Abstract
The genus Hevea is native to the Brazilian Amazon forest, and H. brasiliensis, popularly known as the rubber tree, is the main source of raw material for the production of natural rubber in the world. To characterize the fungal communities that inhabit the tissues of this species, a total of 550 endophytic fungi were isolated, of which 212 were from native trees located in the state of Acre and 338 in the state of Amazonas. These fungi were grouped into 115 OTUs. The phylum Ascomycota was dominant (93%) and the most abundant isolates belonged to the families Glomerallaceae (genus Colletotrichum), Diaporthaceae (genus Diaporthe), Nectriaceae (genus Fusarium), Hypocreaceae (genus Trichoderma), and Trichocomaceae (genus Penicillium). The diversity and richness of fungi in the state of Acre did not differ significantly between leaves, stems, and roots; however, in the state of Amazonas, the diversity was greater in the stems and roots than in the leaves. In general, the diversity of endophytic fungi was greater in the state of Acre. Comparisons between communities of fungi showed more differences between those that inhabit different tissues than in different states. Furthermore, the fungal communities of roots and stems were similar, and both these were dissimilar from leaves. Isolates identified in this study will be tested for their potential to produce metabolites of interest for industry and for the sustainable development of agribusiness.
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References
Angelini P, Rubini A, Gigante D et al (2012) The endophytic fungal communities associated with the leaves and roots of the common reed (Phragmites australis) in Lake Trasimeno (Perugia, Italy) in declining and healthy stands. Fungal Ecol 5:683–693. https://doi.org/10.1016/j.funeco.2012.03.001
Araújo KS, Brito VN, Veloso TGR et al (2018) Diversity of culturable endophytic fungi of Hevea guianensis: a latex producer native tree from the Brazilian Amazon. Afr J Microbiol Res 12(42):953–964. https://doi.org/10.5897/AJMR2018.8980
Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66. https://doi.org/10.1016/j.fbr.2007.05.003
Asnicar F, Weingart G, Tickle TL et al (2015) Compact graphical representation of phylogenetic data and metadata with GraPhlAn. PeerJ 3:e1029 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4476132/
Babu AG, Kim SW, Yadav DR, Hyum U, Adhikari M, Lee YS (2015) Penicillium menonorum: a novel fungus to promote growth and nutrient management in cucumber plants. Mycobiology 43(1):49–56
Castellani A (1939) Viability of some pathogenic fungi in distilled water. J Trop Med Hyg 24:270–276
Chao A, Gotelli NJ, Hsieh TC et al (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67. https://doi.org/10.1890/13-0133.1
Chaverri P, Gazis RO, Samuels GJ (2011) Trichoderma amazonicum, a new endophytic species on Hevea brasiliensis and Hevea guianensis from the Amazon basin. Mycologia 103:139–151 10.3852/10–078
Coleman-Derr D, Desgarennes D, Fonseca-Garcia C et al (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209:798–811. https://doi.org/10.1111/nph.13697
Contina JB, Dandurand LM, Knudsen GR (2017) Use of GFP-tagged Trichoderma harzianum as a tool to study the biological control of the potato cyst nematode Globodera pallida. Appl Soil Ecol 115:31–37. https://doi.org/10.1016/j.apsoil.2017.03.010
Core Team R (2020) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/
Evans H, Holmes K, Thomas S (2003) Endophytes and mycoparasites associated with an indigenous forest tree, Theobroma gileri, in Ecuador and a preliminary assessment of their potential as biocontrol agents of cocoa diseases. Mycol Prog 2:149–160. https://doi.org/10.1007/s11557-006-0053-4
Ferreira MC, Vieira MLA, Zani CL et al (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. https://doi.org/10.1016/j.bse.2014.12.017
Ferreira MC, Cantrell CL, Wedge DE et al (2017) Diversity of the endophytic fungi associated with the ancient and narrowly endemic neotropical plant Vellozia gigantea from the endangered Brazilian rupestrian grasslands. Biochem. Syst Ecol 71:163–169. https://doi.org/10.1016/j.bse.2017.02.006
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Gasparotto L, Figueredo AS, Rezende JCP, Alves FF (2012) Doenças da seringueira no Brasil. Embrapa, 2nd ed. Brasília, DF
Gazis RO (2012) Evaluating the endophytic fungal community in planted and wild rubber trees (Hevea brasiliensis). University of Maryland, ProQuest Dissertation
Gazis R, Chaverri P (2010) Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol 3:240–254. https://doi.org/10.1016/j.funeco.2009.12.001
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. https://doi.org/10.1111/j.1365-294X.2011.05110.x
Gazis R, Miadlikowska J, Lutzoni F, Arnold AE, Chaverri P (2012) Culture-based study of endophytes associated with rubber trees in Peru reveals a new class of Pezizomycotina: Xylonomycetes. Mol Phylogenet Evol 65:294–304. https://doi.org/10.1016/j.ympev.2012.06.019
Guijarro B, Larena I, Melgarejo P, De Cal A (2017) Adaptive conditions and safety of the application of Penicillium frequentans as a biocontrol agent on stone fruit. Int J Food Microbiol 254:25–35. https://doi.org/10.1016/j.ijfoodmicro.2017.05.004
Hanada RE, Pomella AWV, Costa HS et al (2010) Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuaçu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biol 114:901–910. https://doi.org/10.1016/j.funbio.2010.08.006
Hora Júnior BT, Macedo DM, Barreto RW et al (2014) Erasing the past: a new identity for the damoclean pathogen causing South American leaf blight of rubber. PLoS One 9:104750. https://doi.org/10.1371/journal.pone.0104750
Hsieh C, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7:1451–1456. https://doi.org/10.1111/2041-210X.12613
Johnson M, Zaretskaya I, Raytselis Y et al (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5–W9. https://doi.org/10.1093/nar/gkn201
Leite TS, Cnossen-Fassoni A, Pereira OL et al (2013) Novel and highly diverse fungal endophytes in soybean revealed by the consortium of two different techniques. J Microbiol 51:56–69. https://doi.org/10.1007/s12275-013-2356-x
Li Q, Guo R, Li Y, Hartman WH, Li S, Zhang Z, Wang H (2019) Insight into the bacterial endophytic communities of peach cultivars related to crown gall disease resistance. Appl Environ Microbiol 85(9):e02931–e02918
Lopez DC, Zhu-Salzman K, Ek-Ramos MJ, Ulissa Sword GA (2014) The entomopathogenic fungal endophytes Purpureocillium lilacinum (formerly Paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions. PLoS One 9:e103891. https://doi.org/10.1371/journal.pone.0103891
Martin R, Gazis R, Skaltsas D, Chaverri P, Hibbett D (2015) Unexpected diversity of basidiomycetous endophytes in sapwood and leaves of Hevea. Mycologia 107:284–297. https://doi.org/10.3852/14-206
Martins F, Pereira JA, Bota P, Bento A, Baptista P (2016) Fungal endophyte communities in above- and belowground olive tree organs and the effect of season and geographic location on their structures. Fungal Ecol 20:193–201. https://doi.org/10.1016/j.funeco.2016.01.005
Mbarga JB, Begoude BAD, Ambang Z et al (2014) A new oil-based formulation of Trichoderma asperellum for the biological control of cacao black pod disease caused by Phytophthora megakarya. Biol Control 77:15–22. https://doi.org/10.1016/j.biocontrol.2014.06.004
Molinier M, Guyot J L, Oliveira E, Guimarães V (1995) Les régimes hydrologiques de l’Amazone et de ses affluents. In: L’hydrologie tropicale: géoscience et outil pour le développement. Paris: IAHS. 238p.
Murali M, Amruthesh KN (2015) Plant growth-promoting fungus Penicillium oxalicum enhances plant growth and induces resistance in pearl millet against downy mildew disease. J Phytopathol 163:743–754. https://doi.org/10.1111/jph.12371
Naraghi L, Heydari A, Rezaee S, Razavi M, Jahanifar H (2010) Study on antagonistic effects of Talaromyces flavus on Verticillium albo-atrum, the causal agent of potato wilt disease. Crop Prot 29:658–662. https://doi.org/10.1016/j.cropro.2010.01.011
Nilsson RH, Ryberg M, Abarenkov K, Sjökvist E, Kristiansson E (2009) The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. FEMS Microbiol Lett 296:97–101. https://doi.org/10.1111/j.1574-6968.2009.01618.x
Nilsson RH, Larsson K-H, Taylor AFS et al (2018) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47(D1):D259–D264. https://doi.org/10.1093/nar/gky1022
Oksanen J (2015) Multivariate analysis of ecological communities in R: vegan tutorial. R Doc 43. https://doi.org/10.1016/0169-5347(88)90124-3
Park Y-H, Kim Y, Mishra RC, Bae H (2017) Fungal endophytes inhabiting mountain-cultivated ginseng (Panax ginseng Meyer): diversity and biocontrol activity against ginseng pathogens. Sci Rep 7:16221. https://doi.org/10.1038/s41598-017-16181-z
Petrini O (1991) Fungal Endophytes of Tree Leaves. Microb Ecol Leaves, pp:179–197
Pinho DB, Firmino AL, Ferreira-junior WG, Pereira OL (2012) An efficient protocol for DNA extraction from Meliolales and the description of Meliola centellae sp. nov. Mycotaxon 122:333–345. https://doi.org/10.5248/122.333
Rocha ACS, Garcia D, Uetanabaro APT et al (2011) Foliar endophytic fungi from Hevea brasiliensis and their antagonism on Microcyclus ulei. Fungal Diversity 47:75–84. https://doi.org/10.1007/s13225-010-0044-2
Rojas-Jimenez K, Hernandez M, Blanco J et al (2016) Richness of cultivable endophytic fungi along an altitudinal gradient in wet forests of Costa Rica. Fungal Ecol 20:124–131. https://doi.org/10.1016/j.funeco.2015.12.006
Russell JR, Huang J, Anand P et al (2011) Biodegradation of polyester polyurethane by endophytic fungi. Appl Environ Microbiol 77:6076–6084. https://doi.org/10.1128/AEM.00521-11
Saikkonen K, Faeth SH, Helander M, Sullivan TJ (2011) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343. https://doi.org/10.1146/annurev.ecolsys.29.1.319
Salati E, Marques J, Molion LCB (1978) Origem e distribuição das chuvas na Amazônia. Interciência 3:200–206
Saunders M, Glenn AE, Kohn LM (2010) Exploring the evolutionary ecology of fungal endophytes in agricultural systems: using functional traits to reveal mechanisms in community processes. Evol Appl 3:525–537. https://doi.org/10.1111/j.1752-4571.2010.00141.x
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
Segaran G, Sathiavelu M (2019) Fungal endophytes: a potent biocontrol agent and a bioactive metabolites reservoir. Biocatalysis and Agricultural Biotechnology 101:284
Suryanarayanan TS, Vijaykrishna D (2001) Fungal endophytes of aerial roots of Ficus benghalensis. Fungal Diversity 8:155–161. https://link.springer.com/article/10.1631/jzus.B0860005
Taylor WJ (2011) One fungus = one name: DNA and fungal nomenclature twenty years after PCR. IMA Fungus 2(2):113–120. https://doi.org/10.5598/imafungus.2011.02.02.01
Tiwari CK, Parihar J, Verma RK (2011) Potential of Aspergillus niger and Trichoderma viride as biocontrol agents of wood decay fungi. J Indian Acad Wood Sci 8:169–172. https://doi.org/10.1007/s13196-012-0027-x
Wearn JA, Sutton BC, Morley NJ, Gange AC (2012) Species and organ specificity of fungal endophytes in herbaceous grassland plants. J Ecol 100:1085–1092. https://doi.org/10.1111/j.1365-2745.2012.01997.x
White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA Genes for Phylogenetics. In: PCR Protocols: A Guide to Methods and Applications. Publisher Academic Press 38:315–322
Wirsel SGR, Leibinger W, Ernst M, Mendgen K, Mendgen K (2001) Genetic diversity of fungi closely associated with common reed. New Phytol 149:589–598. https://doi.org/10.1046/j.1469-137.2001.00038.x
Xiang L, Gong S, Yang L et al (2016) Biocontrol potential of endophytic fungi in medicinal plants from Wuhan Botanical Garden in China. Biol Control 94:47–55. https://doi.org/10.1016/j.biocontrol.2015.12.002
Yan L, Zhu J, Zhao X, Shi J, Jiang C, Shao D (2019) Beneficial effects of endophytic fungi colonization on plants. Appl Microbiol Biotechnol 103:3327–3340. https://doi.org/10.1007/s00253-019-09713-2
Zhang Q, Zhang J, Yang L et al (2014) Diversity and biocontrol potential of endophytic fungi in Brassica napus. Biol Control 72:98–108. https://doi.org/10.1016/j.biocontrol.2014.02.018
Zheng YK, Miao CP, Chen HH, Huang FF, Xia YM, Chen YW, Zhao LX (2017) Endophytic fungi harbored in Panax notoginseng: diversity and potential as biological control agents against host plant pathogens of root-rot disease. Journal of Ginseng Research 41(3):353–360
Acknowledgments
We acknowledge the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)–Finance Code 001, the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for financing the project and for granting the scholarships, as well as the Brazilian Agricultural Research Corporation (Embrapa Acre) of Acre state and the Universidade Federal do Amazonas for providing the infrastructure and the employees of these institutions for their assistance during the collection of the samples. In addition, we are grateful to Dr. Harry C. Evans (CABI Bioscience) for correcting the English grammar.
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Online Resource 1
Geographic coordinates of collection points in the states of Acre (AC) and Amazonas (AM). (DOCX 14 kb)
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Taxonomic assignment of endophytic fungi isolate and their respective OTUs and accession numbers in GenBank (NCBI). All isolates identified as Phomopsis sp., Talaromyces sp. and Nodulisporium sp. in the table below, according with Genbank (NCBI), were assigned as Diaporthe sp., Penicillium sp. and Daldinia sp, respectively, in the manuscript, following the taxonomic nomenclature: one fungus, one name (Taylor 2011). (DOCX 80 kb)
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Operational taxonomic units (OTU)s and number of endophytic fungi isolated from leaf, stem and roots of rubber tree in the states of Acre and Amazonas of the Amazon forest. The OTUs identified as Phomopsis sp., Talaromyces sp. and Nodulisporium sp. in the table below, according with Genbank (NCBI), were assigned and quantified as Diaporthe sp., Penicillium sp. and Daldinia sp., respectively, in the manuscript, following the taxonomic nomenclature: one fungus, one name (Taylor 2011). (DOCX 38 kb)
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Araújo, K.S., Brito, V.N., Veloso, T.G.R. et al. Diversity and distribution of endophytic fungi in different tissues of Hevea brasiliensis native to the Brazilian Amazon forest. Mycol Progress 19, 1057–1068 (2020). https://doi.org/10.1007/s11557-020-01613-4
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DOI: https://doi.org/10.1007/s11557-020-01613-4