Anatomia comparada dos órgãos do sistema vegetativo de três espécies de Encyclia (Orchidaceae: Epidendroideae)
Comparative anatomy of the organs of the vegetative system of three Encyclia Hook species (Orchidaceae: Epidendroideae)
DOI:
https://doi.org/10.21826/2446-82312021v76e2021003Keywords:
Laeliinae, micromorphology, orchids, savannasAbstract
Encyclia comprises 150 species distributed in forest or savanic vegetations of the Americas. The anatomy of their vegetative organs is diversified and useful on taxonomic grounds. We aimed to describe the morphoanatomy of the vegetative system of Encyclia chapadensis L. C. Menezes, E. linearifolioides (Kraenzl.) Hoehne, and E. osmantha (Barb. Rodr.) Schltr., emphasizing these characters that are both, helpful to set them apart
and reflect the ecological conditions of their habitats. Some observed characters reflect adaptations to water restriction (hypostomatic leaves with hypodermis, roots with thick velamen, differentiated in endo and epivelamen, pseudobulbs with water- storage cells and thick cuticle) and mechanical reinforcement for support tissues (vascular bundles with fibers, presence of extravascular fibers and thickening in “fi” in the radicular cortex), indicating that some anatomical features reflect some abiotic conditions of the environment. The studied taxa can be differentiated through leaf, stem and root characters.
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Andreota, R.C., Barros, F. & Sajo, M.G. 2015. Root and leaf anatomy of some terrestrial representatives of the Cranichideae tribe (Orchidaceae). Brazilian Journal of Botany 38(2):367−378.
Baker, R.K. 1972. Foliar anatomy of the Laeliinae (Orchidaceae). Ph.D. dissertation, Washington University, St. Louis, Missouri, USA.
Barbosa-Rodrigues, J. 1882. Genera et species orchidearum novarum quas collegit, descripsit et iconibus illustravit 2: Adeneleuterophora - Rodriguezia. In: Genera et species orchidearum novarum 2. Typographia Nacional, Rio de Janeiro, p. 305.
Barbosa-Rodrigues, J. 1891. Genera et species orchidearum novarum. Vellosia 1:115−133.
Bastos, C.A., Meneguzzo, T.E.C. & van den Berg, C. 2015. Taxonomic notes on Brazilian Encyclia (Orchidaceae: Laeliinae). Phytotaxa 218:77−83.
Benzing, D.H. & Ott, D.W. 1981. Vegetative Reduction in Epiphytic Bromeliaceae and Orchidaceae: Its Origin and Significance. Biotropica 13(2):131−140.
Benzing, D.H., Ott, D.W. & Friedman, W.E. 1982. Roots of Sobralia macrantha (Orchidaceae): structure and function of the velamen-exodermis complex. American Journal of Botany 69:608−614.
Benzing, D.H. & Pridgeon, A.M. 1983. Foliar trichomes of Pleurothallidinae (Orchidaceae): functional significance. American Journal of Botany 70(2):173−180.
Benzing, D.H., Friedman, W.E., Peterson, G. & Renfrow, A. 1983. Shootlessness, velamentous roots, and the pre-eminence of Orchidaceae in the epiphytic biotope. American Journal of Botany 70:121−133.
Blanco, G.D. 2017. Estudo Etnobotânico e Morfoanatômico de espécies de Orchidaceae utilizadas por grupos Guaraní. Dissertação 155 f., Universidade Federal de Santa Catarina, Santa Catarina.
Bonates, L.C.M. 1993. Estudos ecofisiológicos de Orchidaceae da Amazônia. II-Anatomia ecológica foliar de espécies com metabolismo CAM de uma campina da amazônia central. Acta Amazonica 23:315−348.
Bonates, L.C.M. 2007. Anatomia ecológica da folha e da raíz e aspectos ecofisiológicos de Orchidaceae epífitas de uma campina da Amazônia Central. Tese 498 f., Universidade Federal do Amazonas, Amazonas.
Bray, C.M. & West, C.E. 2005. DNA repair mechanisms in plants: crucial sensors and effectors for the maintenance of genome integrity. New Phytologist 168:511–528.
Brighigma, L., Fiordi, A.C. & Palandri, M.R. 1984. Structural characteristics of mesophyll in some Tillandsia species. Phytomorphology 34:191−200.
Bukatsch, F. 1972. Bermerkungen zur Doppelfrbung Astrablau-Safranin. Mikrokosmos 61:255.
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.
Carlsward, B.S., Stern, W.L. & Bytebier, B. 2006. Comparative vegetative anatomy and systematics of the Angraecoids (Vandae, Orchidaceae) with an emphasis on the leafless habit. Botanical Journal of Linnean Society 151:165−218.
Carlsward, B.S. & Stern, W.L. 2009a. Comparative vegetative anatomy and systematics of Laeliinae (Orchidaceae). Botanical Journal of the Linnean Society 160:21−41.
Carlsward, B.S. & Stern, W.L. 2009b. Vegetative anatomy and systematics of Triphorinae (Orchidaceae). Botanical Journal of the Linnean Society 159:203−210.
Chamberlain, C.J. 1932. Methods in plant histology. 5 ed. University of Chicago Press, Chicago. 416 p.
Chomicki, G., Bidel, L.P.R., Ming, F., Coiro, M., Zhang, X., Wang, Y., Baissac, Y., Jay-Allemand, C., & Renner, S.S. 2014a. The velamen protects photosynthetic orchid roots against UV-B damage, and a large dated phylogeny implies multiple gains and losses of this function during the Cenozoic. New Phytologist 205:1330–1341.
Chomicki, G., Bidel, L.P.R. & Jay-Allemand, C. 2014b. Exodermis structure controls fungal invasion in the leafless epiphytic orchid Dendrophylax lindenii Lindl. Benth. ex Rolfe. Flora 209:88–94.
Christodoulakis, N.S. & Psaras, G.K. 1987. Stomata on the primary root of Ceratonia siliqua. Annals of Botany 60:295−297.
Cogniaux, A.C. 1898. Orchidaceae: Epidendrum. In: Flora brasiliensis 3(5). Typographia Regia (Martius, C.F.P., Eicher, A.G. & Urban, I. eds.), Munich, p. 29−185.
Costa, C.G. 1989. Morfologia e anatomia dos órgãos vegetativos em desenvolvimento de Marcgravia polyantha Delp. (Marcgraviaceae). Tese 227 f., Universidade de São Paulo, São Paulo.
Costa, N.M., Silva, N.A., Carvalho, R., Saoncella, A.L., Souza-Leal, T. & Pedroso-de-Moraes, C. 2012. Anatomia radicial de Oncidium flexuosum Sims. e Oncidium Sharry Baby (Orchidaceae). Natureza on line 10(4):179−182.
Dangat, B.T. & Gurav, R.V. 2016. Stomatal studies in the genus Habenaria (Orchidaceae). Richardiana 232−240.
Dearnaley, J.D.W. 2007. Further advances in orchid mycorrhizal research. Mycorrhiza 17:75−486.
Dettke, G.A., Sanches-Marques, A.M. & Milaneze-Gutierre, A. 2007. Anatomia vegetativa de três espécies de Maxillaria Ruiz et Pavón (Orchidaceae). Revista Brasileira de Biociências 5(1):531−533.
Dressler, R.L. 1993. Phylogeny and classification of the orchid family. Dioscorides Press, Portland. 330 p.
Dycus, A.M. & Knudson, L. 1957. The role of the velamen of the aerial roots of orchids. Botanical Gazette 119:78−87.
Eames, A.J. & MacDaniels, L.H. 1925. An introduction to plant anatomy. New York: McGraw-Hill Book Company. 364 p.
Einzmann, H.J.R., Schickenberg, N. & Zotz, G. 2019. Variation in root morphology of epiphytic orchids along small-scale and large-scale moisture gradients. Acta Botanica Brasilica 1−8.
Engard, C.J. 1944. Morphological identity of the velamen and exodermis in orchids. Botanical Gazette 105(4):457−462.
Esau, K. 1974. Anatomia das plantas com sementes. São Paulo: Edgard Blücher Ltda., São Paulo. 293 p.
Fernández-García, N., López-Berenguer, C. & Olmos, E. 2014. Role of phi cells under abiotic stress in plants. In: Root engineering (Morte, A. & Varma, A. eds.), Heidelberg: Springer, p. 23–37.
Figueroa, C., Salazar, G.A., Zavaleta, H.A. & Engleman, E.M. 2008. Root character evolution and systematics in Cranichidinae, Prescottiinae and Spiranthinae (Orchidaceae, Cranichideae). Annals of Botany 101:509−520.
Haberlandt, G.F.J. 1914. Physiological plant anatomy. Macmillan Co. London.
Haas, D.L., Carothers, Z.B. & Robbins, R.R. 1976. Observations on the phithickenings and casparian strips in Pelargonium roots. American Journal of Botany 63:863−867.
Holttum, R. 1955. Growth habitats of monocotyledons: variations on a theme. Phytomorphology 5:399−413.
Holtzmeier, M.A.N.N., Stern, W.L. & Judd, W.S. 1998. Comparative anatomy and systematics of Senghas’s cushion species of Maxillaria (Orchidaceae). Botanical Journal of Linnean Society 127:43−82.
Idris, N.A. & Collings, D.A. 2015. The life of phi: the development of phi thickenings in roots of the orchids of the genus Miltoniopsis. Planta 241:489−506.
Jansen, M.A., Gaba, V. & Greenberg, B.M. 1998. Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends in Plant Science 3:131–135.
Joca, T.A.C., Oliveira, D.C., Zotz, G., Winkler, U., & Moreira, A.S.F.P. 2017. The velamen of epiphytic orchids: Variation in structure and correlations with nutrient absorption. Flora 230:66−74.
Joca, T.A.C., Oliveira, D.C., Zotz, G., Cardoso, J.C.F. & Moreira, A.S.F.P. 2020. Chemical composition of cell walls in velamentous roots of epiphytic Orchidaceae. Protoplasma 257:103−118.
Johansen, D.A. 1940. Plant microtechnique. McGraw-Hill Book Co., New York.
Kedrovski, H.R. 2014. Anatomia radicular de espécies da subtribo Pleurothallidinae (Orchidaceae). Dissertação 113 f., Universidade Federal de Santa Catarina, Santa Catarina.
Krahl, A.H., Holanda, S.S., Krahl, D.R.P., Correa, M.M., Oliveira, R.L.C. & Valsko, J.J. 2013. Anatomia foliar de Ananas lucidus Mill. (Bromeliaceae). Natureza on line 11(4):161−165.
Krahl, A.H. & Krahl, D.R.P. 2017. Anatomia foliar de Orleanesia yauaperyensis Barb. Rodr. (Orchidaceae). Biota Amazônia 7(4):63−65.
Kraus, B.H. 1949. Anatomy of vegetative organs of the pineapple Ananas comosus (L.) Merr. II. The leaf. Botanical Gazette 110(3):303−404.
Kraus, J.E. & Arduin, M. 1997. Manual básico de métodos em morfologia vegetal. EDUR (Editora Universidade Rural), Rio de Janeiro. 198 p.
Kurzweil, H., Linder, H.P., Stern, W.L. & Pridgeon, A.M. 1995. Comparative vegetative anatomy and classification of Diseae (Orchidaceae). Botanical Journal of the Linnean Society 117:171−220.
Leite, V.M.C. & Oliveira, P.L. 1987. Morfo-anatomia foliar de Cattleya intermedia (Orchidaceae). Napea 2:1−10.
Madison, M. 1977. Vascular epiphytes: their systematic occurrence and salient features. Selbyana 2 (1):1−13.
Mackenzie, K.A.D. 1979. The development of the endodermis and phi layer of apple roots. Protoplasma 100:21−32.
Melville, L.H., Massicote, H.B. & Peterson, R.L. 1987. Ontogeny of early stages of ectomycorrhizae synthesized between Dryas integrifolia and Hebeloma cylindrosporum. Botanical Gazette 148:332−341.
Meneguzzo, T.E.C., Bianchetti, L.B. & Proença, C.E.B. 2012. O gênero Encyclia (Orchidaceae) no Distrito Federal, Goiás e Tocantins. Rodriguésia 63:277−292.
Mohana Rao, P.R. & Khasim, S.M. 1987. Anatomy of three species of Bulbophyllum (Orchidaceae) with comments on their ecological adaptability and taxonomy. Proceedings Indian Academy Sciences (Plant Science) 97:391−397.
Moreira, A.S.F.P. & Isaias, R.M.S. 2008. Comparative anatomy of the absorption roots of terrestrial and epiphytic orchids. Brazilian Archives of Biology and Technology 51:83−93.
Moreira, A.S.F.P., Fuhro, D. & Isaias, R.M.S. 2008. Anatomia floral de Epidendrum fulgens Brongn. (Orchidaceae—Epidendroideae) com ênfase no nectário e sua funcionalidade. Revista de Biologia Neotropical 5(1):23–29.
Moreira, A.S.F.P., Filho, J.P.L., Zotz, G. & Isaias, R.M.S. 2009. Anatomy and photosynthetic parameters of roots and leaves of two shade-adapted orchids, Dichaea cogniauxiana Shltr. and Epidendrum secundum Jacq. Flora 204:604–611.
Möbius, M. 1887. Über den anatomischen Bau der Orchideenblätter und dessen Bedeutung für das System dieser Familie. Jahrbücher für Wissenschaftliche Botanik 18:530−607.
Noguera-Savelli, E. & Jáuregui, D. 2011. Anatomía foliar comparada y relaciones filogenéticas de 11 especies de Laeliinae con énfasis en Brassavola (Orchidaceae). Revista de Biología Tropical 59(3):1047−1059.
Oliveira, V.C. & Sajo, M.G. 1999. Anatomia foliar de espécies epífitas de Orchidaceae. Revista Brasileira de Botânica 22:365−374.
Oliveira, V.C. & Sajo, M.G. 2001. Morfo-anatomia caulinar de nove espécies de Orchidaceae. Acta Botanica Brasilica 15(2):177−188.
Oudemans, C. 1861. Ueber den Sitz der Oberhaut bei den Luftwurzeln der Orchideen. Verh Kon Ned Akad Wetensch 9:1−32.
Pan, C.X., Nakao, Y. & Nii, N. 2006. Anatomical development of phi thickening and the Casparian strip in loquat roots. Journal of the Japanese Society for Horticultural Science 75:445−449.
Parrilla Díaz, A.T. & Ackerman, J.D. 1990. Epiphyte roots: anatomical correlates to environmental parameters in Puerto Rican orchids. Orquídea 12(1):105−116.
Passioura, J.B. 1988. Water transport in and to roots. Annual Review of Plant Physiology and Plant Molecular Biology 39:245−265.
Pereira, O.L., Rollemberg, C.L. & Kasuya, M.C.M. 2003. Association des mycorhizies dans les orchidees - perspectives d‘utilisation dans les programmes de propagation symbiotique. Orchidees 55:24−27.
Pereira, O.L., Kasuya, M.C.M., Rollemberg, C.L. & Chaer, G.M. 2005. Isolamento e identificação de fungos micorrízicos rizoctonióides associados a três espécies de orquídeas epífitas neotropicais no Brasil. Revista Brasileira de Ciências do Solo 29:191−197.
Peterson, C.A., Emanuel, M.E. & Weerdenburg, C.A. 1981. The permeability of phi thickenings in apple (Pyrus malus) and geranium (Pelargonium hortorum) roots to an apoplastic fluorescent dye tracer. Canadian Journal of Botany 59:1107−1110.
Peterson, R.L., Uetake, Y. & Zelmer, C. 1998. Fungal symbioses with orchid protocorms. Symbiosis 25:29−55.
Piazza, L.D., Smidt, E.C. & Bona, C. 2015. Anatomia comparada dos órgãos vegetativos de espécies de Bulbophyllum seção Didactyle (Lindl.) Cogn. e Bulbophyllum seção Xiphizusa Rchb.f. (Orchidaceae). Hoehnea 42(1):171−183.
Pires, M.F.O., Semir, J., Pinna, G.F.M. & Felix, L.P. 2003. Taxonomic separation of the genera Prosthechea and Encyclia (Laeliinae: Orchidaceae) using leaf and root anatomical features. Botanical Journal of the Linnean Society 143:293−303.
Porembski, S. & Barthlott, W. 1988. Velamen radicum micromorphology and classification of Orchidaceae. Nordic Journal of Botany 8:117−137.
Pratikakis, E., Rhizopoulou, S. & Psaras, G.K. 1998. A phi layer in roots of Ceratonia siliqua L. Botanica Acta 111:93−98.
Pridgeon, A.M., Stern, W.L. & Benzing, D.H. 1983. Tilosomes in roots of Orchidaceae: morphology and systematic occurrence. American Journal of Botany 70(9):1365−1377.
Pridgeon, A.M. 1986. Anatomical adaptations in Orchidaceae. Lindleyana 1:90−101.
Pridgeon, A.M. 1987. The velamen and exodermis of orchid roots. In: Orchid biology: reviews and perspectives IV (Arditti, J. ed.). Cornell University Press, Ithaca, p. 139−192.
Pupulin, F. & Bogarín, D. 2012. A taxonomic revision of Encyclia (Orchidaceae: Laeliinae) in Costa Rica. Botanical Journal of the Linnean Society 168:395−448.
Ramírez, M., Niño, S. & Berrío, T. 2016. Anatomía de la raíz de Encyclia cordigera (Kunth) Dressler (Orchidaceae). Revista Unellez de Ciencia y Tecnología 34:58−61.
Ribeiro, J.P.O., Paula-Souza, J. & Silva, C.J. 2020. Morphoanatomy of vegetative organs of two species of Cattleya (Orchidaceae) native to Brazil. Rodriguésia 71:e01672017.
Rosa-Manzano, E., Andrade, J.L., Zotz, G. & Reyes-García, C. 2014. Respuestas fisiológicas a la sequía, de cinco especies de orquídeas epífitas, en dos selvas secas de la Península de Yucatán. Botanical Sciences 92(4):607−616.
Rasmussen, H. 1987. Orchid stomata - structure, differentiation, function, and phylogeny. In: Orchid biology: reviews and perspectives, IV (Arditti, J. ed.). Cornell University Press, New York. 105–138 p.
Rosso, S.W. 1966. The vegetative anatomy of the Cypripedioideae (Orchidaceae). Botanical Journal of the Linnean Society 59:309–341.
Saoncella, A.L., Marteline, M.A. & Pedroso-de-Moraes, C. 2017. Anatomia dos órgãos vegetativos de Cattleya violacea (Kunth) Rolfe (Orchidaceae). Iheringia, Série Botânica 72(1):114−126.
Sass, J.E. 1951. Botanical Microtechnique. 2ª ed. Ames, The Iowa State College Press, Iowa. 391 p.
Scatena, V.L. & Nunes, A.C. 1996. Anatomia de Pleurothallis rupestris. Lindl. (Orchidaceae) dos campos rupestres. Boletim de Botânica da Universidade de São Paulo 15:35−43.
Silva, C.I. & Milaneze-Gutierre, M.A. 2004. Caracterização morfoanatômica dos órgãos vegetativos de Cattleya walkeriana Gardner (Orchidaceae). Acta Scientiarum. Biological Sciences 26(1):91−100.
Silva, I.V., Meira, R.M.S.A., Azevedo, A.A. & Euclydes, R.M.A. 2006. Estratégias anatômicas foliares de treze espécies de Orchidaceae ocorrentes em um campo de altitude no Parque Estadual da Serra do Brigadeiro (PESB) - MG, Brasil. Acta Botanica Brasilica 20(3):741−750.
Sinha, R.P. & Häder, D.P. 2002. UV-induced DNA damage and repair: a review. Photochemical & Photobiological Sciences 1:225–236.
Solereder, H. & Meyer, F. 1930. Systematische Anatomie der Monokotyledonen. 6:92–242.
Staebner, A.N. 2012. The functional anatomy of aerial roots in orchids. Bachelorarbeit. 43 f., Universität Oldenburg, Alemanha.
Stern, W.L. & Morris, M.W. 1992. Vegetative anatomy of Stanhopea (Orchidaceae) with special reference to pseudobulb water-storage cells. Lindleyana 7:34−53.
Stern, W.L., Cheadle, V.I. & Thorsch, J. 1993a. Apostasiads, systematic anatomy, and the origins of Orchidaceae. Botanical Journal of the Linnean Society 111:411−455.
Stern, W.L., Aldrich, H.C., McDowell, L.M., Morris, M.W. & Pridgeon, A.M. 1993b. Amyloplasts from cortical root cells of Spiranthoideae (Orchidaceae). Protoplasma 172:49−55.
Stern, W.L., Morris, M.W., Judd, W.S., Pridgeon, A.M. & Dressler, R.L. 1993c. Comparative vegetative anatomy and systematics of Spiranthoideae (Orchidaceae). Botanical Journal of the Linnean Society 113:161−197.
Stern, W.L. & Judd, W.S. 2001. Comparative anatomy and systematics of Catasetinae (Orchidaceae). Botanical Journal of the Linnean Society 136:153−178.
Stern, W.L., Judd, W. & Carlsward, B.S. 2004. Systematic and comparative anatomy of Maxillarieae (Orchidaceae), sans Oncidiinae. Botanical Journal of the Linnean Society 144:251−274.
Stern, W.L. & Carlsward, B.S. 2006. Comparative vegetative anatomy and systematics of the Oncidiinae (Maxillarieae, Orchidaceae). Botanical Journal of the Linnean Society 152:91−107.
Stern, W.L. & Carlsward, B.S. 2009. Comparative vegetative anatomy and systematics of Laeliinae (Orchidaceae). Botanical Journal of the Linnean Society 160:21−41.
Stern, W.L. 2014. Anatomy of the Monocotyledons: X. Orchidaceae. University Press, Oxford. 288 p.
Takane, R.J., Yanagisawa, S.S. & Pivetta, K.F.L. 2010. Cultivo moderno de orquídeas: Cattleya e seus híbridos. Universidade Federal do Ceará, 179 p.
Thorsch, J. & Stern, W.L. 1997. Tracheary studies and the terrestrial ancestry of Orchidaceae. International Journal of Plant Sciences 158(2):222−227.
van den Berg, C., Higgins, W.E., Dressler, R.L., Whitten, W.M., Soto-Arenas, M.A. & Chase, M.W. 2009. A phylogenetic study of Laeliinae (Orchidaceae) based on combined nuclear and plastid DNA sequences. Annals of Botany 104:417−430.
Van Tieghgem, P. 1888. Le réseau de soutien de l’ecorce de la racine. Annales des Sciences Naturelles, Botanique Series 7/8:375−378.
Van Tieghem, P. 1871. Recherches sur la symetrie de structure des plantes vasculaires. Annales des Sciences Naturelles, Botanique Series 13:3−315.
Vieira, A.C.M., Lainetti, R. & Soares, A.P.C. 2000. Estudos farmacognósticos do Sumaré - Cyrtopodium paranaense Schltr. (Orchidaceae). Revista Brasileira de Farmacologia 81:11−13.
Weerdenburg, C.A. & Peterson, C.A. 1983. Structural changes in phi thickenings during primary and secondary growth in roots. 1. Apple (Pyrus malus) Rosaceae. Canadian Journal of Botany 61:2570−2576.
Weltz, M. 1897. Zur Anatomie der monandrischen sympodialen Orchideen. PhD Thesis 65 f., University of Heidelberg, Alemanha.
Williams, C.A. 1979. The leaf flavonoids of the Orchidaceae. Phytochemistry 18:803−813.
Withner, C.L., Nelson, P.K. & Wwjksnora, P.J. 1974. The anatomy of orchids. In: The orchids: scientific studies (Withner, C.L. ed.). John Wiley Co, New York, p. 267−334.
Yim, B., Smalla, K. & Winkelmann, T. 2013. Evaluation of apple replant problems based on different soil disinfection treatments-links to soil microbial community structure? Plant and Soil 366:617−631.
Yukawa, T. & Stern, W.L. 2002.Comparative vegetative anatomy and systematics of Cymbidium (Cymbidieae: Orchidaceae). Botanical Journal of the Linnean Society 138:383−419.
Zanenga-Godoy, R. & Costa, C.G. 2003. Anatomia foliar de quatro espécies do gênero Cattleya Lindl. (Orchidaceae) do Planalto Central Brasileiro. Acta Botanica Brasilica 17(1):101−118.