Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-19T04:16:43.111Z Has data issue: false hasContentIssue false

Ontogenesis of Resin Ducts and Secretory Process in Protium spruceanum (Burseraceae) Stems

Published online by Cambridge University Press:  22 March 2022

Wanessa Stéfanne de Jesus Silva Bruzinga
Affiliation:
Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes Claros, MG 39401-089, Brazil
Leonardo Monteiro Ribeiro
Affiliation:
Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes Claros, MG 39401-089, Brazil
Yule Roberta Ferreira Nunes
Affiliation:
Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes Claros, MG 39401-089, Brazil
Lúcia Pinheiro Santos Pimenta
Affiliation:
Departamento de Química, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil
Mariana Araujo Thibau de Almeida
Affiliation:
Departamento de Química, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil
Martha Grasielle Alves Mendes
Affiliation:
Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes Claros, MG 39401-089, Brazil
Maria Olívia Mercadante-Simões*
Affiliation:
Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes Claros, MG 39401-089, Brazil
*
*Corresponding author: Maria Olívia Mercadante-Simões, E-mail: [email protected]
Get access

Abstract

The objective of this work was to characterize the ontogenesis of Protium spruceanum secretory ducts, to evaluate the effects of seasonality on that process, and to characterize the chemical nature of the resin. Morphometric, anatomical, micromorphometric, histochemical, and ultrastructural evaluations of shoot apexes and chemical analyses of the resin were performed. The ducts of schizolysigenous origin are distributed in the primary and secondary phloem. The subsecretory tissue is meristematic and can restore the secretory epithelium. Secretory epithelial cells have wall thickening resembling that of the Casparian strip that regulates secretion reflux. The main resin compounds are pentacyclic triterpenoids, α- and β-amyrins, and α- and β-amyrenones, which are reported here for the first time for this species. The presence of electron-dense and electron-opaque structures, in the secretory epithelial cells, are compatible with the triterpenes and mucilage identified in the resin. Rising temperatures, rainfall, and increasing day length induce the formation of ducts in the vascular cambium throughout Spring/Summer. The abundant production of resin rich in pentacyclic triterpenes indicates the potential use of the species for medicinal and cosmetic purposes. The understanding that secretory processes are concentrated during the Spring/Summer seasons will contribute to the definition of resin extraction management strategies.

Type
Biological Applications
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amparo, TR, Seibert, JB, Mathias, FAS, Vieira, JFP, Soares, RDOA, Freitas, KM, Cabral, VAR, Brandão, GC, Santos, ODH, Souza, GHB & Vieira, PMA (2019). Anti-inflammatory activity of Protium spruceanum (Benth.) Engler is associated to immunomodulation and enzymes inhibition. J Ethnopharmacol 241, 112024. doi:10.1016/j.jep.2019.112024CrossRefGoogle ScholarPubMed
Begum, S, Nakaba, S, Yamagishi, Y, Oribe, Y & Funada, R (2012). Regulation of cambial activity in relation to environmental conditions: Understanding the role of temperature in wood formation of trees. Physiol Plant 147, 4654. doi:10.1111/j.1399-3054.2012.01663.xCrossRefGoogle Scholar
Bhatt, JR (1987). Development and structure of primary secretory ducts in the stem of Commiphora wightii (Burseraceae). Ann Bot 60, 405416. doi:10.1093/oxfordjournals.aob.a087461CrossRefGoogle Scholar
Blake, GR & Hartge, KH (2018). Bulk density. In Soil Science SSSA Book Series, Klute, A (Eds.), pp. 363375. Madison, WI: Society of America, American Society of Agronomy.Google Scholar
Blanche, CA, Lorio, PL, Sommers, RA, Hodges, JD & Nebeker, TE (1992). Seasonal cambial growth and development of Loblolly pine: Xylem formation, inner bark chemistry, resin ducts, and resin flow. Forest Ecol Manag 49, 151165. doi:10.1016/0378-1127(92)90167-8CrossRefGoogle Scholar
Brasil, MCO, Lacerda, GA, Arrudas, SR & Veloso, MDM (2018). Essential oil content and composition of Almescla resin (Protium spruceanum (Benth.) Engl., Burseraceae. J Agric Sci 10, 442. doi:10.5539/jas.v10n11p442Google Scholar
Carvajal, D, Alvarez, R & Osorio, E (2016). Chemical variability of essential oils of Protium colombianum from two tropical life zones and their in vitro activity against isolates of Fusarium. J Pest Sci 89, 241248. doi:10.1007/s10340-015-0667-xCrossRefGoogle Scholar
Carvalho, KMMB, Marinho Filho, JDB, Melo, TS, Araújo, AJ, Quetz, JS, Cunha, MPSS, Melo, KM, Silva, AACA, Tomé, AR, Havt, A, Fonseca, SGC, Brito, GAC, Chaves, M, Rao, VS & Santos, FA (2015). The resin from Protium heptaphyllum prevents high-fat diet-induced obesity in mice: Scientific evidence and potential mechanisms. Evid-Based Compl Alt 2015, 113. doi:10.1155/2015/106157CrossRefGoogle ScholarPubMed
Coley, PD & Barone, JA (1996). Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27, 305335.CrossRefGoogle Scholar
Costa, ER, Tangerina, MMP, Ferreira, MJP & Demarco, D (2021). Two origins, two functions: The discovery of distinct secretory ducts formed during the primary and secondary growth in Kielmeyera. Plants 10, 877. doi:10.3390/plants10050877CrossRefGoogle ScholarPubMed
David, R & Carde, JP (1964). Coloration différentielle dês inclusions lipidique et terpeniques dês pseudophylles du Pin maritime au moyen du reactif nadi. C R Acad Sci Paris D 258, 13381340.Google Scholar
Fahn, A (1979). Secretory Tissues in Plants. London: Academic Press.Google Scholar
Fahn, A (2000). Structure and function of secretory cells. In Advances in Botanical Research, Incorporating Advances in Plant Pathology, Plant Trichomes, Hallahan, DL, Gray, JC & Callow, JA (Eds.), pp. 3766. Academic Press, London. doi:10.1016/S0065-2296(00)31006-0Google Scholar
Furr, M & Mahlberg, PG (1981). Histochemical analyses of lacticifers and glandular trichomes in Cannabis sativa. J Nat Prod 4, 153159.CrossRefGoogle Scholar
Karnovsky, MJ (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27, 137138.Google Scholar
Langenheim, JH (2003). Plant Resins: Chemistry, Evolution, Ecology, Ethnobotany. Cambridge, UK: Timber Press.Google Scholar
Lara, NOT & Marcati, CR (2016). Cambial dormancy lasts 9 months in a tropical evergreen species. Trees 30, 13311339. doi:10.1007/s00468-016-1369-6CrossRefGoogle Scholar
Lima, EM, Nascimento, AM, Lenz, D,D, Scherer, R, Meyrelles, SS, Boëchat, GAP, Andrade, TU & Endringer, DC (2014). Triterpenes from the Protium heptaphyllum resin – Chemical composition and cytotoxicity. Braz J Pharmacog 24, 399407. doi:10.1016/j.bjp.2014.06.003CrossRefGoogle Scholar
Machado, LB, Zoghbi, MGB & Andrade, EHA (2003). Seasonal variation in the composition of the essential oils from the leaves, thin branches and resin of Protium spruceanum (Benth.) Engl. Flavour Fragr J 18, 338341. doi:10.1002/ffj.1238CrossRefGoogle Scholar
Machado, SR, Canaveze, Y & Rodrigues, TM (2016). Structure and functioning of oil cavities in the shoot apex of Metrodorea nigra A. St.-Hil. (Rutaceae). Protoplasma 254, 16611674. doi:10.1007/s00709-016-1056-xCrossRefGoogle Scholar
Maia, RM, Barbosa, PR, Cruz, FG, Roque, NF & Fascio, M (2000). Triterpenos da resina de Protium heptaphyllum March (Bourseraceae): Caracterização em misturas binárias. Quim Nova 23, 623626. doi:10.1590/S0100-40422000000500010CrossRefGoogle Scholar
Marcati, CR, Machado, SR, Podadera, DS, Lara, NOT, Bosio, F & Wiedenhoeft, AC (2016). Cambial activity in dry and rainy season on branches from woody species growing in Brazilian Cerrado. Flora 223, 110. doi:10.1016/j.flora.2016.04.008CrossRefGoogle Scholar
Melo, KM, Oliveira, FTB, Costa Silva, RA, Gomes Quinderé, AL, Marinho Filho, JDB, Araújo, AJ, Pereira, EDB, Carvalho, AA, Chaves, MH, Rao, VS & Santos, FA (2019). α, β-amyrin, a pentacyclic triterpenoid from Protium heptaphyllum suppresses adipocyte differentiation accompanied by down regulation of PPARγ and C/EBPα in 3T3-L1 cells. Biomed Pharmacother 109, 18601866. doi:10.1016/j.biopha.2018.11.027CrossRefGoogle Scholar
Milliken, W, Miller, RP, Pollard, SR & Wandelli, EV (1986). The Ethnobotany of the Waimiri Atroari Indians of Brazil. Kew: Royal Botanic Gardens.Google Scholar
Nair, MNB & Subrahmanyam, SV (1998). Ultrastructure of the epithelial cells and oleogumresin secretion in Boswellia serrata (Burseraceae). IAWA J 19, 415427. doi:10.1163/22941932-90000662CrossRefGoogle Scholar
Nogueira, AO, Oliveira, YIS, Adjafre, BL, Moraes, MEA & Aragão, GF (2019). Pharmacological effects of the isomeric mixture of alpha and beta amyrin from Protium heptaphyllum: A literature review. Fund Clin Pharmacol 33, 412. doi:10.1111/fcp.12402, 2019CrossRefGoogle ScholarPubMed
O'Brien, TP, Feder, N & Mc Cully, ME (1964). Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59, 368373.CrossRefGoogle Scholar
Oliveira, JM, Santarosa, E, Pillar, VD & Roig, FA (2009). Seasonal cambium activity in the subtropical rain forest tree Araucaria angustifolia. Trees 23, 107115. doi:10.1007/s00468- 008- 0259-yCrossRefGoogle Scholar
Oliveira-Filho, AT & Ratter, JA (1995). A study of the origin of central Brazilian forests by the analysis of plant species distribution patterns. Edinb J Bot 52, 141. doi:10.1017/S0960428600000949CrossRefGoogle Scholar
Paiva, EAS (2016). How do secretory products cross the plant cell wall to be released? A new hypothesis involving cyclic mechanical actions of the protoplast. Ann Bot 117, 533540. doi:10.1093/aob/mcw012CrossRefGoogle ScholarPubMed
Palermo, FH, Rodrigues, MIA, Nicolai, J, Machado, SR & Rodrigues, TM (2018). Resin secretory canals in Protium heptaphyllum (Aubl.) Marchand. (Burseraceae): A tridimensional branched and anastomosed system. Protoplasma 255, 899910. doi:10.1007/s00709-017-1197-6CrossRefGoogle ScholarPubMed
Pinto, SAH, Pinto, LM, Guedes, MA, Cunha, GMA, Chaves, MH, Santos, FA & Rao, VS (2008). Antinoceptive effect of triterpenoid α, β-amyrin in rats on orofacial pain induced by formalin and capsaicin. Phytomedicine 15, 630634. doi:10.1016/j.phymed.2007CrossRefGoogle Scholar
Piva, LRO, Jardine, KJ, Gimenez, BO, Perdiz, RO, Menezes, VS, Durgante, FM, Cobello, LO, Higuchi, N & Chambers, JQ (2019). Volatile monoterpene ‘fingerprints’ of resinous Protium tree species in the Amazon rainforest. Phytochemistry 160, 6170. doi:10.1016/j.phytochem.2019.01.014CrossRefGoogle ScholarPubMed
Ramos, MV, Demarco, D, Costa Souza, IC & Freitas, CDT (2019). Laticifers, latex, and their role in plant defense. Trends Plant Sci 24, 553567. doi:10.1016/j.tplants.2019.03.006CrossRefGoogle ScholarPubMed
Reboita-Simões, M, Rodrigues, M, Silva, LF & Alves, MA (2015). Aspectos climáticos do estado de Minas Gerais. Rev Bras Climatol. doi:10.5380/abclima.v17i0.41493Google Scholar
Rodrigues, TM, Santos, DC & Machado, SR (2011). The role of the parenchyma sheath and PCD during the development of oil cavities in Pterodon pubescens (Leguminosae-Papilionoideae). C R Biol 334, 535543. doi:10.1016/j.crvi. 2011.04.005CrossRefGoogle Scholar
Roland, AM (1978). General preparations and staining of thin sections. In Electron Microscopy and Cytochemistry of Plant Cells, Hall, JL (Eds.), pp. 162. New York: Elsevier.Google Scholar
Rosalem, PF, Picão, TB, Rodrigues-Lisoni, FC & Martins, AR (2017). Leaf anatomy of Protium ovatum and its antiproliferative potential in cervical cells. Braz J Pharmacog 27, 673678. doi:10.1016/j.bjp.2017.09.001CrossRefGoogle Scholar
Royo, VA, Mercadante-Simões, MO, Ribeiro, LM, Oliveira, DA, Aguiar, MMR, Costa, ER & Ferreira, PRB (2015). Anatomy, histochemistry, and antifungal activity of Anacardium humile (Anacardiaceae) leaf. Microsc Microanal 21, 15491561. doi:10.1017/S1431927615015457CrossRefGoogle ScholarPubMed
Setia, RC, Parthasarathy, MV & Shah, JJ (1977). Development, histochemistry and ultrastructure of gum-resin ducts in Commiphora mukul Engl. Ann Bot 41, 9991004. doi:10.1093/oxfordjournals.aob.a085397CrossRefGoogle Scholar
Silva, JRA, Zoghbi, MGB, Pinto, AC, Godoy, RLO & Amaral, AC (2009). Analysis of the hexane extracts from seven oleoresins of Protium species. J Essent Oil Res 21, 305308. doi:10.1080/10412905.2009.9700178CrossRefGoogle Scholar
Silveira, AF, Mercadante-Simões, MO, Ribeiro, LM, Nunes, YRF, Duarte, LP, Lula, IS, Aguilar, MG & Sousa, GF (2020). Mucilaginous secretions in the xylem and leaf apoplast of the swamp palm Mauritia flexuosa L.f. (Arecaceae). Microsc Microanal 26, 609621. doi:10.1017/S1431927620001543CrossRefGoogle Scholar
Soukup, A & Tylová, E (2018). Apoplastic barriers: Their structure and function from a historical perspective. In Concepts in Cell Biology - History and Evolutionvol 23, Sahi, VP & Baluška, F (Eds.), pp. 155183. Cham: Springer International Publishing. doi:10.1007/978-3-319-69944-8_8CrossRefGoogle Scholar
Sousa, AMS, Lopes, PSN, Ribeiro, LM, Andrade, MS & Mercadante-Simões, MO (2017). Structural aspects of germination control in pyrenes of Caryocar brasiliense (Caryocaraceae). Trees 31, 887902. doi:10.1007/s00468-016-1514-2CrossRefGoogle Scholar
Souza, LR, Trindade, FG, Oliveira, RA, Costa, LCB, Gomes, VM & Cunha, M (2016). Histochemical characterization of secretory ducts and essential oil analysis of Protium species (Burseraceae). J Essent Oil Res 28, 166171. doi:10.1080/10412905.2015.1092478CrossRefGoogle Scholar
Souza, MJ, Mercadante-Simões, MO & Ribeiro, LM (2020). Secondary-cell-wall release: A particular pattern of secretion in the mucilaginous seed coat of Magonia pubescens. Am J Bot 107, 3144. doi:10.1002/ajb2.1415CrossRefGoogle ScholarPubMed
Souza, SR, Trindade, IC, Mercadante-Simões, MO, Duarte, LP, Silva, GDF, Messias, MCTB, Santos, AC & Vieira-Filho, SA (2017). Leaf morphoanatomy of the medicinal Maytenus imbricata (Celastraceae): An ecological approach. Bot Sci 95, 18. doi:10.17129/botsci.894Google Scholar
Stefi, AL & Christodoulakis, NS (2021). Approaching the “secrets” of the resin ducts in the mastic tree (Pistacia lentiscus L. cv. chia). Flora 285, 151940. doi:10.1016/j.flora.2021.151940CrossRefGoogle Scholar
Stefi, AL, Nikou, T, Vassilacopoulou, D, Vassilacopoulou, D, Skaltsounis, L, Halabalaki, M & Christodoulakis, NS (2021). Structure and organization of the secretion apparatus of the mastic tree (Pistacia lentiscus L.) and LC–HRMS analysis of leaf extracts. Planta 253, 70. doi:10.1007/s00425-021-03588-2CrossRefGoogle ScholarPubMed
Tanamatayarat, P (2016). Antityrosinase, antioxidative activities, and brine shrimp lethality of ethanolic extracts from Protium serratum (Wall. ex Colebr.) Engl. Asian-Pac J Trop Biomed 6, 10501055. doi:10.1016/j.apjtb.2016.10.001CrossRefGoogle Scholar
Tegasne, C, Kapche, GDWF, Mawabo, IK, Talla, RM, Jouda, J-B, Happi, GM, Lenta, BN, Frese, M, Abegaz, BM & Sewald, N (2020). Bioguided chemical study of Boswellia dalzielii Hutch. (Burseraceae) for antibacterial agents and a new glucopyranoxylmethoxybenzyle. Nat Prod Res, 110. doi:10.1080/14786419.2020.1794863Google Scholar
Vidal, BC (1977). Acid glycosaminoglycans and endochondral ossification: Microespectrophotometric evaluation and macromolecular orientation. Cell Mol Biol 22, 4564.Google Scholar
Wagner, H, Bladt, S & Zgainski, EM (1984). Plant Drug Analysis. Müchen: Institut für Pharmazeutische Biologie der Universität.CrossRefGoogle Scholar
Yamamoto, F, Iwanaga, F, Al-Busaidi, A & Yamanaka, N (2020). Roles of ethylene, jasmonic acid, and salicylic acid and their interactions in frankincense resin production in Boswellia sacra Flueck. trees. Sci Rep 10, 16760. doi:10.1038/s41598-020-73993-2CrossRefGoogle ScholarPubMed