Endophytic fungi in roots of native orchids of rupestrian grasslands (campos rupestres) in Serra do Cipó, Brazil
DOI:
https://doi.org/10.21826/2446-82312021v76e2021021Parole chiave:
Endófitos, Fungo micorrízico, Orquídea endêmicaAbstract
Fungos endofíticos radiculares são essenciais para o ciclo de vida das orquídeas. Muitos deles atuam como promotores de crescimento da planta hospedeira e os endófitos micorrízicos são indispensáveis a germinação de sementes. Este estudo objetivou avaliar a riqueza de fungos endofíticos cultiváveis de cinco orquídeas nativas de Campos Rupestres na Serra do Cipó, Brasil. Raízes saudáveis foram amostradas e os endófitos isolados. Cada isolado teve seu DNA total extraído e a região ITS (Internal Transcribed Spacer) amplificada e sequenciada. A análise de 32 sequências fúngicas permitiram a identificação de 25 espécies pertencentes aos filos Ascomycota e Basidiomycota. Nove isolados pertenciam aos gêneros Sebacina Tul. & C. Tul. and Tulasnella J. Schröt. do filo Basidiomycota, que são importantes gêneros de fungos micorrízicos de orquídeas. A mesma espécie fúngica foi obtida de diferentes orquídeas crescendo em substratos distintos. A identificação molecular dos fungos indicou alta riqueza de endófitos sustentando o ciclo de vida das orquídeas em campos rupestres.
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Abarenkov, K., Zirk, A., Piirmann, T., Pöhönen, R., Ivanov, F., Nilsson, R.H., Kõljalg, U. 2020. Full UNITE+INSD dataset for Fungi. UNITE Community. 10.15156/BIO/786372.
Abreu, M.E.P., Garcia, Q.S. 2005. Efeito da luz e da temperatura na germinação de quatro espécies de Xyris l. (Xyridaceae) ocorrentes na Serra do Cipó, MG, Brasil. Acta Botanica Brasilica 19:149-154.
Altschul, S.F., Madden T.L., Schaffer A.A. et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25:3389-3402.
Antoniolli ZI, Kaminski J. 1991. Micorrizas. Ciência Rural. V1, n3, P 441-455
Azevedo, J.L. 1998. Micro-organismos endofíticos. In: Melo IS, Azevedo JL (Eds.) Ecologia Microbiana. Jaguariuna: Embrapa – CNPMA. 4:117-137
Bayman, P.J., Otero, T. 2006. Microbial Endophytes of Orchid Roots. In: Schulz B, Boyle C, Sieber T (Ed.) Microbial Root Endophytes. Berlin: Springer-Verlag.
Boldrini, R.F., Santos, W.O., Cruz, Z.M.A., Ramos, A.C. 2010. Bases da associação micorrízica orquidóide. Natureza online 8:140-145.
Cardoso, J.C., Israel, M. 2005. Levantamento de espécies da família Orchidaceae em Águas de Sta. Bárbara - SP e seu cultivo. Horticultura Brasileira 23:169-173.
Cevallos, S., Herrera, P., Sanchez-Rodríguez, A., Declerck, S., Suarez, J.P. 2018. Untangling factors that drive community composition of root associated fungal endophytes of Neotropical epiphytic orchids. Fungal Ecology 34 :67-75.
Chen, Y., Gao, Y., Song, L., Zhao, Z., Guo, S., Xing, X. 2019. Mycorrhizal fungal community composition in seven orchid species inhabiting Song Mountain, Beijing, China. Science China Life Sciences 62(6):838–847.
Dearnaley, J.D.W., Martos, F., Selosse, M.A. 2012. Orchid mycorrhizas: molecular ecology, physiology, evolution and conservation aspects. In: Hock, B. (Ed). The Mycota. IX: Fungal associations, 2nd ed. Berlin: Springer-Verlag.
Dearnaley, J., Perotto, S., Selosse, M.A. 2017. Structure and development of orchid mycorrhizas. In: Martin, F. (Ed.) Molecular mycorrhizal symbiosis, John Wiley & Sons, Inc.
Dutta, D., Puzari, K.C., Gogoi, R., Dutta, P. 2014. Endophytes: Exploitation as a Tool in Plant Protection. Brazilian Archives of Biology and Technology 57: 21-629.
Fay, M.F. 2018. Orchid conservation: how can we meet the challenges in the twenty-first century? Botanical Studies 59:16.
García, V.G., Onco, M.A.P., Susan, V.R. 2006. Review. Biology and Systematics of the form genus Rhizoctonia. Spanish Journal of Agricultural Research 4:55-79
Gardes, M., Bruns, T.D. 1993. ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rust. Molecular Ecology 2:113-118.
Geiser, D.M., Gueidan, C., Miadlikowska, J. et al. 2006. Eurotiomycetes: Eurotiomycetidae and Chaetothyriomycetidae. Mycologia 98:1053-1064.
Guimarães, F.A.R., Pereira, M.C., Felício, C.S., Torres, D.P., Oliveira, S.F., Veloso, T.G.R., Kasuya, M.C.M. 2013. Symbiotic propagation of seedlings of Cyrtopodium glutiniferum Raddi (Orchidaceae). Acta Botanica Brasilica 27:590-596.
Herrera, P., Suarez, J.P., Sanchez-Rodríguez, A., Molina, M.C., Prieto, M., Mendez, M. 2019. Many broadly-shared mycobionts characterize mycorrhizal interactions of two coexisting epiphytic orchids in a high elevation tropical forest. Fungal Ecology 39:26e36.
Hibbett, D.S., Binder, M., Bischoff, J.F. 2007. A higher-level phylogenetic classification of the Fungi. Mycological Research 111:509–547
Jacquemyn, H., Waud, M., Lievens, B., Brys, R. 2016. Differences in mycorrhizal communities between Epipactis palustris, E. helleborine and its presumed sister species E. neerlandica. Annals of Botany 118: 105–114.
Jones, D.L. 2006. A complete guide to native orchids of Australia including the Island Territories. Sydney: Reed New Hol.
Katoh, K., Kuma, K.I., Toh, H., Miyata, T. 2005. MAFFT version 5: Improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33:511-518.
Kuga, Y., Sakamoto, N., Yurimoto, H. 2014. Stable isotope cellular imaging reveals that both live and degenerating fungal pelotons transfer carbon and nitrogen to orchid protocorms. New Phytologist 202:594-605.
Lee, B.H., Eom, A.H. 2017. Five Species of Endophytic Fungi Isolated from Roots of Native Orchid Plants from Korea. The Korean Journal of Mycology 45:355–361.
Lee, B.H., Kwon, W.J., Kim, J.Y., et al. 2017. Differences among endophytic fungal communities Isolated from the roots of Cephalanthera longibracteata collected from different sites in Korea. Mycobiology 45:312-317.
Ma, X., Kang, J., Nontachaiyapoom, S., Wen, T., Hyde, K.D. 2015. Non-mycorrhizal endophytic fungi from orchids. Current Science 109:72-87.
McCormick, M.K., Taylor, D.L., Whigham, D.F., Burnett, R.K. 2016. Germination patterns in three terrestrial orchids relate to abundance of mycorrhizal fungi. Journal of Ecolology 104:744-754.
Miller, M.A., Pfeiffer, W., and Schwartz, T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA pp 1 - 8.
Mosquera-Espinosa, A.T., Bayman, P., Prado, G.A. et al. 2013. The double life of Ceratobasidium : orchid mycorrhizal fungi and their potential for biocontrol of Rhizoctonia solani sheath blight of rice. Mycologia. 105:141-150.
Nylander, J.A.A. 2004. MrModeltest v2 Program distributed by the author. Uppsala University, Sweden, Evolutionary Biology Centre.
Pereira, O.L., Kasuya, M.C.M., Rollemberg, C.L., Borges, G.M. 2005. Isolamento e identificação de fungos micorrízicos rizoctonióides associados a três espécies de orquídeas epífitas neotropicais no Brasil. Revista Brasileira de Ciência do Solo 29:191-197.
Pereira, M.C., Torres, D.P., Guimarães, F.A.R., Pereira, O.L., Kasuya, M.C.M. 2011. Germinação de sementes e desenvolvimento de protocormos de Epidendrum secundum Jacq. (Orchidaceae) em associação com fungos micorrízicos do gênero Epulorhiza. Acta Botanica Brasilica 25:534-541.
Pereira, M.C., Coelho, I.S., Valadares, R.B.S., Oliveira, S.F., Bocayuva, M., Pereira, O.L., Araújo, E.F., Kasuya, M.C.M. 2014. Morphological and molecular characterization of Tulasnella spp. fungi isolated from the roots of Epidendrum secundum, a widespread Brazilian orchid. Symbiosis 62:111-121.
Pereira, M.C., Rocha, D.I., Veloso, T.G.R., Pereira, O.L., Francino, D.M.T., Meira, R.M.S.A., Kasuya, M.C.M. 2015. Characterization of seed germination and protocorm development of Cyrtopodium glutiniferum (Orchidaceae) promoted by mycorrhizal fungi Epulorhiza spp. Acta Botanica Brasilica 29:567-574.
Peterson, R.L., Massicotte, H.B., Melville, L.H. 2004. Mycorrhizas: Anatomy and Cell Biology. NRC Research Press, Ottawa.
Rambaut, A., Drummond, A.J., Xie, D., Baele, G., Suchard, M.A. 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology. syy032. doi:10.1093/sysbio/syy032
Rasmussen, H.N., Dixon, K.W., Jersáková, J., Tesitelová, T. 2015. Germination and seedling establishment in orchids: a complex of requirements. Annals of Botany 116:391-402.
Roberts, P. 1999. Rhizoctonia-forming Fungi: a taxonomic guide. Royal Botanical Gardens, Kew Publishing.
Ronquist, F., M. Teslenko, P. van der Mark, D.L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M.A. Suchard, and J.P. Huelsenbeck. 2012. MRBAYES 3.2: Efficient Bayesian phylogenetic inference and model selection across a large model space. Systematic Biology 61:539-542.
Salazar-Cerezo, S., Martinez-Montiel, N., Cruz-Lopez, M.C., Martinez-Contreras, R.D. 2018. Fungal diversity and community composition of culturable fungi in Stanhopea trigrina cast gibberellin producers. Frontiers in Microbiology 9: 612.
Salifah, H.A.B., Muskhazli, M., Rusea, G., Nithiyaa, P. 2011. Variation in mycorrhizal specificity for in vitro symbiotic seed germination of Grammatophyllum speciosum Blume. Sains Malaysiana 40:451-455.
Shao, S.C., Burgess, K.S., Cruse-Sanders, J.M. et al. 2017. Using in situ symbiotic seed germination to restore over-collected medicinal orchids in Southwest China. Frontiers in Plant Science 8: 888.
Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J. and Sahl, J.W. 2009. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75(23):7537-41.
Schoch, C.L., Shoemaker, R.A., Seifert, K.A. et al. 2006. A multigene phylogeny of the Dothideomycetes using four nuclear loci. Mycologia 98:1041-1052.
Selosse, M.A., Faccio, A., Scappaticci, G., Bonfante, P. 2004. Chlorophyllous and Achlorophyllous Specimens of Epipactis microphylla (Neottieae, Orchidaceae) Are Associated with Ectomycorrhizal Septomycetes, including Truffles. Microbial Ecology 47:416-426.
Selosse, M.A., Richard, F., He, X., Simard, S.W. 2006. Mycorrhizal networks: des liaisons dangereuses? TRENDS in Ecology and Evolution 21:621-628.
Shah, S., Shrestha, R., Maharjan, S., Selosse, M., Pant, B. 2019. Isolation and Characterization of Plant Growth-Promoting Endophytic Fungi from the Roots of Dendrobium moniliforme. Plants 8:5.
Smith, S.E., Read, D.J. 2008. Mycorrhizal symbiosis. 3 ed. San Diego: Academic Press.
Stecher, G., Tamura, K. and Kumar, S. 2020. Molecular evolutionary genetics analysis (MEGA) for macOS. Molecular Biology and Evolution, 37(4), pp.1237-1239.
Suarez, J.P., Weiß, M., Abele, A., Garnica, S., Oberwinkler, F., Kottke, I. 2006. Diverse tulasnelloid fungi form mycorrhizas with epiphytic orchids in an Andean cloud forest. Mycological Research 110: 1257–1270.
The Plant List. 2020. The plant list, ver. 1. http://www.theplantlist.org. Accessed 10 Fev. 2020.
Valadares, R.B.S., Pereira, M.C., Otero, J.T., Cardoso, E.J. 2012. Narrow fungal mycorrhizal diversity in a population of the orchid Coppensia doniana. Biotropica 44:114-122.
Valadares, R.B.S., Otero, J.T., Pereira, M.C., Cardoso, E.J.B.N. 2015. The epiphytic orchids Ionopsis utricularioides and Psygmorchis pusilla associate with different Ceratobasidium lineages at Valle del Cauca, Colombia. Acta Botanica Brasilica 29:40-44.
Wang, Z., Johnston, P.R., Takamatsu, S., et al. 2006a. Toward a phylogenetic classification of the Leotiomycetes based on rDNA data. Mycologia 98:1065-1075.
Wang, Z., Binder, M., Schoch, C.L., Johnston, P.R., Spatafora, J.W., Hibbett, D.S. 2006b. Evolution of helotialean fungi (Leotiomycetes, Pezizomycotina): a nuclear rDNA phylogeny. Molecular Phylogenetics and Evolution 41:295–312.
Waud, M., Busschaert, P., Lievens, B., Jacquemyn, H. 2016. Specificity and localised distribution of mycorrhizal fungi in the soil may contribute to co-existence of orchid species. Fungal Ecology 20:155-165.
Weiss, M., Selosse, M., Rexer, K., Urban, A., Oberwinkler, F. 2004. Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycological Research 108(9): 1003–1010.
Weiß, M., Waller, F., Zuccaro, A., Selosse, M. 2016. Sebacinales – one thousand and one interactions with land plants. New Phytologist 211: 20–40.
White, T.J., Bruns, T.D., Lee, S., Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: a guide to methods and applications. San Diego: Academic Press.
Yeh, C., Chung, K., Liang, C., Tsai, W. 2019. New Insights into the Symbiotic Relationship between Orchids and Fungi. Applied Sciences 9: 585.
Zhang, N., Castlebury, L.A., Miller, A.N. et al. 2006. An overview of the systematics of the Sordariomycetes based on a four-gene phylogeny. Mycologia 98:1076-1087.