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Leaflet Blade Epidermis and Its Taxonomic Significance in 13 Species of Bignonieae (Bignoniaceae) from Pico Do Jabre, Paraíba, Northeast of Brazil

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Leaflet Blade Epidermis and Its Taxonomic Significance in 13 Species of Bignonieae (Bignoniaceae) from Pico Do Jabre, Paraíba, Northeast of Brazil Botany Leaflet blade epidermis and its taxonomic significance in 13 species of Bignonieae (Bignoniaceae) from Pico do Jabre, Paraíba, Northeast of Brazil Journal: Botany Manuscript ID cjb-2020-0051.R4 Manuscript Type: Article Date Submitted by the 08-Sep-2020 Author: Complete List of Authors: Lopes-Silva, Rafael ; Universidade Federal da Paraíba, Programa de Pós- Graduação em Biodiversidade Silva, Anauara; Universidade Federal da Paraíba, Programa de Pós- GraduaçãoDraft em Produtos Naturais e Sintéticos Bioativos Santos, Ednalva ; Universidade Federal da Paraíba, Programa de Pós- Graduação em Biodiversidade Agra, Maria de Fátima; Universidade Federal da Paraíba, Programa de Pós-Graduação em Produtos Naturais e Sintéticos Bioativos epicuticular waxes, idioblasts, leaf anatomy, micromorphology, Keyword: neotropical lianas Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : © The Author(s) or their Institution(s) Page 1 of 42 Botany Leaflet blade epidermis and its taxonomic significance in 13 species of Bignonieae (Bignoniaceae) from Pico do Jabre, Paraíba, Northeast of Brazil Rafael Francisco Lopes-Silva1, Anauara Lima e Silva2, Ednalva Alves Vital dos Santos1 and Maria de Fátima Agra1,2,3 1Programa de Pós-graduação em Biodiversidade, Centro de Ciências Agrárias, Universidade Federal da Paraíba, Areia, Paraíba, Brazil. E-mail: [email protected] and E-mail: [email protected] 2Programa de Pós-graduação em Produtos Naturais e Sintéticos Bioativos, Universidade Federal da Paraíba, João Pessoa, Paraíba, Brazil. E-mail: [email protected] Draft 3Author for correspondence: Maria de Fátima Agra UFPB – Universidade Federal da Paraíba, Centro de Biotecnologia, R. Tab. Stanislau Eloy, 41-769 - Castelo Branco, João Pessoa - PB, 58033-455. +5583988077888 E-mail: [email protected] 1 © The Author(s) or their Institution(s) Botany Page 2 of 42 Abstract: Bignonieae is the largest tribe of Bignoniaceae, with 21 genera and 393 species of lianas and shrubs, 2–3-foliolate with the terminal leaflet modified as tendrils. We examined the micromorphologies of the leaflet blade epidermises of 13 species of Bignonieae belonging to Amphilophium, Anemopaegma, Bignonia, Cuspidaria, Dolichandra, Fridericia, Pyrostegia, Tanaecium, and Xylophragma, from Pico do Jabre, Paraíba, Brazil. These are lianas except for Tanaecium parviflorum (shrubby). We sought to identify epidermal leaflet parameters to support their taxonomy subject to great similarities between their vegetative characters, mainly in species of the same genus and related genera. Analyses were performed using light and scanning electron microscopy, and showed five types of epicuticular waxes, four cuticle types, three epidermal cell anticlinal wall types, and non-glandular and glandular trichomes. Hypostomatic leaves showed ten different types of stomata, with stomatal indices from 6.21% (Bignonia ramentacea) to 23.52% (Tanaecium parviflorum) and stomatal densitiesDraft from 76 stomata/mm² (Pyrostegia venusta) to 752.9 (T. parviflorum). The presence of raphides in Amphilophium crucigerum and styloids in Fridericia pubescens constitute the first records for these genera. Epidermal micromorphology provided a set of distinctive characters to separate these species, representing an additional tool to support their taxonomies, as well as that of tribe Bignonieae. Key words: epicuticular waxes, idioblasts, leaf anatomy, micromorphology, Neotropical lianas. 2 © The Author(s) or their Institution(s) Page 3 of 42 Botany Résumé: Bignonieae est la plus grande tribu de Bignoniaceae avec 21 genres et 393 espèces de lianes et d’arbustes, 2–3-foliolés avec la foliole terminale modifiée en vrille. Nous avons examiné la micromorphologie des épidermes de folioles de 13 espèces appartenant à Amphilophium, Anemopaegma, Bignonia, Cuspidaria, Dolichandra, Fridericia, Pyrostegia, Tanaecium et Xylophragma, du Pico do Jabre, Paraíba, Brésil. Ces espèces sont toutes des lianes sauf Tanaecium parviflorum (espèce arbustive). Nous cherchons à identifier les paramètres de l'épiderme foliolaire en soutien à la taxonomie au regard des grandes similitudes des caractères végétatifs, en particulier entre espèces du même genre et genres apparentés. Les analyses ont été effectuées en utilisant la microscopie optique et la microscopie électronique à balayage, et démontrent cinq types de cires épicuticulaires, quatre types de cuticules, trois formes de parois anticlinales de cellules épidermiques et des trichomes non glandulaires et glandulaires. Les feuilles hypostomatiques présentent dix types de stomates, et des indices stomatiques variantDraft de 6,21% chez Bignonia ramentacea à 23,52% chez Tanaecium parviflorum et des densités stomatiques variaient de 76 stomates/mm² chez Pyrostegia venusta à 753 chez T. parviflorum. La présence de raphides chez Amphilophium crucigerum et de styloïdes chez Fridericia pubescens font l’objet de premières descriptions de ces types d'idioblastes pour ces genres. La micromorphologie épidermique a fourni un ensemble de caractères distinctifs pour séparer ces taxons et offre un outil additionnel pour soutenir la taxonomie des espèces et de la tribu Bignonieae. Mots-clés: anatomie foliaire, cires épicuticulaires, idioblastes, lianes Néotropicales, micromorphologie. 3 © The Author(s) or their Institution(s) Botany Page 4 of 42 Introduction Bignoniaceae Juss. is divided into eight main clades, of which Bignonieae is the largest Neotropical clade of the family, comprising about 21 genera and 393 species (Lohmann and Taylor 2014), of which 327 occur in Brazil, mainly in the Amazon, Atlantic Forest, and dry forest domains (BFG 2015). The Bignonieae clade constitutes the most diverse and abundant clade of lianas in the Neotropics (Lohmann 2006; Lohmann and Taylor 2014) and, according to Gentry (1980), those Brazilian domains are the centers of diversity of the family. The Bignonieae clade is formed predominantly of lianas and shrubs species, with the greatest morphological diversity among neotropical lianas (Lohmann 2006). Their compound leaves are usually 2–3-foliolate with the terminal leaflets modified as simple, bifid, or multifid tendrils (Sousa- Baena et al. 2014). The flowers are showy and are visited by a broad range of floral visitors and pollinators (Alcantara and Lohmann 2010).Draft The monophyly of the group is supported by molecular, morphological, and anatomical characters. Morphological and anatomical synapomorphies can be observed in the modification of terminal leaflets as tendrils, the fruits are septicidal capsules with the septum parallel to the fruit valves (Olmstead et al. 2009), and irregular stem growth (which results in the formation of four to thirty-two phloem wedges that interrupt the xylem) (Santos 1995; Lohmann and Taylor 2014). Anatomical characters constitute an important tool for the taxonomy of flowering plants (Metcalfe 1946; Metcalfe and Chalk 1950, 1979; Dickison 1975). Leaf epidermal anatomy has revealed important characters in the taxonomy of distinct groups of Angiosperms with diagnostic values at various levels. Carlquist (1961) viewed the leaf as the most variable organ among angiosperms, those anatomical variations are often closely related to the generic and specific (and sometimes family) levels. The leaf epidermis has revealed several important anatomical structures whose characters have been found to be useful in the taxonomy of various groups of vascular plants, with diagnostic value at different taxonomic levels (Dilcher 1974; Metcalfe and Chalk 1979). According to 4 © The Author(s) or their Institution(s) Page 5 of 42 Botany Dickison (1975), anatomical characters of the leaf epidermis hold systematic value and phylogenetic potential, which allow the identification of plants and the resolution of taxonomic problems in different groups of vascular plants. Among the characters of the leaf epidermis that most stand out are the morphology of epidermal cuticle and epicuticular waxes (Barthlott 1998), the presence of inorganic idioblasts with different types of crystals (raphides, druses, and crystal sands) and lithocysts, as well as epidermal appendages, including different types of stomata and trichomes. The value of epidermal characters in supporting the taxonomy of Bignoniaceae has been demonstrated for some African species (Ogundipe and Wujek 2004; Ugbabe and Ayodele 2008) as well as for Brazilian species of Tabebuia Gomes ex DC. and Handroanthus Mattos (Silva et al. 2009). Additionally, the wood anatomy of Bignoniaceae has corroborated and supported relationships established within the family (Gerolamo and Angialossy 2017; Santos 2017), and within the tribe Bignonieae, revealing theDraft importance of anatomical studies for the current classification of Bignoniaceae tribes and for understanding their evolution (Pace et al. 2009; Pace et al. 2015). Additionally, other studies have focused on the quality control of medicinal species (Mauro et al. 2007; Souza et al. 2007), epidermal structures (Gonzalez 2013), the ontogeny of stomata (Paliwal 1970), and their taxonomic implications (Nogueira et al. 2013; Firetti-Leggieri et al. 2014; Sousa-Baena et al. 2014). The identification of Bignonieae taxa is quite complex without considering reproductive traits (Gentry 1992), due to their great diversity and numerous patterns of morphological variation, which often requires analyses of additional diagnostic characters (Lohmann 2006). The importance of many species of Bignonieae species for ethnobotanical uses,
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