Anatomical and histochemical characterization of Dipteryx odorata and Taralea oppositifolia, two native Amazonian species

Abstract

Dipteryx odorata (Aubl.) Willd. and Taralea oppositifolia Aubl., Fabaceae: Dipterygeae, are two Amazonian species of great economic and pharmacological potential. The anatomy of these species, however, remains poorly studied. The aim of this work was to inventory leaf anatomical characteristics of D. odorata and T. oppositifolia and to locate and identify secretory structures and determine the main classes of metabolites they store. Vegetative branches were collected in Parque Ecológico de Gunma, Belém, state of Pará, Brazil. Some of the branches were destined for herborization while the remainder was submitted to standard protocols for anatomical analysis and histochemical tests. Both species were found to possess an unstratified epidermis, with D. odorata being amphistomatic and T. oppositifolia being hypostomatic, and dorsiventral mesophyll with spongy parenchyma and wide cellular space. The two species were also found to possess idioblasts and secretory cavities that produce a heterogeneous exudate consisting of polysaccharides, lipids, alkaloids and phenolic compounds. The species presented differences in leaf anatomy and chemical composition of the secretory structures, which may be useful in their differentiation.

References

  1. Almeida, E.F., Potiguara, R.C.V., Macedo, E.G., Lins, A.L.F., 2009. Anatomia foliar de espécies de Xylopia L. (Annonanaceae) ocorrentes no Parque Ecológico de Gunma, Santa Bárbara Estado do Pará. Bol. Mus. Para. Emílio Goeldi. Cienc. Nat. 4, 175–194.

    Google Scholar 

  2. Alves, C.Z., Godoy, A.R., Oliveira, N.C., 2012. Efeito da remoção da mucilagem na germinaçãoe vigor de sementes de Hylocereus undatus Haw. Rev. Bras. deCiênc. Agrar. 7, 586–589.

    Google Scholar 

  3. Araújo, M.G.P., Mendonça, M.S., 1998. Escleromorfismo foliar de Aldina heterophylla Spruce ex Benth (Leguminosae: Papilionoideae) em três campinas da Amazônia Central. Acta Amaz. 28, 353–371.

    Google Scholar 

  4. Barroso, G.M., Morim, M.P., Peixoto, A.L., Ichasso, CL., 1999. Frutos e sementes: morfologia aplicada à sistemática de dicotiledôneas. UFV, Viçosa, pp. 443p.

    Google Scholar 

  5. Bessa, D.T.O., Mendonça, M.S., Araújo, M.G.P., 2001. Morfo-anatômico de sementes de Dipteryx odorata (Aubl) Will. (Fabaceae) como contribuição ao estudo farmacognóstico de plantas da região. Rev. Acta Amaz. 31, 357–364.

    Google Scholar 

  6. Bozzola, J.J., Russel, L.D., 1991. Eletron Microscopy: principles and techniques for biologists. Jones and Barlett Publishers, Boston, London, Singapore.

    Google Scholar 

  7. Braga, F.G., Bouzada, M.L., Fabri, R.L., Matos, O.M., Moreira, F.O., Scio, E., Coimbra, E.S., 2007. Antileishmanial and antifungal activity of plants used in traditional medicine in Brazil. J. Ethnopharmacol. 111, 396–402.

    Google Scholar 

  8. Breitbach, U.B., Niehues, M., Lopes, N.P., Faria, J.Q., Brandão, M.G.L., 2013. Amazonian Brazilian medicinal plants described by C.F.P. Von Martius in the 19th century. J. Ethnopharmacol. 147, 180–189.

    PubMed  Google Scholar 

  9. Bukatsch, F., 1972. Bemerkungen Zur Doppelfarbung Astrablau-Safranin. Mikrokosmos. 61, 255.

    Google Scholar 

  10. Cain, A.J., 1947. The use of Nile blue in examination of lipoids. Q. J. Microsc. Sci. 33, 383–392.

    Google Scholar 

  11. Cardoso, D., Pennington, R.T., Queiroz, L.P., Boatwright, J.S., Van Wyk, B.E., Wojciechowski, M.F., Lavin, M., 2013. Reconstructing the deep-branching relationships of the papilionoid legumes. S. Afr.J. Bot. 89, 58–75.

    CAS  Google Scholar 

  12. Carlquist, S., 1961. Comparative Plant Anatomy. Holt, Rinchart and Winston, New York.

    Google Scholar 

  13. Carvalho, P.E.R., 2009. Cumaru-Ferro, Dipteryx odorata. In: Embrapa Florestas, Comunicado Técnico, n. 225, Colombo, PR. https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/578657/1/CT225.pdf, (Accessed 10 April 2019).

    Google Scholar 

  14. Coutinho, I.A.C., Rando, J.G., Conceição, A.S., Meira, R.M.S.A., 2016. A study of the morphoanatomical characters of Chamaecrista sect. Apoucouita. Acta Bot. Bras. 30, 205–222.

    Google Scholar 

  15. Cowan, J.M., 1950. The Rhododendron Leaf, a Study of the Epidermal Appendages. Oliverand Boyd, Edinburgo.

    Google Scholar 

  16. David, R., Carde, J.P., 1964. Coloration differentielle dês inclusions lipidique et ter- peniques des pseudophylles Du Pin maritime au moyen du resctif Nadi. Comptes Rendus de L’academie des Sciences Paris. 258, 1338–1340.

    CAS  Google Scholar 

  17. Duarte, M.R., Debur, M.C., 2003. Caracteres morfo-anatômicos de folha e caule de Bauhinia microstachya (Raddi) J. F. Macbr. (Fabaceae). Rev. Bras. Farmacogn. 13, 7–15.

    Google Scholar 

  18. Esau, K., 1997. Anatomy of Seed Plants. Jonh Wiley, New York.

    Google Scholar 

  19. Fahn, A., 1985. Anatomia Vegetal. Ediciones Pirámide S.A., Madrid.

    Google Scholar 

  20. Faria, S.M., Lima, H.C.L., 2002. Levantamento de nodulação em leguminosas arbóreas e arbustivas em áreas de influência da mineração Rio do Norte - Porto Trombetas/PA. In: Embrapa, Agrobiologia, Documentos 159. https://ainfo.cnptia.embrapa.br/digital/bitstream/CNPAB-2010/27941/1/doc159.pdf, (Accessed 10 April 2019).

    Google Scholar 

  21. Francisco, V.M.CR., 2010. Filogenia Molecular e Morfológica da Tribo Dipterygeae (Papilionoideae, Leguminosae). In: Rio de janeiro, Dissertacão de Mestrado, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro., pp. 91.

    Google Scholar 

  22. Franklin, G.L., 1945. Preparation ofthin sections of synthetic resins and wood-resin composites, and a new macerating method forwood. Nature 51, 24–39.

    Google Scholar 

  23. Furr, M., Mahlberg, P.G., 1981. Histochemical analyses of laticifers and glandular trichomes in Cannabis sativa. J. Nat. Prod. 44, 153–159.

    Google Scholar 

  24. Gasson, P., 1999. Wood anatomy of the tribe Dipterygeae with comments on related Papilionoid and Caesalpinioid Leguminosae. IAWAJ. 20, 441–455.

    Google Scholar 

  25. Herrero-Jáuregui, C., Sist, P., Casado, M.A., 2012. Population structure of two low-density neotropical tree species under different management systems. Forest Ecol. Manag. 280, 31–39.

    Google Scholar 

  26. High, O.B., 1985. Lipid Histochemistry. Oxford University Press, New York.

    Google Scholar 

  27. Johansen, D.A., 1940. Plant Microtechnique. Mcgraw-Hill, New York.

    Google Scholar 

  28. Kaiser, E., 1880. Verfahren zur herstellung einer tadellosen glycerin-gelatine. Botanisch Zentralb, Stuttgart 180, 25–26.

    Google Scholar 

  29. Lackey, JA., 1978. Leaflet anatomy of Phaseoleae (Leguminosae: papilionoideae) and its relation to taxonomy. Bot. Gaz. 139, 436–446.

    Google Scholar 

  30. Langenheim, J.H., 2003. Plant Resins: Chemistry, Evolution, Ecology and Ethnobotany. Timber Press, Portland, Cambridge.

    Google Scholar 

  31. Leal-Costa, M.V., Aragão, F.J.L., Reinert, F., Tavares, E.S., 2008. Anatomia foliar de plantas transgênicas e não transgênicas de Glycine max (L.) Merrill (Fabaceae). Rev. Biociênc. 14, 23–31.

    Google Scholar 

  32. Leelavathi, P., Ramayya, N., Prabhakar, M., 1980. Foliar stomatal distribution patterns in Leguminosae and their taxonomic significance. Phytomorphology 30, 195–204.

    Google Scholar 

  33. Leite, V.G., Mansano, V.F., Teixeira, S.P., 2014. Floral ontogeny in Dipterygeae (Fabaceae) reveals new insights into one of the earliest branching tribes in papilionoid legumes. Bot. J. Linn. Soc. 174, 529–550.

    Google Scholar 

  34. Lillie, R.D., 1965. Histopathologic Technic and Pratical Histochemistry, 3rd ed. McGraw Hill, New York.

    Google Scholar 

  35. Lima, A.K., Elba, L.C.A., Aquino, T.M., Lima, C.S.A., Pimentel, R.M.M., Higino, J.S., Albuquerque, U.P., 2003. Estudo farmacognóstico de Indigofera microcarpa Desv. (Fabaceae). Rev. Bras. Cienc. Farm. 39, 373–379.

    Google Scholar 

  36. Lucena, R.B., Rissi, D.R., Maia, L.A., Flores, M.F., Dantas, A.F.M., Nobre, V.M.T., Riet-Correa, F., Claudio, S.L., Barros, C.S.L., 2010. Intoxicação por alcaloides pirrolizidínicos em ruminantes e equinos no Brasil. Pesqui. Vet. Bras. 3, 447–452.

    Google Scholar 

  37. Lusa, M.G., Bona, C., 2009. Análise morfoanatômicacomparativada folhade Bauhinia forficata Link e Bauhinia variegata Linn. (Leguminosae, Caesalpinioideae). Acta Bot. Bras. 23, 196–211.

    Google Scholar 

  38. Mastroberti, A.A., Mariath, J.EA, 2008. Immunocytochemistry of the mucilage cells of Araucariaangustifolia (Bertol.) Kuntze (Araucariaceae). Rev. Bras. Bot. 31, 1–13.

    Google Scholar 

  39. Matos, F.J.A., Lorenzi, H., Santos, L.F.L., Matos, M.E.O., Silva, M.G.V., Sousa, M.P., 2011. Plantas Tóxicas: Estudo de Fitotoxicologia Química de Plantas Brasileiras. Plantarum, Flora, Nova Odessa.

    Google Scholar 

  40. McManus, J.F.A., 1946. Histological demonstration of mucin after periodic acid. Nature 158, 202–211, https://doi.org/10.1038/158202a0.

    PubMed  CAS  Google Scholar 

  41. Metcalfe, CR., Chalk, L., 1950. Anatomy of the Dicotyledons Leaves, Stem and Wood in Relation to Taxonomy With Notes on Economy Uses. Clarendon Press, Oxford.

    Google Scholar 

  42. Metcalfe, CR., Chalk, L., 1979. Anatomy of the Dicotyledons, 2nd ed. Claredon Press, Oxford.

    Google Scholar 

  43. Moreira-Coneglian, I.R., Oliveira, D.T., 2006. Anatomia comparada dos limbos cotiledonares e eofilares de dez espécies de Caesalpinoideae (Fabaceae). Rev. Bras. Bot. 29, 193–207.

    Google Scholar 

  44. Palermo, F.H., Teixeira, S.P., Mansano, V.F., Leite, V.G., Rodrigues, T.M., 2017. Secretory spaces in species of the clade Dipterygeae (Leguminosae, papilionoideae). Acta Bot. Bras. 31, 374–381.

    Google Scholar 

  45. Pearse, A.G.E., 1980. Histochemistry Theretical and Applied, 4 ed. Longman group Limited., Baltimore.

    Google Scholar 

  46. Pereira, L.B.S., Costa-Silva, R., Felix, L.P., Agra, M.F., 2018. Leaf morphoanatomy of “mororó” (Bauhinia and Schnella, Fabaceae). Rev. Bras. Farmacogn. 28, 383–392.

    Google Scholar 

  47. Pesce, C., 2009. Oleaginosas da Amazônia, 2nd ed. Museu Paraense Emílio Goeldi, Belém-PA http://repiica.iica.int/docs/B2252p/B2252p.pdf.

    Google Scholar 

  48. Pimentel, R.R., Machado, S.R., Rocha, J.F., 2011. EstruturassecretorasdePavoniaalni- folia (Malvaceae), uma espécie ameaçada de extinção. Rodrigusia 62, 253–262.

    Google Scholar 

  49. Pizzolato, T.D., Lillie, R.D., 1973. Mayer’s tannic acid-ferric chloride stain for mucins. J. Histochem. Cytochem. 21, 56–64.

    CAS  Google Scholar 

  50. Purvis, M.J., Collier, D.C., Walls, D., 1964. Laboratory Techniques in Botany. Butter-worths, London.

    Google Scholar 

  51. Ramalingam, S., Rajendran, S., Ganesan, P., Govindasamy, M., 2018. Effect of operating parameters and antioxidant additives with biodiesels to improve the performance and reducing the emissions in a compression ignition engine—a review. Renew. Sust. Energ. Rev. 81, 775–788.

    CAS  Google Scholar 

  52. Rocha, J.F., Pimentel, R.R., Machado, S.R., 2011. Estruturas secretoras de mucilagem em Hibiscus pernambucensis Arruda (Malvaceae): distribuição, caracterização morfoanatômica e histoquímica. Acta Bot. Bras. 25, 51–763.

    Google Scholar 

  53. Rodrigues, I.M.C., Souza Filho, A.P.S., Ferreira, F.A., Ilkiu-Borges, F., Gurgel, E.S.C., 2009. Anatomia e histoquímica das folhas de Senna alata. Planta Daninha 27, 515–526.

    Google Scholar 

  54. Silva, CM., Bolzan, A.A., Heinzmann, B.M., 2006. Alcalóides pirrolizidínicos em espécies do gênero Senecio. Quím. Nova. 29, 1047–1053.

    Google Scholar 

  55. Silva, M.S., Reis, C., Pontes-Pires, A.F.P., 2012. Anatomical characteristics of leaf of five species of family Fabaceae found in Sinop, MT. Sci. Electron. Arch. 1, 16–19.

    Google Scholar 

  56. Silva, N.F., Arruda, R.C.O., Alves, F.M., Sartori, A.L.B., 2018. Leaflet anatomy of the Dipterygeae clade (Faboideae: fabaceae): evolutionary implications and system-atics. Bot. J. Linn. Soc. 187, 99–117.

    Google Scholar 

  57. Simões, M.O.M., Lopes, P.S.N., Oliveira, M.N.S., Junior, E.M.F., Ribeiro, L.M., 2003. Estudoanatômicodomesofilo foliar de Albizia spp(Leguminosae/Mimosoideae). Rev. Unimontes Científica 5, 1–9.

    Google Scholar 

  58. Solereder, H., 1908. Systematic anatomy of the dicotyledons. Introduction, polypetalae, Gamopetalae. Oxford at the Carendon press.

    Google Scholar 

  59. Soriano, M., Kainer, K.A., Staudhammer, CL., Soriano, E., 2012. Implementing multiple forest management in Brazil nut-rich community forests: effects of logging on natural regeneration and forest disturbance. Forest Ecol. Manag. 268, 92–102.

    Google Scholar 

  60. Sousa, M.A.R., Moutinho, V.H.P., Silva, S.S., 2007. Levantamento das espécies comer-cializadas vernacularmente como cumaru no Estado do Pará. Rev. Bras. Biocienc. 5, 81–83.

    Google Scholar 

  61. Sudam, 1984. Atlas Climatológico da Amazônia Brasileira. SUDAM/PHCA, Belém.

    Google Scholar 

  62. Sverdsen, A.B., Verpoorte, R., 1983. Chromatography of Alkaloids. Elsevier Scientific Publish Company, New York.

    Google Scholar 

  63. Takemoto, E., Okada, I.A., Garbelotti, M.M., Tavares, M., Aued-Pimenel, S., 2001. Composição química da semente e do óleo de baru (Dipteryx alada Vog.) nativo domunicípiodePirenópolis, Estado de Goiás. Rev. Inst. Adolfo Lutz 60, 113–117.

    CAS  Google Scholar 

  64. Teixeira, S.P., Gabrielli, A.C., 2000. Anatomia de eixo vegetativo de Dahlstedtia pinna (Benth.) Malme e D. pentaphylla (Taub.) Burk (Leguminosae, Papilionoideae). Rev. Bras. Bot. 23, 1–11.

    Google Scholar 

  65. Thadeo, M., Meira, R.M.S.A., Azevedo, A.A., Araújo, J.M., 2009. Anatomia e histoquímica das estruturas secretoras da folha de Casearia decandra Jacq. (Salicaceae). Rev. Bras. Bot. 32, 329–338.

    Google Scholar 

  66. Tomlinson, P.B., 1969. Anatomy of the Monocotyledons III. Commelinales - Zingiberales. Clarendon press, Oxford.

    Google Scholar 

  67. Uchida, T., Campos, MA, 2000. Influência do sombreamento no crescimento de mudas de cumaru (Dipteryx odorata (Aubl.) Willd. Fabaceae), cultivadas em viveiro. Acta Amaz. 30, 107–114.

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Eduardo Oliveira Silva.

Additional information

Authors’ contributions

PMFS contributed in collecting plant samples, and conducted the laboratory work. PMFS, EOS and AISS wrote the text. MSCR and LMRC contributed to critical reading of the manuscript. All of the authors have read the final manuscript and approved its submission.

Rights and permissions

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

da Silva, P.M.F., Silva, E.O., de Rêgo, M.S.C. et al. Anatomical and histochemical characterization of Dipteryx odorata and Taralea oppositifolia, two native Amazonian species. Rev. Bras. Farmacogn. 29, 425–433 (2019). https://doi.org/10.1016/j.bjp.2019.05.004

Download citation

Keywords

  • Fabaceae
  • Idioblasts
  • Leaflet blade
  • Medicinal plants
  • Secretory structures