google Scholar 

  38. Peršoh D (2015) Plant-associated fungal communities in the light of meta’omics. Fungal Divers 75:1–25

    Article  Google Scholar 

  39. Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer-Verlag, New York, pp 179–197

    Chapter  Google Scholar 

  40. Podani J, Miklós I (2002) Resemblance coefficients and the horseshoe effect in principal coordinates analysis. Ecol 83:3331–3343

    Article  Google Scholar 

  41. Ramesh N, Viswanathan MB, Saraswathy A, Balakrishna K, Brindha P, Lakshmanaperumalsamy P (2002) Phytochemical and antimicrobial studies of Begonia malabarica. J Ethnopharmacol 79:129–132

    Article  CAS  PubMed  Google Scholar 

  42. Sanchez-Azofeifa A, Oki Y, Fernandes GW, Ball RA, Gamon J (2012) Relationships between endophyte diversity and leaf optical properties. Trees 26:291–299

    Article  Google Scholar 

  43. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 109:6241–6246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Sebastianes FLS, Romão-Dumaresq AS, Lacava PT, Harakava R, Azevedo JL, Melo IS, Pizzirani-Kleiner AA (2013) Species diversity of culturable endophytic fungi from Brazilian mangrove forests. Curr Genet 59:153–166

    Article  CAS  Google Scholar 

  46. Smith SA, Tank DC, Boulanger LA, Bascom-Slack CA, Eisenman K et al (2008) Bioactive endophytes warrant intensified exploration and conservation. PLoS ONE 3:e3052

    Article  PubMed  PubMed Central  Google Scholar 

  47. Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502

    Article  CAS  Google Scholar 

  48. Suryanarayanan TS, Venkatesan G, Murali TS (2003) Endophytic fungal communities in leaves of tropical forest trees: diversity and distribution patterns. Curr Sci 85:489–493

    Google Scholar 

  49. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2735–2729

    Article  Google Scholar 

  50. Udayanga D, Liu X, Crous PW, McKenzie EHC, Chukeatirote E, Hyde KD (2012) A multi-locus phylogenetic evaluation of Diaporthe (Phomopsis). Fungal Divers 56:157–171

    Article  Google Scholar 

  51. U’Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 99:898–914

    Article  PubMed  Google Scholar 

  52. Vaz ABM, Fontenla S, Rocha FS, Brandão LR, Vieira MLA, Garcia V, Goes-neto A, Rosa CA (2014) Fungal endophyte β-diversity associated with Myrtaceae species in an Andean Patagonian forest (Argentina) and an Atlantic forest (Brazil). Fungal Ecol 8:28–36

    Article  Google Scholar 

  53. Vieira WAS, Michereff SJ, Morais MA, Hyde KD, Câmara MPS (2014) Endophytic species of Colletotrichum associated with mango in northeastern Brazil. Fungal Divers 67:181–202

    Article  Google Scholar 

  54. Vincent JB, Weiblen GD, May G (2016) Host associations and beta diversity of fungal endophyte communities in New Guinea rainforest trees. Mol Ecol 25:825–841

    Article  CAS  PubMed  Google Scholar 

  55. Walther G, Pawłowska J, Alastruey-Izquierdo A, Wrzosek M, Rodriguez-Tudela JL, Dolatabadi S, Chakrabarti A, Hoog GS (2013) DNA barcoding in Mucorales: an inventory of biodiversity. Persoonia 30:11–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Wanderley MGL, Shepherd GJ, Melhem TSA, Giulietti AM, Martins SE, Romanini RP, Pirani JR, Kirizawa M, Melo MMRF., Cordeiro I, Kinoshita LS (2012) Flora fanerogâmica do estado de São Paulo. Instituto de Botânica, São Paulo

    Google Scholar 

  57. Wang B, Yu Y, Wang L (2014) Penicillium fusisporum and P. zhuangii, two new monoverticillate species with apical-swelling stipes of section Aspergilloides isolated from plant leaves in China. PLoS ONE 9:e101454

    Google Scholar 

  58. Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S (2015) Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol 99:2955–2965

    Article  CAS  PubMed  Google Scholar 

  59. Wilson D (1995) Endophyte: the evolution of a term and clarification of its use and definition. Oikos 73:274–276

    Article  Google Scholar 

  60. Zhang T, Xiang HB, Zhang YQ, Liu HY, Wei YZ, Zhao LX, Yu LY (2013) Molecular analysis of fungal diversity associated with three bryophyte species in the Fildes Region, King George Island, maritime Antarctica. Extremophiles 17:757–765

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank “Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)” for providing financial support (Grants # 2013/50228-8 and 2014/15760-3) and also for a scholarship to the first author (process # 2014/12021-5). We thank Sergio Birello Sartori for helping during fieldwork, Sergio Kakazu for helping with DNA sequencing, and Dr. Tassio B. de Oliveira for helpful comments on this manuscript. We also thank Prof. Dr. Ludovic Jean Charles Kollmann for the identification of Begonia species. We would like to thank ICMBio for the collecting permits issued to AR (# 37256-3) and to SPL (# 21774-1).

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Authors and Affiliations

  1. Department of Biochemistry and Microbiology, Institute of Biosciences, São Paulo State University (UNESP), Av. 24-A, n 1515, Bela Vista, 13506-900, Rio Claro, Brazil

    Ana M. L. Correia & Andre Rodrigues

  2. Department of Exact Sciences, Luiz de Queiroz College of Agriculture, Piracicaba, Brazil

    Simone P. Lira

  3. Department of Botany, Institute of Biosciences, São Paulo State University (UNESP), Rio Claro, Brazil

    Marco A. Assis

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  1. Ana M. L. Correia
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  2. Simone P. Lira
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Correspondence to Andre Rodrigues.

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Correia, A.M.L., Lira, S.P., Assis, M.A. et al. Fungal Endophyte Communities in Begonia Species from the Brazilian Atlantic Rainforest. Curr Microbiol 75, 441–449 (2018). https://doi.org/10.1007/s00284-017-1400-1

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