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Asteraceae) from the Campos Rupestres Anais da Academia Brasileira de Ciências (2015) 87(2): 797-812 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201520140214 www.scielo.br/aabc Anatomy and fructan distribution in vegetative organs of Dimerostemma vestitum (Asteraceae) from the campos rupestres TAIZA M. SILVA1, DIVINA A.A. VILHALVA2*, MOEMY G. MORAES2 and RITA DE CÁSSIA L. FIGUEIREDO-RIBEIRO3 1Programa de Pós-Graduação em Biodiversidade Vegetal, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Campus Samambaia, Av. Esperança, s/n, 74690-900 Goiânia, GO, Brasil 2Instituto de Ciências Biológicas, Universidade Federal de Goiás, Campus Samambaia, Av. Esperança, s/n, 74690-900 Goiânia, GO, Brasil 3Núcleo de Pesquisa em Fisiologia e Bioquímica, Instituto de Botânica, Av. Miguel Stéfano, 3687, Água Funda, 04301-902 São Paulo, SP, Brasil Manuscript received on April 28, 2014; accepted for publication on October 24, 2014 ABSTRACT Among the compounds stored by plants, several functions are assigned to fructans, such as source of energy and protection against drought and extreme temperatures. In the present study we analyzed the anatomy and distribution of fructans in vegetative organs of Dimerostemma vestitum (Asteraceae), an endemic species from the Brazilian campos rupestres. D. vestitum has amphistomatic and pubescent leaves, with both glandular and non-glandular trichomes. In the basal aerial stem the medulla has two types of parenchyma, which differ from the apical portion. The xylopodium has mixed anatomical origin. Interestingly, although inulin-type fructans with high degree of polymerization were found in all analyzed organs except the leaves, the highest amount and maximum degree of polymerization were detected in the xylopodium. Inulin sphero-crystals were visualized under polarized light in the medulla and in the vascular tissues mainly in the central region of the xylopodium, which has abundant xylem parenchyma. Secretory structures accumulating several compounds but not inulin were identified within all the vegetative organs. The presence of these compounds, in addition to inulin, might be related to the strategies of plants to survive adverse conditions in a semi-arid region, affected seasonally by water restriction and frequently by fire. Key words: Campo rupestre, fructans, inulin spherocrystals, secretory structures, xylopodium. INTRODUCTION of São Paulo, Rio de Janeiro, Minas Gerais, Bahia Campo rupestre is a vegetation characterized by and Goiás, predominantly in areas with about shrubby-herbaceous species growing on mountains 900 m altitude (Neves and Conceição 2010). This of quartzite and sandstone in the Brazilian states Cerrado physiognomy presents a highly diverse and endemic flora with a high number of endangered Correspondence to: Moemy Gomes de Moraes species (Echternacht et al. 2011). Several adaptive E-mail: [email protected] *Bolsista DCR/CNPq/FAPEG traits are exhibited by such species, which are An Acad Bras Cienc (2015) 87 (2) 798 TAIZA M. SILVA et al. interpreted as strategies to cope with unfavorable originated from the radial growth of roots, stems or environmental factors including low availability of a mixture of both structures. Therefore, xylopodia water and nutrients, and fire (Coutinho 2002). are characterized by self-grafting of different stem The presence of underground reserve organs is a axes with bud-forming capacity (Appezzato-da- distinct characteristic of several herbaceous species in Glória et al. 2008a). the campo rupestre, which provides a rapid sprouting Dimerostemma vestitum (Baker) SF Blake after fire (Neves and Conceição 2010, Hoffmann is an herbaceous-subshrubby species of the et al. 2012). In general, underground organs Heliantheae tribe (Asteraceae) with a typical and accumulate carbohydrates such as starch, sucrose, conspicuous xylopodium. This species is endemic oligosaccharides and soluble polysaccharides to Brazil and abundant in campos rupestres from when the production of photoassimilates exceeds Goiás, Distrito Federal and Minas Gerais (Moraes the demand (Pollock 1986). A screening of and Semir 2009), but it has not yet been studied underground organs of Cerrado plants revealed with regards to fructan occurrence or the anatomy the occurrence of soluble carbohydrates, starch of the vegetative organs. and proteins in different species and types of Many Asteraceae species accumulate fructans underground systems, with soluble carbohydrates mainly in the vacuole of parenchyma cells of being more abundant than starch in several species thickened underground organs, where they (Figueiredo-Ribeiro et al. 1986). fulfill the main role of storing carbohydrates. In Asteraceae is one of the most endemic and addition, these compounds are thought to stabilize abundant families in campo rupestre (Giulietti et al. membranes, to function as osmoregulators (Car- 1987). The abundance of secretory structures rich valho et al. 2007, Livingston et al. 2009) and to in secondary metabolites, in aerial and underground protect plants against reactive oxygen species organs is an interesting feature of the Asteraceae, (Peshev et al. 2013). Fructans are fructose and is possibly related to defense mechanisms polymers containing one internal or terminal against herbivores, pathogenic microorganisms glucose unit. Inulin-type fructans consist of and/or associated with attraction of pollinators linear molecules with β 2,1 linkages, based on (Melo-de-Pinna and Menezes 2002, Vilhalva and the trisaccharide 1-kestose, occurring mainly in Appezzato-da-Glória 2006a, Cury and Appezzato- eudicot species, and reaching nearly 80% of the da-Glória 2009). Glandular trichomes accumulating dry mass in storage organs of temperate (Edelman several secondary substances were reported in both and Jefford 1968) and subtropical Asteraceae aerial (leaf and bud) and underground reserve species (Carvalho et al. 2007). organs of two Chrysolaena species (Vernonieae, In this work, we studied the anatomy and the Asteraceae) from the Cerrado (Appezzato-da- location of reserve compounds in the vegetative Glória et al. 2012). Another marked feature in organs of Dimerostemma vestitum from the Asteraceae is the diversity of underground reserve campo rupestre and described accumulation of organs, as exemplified by Calea verticillata (Klatt) high amounts of inulin in the xylopodium. This Pruski, Isostigma megapotamicum (Spreng.) Sherff feature, in addition to the presence of several (Vilhalva and Apezzato-da-Glória 2006b), both secondary compounds in the buds are possibly presenting xylopodium, and Vernonia grandiflora related to the ecophysiological strategies of the Less (Hayashi and Apezzato-da-Glória 2007), plant to survive adverse conditions in a semi-arid with tuberous roots and xylopodium. Generally, region affected seasonally by water restriction xylopodia are morphologically complex structures, and frequently by fire. An Acad Bras Cienc (2015) 87 (2) FRUCTANS IN Dimerostemma vestitum 799 MATERIALS AND METHODS xylopodium samples were dehydrated in a graded ethanol series, and embedded in Leica Historesin®. PLANT MATERIAL Serial sections (7-10 µm thick) were cut on a rotary For this study adult individuals of Dimerostemma microtome RM 2245 (Leica, Germany), stained vestitum were collected in the flowering phase with with 0.05% toluidine blue in a Mcllvaine buffer of 7-9 fully developed nodal regions in a preserved area pH 4.0 (Vidal 1977) and mounted in synthetic resin. of campo rupestre at the “Reserva Biológica Prof. For scanning electron microscopy (SEM) José Ângelo Rizzo - Serra Dourada” - Mossâmedes, analyses, samples of mature leaves and xylopodia Goiás, Brazil (16°06′02″ - 16°03′52″ S and 50°10′59″ from three plants were fixed in Karnovsky solution - 50°10′12″ W). D. vestitum is a perennial herb or (Karnovsky 1965), dehydrated in graded ethanol subshrub measuring 1 m, woody at the base, mostly series and dried to the CO2 critical-point. Following, caespitose, from the xylopodium. Leaf blades are the samples were mounted on stubs, coated with chartaceous and tomentose to subtomentose (Moraes gold (30 - 40 nm) and examined under a JSM-6610 and Semir 2009). A voucher specimen (UFG 46597) microscope (JEOL, Japan). was deposited in the Herbarium UFG of the Federal Free-hand sections from fixed and fresh University of Goiás (Brazil). material of six individuals were stained for the Samples of the aerial parts (fully expanded histochemical tests with Sudan IV (Gerlach 1984) leaves from the third nodal region and young stems and Steinmetz reagent (Costa 1970) for total lipids; from the first and the basal internodes) and of the Periodic acid-Schiff’s reagent (PAS) for total neutral underground organs (xylopodium and lateral roots) polysaccharides (McManus 1948); Comassie blue were selected for structural, histochemical and (Fisher 1968) and Xylidine Ponceau reagent (Vidal reserve carbohydrate analyses. The xylopodium 1977) for total proteins; Zinc chloride iodine (Kraus was transversely divided into proximal, medium and and Arduin 1997) and Lugol reagent (Johansen 1940) distal regions for ultrastructural and histochemical for starch. Samples were also fixed in Formalin- analyses and sectioned in central (medullar ferrous sulfate reagent (Johansen 1940) for the parenchyma) and peripheral regions (cortex and detection of phenolic compounds. In order to identify vascular cylinder) for quantitative and qualitative inulin-type fructans, samples of the xylopodium
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