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Secretory Structures in Leaves and Flowers of Two Dragon’S Blood Croton (Euphorbiaceae): New Evidence and Interpretations

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Secretory Structures in Leaves and Flowers of Two Dragon’S Blood Croton (Euphorbiaceae): New Evidence and Interpretations Int. J. Plant Sci. 177(6):511–522. 2016. q 2016 by The University of Chicago. All rights reserved. 1058-5893/2016/17706-0004$15.00 DOI: 10.1086/685705 SECRETORY STRUCTURES IN LEAVES AND FLOWERS OF TWO DRAGON’S BLOOD CROTON (EUPHORBIACEAE): NEW EVIDENCE AND INTERPRETATIONS Ana Carla Feio,* Ricarda Riina,† and Renata Maria Strozi Alves Meira1,* *Departamento de Biologia Vegetal, Anatomia Vegetal, Universidade Federal de Viçosa, Viçosa 36570-900, Brazil; and †Real Jardín Botánico, Consejo Superior de Investigaciones Científicas (RJB-CSIC), Plaza de Murillo 2, 28014 Madrid, Spain Editor: Patrick S. Herendeen Premise of research. Previous studies of secretory structures in species of the Neotropical dragon’s blood Croton (section Cyclostigma) show inconsistencies in their classification. An accurate assessment of the iden- tity and homology of such structures is essential for taxonomic and evolutionary studies. Methodology. Field-collected leaves, stipules, and flowers at different developmental stages were sampled. The material was subjected to standard anatomical study by light microscopy and SEM, and secretions were evaluated by histochemical analyses. Pivotal results. Leaves and flowers of Croton echinocarpus and Croton urucurana present five secretory structures (idioblasts, laticifers, colleters, extrafloral nectaries, and floral nectaries) with high similarity between the two species. Idioblasts secrete compounds of a mixed nature; laticifers are branched and nonarticulated; and colleters and nectaries present hydrophilic secretion. The leaf marginal glands previously described as extra- floral nectaries are actually colleters of the standard type. We found colleters in staminate and pistillate flowers. The histochemical tests detected proteins in the secretions of all structures. Conclusions. The classes of secondary metabolites detected support the biological activities of secretion described in the literature. The correct identification of colleters in flowers establishes a new register of these structures in flowers of this genus. We show that an approach integrating anatomic structure, histochemistry, and period of secretion activity allows for a more accurate classification and homology assessment of secretory elements in this genus, which is exceptionally rich in this type of structures. Keywords: anatomy, colleters, Crotoneae, histochemistry, nectaries, stipules. Introduction ginal glands have been described as colleters of the standard type in different sections of Croton and other Crotoneae gen- Croton echinocarpus Müll. Arg. and Croton urucurana Baill. era (Astraea Klotzsch and Brasiliocroton P.E. Berry & Cordeiro; are members of section Cyclostigma, a group of tree species Riina et al. 2014, 2015; Vitarelli et al. 2015). De-Paula et al. popularly known as dragon’s blood because of the exudation (2011), in a study of the floral morphology and anatomy of sev- of abundant red latex (Riina et al. 2009; van Ee et al. 2011) eral Crotoneae species, including C. urucurana, found glands that is used for medicinal purposes across the Neotropics. Be- alternate to floral nectaries that they described as filamentous sides laticifers, four other secretory structures (colleters, idio- structures. These authors also reported glands along the surface blasts, extrafloral nectaries, and secretory trichomes) have been of sepals as secretory trichomes, although they noted their sim- identified in the leaves of several Croton lineages from sections ilarity to colleters (De-Paula et al. 2011). other than Cyclostigma (Vitarelli et al. 2015). Previous anatom- For an accurate classification of a secretory structure, its an- ical surveys on members of Cyclostigma included the two spe- atomical characterization must be accompanied by an analysis cies studied here and described secretory structures from both of the chemical nature of its exudate and an evaluation of the leaves and flowers (Sá-Haiad et al. 2009; De-Paula et al. 2011); period of secretory activity. Descriptions based solely on mor- however, classification and homology assessment of such struc- phology are not sufficient to assign a role to a structure (Lersten tures remain unclear and require further investigation. and Curtis 1996) or to determine the importance of the exudate Extrafloral nectaries have been recorded to occur on the for the plant. In addition, morphologically similar structures margin, base, and blade of leaves of C. echinocarpus and may play different functional roles. Extrafloral nectaries can C. urucurana (Sá-Haiad et al. 2009). However, similar mar- be confused with other secretory structures, such as colleters, because the latter are also external structures that can have sim- 1 Author for correspondence; e-mail: [email protected]. ilar anatomy and topology. However, the period of activity and Manuscript received October 2015; revised manuscript received December the composition of the secretion show that the activity of 2015; electronically published May 24, 2016. colleters is earlier than that of nectaries, and the colleters’ secre- 511 This content downloaded from 161.111.170.152 on August 27, 2018 23:52:10 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 512 INTERNATIONAL JOURNAL OF PLANT SCIENCES tion is characterized by the presence of mucilage, lipids, and pro- et al. 1965), and slides were mounted with synthetic resin (Per- teins and the absence of sugar (Fahn 1979; Thomas 1991; Cruz mount, Fisher Scientific, Fair Lawn, NJ). et al. 2002; Klein et al. 2004; Barreiro and Machado 2007). Nec- Part of each sample was also dehydrated through a tert- taries, on the other hand, secrete nectar, a sugary substance con- butanol series (Johansen 1940), embedded in histological par- sisting mainly of glucose, fructose, and sucrose (Fahn 1979; affin with DMSO (Histosec, Merck, Darmstadt, Germany), and Bentley and Elias 1983). serially sectioned at 10–12-mm thickness on a rotary microtome Because of inconsistencies in distinguishing between nectaries (Spencer 820, American Optical, Buffalo, NY). For structural and colleters in previous studies of Croton and the importance of characterization, longitudinal and cross sections were stained an accurate classification of such structures for taxonomy and with Astra blue 1% (Kropp 1972) and Safranin O 1% (Bukatsch evolutionary studies requiring accurate homology assessment, 1972, adapted) and mounted with synthetic resin. For structural we analyze the structure and histochemistry of leaf and floral se- characterization and histochemical tests, floral samples were cretory structures of C. echinocarpus and C. urucurana. We also dehydrated through tert-butanol series and embedded in histo- discuss the relationship between structure, secretion composi- logical paraffin with DMSO. tion, and function as well as the chemical nature of the secretions For detection of the main classes of secondary compounds, and its connections to the phytochemistry findings and medici- the following histochemical tests were carried out: periodic nal uses reported for both species in the literature. acid–Schiff reagent for total polysaccharides (McManus 1948); ruthenium red for acidic mucilage (Gregory and Baas 1989); Material and Methods tannic acid/ferric chloride for neutral mucilage (Pizzolato and Lillie 1973); Sudan black B (Pearse 1985) and neutral red (Kirk Croton echinocarpus is endemic to the Atlantic Forest of 1970) for total lipids in visible and UV light, respectively; NADI southeastern Brazil (Caruzo and dos Santos 2015), while Cro- reagent for terpenoids (David and Carde 1964); copper acetate/ ton urucurana is more widely distributed in southern South rubeanic acid for fatty acids (Ganter and Jollés 1969–1970); America (Brazil, Argentina, Paraguay, and Bolivia), occurring Nile blue for neutral and acidic lipids (Cain 1947); vanillin/ as a pioneer species in riparian forest (Caruzo and Cordeiro hydrochloric acid for tannins (Mace and Howell 1974); Wag- 2007; Cordeiro et al. 2015). Both species occur spontaneously ner’s reagent for alkaloids (Furr and Mahlberg 1981); and in Minas Gerais state, as well as around the Universidade Fede- xilidine ponceau (O’Brien and McCully 1981) and ninhydrin/ ral de Viçosa campus (20745010.10900S, 42752016.16700W) and Schiff’s reagent (Pearse 1985) for protein. Standard control pro- along the BR-356 road (2075403.93900S, 42739012.85700W), where cedures were carried out simultaneously as required for each fieldwork for this study was conducted. Samples were collected test, and the slides were mounted in glycerinated gelatin (Kaiser from vegetative and reproductive branches of both species. Her- 1880). To verify the occurrence of glucose in the secretion, barium vouchers were deposited at the VIC herbarium (Cou- Glicofita Plus (Accu-Chek Active, Hoffmann-La Roche) was tinho et al. 337, 338, 25/I/2014 [VIC]). Leaves at different de- used directly on the secretion. velopmental stages (shoot apex, leaf primordium, and mature Observations and photographic documentation were per- leaves), stipules, and staminate and pistillate flowers in different formed with a light microscope (Model AX70TRF, Olympus Op- stages of development were sampled (from bud to early fruit). tical, Tokyo) equipped with a U-Photo system and a digital camera Three fixative treatments were used for three different sets (AxioCam HRc, Carl Zeiss, Göttingen, Germany), an epifluo- of samples. The first set was fixed in FAA (formalin∶acetic rescence HBO 50-W mercury vapor lamp, and a filter block A (ex- acid∶ethanol
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