Successful Tulasnella amonilioides isolation from wild Cattleya intermedia and effectiveness of the mycobiont on in vitro propagation of this threatened Orchidaceae

Autores

  • Delio Endres Júnior Universidade Feevale
  • Genivaldo Alves-Silva Universidade Federal do Rio Grande do sul
  • Márcio Hisayuki Sasamori Universidade Feevale
  • Rosa Mara Borges da Silveira Universidade Federal do Rio Grande do sul
  • Annette Droste Universidade Feevale

DOI:

https://doi.org/10.24221/jeap.8.1.2023.5160.009-029

Palavras-chave:

Epiphytic orchid, Epulorhiza sp., orchid conservation, phylogenetic analysis, symbiosis

Resumo

This is the first study that reports symbiosis in Cattleya, aiming to isolate and identify mycorrhizal fungi capable of promoting the germination of this orchid and to evaluate the development of symbiotically propagated individuals. We compared seed germination percentage, growth index, and morphometric variables of seedlings propagated symbiotically in oatmeal agar (OMA) medium with individuals that were non-symbiotically propagated in Murashige and Skoog (MS) medium. Fungi isolates were identified by phylogenetic analysis and eight of the nine isolates that were efficient in C. intermedia propagation were identified as Tulasnella amonilioides. The mycobiont improved C. intermedia seed germination and plant development when compared with OMA medium without fungi (negative control). Seedlings propagated by symbiotic culture with T. amonilioides produced more leaves and longer roots, while shoot height and a number of roots were lower than for seedlings propagated in MS medium with the addition of activated charcoal. The fresh mass of seedlings propagated by symbiotic and a symbiotic techniques was equal, except when seedlings were grown in MS without activated charcoal. T. amonilioides enhance the in vitro propagation of C. intermedia and provide plants that facilitate symbiotic processes in reintroduction environments.

Downloads

Não há dados estatísticos.

Biografia do Autor

Delio Endres Júnior, Universidade Feevale

Doutor em Qualidade Ambiental, Pós-doutorando do programa de Pós-graduação em Qualidade Ambiental, Universidade Feevale. 

Genivaldo Alves-Silva, Universidade Federal do Rio Grande do sul

Doutor em Botânica, Universidade Federal do Rio Grande do Sul. Pós-doutorando do Programa de Pós-Graduação em Biologia de Fungos, Algas e Plantas, Universidade Federal de Santa Catarina 

Márcio Hisayuki Sasamori, Universidade Feevale

Doutor em Qualidade Ambiental, Programa de Pós-graduação em Qualidade Ambiental, Universidade Feevale.

Rosa Mara Borges da Silveira, Universidade Federal do Rio Grande do sul

Doutora em Ciências Biológicas pelo Universidad de Buenos Aires, Argentina, Professora titular do Programa de Pós-Graduação em Botânica, Universidade Federal do Rio Grande do Sul.

Annette Droste, Universidade Feevale

Doutora em Genética e Biologia Molecular, Universidade Federal do Rio Grande do Sul. Professora titular do Programa de Pós-graduação em Qualidade Ambiental da Universidade Feevale. 

Referências

Aggarwal, S.; Nirmala, C.; Beri, S.; Rastogi, S.; Adholeya, A. 2012. In vitro symbiotic seed germination and molecular characterization of associated endophytic fungi in a commercially important and endangered indian orchid Vanda coerulea Griff. Ex Lindl. European Journal of Environmental Sciences, 2, 33-42. https://doi.org/10.14712/23361964.2015.36

Aggarwal, S.; Zettler, L. W. 2010. Reintroduction of an endangered terrestrial orchid, Dactylorhiza hatagirea (D. Don) Soo, assisted by symbiotic seed germination: first report from the Indian subcontinent. Nature and Science, 8, 139-145.

Almeida, P. R. M.; Van den Berg, C.; Góes-Neto, A. 2014. Epulorhiza amonilioides sp. nov.: a new anamorphic species of orchid mycorrhiza from Brazil. Neodiversity, 7, 1-10. http://dx.doi.org/10.13102/neod.71.1

Alomía, Y. A.; Mosquera-Espinosa, A. T.; Flanagan, N. S.; Otero, J. T. 2017. Seed viability and symbiotic seed germination in Vanilla spp. (Orchidaceae). Research Journal of Seed Science, 10, 43-52. https://doi.org/10.3923/rjss.2017.43.52

Arditti, J. 1967. Factors affecting the germination of orchid seeds. The Botanical Review, 33, 1-97.

Arditti, J. 1992. Fundamentals of orchid biology. John Wiley & Sons, New York. 704p.

Bidartondo, M. I.; Bruns, T. D.; Weiß, M.; Sérgio, C.; Read, D. J. 2003. Specialized cheating of the ectomycorrhizal symbiosis by an epiparasitic liverwort. Proceedings of the Royal Society B: Biological Sciences, 270, 835-842. https://doi.org/10.1098/rspb.2002.2299

Bonnardeaux, Y.; Brundrett, M.; Batty, A.; Dixon, K.; Koch, J.; Sivasithamparam, K. 2007. Diversity of mycorrhizal fungi of terrestrial orchids: compatibility webs, brief encounters, lasting relationships and alien invasions. Mycology Research, 111, 51-61. https://doi.org/10.1016/j.mycres.2006.11.006

Brundrett, M. C.; Scade, A.; Batty, A. L.; Dixon, K. W.; Sivasithamparam, K. 2003. Development of in situ and ex situ seed baiting techniques to detect mycorrhizal fungi from terrestrial orchid habitats. Mycological Research, 107, 1210-1220. https://doi.org/10.1017/S0953756203008463

Cameron, D. D.; Johnson, I.; Leake, J. R.; Read, D. J. 2007. Mycorrhizal acquisition of inorganic phosphorus by the green-leaved terrestrial orchid Goodyera repens. Annals of Botany, 99, 831-834. https://doi.org/10.1093/aob/mcm018

Cameron, D. D.; Johnson, I.; Leake, J. R.; Read, D. J. 2008. Giving and receiving: measuring the carbon cost of mycorrhizas in the green orchid, Goodyera repens. New Phytologyst, 180, 176-184. https://doi.org/10.1111/j.1469-8137.2008.02533.x

Cameron, D. D.; Leake, J. R.; Read, D. J. 2006. Mutualistic mycorrhiza in orchids: evidence from plant-fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens. New Phytologist, 171, 405-416. https://doi.org/10.1111/j.1469-8137.2006.01767.x

Cevallos, S.; Sánchez-Rodríguez, A.; Decock, C.; Declerck, S.; Suárez, J. P. 2017. Are there keystone mycorrhizal fungi associated to tropical epiphytic orchids? Mycorrhiza, 27, 225-232. https://doi.org/10.1007/s00572-016-0746-8

Crous, P. W. et al. 2015. Fungal Planet description sheets:320–370. Persoonia Molecular Phylogeny and Evolution of Fungi, 34, 167-266. https://doi.org/10.3767/003158515X688433

Cruz, D.; Suarez, J. P.; Kottke, I.; Piepenbring, M. 2014. Cryptic species revealed by molecular phylogenetic analysis of sequences obtained from basidiomata of Tulasnella. Mycologia, 106, 708-722. https://doi.org/10.3852/12-386

Currah, R. S.; Zettler, L. W.; Mcinnis, T. M. 1997. Epulorhiza inquilina sp. nov. from Platanthera (Orchidaceae) and a key to Epulorhiza species. Mycotaxon, 61, 338-342.

Dentinger, B. T. M.; Margaritescu, S.; Moncalvo J-M. M. 2010. Rapid and reliable high-throughput methods of DNA extraction for use in barcoding and molecular systematics of mushrooms. Molecular Ecology Resources, 10, 628-633. https://doi.org/10.1111/j.1755-0998.2009.02825.x

Deshmukh, S.; Hückelhoven, R.; Schäfer, P.; Imani, J.; Sharma, M.; Weiss, M.; Waller, F.; Kogel, K.-H. 2006. The root endophytic fungus Pirifomospora indica requires host cell for proliferation during mutualistic symbiosis with barley. Proceedings of the National Academy of Sciences of the United States of America, 103, 18450-18457. https://doi.org/10.1073/pnas.0605697103

Dixon, K. 1987. Raising terrestrial orchids from seed. In: Harris, W. K. [ed.]. Modern orchid growing for pleasure and profit, Orchid Club of South Australia Inc., Adelaide. pp. 47-100,

Downing, J. L. 2016. Consequences of anthropogenic and global change on orchids: an emphasis on biotic interactions. Doctoral thesis, Florida International University. Miami, United States of America. 188p.

Durán-López, M. E.; Caroca-Cáceres, R.; Jahreis, K.; Narváez-Vera, M.; Ansaloni, R.; Cazar, M. E. 2019. The micorryzal fungi Ceratobasidium sp. and Sebacina vermifera promote seed germination and seedling development of the terrestrial orchid Epidendrum secundum Jacq. South African Journal of Botany, 125, 54-61. https://doi.org/10.1016/j.sajb.2019.06.029

Endres Júnior, D.; Alves-Silva, G.; Sasamori, M. H.; Silveira, R. M. B.; Droste, A. 2022. "Data for: Successful Tulasnella amonilioides isolation from wild Cattleya intermedia and effectiveness of the mycobiont on in vitro propagation of this threatened Orchidaceae", https://doi.org/10.7910/DVN/CESMZX, Harvard Dataverse, V1

Endres Júnior, D.; Sasamori, M. H.; Silveira, T.; Schmitt, J. L.; Droste A. 2015. Reintrodução de Cattleya intermedia Graham (Orchidaceae) em borda e interior de um fragmento de Floresta Estacional Semidecidual no sul do Brasil. Revista Brasileira de Biociências, 13, 33-40.

Fowlie, J. A. 1977. The Brazilian bifoliate Cattleyas and their color varieties: their speciation, distribution, literature, and cultivation: a monographic revision. Day Printing Corporation, California.

Fridborg, G.; Pedersen, M.; Landstorm, L. E.; Eriksson, T. 1978. The effect of activated charcoal on tissue culture; absorption of metabolites inhibiting morphogenesis. Physiologia Plantarum, 43, 104-106.

Fujimori, S.; Abe, J. P.; Okane, I.; Yamaoka, Y. 2019. Three new species in the genus Tulasnella isolated from orchid mycorrhiza of Spiranthes sinensis var. amoena (Orchidaceae). Mycoscience, 60, 71-81. https://doi.org/10.1016/j.myc.2018.09.003

George, P. S.; Ravishankar, G. A. 1997. In vitro multiplication of Vanilla planifolia using axillary bud explants. Plant Cell Reports, 16, 490-494.

Góes-Neto, A.; Loguercio-Leite, C.; Guerrero, R. T. 2005. DNA extraction from frozen field- collected and dehydrated herbarium fungal basidiomata: performance of SDS and CTAB-based methods. Biotemas, 18, 19-32.

Gónzalez, D.; Rodriguez-Carres, M.; Boekhout, T.; Stalpers, J.; Kuramae, E. E.; Nakatani, A. K.; Vilgalys, R.; Cubeta, M. 2016. Phylogenetic relationships of Rhizoctonia fungi within the Cantharellales. Fungal Biology, 120, 603-619. https://doi.org/10.1016/j.funbio.2016.01.012

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. https://doi.org/10.1590/S0102-33062013000300016

Herrera, H.; Valadares, R.; Contreras, D.; Bashan, Y.; Arriagada, C. 2017. Mycorrhizal compatibility and symbiotic seed germination of orchids from the Coastal Range and Andes in south central Chile. Mycorrhiza, 27, 175-188. https://doi.org/10.1007/s00572-016-0733-0

IBGE-Instituto Brasileiro de Geografia e Estatística, MMA – Ministério do Meio Ambiente. 2004. Biomas do Rio Grande do Sul. Available at: http://www.atlassocioeconomico.rs.gov.br/biomas. Access at: 13 May 2022.

Jiang, J. H.; Lee, Y. I.; Cubeta, M. A.; Chen, L. C. 2015. Characterization and colonization of endomycorrhizal Rhizoctonia fungi in the medicinal herb Anoectochilus formosanus (Orchidaceae). Mycorrhiza, 25, 431-445. https://doi.org/10.1007/s00572-014-0616-1

Katoh, K.; Standley, D. M. 2013. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Molecular Biology and Evolution, 30, 772-780. https://doi.org/10.1093/molbev/mst010

Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; Buxtin, S.; Cooper, A.; Markowitz, S.; Duran, C.; Thierer, T.; Ashton, B.; Meintjes, P.; Drummond, A. 2012. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647-1649. https://doi.org/10.1093/bioinformatics/bts199

Kim, D. H.; Kang, K. W.; Enkhtaivan, G.; Jan, U.; Sivanesan, I. 2019. Impact of activated charcoal, culture medium strength and thidiazuron on non-symbiotic in vitro seed germination of Pecteilis radiata (Thunb.) Raf. South African Journal of Botany, 124, 144-150. https://doi.org/10.1016/j.sajb.2019.04.015

Knudson, L. 1921. La germinación no simbiótica de las semillas de orquídeas. Boletín de la Sociedad Española de Historia Natural, 21, 250-260.

Kristiansen, K. A.; Rasmussen, F. N.; Rasmussen, H. N. 2001. Seedlings of Neuwiedia (Orchidaceae subfamily Apostasioideae) have typical orchidaceous mycotrophic protocorms. American Journal of Botany, 88, 956-959.

Kumar, S.; Stecher, G.; Tamura, K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33, 1870-1874. https://doi.org/10.1093/molbev/msw054

Liebel, H. T.; Bidartondo, M. I.; Gebauer, G. 2015. Are carbon and nitrogen exchange between fungi and the orchid Goodyera repens affected by irradiance? Annals of Botany, 115, 251–261. https://doi.org/10.1093/aob/mcu240

Linde, C. C.; May, T. W.; Phillips, R. D.; Ruibal, M.; Smith, L. M.; Peakall, R. 2017. New species of Tulasnella associated with terrestrial orchids in Australia. IMA Fungus, 8, 27-47. https://doi.org/10.5598/imafungus.2017.08.01.03

Ma, M.; Tan, T. K.; Wong, S. M. 2003. Identification and molecular phylogeny of Epulorhiza isolates from tropical orchids. Mycology Research, 107, 1041–1049. https://doi.org/10.1017/S0953756203008281

Machado Neto, N. B.; Vieira, L. G. E. 2011. Assessment of genetic diversity in Cattleya intermedia Lindl. (Orchidaceae). Brazilian Archives of Biology and Technology, 54, 939-946. https://doi.org/10.1590/S1516-89132011000500011

Matheny, P. B.; Curtis, J. M.; Hofstetter, V.; Aime, M. C.; Moncalvo, J.-M.; Ge, Z.-W.; Yang, Z.-L.; Slot, J. C.; Ammirati, J. F.; Baroni, T. J.; Bougher, N. L.; Hughes, K. W.; Lodge, D. J.; Kerrigan, R. W.; Seidl, M. T.; Aanen, D. K.; DeNitis, M.; Daniele, G. M.; Desjardim, D. E.; Kropp, B. R.; Norvell, L. L.; Parker, A.; Vellinga, E. C.; Vilgalys, R.; Hibbett, D. S. 2006. Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia, 98, 982-995. https://doi.org/10.3852/mycologia.98.6.982

McCormick, M. K.; Whigham, D. F.; O’Neill, J. 2004. Mycorrhizal diversity in photosynthetic terrestrial orchids. New Phytologist, 163, 425–438. https://doi.org/10.1111/j.1469-8137.2004.01114.x

McNeill, J.; Barrie, F. F.; Buck, W. R.; Demoulin, V.; Greuter, W.; Hawksworth, D. L.; Herendeen, P. S.; Knapp, S.; Marhold, K.; Prado, J.; Prud’Homme Nan Reiine, W. F.; Smith, G. F.; Wiersema, J. H. [eds.]. 2012. International Code of Nomenclature for algae, fungi, and plants (Melbourne Code). [Regnum vegetabile no. 154.] Koeltz Scientific Books, Königstein.

Menini Neto, L.; Barros, F.; Vinhos, F.; Furtado, S. G.; Judice, D. M.; Fernandez, E. P.; Sfair, J. C.; Barros, F. S. M.; Prieto, P. V.; Kutschenko, D. C.; Moraes, M. A.; Zanata, M. R. V.; Santos Filho, L. A. F. 2013. Orchidaceae. In: Martinelli, G. & Moraes, M. A. [eds.]. Livro vermelho da flora do Brasil. Jardim Botânico do Rio de Janeiro, Rio de Janeiro. pp. 749-818. Available at: https://dspace.jbrj.gov.br/jspui/handle/doc/26. Access at: 18 Jan 2023.

Merckx, V. S. F. T. 2013. Mycoheterotrophy: An introduction. In: Merckx, V. S. F. T. [ed.]. Mycoheterotrophy: The biology of plants living on fungi, pp. 1-17, Springer, New York. https://doi.org/10.1007/978-1-4614-5209-6_1

Miller, M. A.; Pfeiffer, W.; Schwartz, T. 2011. The CIPRES science gateway: A community resource for phylogenetic analyses. In: Proceedings of the 2011 TeraGrid Conference: extreme digital discovery, ACM, New York, pp. 1-8.

Moncalvo, J.; Nilsson, R. H.; Koster, B.; Dunham, S. M.; Bernauer, T.; Matheny, P. B.; Porter, T. M.; Margaritescu, S.; Wei?, M.; Garnica, S.; Danell, E.; Langer, G.; Langer, E.; Larsson, E.; Larsson, K.-H.; Vilgalys, R. 2006. The Cantharelloid Clade: Dealing with incongruent gene trees and phylogenetic reconstruction methods. Mycologia, 98, 937-948. https://doi.org/10.1080/15572536.2006.11832623

Moore, R. T. 1987. The genera of Rhizoctonia-like fungi: Ascorhizoctonia, Ceratorhiza gen. nov., Epulorhiza gen. nov., Moniliopsis, and Rhizoctonia. Mycotaxon, 29, 91-99.

Murashige, T.; Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum, 15, 473-497.

Nogueira, R. E.; Pereira, O. L.; Kasuya, M. C. M.; Lanna, M. C. S.; Mendonça, M. P. 2005. Fungos micorrízicos associados a orquídeas em campos rupestres na região do Quadrilátero Ferrífero, MG, Brasil. Acta Botanica Brasilica, 19, 417-424. https://doi.org/10.1590/S0102-33062005000300001

Nontachaiyapoom, S.; Sasirat, S.; Manoch, L. 2010. Isolation and identification of Rhizoctonia-like fungi from roots of three orchid genera, Paphiopedilum, Dendrobium, and Cymbidium, collected in Chiang Rai and Chiang Mai provinces of Thailand. Mycorrhiza, 20, 459-471. https://doi.org/10.1007/s00572-010-0297-3

Nontachaiyapoom, S.; Sasirat, S.; Manoch, L. 2011. Symbiotic seed germination of Grammatophyllum speciosum Blume and Dendrobium draconis Rchb. f., native orchids of Thailand. Scientia Horticulturae, 130, 303-308. https://doi.org/10.1016/j.scienta.2011.06.040

Novotná, A.; Benítez, Á.; Herrera, P.; Cruz, D.; Filipczyková, E.; Suárez, J. P. 2018. High diversity of root-associated fungi isolated from three epiphytic orchids in southern Ecuador. Mycoscience, 59, 24-32. https://doi.org/10.1016/j.myc.2017.07.007

Nylander, J. 2004. MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. Available at: https://github.com/nylander/MrModeltest2

Ogura-Tsujita, Y.; Yokoyama, J.; Miyoshi, K.; Yukawa, T. 2012. Shifts in mycorrhizal fungi during the evolution of autotrophy to mycoheterotrophy in Cymbidium (Orchidaceae). American Journal of Botany, 99, 1158-1176. https://doi.org/10.3732/ajb.1100464

OrchidRoots. 2022. Available at: http://bluenanta.com/orchid/search_match/?q=cattleya+intermedia. Access at: 10 June 2022.

Otero, J. T. O.; Bayman, P. 2009. Germinación simbiótica y asimbiótica en semillas de orquídeas epi?tas. Acta Agronómica, 58, 270-276.

Otero, J. T.; Bayman, P.; Ackerman, J. D. 2005. Variation in mycorrhizal performance in the epiphytic orchid Tolumnia variegata in vitro: the potential for natural selection. Evolutionary Ecology, 19, 29-43. https://doi.org/10.1007/s10682-004-5441-0

Otero, J. T.; Flanagan, N. S.; Herre, E. A.; Ackerman, J. D.; Bayman, P. 2007. Widespread mycorrhyzal specificity correlates to mycorrhyzal function in the Neotropical, epiphytic orchid Ionopsis utricularioides (Orchidaceae). American Journal of Botany, 94, 1944-1950. https://doi.org/10.3732/ajb.94.12.1944.

Pan, M. J.; Van Staden, J. 1998. The use of charcoal in vitro culture-a review. Plant Growth Regulation, 26, 155-163.

Pattengale, N. D.; Alipour, M.; Bininda-Emonds, O. R. P.; Moret, B. M. E.; Stamatakis, A. 2009. How many bootstrap replicates are necessary? Lecture Notes in Computer Science (Including Subseries Lecture Notes in Artificial Intelligence and Lecture Notes in Bioinformatics), 5541, 184-200. http://dx.doi.org/10.1007/978-3-642-38886-6

Paul, S.; Kumaria, S.; Tandon, P. 2012. An effective nutrient medium for asymbiotic seed germination and large-scale in vitro regeneration of Dendrobium hookerianum, a threatened orchid of northeast India. AoB Plants, 2012, plr032. https://doi.org/10.1093/aobpla/plr032

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. https://doi.org/10.1007/s13199-014-0276-0

Pereira, M. C.; Pereira, O. L.; Costa, M. D.; Rocha, R. B.; Kasuya, M. C. M. 2009. Diversidade de fungos micorrízicos Epulorhiza spp. isolados de Epidendrum secundum (Orchidaceae). Revista Brasileira de Ciência do Solo, 33, 1187-1197. https://doi.org/10.1590/S0100-06832009000500012

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. https://doi.org/10.1590/0102-33062015abb0078

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. https://doi.org/10.1590/S0102-33062011000300004

Pereira, O. L.; Kasuya, M. C. M.; Borges, A. C.; Araújo, E. F. 2005. Morphological and molecular characterization of mycorrhizal fungi isolated from neotropical orchids in Brazil. Canadian Journal of Botany, 83, 54-65. https://doi.org/10.1139/b04-151

Pereira, O. L.; Rollemberg, C. L.; Borges, A. C.; Matsuoka, K.; Kasuya, M. C. M. 2003. Epulorhiza epiphytica sp. nov. isolated from mycorrhizal roots of epiphytic orchids in Brazil. Mycoscience, 44, 153-155. https://doi.org/10.1007/S10267-002-0087-7

Peterson, R. L.; Massicotte, H. B.; Melville, L. H. 2004. Mycorrhizas: anatomy and cell biology. NRC Research Press, Ottawa. 173p.

Peterson, R. L.; Uetake, Y.; Zelmer, C. 1998. Fungal symbioses with orchid protocorms. Symbiosis, 25, 29-55.

Porras-Alfaro, A.; Bayman, P. 2007. Mycorrhizal fungi of Vanilla: diversity, specificity and effects on seed germination and plant growth. Mycologia, 99, 510-525. https://doi.org/10.3852/mycologia.99.4.510

Rasmussen, H. N. 1995. Terrestrial orchids from seed to mycotrophic plant. Cambridge University Press, Cambridge. 444p.

Rasmussen, H. N.; Dixon, K. W.; Jersáková, J.; T?šitelová, T. 2015. Germination and seedling establishment in orchids: a complex of requirements. Annals of Botany, 116, 391-402. https://doi.org/10.1093/aob/mcv087

Reiter N.; Lawrie, A. C.; Linde, C. C. 2018. Matching symbiotic associations of an endangered orchid to habitat to improve conservation outcomes. Annals of Botany, 122, 947-959. https://doi.org/10.1093/aob/mcy094

Reiter, N.; Whitfield, J.; Pollard, G.; Bedggood, W.; Argall, M.; Dixon, K.; Davis, B.; Swarts, N. 2016. Orchid re-introductions: an evaluation of success and ecological considerations using key comparative studies from Australia. Plant Ecology, 217, 81-95. https://doi.org/10.1007/s11258-015-0561-x

Ronquist, F.; Teslenko, M.; Van der Mark, P.; Ayres, D.; Darling, A.; Höhna, S.; Larget, B.; Liu, L.; Suchard, M. A.; Huelsenbeck, J. P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539-542. https://doi.org/10.1093/sysbio/sys029

Rossman, A. Y.; Allen, W. C.; Braun, U.; Castlebury, L. A.; Chaverri, P.; Crous, P. W.; Hawksworth, D.; Hyde, K. D.; Johnston, P.; Lombard, L.; Romberg, M.; Samson, R. A.; Seifert, K. A.; Stone, J. K.; Udayanga, D.; White, J. F. 2016. Overlooked competing asexual and sexually typified generic names of Ascomycota with recommendations for their use or protection. IMA Fungus, 7, 289-308. https://doi.org/10.5598/imafungus.2016.07.02.09

Sasamori, M. H.; Endres Júnior, D.; Droste, A. 2015. Asymbiotic culture of Cattleya intermedia Graham (Orchidaceae): the influence of macronutrient salts and sucrose concentrations on survival and development of plantlets. Acta Botanica Brasilica, 29, 292-298. https://doi.org/10.1590/0102-33062014abb0054

Sathiyadash, K.; Muthukumar, T.; Murugan, S. B.; Sathishkumar, R.; Pandey, R. R. 2014. In vitro symbiotic seed germination of South Indian endemic orchid Coelogyne nervosa. Mycoscience, 55, 183-189. https://doi.org/10.1016/j.myc.2013.08.005

Selosse, M. A. 2014. The latest news from biological interactions in orchids: in love, head to toe. New Phytologist, 202, 337-340. https://doi.org/10.1111/nph.12769

Sharma, J.; Zettler, L. W.; Van Sambeek, J. W.; Ellersieck, M. R.; Starbuck, C. J. 2003. Symbiotic seed germination and mycorrhizae of federally threatened Platanthera praeclara (Orchidaceae). American Midland Naturalist, 149, 104-120. http://dx.doi.org/10.1674/0003-0031(2003)149[0104:SSGAMO]2.0.CO;2

Sommer, J.; Pausch, J.; Brundrett, M. C.; Dixon, K. W.; Bidartondo, M. I.; Gebauer, G. 2012. Limited carbon and mineral nutrient gain from mycorrhizal fungi by adult Australian orchids. American Journal of Botany, 99, 1133-1145. https://doi.org/10.3732/ajb.1100575

Stadler, M.; Kuhnert, E.; Peršoh, D.; Fournier, J. 2013. The Xylariaceae as model example for a unified nomenclature following the “One Fungus-One Name” (1F1N) concept. Mycology, 4, 5-21. https://doi.org/10.1080/21501203.2013.782478

Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312-1313. https://doi.org/10.1093/bioinformatics/btu033

Stewart, S. L.; Kane, M. E. 2006. Symbiotic seed germination of Habenaria macroceratitis (Orchidaceae), a rare Florida terrestrial orchid. Plant Cell, Tissue and Organ Culture, 86, 159-167. https://doi.org/10.1007/s11240-006-9104-4

Stewart, S. L.; Kane, M. E. 2007. Symbiotic seed germination and evidence for in vitro mycobiont specificity in Spiranthes brevilabris (Orchidaceae) and its implications for species-level conservation. In Vitro Cellular & Developmental Biology-Plant, 43, 178-186. https://doi.org/10.1007/s11627-006-9023-4

Stewart, S. L.; Zettler, L. W. 2002. Symbiotic germination of three semi-aquatic rein orchids (Habenaria repens, H. quinquiseta, H. macroceratitis) from Florida. Aquatic Botany, 72, 25-35. https://doi.org/10.1016/S0304-3770(01)00214-5

Suárez, 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. https://doi.org/10.1016/j.mycres.2006.08.004

Suwannarach, N.; Kumla, J.; Rachanarin, C.; Srimuang, K. 2021. In Vitro symbiotic seed germination of Epipactis flava (Orchidaceae) promoted by endophytic fungus, Tulasnella phuhinrongklaensis. Chiang Mai Journal of Science, 48, 787-792. https://epg.science.cmu.ac.th/ejournal/journal-detail.php?id=11502

Taylor, D. L.; Bruns, T. D.; Szaro, T. M.; Hodges, S. A. 2003. Divergence in mycorrhizal specialization within Hexalectris spicata (Orchidaceae), a nonphotosynthetic desert orchid. American Journal of Botany, 90, 1168-1179. https://doi.org/10.3732/ajb.90.8.1168

Taylor, D. L.; McCormick, M. K. 2008. Internal transcribed spacer primers and sequences for improved characterization of basidiomycetous orchid mycorrhizas. New Phytologist, 177, 1020–1033. https://doi.org/10.1111/j.1469-8137.2007.02320.x

Taylor, J. W. 2011. One Fungus = One Name: DNA and fungal nomenclature twenty years after PCR. IMA Fungus, 2, 113-120. https://doi.org/10.5598/imafungus.2011.02.02.01

T?šitelová, T.; Jersáková, J.; Roy, M.; Kubátová, B.; T?šitel, J.; Urfus, T.; Trávní?ek, P.; Suda, J. 2013. Ploidy-specific symbiotic interactions: Divergence of mycorrhizal fungi between cytotypes of the Gymnadenia conopsea group (Orchidaceae). New Phytologist, 199, 1022-1033. https://doi.org/10.1111/nph.12348

T?šitelová, T.; Kotilínek, M.; Jersáková, J.; Joly, F.-X.; Košnar, J.; Tatrenko, I.; Selosse, M.-A. 2015. Two widespread green Neottia species (Orchidaceae) show mycorrhizal preference for Sebacinales in various habitats and ontogenetic stages. Molecular Ecology, 24, 1122-1134. https://doi.org/10.1111/mec.13088

Van den Berg, C. 2020. Cattleya in Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. Available at: http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB11329. Access at: 22 March 2022.

Van Waes, J. M. 1987. Effect of activated charcoal on in vitro propagation of Western European orchids. Acta Horticulturae, 212, 131-138. https://doi.org/10.17660/ActaHortic.1987.212.21

Vu, D.; Groenewald, M.; de Vries, M.; Gehrmann, T.; Stielow, B.; Eberhardt, U.; Al-Hatmi, A.; Groenewald, J. Z.; Cardinal, G.; Houbraken, J.; Boekhout, T.; Crous, P. W.; Robert, V.; Verkley, G. J. M. 2019. Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Studies in Mycology, 92, 135-154. https://doi.org/10.1016/J.SIMYCO.2018.05.001

Warcup, J. H.; Talbot, P. H. B. 1980. Perfect states of rhizoctonias associated with orchids. III. New Phytologist, 86, 267-272. https://doi.org/10.1111/j.1469-8137.1980.tb00787.x

Waterman, R. J.; Bidartondo, M. I.; Stofberg, J.; Combs, J. K.; Gebauer, G.; Savolainen, V.; Barraclough, T.; Pauw, A. 2011 The effects of above- and belowground mutualisms on orchid speciation and coexistence. The American Naturalist, 177, 1-15. https://doi.org/10.1086/657955

Watkins, R. L. S. R. 2012. The biogeography, ecology and endophyte mycorrhiza of the New Zealand Corybas alliance (Orchidaceae) specifically: Nematoceras iridescens (Irwin et Molloy) Molloy, D.L.Jones & M.A.Clem. (species). Doctoral thesis, Massey University. Palmerston North, New Zealand. 243p.

Withner, C. L. 1988. The Cattleyas and their relatives. Volume I The Cattleyas. Timber Press, Portland. 147p.

Xing, X.; Jacquemyn, H.; Gai, X.; Gao, Y.; Liu, Q.; Zhao, Z.; Guo, S. 2019. The impact of life form on the architecture of orchid mycorrhizal networks in tropical forest. Oikos, 128, 1254-1264. https://doi.org/10.1111/oik.06363

Zettler, L. W. 1997. Terrestrial orchid conservation by symbiotic seed germination: techniques and perspectives. Selbyana, 18, 188-194.

Zettler, L. W.; Burkhead, J. C.; Marshall, J. A. 1999. Use of a mycorrhizal fungus from Epidendrum conopseum to germinate seed of Encyclia tampensis in vitro. Lindleyana, 14, 102-105.

Zettler, L. W.; Corey, L. L.; Jacks, A. L.; Gruender, L. T.; Lopez, A. M. 2013. Tulasnella irregularis (Basidiomycota: Tulasnellaceae) from roots of Encyclia tampensis in South Florida, and confirmation of its mycorrhizal significance through symbiotic seed germination. Lankesteriana, 13, 119-128. https://doi.org/10.15517/lank.v0i0.11552

Zettler, L. W.; Dvorak, C. J. 2021. Tulasnella calospora (UAMH 9824) retains its effectiveness at facilitating orchid symbiotic germination in vitro after two decades of subculturing. Botanical Studies, 62, 1-8. https://doi.org/10.1186/s40529-021-00321-w

Zettler, L. W.; Piskin, K. A. 2011. Mycorrhizal fungi from protocorms, seedlings and mature plants of the Eastern Prairie Fringed orchid, Platanthera leucophaea (Nutt.) Lindley: a comprehensive list to augment conservation. The American Midland Naturalist, 166, 29-39. https://doi.org/10.1674/0003-0031-166.1.29

Zettler, L. W.; Poulter, S. B.; McDonald, K. I. 2007. Conservation-driven propagation of an epiphytic orchid (Epidendrum nocturnum) with a mycorrhizal fungus. Hortscience, 42, 135-139. https://doi.org/10.21273/HORTSCI.42.1.135

Downloads

Publicado

2023-03-06

Como Citar

Endres Júnior, D., Alves-Silva, G. ., Sasamori, M. H., Silveira, R. M. B. da, & Droste, A. (2023). Successful Tulasnella amonilioides isolation from wild Cattleya intermedia and effectiveness of the mycobiont on in vitro propagation of this threatened Orchidaceae. Journal of Environmental Analysis and Progress, 8(1), 009–029. https://doi.org/10.24221/jeap.8.1.2023.5160.009-029