Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T10:10:19.728Z Has data issue: false hasContentIssue false
  • English
  • Français

Mucilaginous Secretions in the Xylem and Leaf Apoplast of the Swamp Palm Mauritia flexuosa L.f. (Arecaceae)

Part of: Micrographia Collection

Published online by Cambridge University Press:  04 June 2020

Alessandra Flávia Silveira ,
Maria Olívia Mercadante-Simões Open the ORCID record for Maria Olívia Mercadante-Simões [Opens in a new window] ,
Leonardo Monteiro Ribeiro ,
Yule Roberta Ferreira Nunes ,
Lucienir Pains Duarte ,
Ivana Silva Lula ,
Mariana Guerra de Aguilar  and
Grasiely Faria de Sousa
Alessandra Flávia Silveira
Affiliation:
Plant Anatomy Laboratory, General Biology Department, State University of Montes Claros, Montes Claros39401-089, Brazil
Maria Olívia Mercadante-Simões*
Affiliation:
Plant Anatomy Laboratory, General Biology Department, State University of Montes Claros, Montes Claros39401-089, Brazil
Leonardo Monteiro Ribeiro
Affiliation:
Plant Micropropagation Laboratory, General Biology Department, State University of Montes Claros, Montes Claros39401-089, Brazil
Yule Roberta Ferreira Nunes
Affiliation:
Plant Ecology Laboratory, General Biology Department, State University of Montes Claros, Montes Claros39401-089, Brazil
Lucienir Pains Duarte
Affiliation:
Medicinal Plants Study Center, Chemistry Department, Federal University of Minas Gerais, Belo Horizonte31270-901, Brazil
Ivana Silva Lula
Affiliation:
Medicinal Plants Study Center, Chemistry Department, Federal University of Minas Gerais, Belo Horizonte31270-901, Brazil
Mariana Guerra de Aguilar
Affiliation:
Medicinal Plants Study Center, Chemistry Department, Federal University of Minas Gerais, Belo Horizonte31270-901, Brazil
Grasiely Faria de Sousa
Affiliation:
Medicinal Plants Study Center, Chemistry Department, Federal University of Minas Gerais, Belo Horizonte31270-901, Brazil
*
*Author for correspondence: Mercadante-Simões, E-mail: omercadante@hotmail.com.
Get access

Abstract

Mauritia flexuosa palms inhabit wetland environments in the dry, seasonal Brazilian savanna (Cerrado) and produce mucilaginous secretions in the stem and petiole that have a medicinal value. The present study sought to characterize the chemical natures of those secretions and to describe the anatomical structures involved in their synthesis. Chemical analyzes of the secretions, anatomical, histochemical analyses, and electron microscopy studies were performed on the roots, stipes, petioles, and leaf blades. Stipe and petiole secretions are similar, and rich in cell wall polysaccharides and pectic compounds such as rhamnose, arabinose, xylose, mannose, galactose, and glucose, which are hydrophilic largely due to their hydroxyl and carboxylate groups. Mucilaginous secretions accumulate in the lumens of vessel elements and sclerenchyma fibers of the root, stipe, petiole, and foliar veins; their synthesis involves cell wall loosening and the activities of dictyosomes. The outer faces of the cell walls of the parenchyma tissue in the mesophyll expand to form pockets that rupture and release pectocellulose substances into the intercellular spaces. The presence of mucilage in the xylem, extending from the roots to the leaf veins and continuous with the leaf apoplast, and sub-stomatal chambers suggest a strategy for plant water economy.

Keywords

arabinosepectinplant mucilagerhamnosesclerenchymatic fibervessel element
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 26 , Issue 3 , June 2020 , pp. 609 - 621
Copyright
Copyright © Microscopy Society of America 2020

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

Arend, M, Muninger, M & Fromm, J (2008). Unique occurrence of pectin-like fibrillar cell wall deposits in xylem fibres of poplar. Plant Biol 10, 763–770.CrossRefGoogle ScholarPubMed
Barnes, WJ & Anderson, CT (2017). Release, recycle, rebuild: Cell wall remodeling, autodegradation, and sugar salvage for new wall biosynthesis during plant development. Mol Plant 11, 31–46.CrossRefGoogle ScholarPubMed
Bhatt, JR & Mohan Ram, HY (1992). Development and ultrastructure of primary secretory ducts in the stem of Semecarpus anacardium (Anacardiaceae). Iawa Bull 13, 173–185.CrossRefGoogle Scholar
Bi, CYT, N'guessan, FK, Kouakou, CA, Jacques, N, Casaregola, S & Dje, MK (2016). Identification of yeasts isolated from raffia wine (Raphia hookeri) produced in Côte d'Ivoire and genotyping of Saccharomyces cerevisiae strains by PCR inter-delta. World J Microb Biot echnol 32, 2–9.Google Scholar
Bruyn, A & Loo, JV (1991). The identification by 1H- and 13C-NMR spectroscopy of sucrose, 1-kestose, and neokestose in mixtures present in plant extracts. Carbohyd Res 211, 131–136.CrossRefGoogle Scholar
Cantu-Jungles, TM, Almeida, CP, Iacomini, M, Cipriani, TR & Cordeiro, LMC (2015). Arabinan-rich pectic polysaccharides from buriti (Mauritia flexuosa): An Amazonian edible palm fruit. Carbohyd Polym 122, 276–281.CrossRefGoogle ScholarPubMed
Carnachan, SM & Harris, PJ (2000). Polysaccharide compositions of primary cell walls of the palms Phoenix canariensis and Rhopalostylis sapida. Plant Physiol Biochem 38, 699–708.CrossRefGoogle Scholar
Clifford, SC, Arndt, SK, Popp, M & Jones, HG (2001). Mucilages and polysaccharides in Ziziphus species (Rhamnaceae): Localization, composition and physiological roles during drought-stress. J Exp Bot 53, 131–138.CrossRefGoogle Scholar
Cordeiro, LMC, Almeida, CP & Iacomini, M (2015). Unusual linear polysaccharides: (1→5)-((L-Arabinan, (1→3)-(1→4)-((D-glucan and (1→4)- ((-D-xylan from pulp of buriti (Mauritia flexuosa), an edible palm fruit from the Amazon region. Food Chem 173, 141–146.CrossRefGoogle Scholar
Dias, JE & Laureano, LC (2000). Farmacopéia Popular do Cerrado. Goiás, BR: Articulação Pacari.Google Scholar
Fahn, A (1979). Secretory Tissues in Plants. London, NY: Academic Press.Google Scholar
Fahn, A & Evert, RF (1974). Ultrastructure of secretory ducts of Rhus glabra L. Am J Bot 61, 1–14.CrossRefGoogle Scholar
Ghanem, ME, Han, R-N, Classen, B, Quetin-Leclerq, J, Mahy, G, Cheng-Jiang, R, Quin, P, Perez-alfocea, F & Lutts, S (2010). Mucilage and polysaccharides in the halophyte plant species Kosteletzkya virginica: Localization and composition in relation to salt stress. J Plant Physiol 167, 382–392.CrossRefGoogle Scholar
Gorshkova, T, Brutch, N, Chabbert, B, Deyholos, M, Hayashi, T, Lev-Yadun, S, Mellerowicz, EJ, Morvan, C, Neutelings, G & Pilate, G (2012). Plant fiber formation: State of the art, recent and expected progress, and open questions. Crit Rev Plant Sci 31, 201–228.CrossRefGoogle Scholar
Holm, JA, Miller, CJ & Cropper, WP Jr. (2008). Population dynamics of the dioecious amazonian palm Mauritia flexuosa: Simulation analysis of sustainable harvesting. Biotropica 40, 550–558.CrossRefGoogle Scholar
Johansen, DA (1940). Plant Microtechnique. New York: Mc Graw-Hill Boo Company.Google Scholar
Karnovsky, MJ (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27, 137–138.Google Scholar
Koolen, HHF, Silva, FMA, Gozzo, FC, Souza, AQL & Souza, ADL (2013). Antioxidant, antimicrobial activities and characterization of phenolic compounds from buriti (Mauritia flexuosa L.f.) by UPLC-ESI-MS/MS. Food Res Int 51, 467–473.CrossRefGoogle Scholar
Lacchia, APS & Carmello-Guerreiro, SM (2009). Aspectos ultra-estruturais dos canais secretores em órgãos vegetativos e reprodutivos de Anacardiaceae. Acta Bot Bras 23, 376–388.CrossRefGoogle Scholar
Lima, NE, Lima-Ribeiro, MS, Tinoco, CF, Terribile, LC & Collevatti, RG (2014). Phylogeography and ecological niche modelling, coupled with the fossil pollen record, unravel the demographic history of a Neotropical swamp palm through the quaternary. J Biogeogr 41, 673–686.CrossRefGoogle Scholar
Lorenzi, H, Kahn, F, Noblick, LR & Ferreira, E (2010). Flora Brasileera: Arecaceae (palmeiras). Nova Odessa: Plantarum.Google Scholar
Lyshede, OB (1977). Studies on the mucilaginous cells in the leaf of Spartocytisus filipes W.B. Planta 133, 255–260.CrossRefGoogle Scholar
Marcon, MV, Carneiro, PIB, Wosiacki, G & Beleski-Carneiro, E (2005). Pectins from apple pomace-characterization by 13C and 1H NMR spectroscopy. Ann Magn Reson 4, 56–63.Google Scholar
Mastroberti, AA & Mariath, JEA (2008). Development of mucilage cells of Araucaria angustifolia (Araucariaceae). Protoplasma 232, 233–245.CrossRefGoogle Scholar
Mauseth, JD (1980). A stereological morphometric study of the ultrastructure of mucilage cells in Opuntia polyacantha (Cactaceae). Bot Gaz 141, 374–378.CrossRefGoogle Scholar
Mercadante-Simões, MO & Paiva, EAS (2013). Leaf colleters in Tontelea micrantha (Celastraceae, Salacioideae): Ecological, morphologicaland structural aspects. C R Biol 336, 400–406.CrossRefGoogle Scholar
Monrroy, M, García, E, Ríos, K & García, JR (2017). Extraction and physicochemical characterization of mucilage from Opuntia cochenillifera (L.) Miller. J Chem 2017, 1–9.CrossRefGoogle Scholar
Morse, SR (1990). Water balance in Hemizonia luzulifolia: The role of extracelular polysaccharides. Plant Cell Environ 13, 39–48.CrossRefGoogle Scholar
Mosti, S, Friedman, CR, Piccolinm, F, Falcom, P & Papini, A (2012). The unusual tegumental tissues of the Lunaria annua (Brassicaceae) seed: A developmental study using light and electron microscopy. Flora 207, 828–837.CrossRefGoogle Scholar
Nair, GM, Venkaiah, K & Shahm, JJ (1983). Ultrastructure of gum-resin ducts in cashew (Anacardium occidentale). Ann Bot 51, 297–305.CrossRefGoogle Scholar
O'Brien, TP (1970). Further observations on hydrolysis of the cell wall in the xylem. Protoplasma 69, 1–14.CrossRefGoogle Scholar
O'Brien, TP, Federm, N & McCully, ME (1964). Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59, 368–373.CrossRefGoogle Scholar
Porto, KCN, Nunesm, YRF & Ribeiro, LM (2017). The dynamics of recalcitrant seed banks of Mauritia flexuosa (Arecaceae) reveal adaptations to marsh microenvironments. Plant Ecol 219, 199–207.CrossRefGoogle Scholar
Reis, SB, Mello, ACMP & Oliveira, DMT (2017). Pericarp formation in early divergent species of Arecaceae (Calamoideae, Mauritiinae) and its ecological and phylogenetic importance. Plant Syst Evol 303, 675–687.CrossRefGoogle Scholar
Ribeiro, JJ & Walter, BMT (2008). Fitofisionomias do bioma Cerrado. In Cerrado: Ambiente e Flora, Sano, SM & Almeida, SP (Eds.), pp. 87–166. Brasília: Embrapa Cerrados.Google Scholar
Ribeiro, VC & Leitão, CAE (2019). Utilisation of Toluidine blue O pH 4.0 and histochemical inferences in plant sections obtained by free-hand. Protoplasma 257, 993–1008.CrossRefGoogle ScholarPubMed
Robards, AW (1978). An introduction to techniques for scanning electron microscopy of plant cells. In Electron Microscopy and Cytochemistry of Plant Cells, Hall, JL (Ed.), pp. 343–403. New York: Elsevier.Google Scholar
Rocha, FJ, Pimentel, RR & Machado, RS (2011). Estruturas secretoras de mucilagem em Hibiscus pernambucensis Arruda (Malvaceae): Distribuição, caracterização morfoanatômica e histoquímica. Acta Bot Bras 25, 751–763.CrossRefGoogle Scholar
Rodrigues, BRA, Nietsche, S, Mercadante-Simões, MO, Pereira, MCT & Ribeiro, LM (2018). Climatic seasonality influences the development of pollen grains and fruiting in Annona squamosa. Envion Exp Bot 150, 240–248.CrossRefGoogle Scholar
Roland, AM (1978). General preparations and staining of thin sections. In Electron Microscopy and Cytochemistry of Plant Cells, Hall, JL (Ed.), pp. 1–62. New York: Elsevier.Google 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, 1549–1561.CrossRefGoogle ScholarPubMed
Sáenz, C, Sepúlveda, E & Matsuhiro, B (2004). Opuntia spp mucilage's: A functional componente with industrial perspectives. J Arid Environ 57, 275–290.CrossRefGoogle Scholar
Silva, AM, Assad, ED & Evangelista, BA (2008). Caracterização climática do bioma Cerrado. In Ecologia e Flora, Sano, SM, Almeida, SP & Ribeiro, JF (Eds.), pp. 69–88. Brasília: Embrapa Informação Tecnológica.Google Scholar
Silva, RJF & Potiguara, RCV (2009). Substâncias ergásticas foliares de espécies amazônicas de Oenocarpus Mart. (Arecaceae): Caracterização histoquímica e ultra-estrutural. Acta Amazon 39, 793–798.CrossRefGoogle Scholar
Silva, RS, Ribeiro, LM, Mercadante-Simões, MO, Nunes, YRF & Lopes, PSN (2014). Seed structure and germination in buriti (Mauritia flexuosa): The swamp palm. Flora 209, 674–685.CrossRefGoogle 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, 1–14.CrossRefGoogle ScholarPubMed
Tamunaidu, P, Matsui, N, Okimori, Y & Saka, S (2013). Nipa (Nypa fruticans) sap as a potential feedstock for etanol production. Biomass Bioenergy 52, 96–102.CrossRefGoogle Scholar
Venkaiah, K (1992). Development, ultrastructure and secretion of gum ducts in Lannea coromandelica (Hout) Merrill (Anacardiaceae). Ann Bot 69, 449–457.CrossRefGoogle Scholar
Virapongse, A (2017). Social mechanisms and mobility: Buriti palm (Mauritia flexuosa) extractivism in Brazil. Hum Ecol 45, 119–129.CrossRefGoogle Scholar
Westhoff, M, Zimmermann, D, Zimmermann, G, Gessner, P, Wegner, LH, Bentrup, F-W & Zimmermann, U (2009). Distribution and function of epistomatal mucilage plugs. Protoplasma 235, 101–105.CrossRefGoogle ScholarPubMed
Yapo, BM & Koffi, K (2006). Yellow passion fruit rind: A potential source of low-methoxyl pectin. J Agric Food Chem 54, 2738–2744.CrossRefGoogle ScholarPubMed
Zimmermann, D, Westhoff, M, Zimmermann, G, Gebner, P, Gessner, A, Wegner, LH, Rokitta, M, Ache, P, Schneider, H, Vásquez, JA, Kruck, W, Shirley, S, Jakob, P, Hedrich, R, Bentrup, F-W, Bamberg, E & Zimmermann, U (2007). Foliar water supply of tall trees: Evidence for mucilage-facilitated moisture uptake from the atmosphere and the impact on pressure bomb measurements. Protoplasma 232, 11–34.CrossRefGoogle ScholarPubMed
Zimmermann, U, Wagner, H-J, Heidecker, M, Mimietz, S, Schneider, H, Szimtenings, M, Haase, A, Mitlöhner, R, Kruck, W, Hoffmann, R & König, W (2001). Implications of mucilage on pressure bomb measurements and water lifting in trees rooting in high-salinity water. Trees 16, 100–111.CrossRefGoogle Scholar
Zimmermann, U, Zhu, JJ, Meinzer, FC, Goldstein, G, Schneider, H, Zimmermann, G, Benkert, R, Thiirmer, F, Melcher, P, Webb, D & Haase, A (1994). High molecular weight organic compounds in the xylem sap of mangroves: Implications for long- distance water transport. Bot Acta 107, 2018–229.CrossRefGoogle Scholar
Zwieniecki, MA, Melcher, PJ & Holbrook, NM (2001). Hydrogel control of xylem hydraulic resistance in plants. Science 291, 1059–1062.CrossRefGoogle ScholarPubMed