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Mucilaginous Secretions in the Xylem and Leaf Apoplast of the Swamp Palm Mauritia Flexuosa L.F

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Mucilaginous Secretions in the Xylem and Leaf Apoplast of the Swamp Palm Mauritia Flexuosa L.F Microscopy and Microanalysis (2020), 1–13 doi:10.1017/S1431927620001543 Micrographia Mucilaginous Secretions in the Xylem and Leaf Apoplast of the Swamp Palm Mauritia flexuosa L.f. (Arecaceae) Alessandra Flávia Silveira1, Maria Olívia Mercadante-Simões1* , Leonardo Monteiro Ribeiro2, Yule Roberta Ferreira Nunes3, Lucienir Pains Duarte4, Ivana Silva Lula4, Mariana Guerra de Aguilar4 and Grasiely Faria de Sousa4 1Plant Anatomy Laboratory, General Biology Department, State University of Montes Claros, Montes Claros 39401-089, Brazil; 2Plant Micropropagation Laboratory, General Biology Department, State University of Montes Claros, Montes Claros 39401-089, Brazil; 3Plant Ecology Laboratory, General Biology Department, State University of Montes Claros, Montes Claros 39401-089, Brazil and 4Medicinal Plants Study Center, Chemistry Department, Federal University of Minas Gerais, Belo Horizonte 31270-901, Brazil 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, histochem- ical 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. Key words: arabinose, pectin, plant mucilage, rhamnose, sclerenchymatic fiber, vessel element (Received 18 June 2019; revised 8 April 2020; accepted 27 April 2020) Introduction An abundant gelatinous secretion exudes from the stipe of M. flexuosa when it is perforated and is harvested by traditional pop- Mauritia flexuosa L.f. (locally “buriti” or “aguaje”) is the most ulations to produce a fermented beverage—buriti wine (Dias & abundant palm tree in Brazil, although it occurs only in hyperhu- Laureano, 2000). The wines produced by the fermented sap of mid habitats and wetlands (Holm et al., 2008; Lorenzi et al., the petioles and floral axes of African and Indian palm trees are 2010). The species originated in the Amazonian rainforest and, used as a beverage and have potential for use as biofuels together with Mauritiella armata (Calamoideae, Mauritiinae), rep- (Tamunaidu et al., 2013; Bi et al., 2016). Despite the importance resent the only swamp palms to adapt to the seasonal Brazilian of those M. flexuosa secretions, there are no studies examining savanna biome with its prolonged dry periods (Lima et al., 2014; their synthesis and distribution, or ecological functions that Reis et al., 2017). M. flexuosa is considered a key species in the could contribute to our botanical knowledge of those palms or Brazilian savanna wetlands (known as “Veredas”), providing food to the development of technologies for their sustainable use. for the local fauna and contributing to the preservation of springs The present work was therefore designed to study the chemi- and other surface waters (Porto et al., 2017). The species provides cal, anatomical, and ultrastructural aspects of the gelatinous secre- important natural resources for traditional populations, as its fruit tions that exude from the stipe and petiole of M. flexuosa, discuss pulp is used in cooking and several plant parts furnish raw mate- their ecological roles, and to respond to the following questions: rials for construction and crafts (Dias & Laureano, 2000; Lorenzi What is the chemical nature of those secretions? Where do they et al., 2010; Virapongse, 2017). Oil extracted from the fruit meso- accumulate in the plant? What are the synthesis and secretion carp is of high quality and valued by pharmaceutical and cosmetic mechanisms? industries—which has stimulated interest in its domestication and agroindustrial production (Koolen et al., 2013). Materials and Methods *Author for correspondence: Mercadante-Simões, E-mail: [email protected]. Secretion Collections Cite this article: Silveira AF, Mercadante-Simões MO, Ribeiro LM, Nunes YRF, Duarte LP, Lula IS, de Aguilar MG, de Sousa GF (2020) Mucilaginous Secretions in Stipe and petiole secretions were collected from three adult the Xylem and Leaf Apoplast of the Swamp Palm Mauritia flexuosa L.f. (Arecaceae). individuals of M. flexuosa growing in the Pandeiros River Microsc Microanal. doi:10.1017/S1431927620001543 Environmental Protection Area in the Brazilian savanna in the © Microscopy Society of America 2020 Downloaded from https://www.cambridge.org/core. East Carolina University, on 04 Jun 2020 at 11:49:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S1431927620001543 2 Alessandra Flávia Silveira et al. Fig. 1. Adult individuals of Mauritia flexuosa L. f. (Arecaceae) and mucilaginous secretions. (a) A wetland area of “Vereda” in the Brazilian Savanna Biome. (b,c) Stipe. Secretion (arrow) exuding from perforations. (d,e) Petiole. Secretion (arrow) exuding from a sectioned petiole. st, stipe; pe, petiole. municipality of Bonito de Minas, northern Minas Gerais State, acid, and the solution was dried at room temperature. The boric Brazil (15°13′48′′S × 44°54′92′′W) (Fig. 1a). The secretions acid was evaporated in the form of trimethyl borate through suc- (Figs. 1b, 1c) were obtained by perforating the stipes (at breast cessive methanol washes, and the alditols formed were acetylated – height) with a hand-held boring tool previously disinfected with in a reaction with 1.0 mL of an Ac2O pyridine mixture (1:1, v/v) 95% alcohol. Petiole secretions (Figs. 1d, 1e) were obtained by for 12 h, with constant stirring at room temperature. Ice was then natural exudation after cutting the leaves. All of the secretions added to the solution and the resulting alditol acetates were were collected in sterile amber glass bottles and immediately extracted with dichloromethane (5 mL). The organic phase was frozen to −20°C. repeatedly washed with 1 M HCl and distilled water. The alditol μ acetates (2.0 L, 2% CHCl3 solution) were analyzed using GC–FID in a HP 7820A (Agilent Technologies, Santa Clara, Neutral Monosaccharide Compositions CA, USA) chromatograph fitted with a BP10 capillary column Stipe and petiole secretions were lyophilized and submitted to (25 m × 0.22 mm i.d.), detector temperature 270°C, injection in total acid hydrolysis. The lyophilized samples (∼5mg) were a split mode (1:20) at 270°C, H2 as the carrier gas (3.0 mL/min), then diluted in 10.0 mL of 2 M TFA with constant stirring and initial temperature 200°C (3 min), then increasing from 200 to refluxed at 100°C for 6 h. After forced-air evaporation, the hydro- 260°C (4°C/min). Glucose, galactose, xylose, mannose, rhamnose, lyzed samples were resuspended in 1.0 mL of distilled water with and arabinose standards were submitted to reduction and 7.5 mg of NaBH4; two drops of basic aqueous solution (1% v/v, acetylation reactions, as previously described. The monosaccha- NH4OH) were then added at room temperature with stirring ride compositions of both secretions were determined using the for 12 h. Excess NaBH4 was eliminated by adding glacial acetic methodology described by Cantu-Jungles et al. (2015), with Downloaded from https://www.cambridge.org/core. East Carolina University, on 04 Jun 2020 at 11:49:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S1431927620001543 Microscopy and Microanalysis 3 some modifications (increase of reaction times, evaporation of the 1978) and analyzed in a Tecnai G2-20-SuperTwin transmission reaction mixture after hydrolysis, addition of 1 mL of water after electron microscope (FEI Company, Eindhoven, Netherlands) at NaBH4 reduction, removal of excess NaBH4 by adding glacial ace- 150 kV. tic acid and evaporation of boric acid in the form of trimethyl Root, petiole, and leaf samples for scanning electron micros- borate through successive methanol washes, addition of ice to copy (SEM) studies were obtained by cryofracture in liquid N2, the solution and alditol acetate extraction with dichloromethane, fixed in 2.5% glutaraldehyde (0.1 M phosphate buffer, pH 7.2), – – and use of GC FID instead of GC MS in the quantification of dehydrated in an ethyl series to the critical point with CO2, coated “alditol acetates”). with a gold layer in a Bal-Tec-MD20 metallizer (Leica Microsystems, Heidelberg, Germany) (Robards, 1978), and ana- lyzed using a Quanta 200 scanning electron microscope (FEI Infrared and Nuclear Magnetic Resonance Company, Eindhoven, Netherlands) at 12–20 kV. To detect the Fourier-transformed infrared (FT-IR) spectra (∼1% KBr solution) presence of
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