ABSTRACT
The leaves extracts of some species of Bauhinia L. s.l. are consumed to treat diabetes, inflammation, pains and several disorders in traditional medicine in austral South America. Despite its wide use and commercialization, sale is not controlled, and botanical quality of samples is not always adequate because of plant misidentification and adulteration. Here, we characterized leaf vein pattern in nineteen taxa to contribute to the recognition and commercial quality control of plant material commercially available. The vein characters intercostal tertiary and quinternary vein fabric, areole development and shape, free ending veinlet branching and marginal ultimate venation allowed to distinguish the main medicinal species in the region.
Keywords:
Areolation; Botanical identification; Freely ending veinlets; Leaf venation pattern; Quality control; Schnella
Introduction
The leaves extracts of some species of Bauhinia L., Fabaceae, so called cow's hoof, "pata-de–vaca", cow's paw or orchid trees, are consumed to treat diabetes, inflammation, pains and several disorders in traditional medicine in austral South America (Oliveira and Saito, 1989Oliveira, F., Saito, M.L., 1989. Alguns vegetais brasileiros empregados no tratamento da diabetes. Rev. Bras. Farmacogn. 2–4, 170-196.; Bortoluzzi et al., 2006Bortoluzzi, R.L.C., Miotto, S.T.S., Reis, A., 2006. Bauhinia. In: Reis, A. (org.), Flora Ilustrada Catarinense, vol. 2. Herbário Barbosa Rodrigues, Itajaí, pp. 29–67.; Barboza et al., 2009Barboza, G.E., Cantero, J.J., Núñez, C., Pacciaroni, A., Espinar, L.A., 2009. Medicinal plants: a general review and a phytochemical and ethnopharmacological screening of the native Argentine Flora. Kurtziana 34, 7-365.; Pizziolo et al., 2011Pizziolo, V.R., Brasileiro, B.G., Oliveira, T.T., Nagem, T.J., 2011. Plantas com possível atividade hipolipidêmica: uma revisão bibliográfica de libros editados no Brasil entre 1998 e 2008. Rev. Bras. Pl. Med. 13, 98-109.; Fortunato, 2012Fortunato, R.H., (Ph.D. thesis) 2012. Género Bauhinia (Caesalpinioideae, Leguminosae) en Austroamérica: caracterización taxonómica, diferenciación morfológica y usos populares. Universidad Nacional de Buenos Aires, Buenos Aires, 238 p.). With 300 species worldwide, Bauhinia s.l. is represented by fifteen species in Argentina, Paraguay, Uruguay and Santa Catarina, Paraná and Rio Grande do Sul states of Brazil (Fortunato, 1986Fortunato, R.H., 1986. Revisión del género Bauhinia (Cercideae, Caesalpinioideae, Fabaceae). Darwiniana 27, 527-557., 1996Fortunato, R.H., 1996. Bauhinia affinis (Fabaceae) una nueva cita para la Flora Argentina. Darwiniana 34, 405-409.; Fortunato et al., 2008Fortunato, R.H., Miotto, S., Izaguirre, P., Beyhaut, R., Bortoluzzi, R.L.C., Ulibarri, E., Gómez-Sosa, E., 2008. Fabaceae. In: Zuloaga, F.O., Morrone, O., Belgrano, M.J. (org.), Catálogo de las Plantas Vasculares del Cono Sur. Monog. Syst. Bot. 107, 2078–2319.; Vaz et al., 2010Vaz, A.M.S.F., Bortoluzzi, R.L.C., Silva, L.A.E., 2010. Checklist of Bauhinia sensu stricto (Caesalpiniaceae) in Brazil. Plant Ecol. Evol. 143, 212-221.).
Bauhinia bauhinioides (Mart.) J.F.Macbr., B. microstachya (Raddi) J.F.Macbr., B. ungulata L., B. holophylla (Bong.) Steud., B. forficata Link, B. cheilantha (Bong.) Steud. and B. rufa (Bong.) Steud. are the main species for which pharmacological activities have been reported. Hypoglycemic, antioxidant, analgesic, antiinflammatory and larvicidal activities along with antitumor potentiality let them auspicious targets for new bioactive substances researching and phytotherapy (Silva and Cechinel Filho, 2002Silva, K.L., Cechinel Filho, V., 2002. Plantas do gênero Bauhinia: composição química e potencial farmacológico. Quim. Nova 25, 449-454.; Sousa et al., 2004Sousa, E., Zanatta, L., Seifriz, I., Creczynski-Pasa, T.B., Pizzolatti, M.G., Szpoganicz, B., Silva, F.R.M.B., 2004. Hypoglycemic effect and antioxidant potential of kaempferol-3,7-O-(α)-dirhamnoside from Bauhinia forficata leaves. J. Nat. Prod. 67, 829-832.; Gadotti et al., 2005Gadotti, V.M., Santos, A.R., Meyre-Silva, C., Schmeling, L.O., Machado, C., Liz, F.H., 2005. Antinociceptive action of the extract and the flavonoid quercitrin isolated from Bauhinia microstachya leaves. J. Pharm. Pharmacol. 57, 1345-1351.; Luna et al., 2005Luna, J.D.S., Santos, A.F., Lima, M.R.F., Omena, M.C., Mendonça, F.A.C., Bieber, L.W., Sant'Ana, A.E.G., 2005. A study of the larvicidal and molluscicidal activities of some medicinal plants from northeast Brazil. J. Ethnopharmacol. 97, 199-206.; Nakahata et al., 2006Nakahata, A.M., Bueno, N.R., Rocha, H.A., Franco, C.R., Chammas, R., Nakaie, C.R., Jasiulionis, M.G., Nader, H.B., Santana, L.A., Sampaio, M.U., Oliva, M.L.V., 2006. Structural and inhibitory properties of a plant proteinase inhibitor containing the RGD motif. Int. J. Biol. Macromol. 40, 22-29.; Cechinel Filho, 2009Cechinel Filho, V., 2009. Chemical composition and biological potential of plants from the genus Bauhinia. Phytother. Res. 23, 1347-1354.; Paula et al., 2014Paula, C.D.S., Canteli, V.C.D., Hirota, B.C.K., Campos, R., Oliveira, V.B.D., Kalegari, M., Silva, C.B., Silva, G.M., Miguel, O.G., Miguel, M.D., 2014. Potencial antioxidante in vitro das folhas da Bauhinia ungulata L. Rev. Cien. Farm. Bas. Apl. 35, 217-222.; Rozza et al., 2015Rozza, A.L., Cesar, D.A.S., Pieroni, L.G., Saldanha, L.L., Dokkedal, A.L., De-Faria, F.M., Souza-Brito, A.R.M., Vilegas, W., Takahira, R.K., Pellizzon, C.H., 2015. Antiulcerogenic activity and toxicity of Bauhinia holophylla hydroalcoholic extract. Evid.-Based Complement. Alternat. Med., http://dx.doi.org/10.1155/2015/439506.
http://dx.doi.org/10.1155/2015/439506...
; Martins-Olivera et al., 2016Martins-Olivera, B.T., Almeida-Reis, R., Theodoro-Júnior, O.A., Oliva, L.V., Santos Nunes, N.N., Olivo, C.R., Brito, M.V., Prado, C.M., Leick, E.A., Arruda Martins, M., Oliva, M.L.V., Righetti, R.F., Tibério, I.F.L.C., 2016. The plant-derived Bauhinia bauhinioides kallikrein proteinase inhibitor (rBbKI) attenuates elastase-induced emphysema in mice. Mediat. Inflamm., http://dx.doi.org/10.1155/2016/5346574.
http://dx.doi.org/10.1155/2016/5346574...
).
These taxa are extensively employed and sold in native American, rural and urban communities in the region and surrounding areas (Bortoluzzi et al., 2006Bortoluzzi, R.L.C., Miotto, S.T.S., Reis, A., 2006. Bauhinia. In: Reis, A. (org.), Flora Ilustrada Catarinense, vol. 2. Herbário Barbosa Rodrigues, Itajaí, pp. 29–67.; Barboza et al., 2009Barboza, G.E., Cantero, J.J., Núñez, C., Pacciaroni, A., Espinar, L.A., 2009. Medicinal plants: a general review and a phytochemical and ethnopharmacological screening of the native Argentine Flora. Kurtziana 34, 7-365.; Hurrell et al., 2011Hurrell, J.A., Ulibarri, E.A., Puentes, J.P., Buet Costantino, F., Arenas, P.M., Pochettino, M.L., 2011. Leguminosas medicinales y alimenticias utilizadas en la conurbación Buenos Aires – La Plata, Argentina. Bol. Latinoam. Caribe 10, 443-455.; Ibarrola and Degen de Arrúa, 2011Ibarrola, D.A., Degen de Arrúa, R.L., 2011. Catálogo Ilustrado de 80 Plantas Medicinales del Paraguay. Facultad de Ciencias Químicas – UNA, Agencia de Cooperación International del Japón (JICA), Asunción.). Despite its wide use and commercialization, sale is not controlled, and botanical quality of samples is not always adequate because of plant misidentification and adulteration. Commercial samples – crude herbs or industrialized herbal medicines – include entire or broken dried leaves, stems and often pods. In general, plants are harvested from their natural habitats, being popularly recognized by their bilobed or bifoliolate leaves. Species are difficult to identify, especially from vegetative stages or in fragmented material, and sample labeling and trading are mostly accomplished by using common names, generic name or incorrect names (Melo et al., 2004Melo, J.G., Nascimento, V.T., Amorim, E.L.C., Andrade Lima, C.S., Albuquerque, U.P., 2004. Avaliação da qualidade de amostras comerciais de boldo (Peumus boldus Molina), pata-de-vaca (Bauhinia spp.) e ginco (Ginkgo biloba L.). Rev. Bras. Farmacogn. 14, 111-120.). These often result in adulterated, falsified or substitute samples, which would interfere with the effectiveness and even the safety of the product (Ferreres et al., 2012Ferreres, F., Gil-Izquierdo, A., Vinholes, J., Silva, S.T., Valentão, P., Andrade, P.B., 2012. Bauhinia forficata Link authenticity using flavonoids profile: relation with their biological properties. Food Chem. 134, 894-904.). Leaf anatomical features are useful for identification and adequate sample botanical quality, in Bauhinia s.l., venation pattern has been utilized in taxonomy, phylogenetic analyses and even in palaeobotany (Vaz, 1979Vaz, A.M.S.F., 1979. Considerações sobre a taxonomia do gênero Bauhinia L. sect. Tylotaea Vogel (Leguminosae – Caesalpinioideae) do Brasil. Rodriguésia 31, 127-234.; Fortunato, 1986Fortunato, R.H., 1986. Revisión del género Bauhinia (Cercideae, Caesalpinioideae, Fabaceae). Darwiniana 27, 527-557.; Zhang, 1994Zhang, D., 1994. Leaf venation of Cercideae. J. Trop. Subtrop. Bot. 2, 45-57.; Lin et al., 2015Lin, Y., Wong, W.O., Shi, G., Shen, S., Li, Z., 2015. Bilobate leaves of Bauhinia (Leguminosae, Caesalpinioideae, Cercideae) from the middle Miocene of Fujian Province, southeastern China and their biogeographic implications. BMC Evol. Biol. 15, http://dx.doi.org/10.1186/s12862-015-0540-9.
http://dx.doi.org/10.1186/s12862-015-054...
).
In this work, we contribute to the recognition and commercial quality control of austral South American medicinal Bauhinia through a study of leaf vein pattern.
Materials and methods
We analyzed 19 austral South American taxa (Appendix 1 Appendix A Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.bjp.2016.10.007. ). The study of leaf venation pattern was carried out following Ellis et al. (2009)Ellis, B., Daily, D.C., Hickey, L.J., Johnson, K.R., Mitchell, J.D., Wilf, P., Wing, S.L., 2009. Manual of Leaf Architecture. Cornell University Press, New York.. For this, fresh or herbarium leaves were cleared according to Dizeo de Strittmatter (1973)Dizeo de Strittmatter, C.G., 1973. Nueva técnica de diafanización. Bol. Soc. Argent. Bot. 15, 126-129. and stained in safranin/80% ethanol. Samples were mounted in DPX (Aldrich Chemical Company, Gillingham, UK) and examined using Zeiss Stereo Microscope a Zeiss Axiolab light microscope (Carl Zeiss, Germany) with a trinocular phototube and a color digital imaging camera. Some venation data were extracted from previous work (Fortunato, 1986Fortunato, R.H., 1986. Revisión del género Bauhinia (Cercideae, Caesalpinioideae, Fabaceae). Darwiniana 27, 527-557., 1996Fortunato, R.H., 1996. Bauhinia affinis (Fabaceae) una nueva cita para la Flora Argentina. Darwiniana 34, 405-409.).
Results and discussion
All taxa analyzed present basal actinodromous primary vein framework, with no naked basal veins, 3–5 (7) basal veins per lobe or leaflet and agrophic veins simple (Fig. 1A and B). Previously, some of these taxa have been described as acrodromous (Fortunato, 1986Fortunato, R.H., 1986. Revisión del género Bauhinia (Cercideae, Caesalpinioideae, Fabaceae). Darwiniana 27, 527-557., 1996Fortunato, R.H., 1996. Bauhinia affinis (Fabaceae) una nueva cita para la Flora Argentina. Darwiniana 34, 405-409.) or campylodromous (Vaz, 1979Vaz, A.M.S.F., 1979. Considerações sobre a taxonomia do gênero Bauhinia L. sect. Tylotaea Vogel (Leguminosae – Caesalpinioideae) do Brasil. Rodriguésia 31, 127-234.), and recently both American Bauhinia s. s. and Schnella are considered actinodromous or acrodromous by Lin et al. (2015)Lin, Y., Wong, W.O., Shi, G., Shen, S., Li, Z., 2015. Bilobate leaves of Bauhinia (Leguminosae, Caesalpinioideae, Cercideae) from the middle Miocene of Fujian Province, southeastern China and their biogeographic implications. BMC Evol. Biol. 15, http://dx.doi.org/10.1186/s12862-015-0540-9.
http://dx.doi.org/10.1186/s12862-015-054...
. Main vein characters (Fig. 1, Table 1) provide a criterion to identification of medicinal species and detection of falsifications or adulteration. The areole development allows differentiating three main groups, some of them, but not all, taxonomically related.
Leaf venation in southern South American Bauhinia. (A and B) General vein pattern. (C–G, I–P, R and S) Areolation. (H and Q) Looped marginal ultimate venation. (A) B. bauhinioides. (B) B. hagenbeckii. (C) Bauhinia affinis. (D) B. angulosa. (E) B. argentinensis. (F) B. bauhinioides. (G and H) B. campestris. (I) B. cheilantha. (J) B. forficata ssp. pruinosa. (K) B. hagenbeckii. (L) B. holophylla. (M) B. microstachya. (N) B. mollis var. mollis. (O) B. mollis var. notophila. (P and Q) B. rufa. (R) B. ungulata var. ungulata. (S) B. uruguayensis. Arrowhead: basal veins. Arrow: agroaphic veins. Scale bar: A and B: 3 mm; C–G, I–P, R and S: 300 µm; H, Q: 1 mm.
Leaf venation pattern in austral South American Bauhinia. FEV, freely ending veinlets; P, pentagonal; PE, percurrent; Q, quadrangular; R, reticulate; T, triangular.
The first group is characterized by a good areole development that is found in some medicinal members of sect. Pauletia ser. Cansenia, in the liana Bauhinia angulosa (= S. angulosa) and in the spiny tree B. uruguayensis (Fig. 1D, L, P–S). The medicinal B. holophylla and B. rufa both display quadrangular and pentagonal, rarely triangular areoles, with absent and unbranched freely ending veinlets (FEV), the first one can be further recognized since FEV in general cross the areola and marginal ultimate venation and quinternary vein fabric venation are absent (Fig. 1L). B. rufa, instead, presents looped marginal ultimate venation and quinternary vein fabric present (Fig. 1P and Q). The medicinal B. ungulata has absent, unbranched and one branched FEV and areola shape more variable (Fig. 1R). Some similar features have been described in others taxa from ser. Cansenia, and Zhang (1994)Zhang, D., 1994. Leaf venation of Cercideae. J. Trop. Subtrop. Bot. 2, 45-57. named it as the Cansenia venation type. B. angulosa is easily distinguished because of the very small areoles lacking FEV and marginal ultimate vein absent (Fig. 1D). B. uruguayensis is the only taxon that presents paxillate areole development without FEV, or just very few FEV (Fig. 1S), these features are similar to the Elayuna type described by Zhang (1994)Zhang, D., 1994. Leaf venation of Cercideae. J. Trop. Subtrop. Bot. 2, 45-57..
By the other side, the second group, composed by the prickly trees and shrubs from sect. Pauletia ser. Aculeatae and the suffrutices and shrubs from ser. Pentandrae, possesses moderate areole development along with marginal ultimate venation absent and quinternary vein fabric present (Fig. 1B–E, J–K, M–O). Comparatively, areoles are larger and more variable in size than in previous group. The medicinal B. forficata (both subspecies), B. argentinensis and B. hagenbeckii show almost the same pattern, with mostly branching FEV (one or more branches) and less frequently, unbranched FEV (Fig. 1J, E, K). B. forficata can be distinguished by the percurrent tertiary vein fabric, while the others are percurrent at the base and reticulate at apex. B. affinis (Fig. 1C), B. amambayensis (not shown) and B. mollis (Fig. 1N, O) have in general both unbranched and branched FEV, in different frequency. The medicinal liana B. microstachya (= S. microstachya) possesses also moderate areole development, mostly unbranched and one branched FEV, but is recognized because of the presence of both looped and absent marginal ultimate venation (Fig. 1M), this report is similar to the one by Fortunato (1986)Fortunato, R.H., 1986. Revisión del género Bauhinia (Cercideae, Caesalpinioideae, Fabaceae). Darwiniana 27, 527-557. but differs from previous (Zhang, 1994Zhang, D., 1994. Leaf venation of Cercideae. J. Trop. Subtrop. Bot. 2, 45-57.).
Finally, the medicinal B. cheilantha and B. campestris (sect. Pauletia ser. Cansenia) present areole development intermediate between good and moderate. B. cheilantha alternates between absent, unbranched and one branched FEV and ultimate venation absent while B. campestris can be distinguished because FEV are in general branched and ultimate venation is looped (Fig. 1I, G and H). The medicinal B. bauhinioides (sect. Pauletia ser. Perlebia) also possess areole development moderate to good but areoles are mostly unbranched and one branched (Fig. 1F).
Interestingly, all species present prismatic crystals of calcium oxalate associated to vascular bundles and often druses in mesophyll cells, more notable in B. affinis, B. argentinensis, B. mollis and B. ungulata var. cuiabensis.
Here we provide a helpful tool for the recognition of the main regional medicinal plants through the analysis of the leaf vein pattern based on the intercostal tertiary and quinternary vein fabric, areole development and shape, free ending veinlet branching and marginal ultimate venation characters.
Acknowledgements
We thank Cristo S. for technical assistance. CONICET (PIP 112-201101-00250), INTA (PNHFA-1106094) and SECyT-UNC (32720160200161CB) are acknowledged for financial support.
Appendix A Supplementary data
Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.bjp.2016.10.007.
References
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- Bortoluzzi, R.L.C., Miotto, S.T.S., Reis, A., 2006. Bauhinia. In: Reis, A. (org.), Flora Ilustrada Catarinense, vol. 2. Herbário Barbosa Rodrigues, Itajaí, pp. 29–67.
- Cechinel Filho, V., 2009. Chemical composition and biological potential of plants from the genus Bauhinia Phytother. Res. 23, 1347-1354.
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» http://dx.doi.org/10.1186/s12862-015-0540-9 - Luna, J.D.S., Santos, A.F., Lima, M.R.F., Omena, M.C., Mendonça, F.A.C., Bieber, L.W., Sant'Ana, A.E.G., 2005. A study of the larvicidal and molluscicidal activities of some medicinal plants from northeast Brazil. J. Ethnopharmacol. 97, 199-206.
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» http://dx.doi.org/10.1155/2016/5346574 - Melo, J.G., Nascimento, V.T., Amorim, E.L.C., Andrade Lima, C.S., Albuquerque, U.P., 2004. Avaliação da qualidade de amostras comerciais de boldo (Peumus boldus Molina), pata-de-vaca (Bauhinia spp) e ginco (Ginkgo biloba L.). Rev. Bras. Farmacogn. 14, 111-120.
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» http://dx.doi.org/10.1155/2015/439506 - Silva, K.L., Cechinel Filho, V., 2002. Plantas do gênero Bauhinia: composição química e potencial farmacológico. Quim. Nova 25, 449-454.
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Publication Dates
-
Publication in this collection
Mar-Apr 2017
History
-
Received
06 Sept 2016 -
Accepted
28 Oct 2016