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Tank-Inflorescence in Nidularium Innocentii (Bromeliaceae): Three-Dimensional Model and Development

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Tank-Inflorescence in Nidularium Innocentii (Bromeliaceae): Three-Dimensional Model and Development See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/320843762 Tank-inflorescence in Nidularium innocentii (Bromeliaceae): Three- dimensional model and development Article in Botanical Journal of the Linnean Society · October 2017 DOI: 10.1093/botlinnean/box059 CITATIONS READS 11 321 7 authors, including: Fernanda Nogueira Sofia Kuhn Universidade Federal do Oeste do Pará Universidade Federal do Rio Grande do Sul 11 PUBLICATIONS 55 CITATIONS 7 PUBLICATIONS 46 CITATIONS SEE PROFILE SEE PROFILE Felipe Luis Palombini Gabriel H. Rua Universidade Federal do Rio Grande do Sul Universidad de Buenos Aires 38 PUBLICATIONS 181 CITATIONS 53 PUBLICATIONS 596 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Conservação e caracterização dos recursos genéticos de espécies de gramíneas nativas do Brasil View project Study of Partial Volume Effect on X-ray Microtomography's images View project All content following this page was uploaded by Fernanda Nogueira on 15 November 2017. The user has requested enhancement of the downloaded file. Botanical Journal of the Linnean Society, 2017, 185, 413–424. With 5 figures. Tank-inflorescence in Nidularium innocentii (Bromeliaceae): three-dimensional model and development FERNANDA M. NOGUEIRA1, SOFIA A. KUHN1, FELIPE L. PALOMBINI2, GABRIEL H. RUA3, AVACIR C. ANDRELLO4, CARLOS ROBERTO APPOLONI4 and JORGE E. A. MARIATH1* 1Laboratory of Plant Anatomy LAVeg, Institute of Biosciences, Department of Botany, Federal University of Rio Grande do Sul (UFRGS), Av. Bento Gonçalves, 9500, Porto Alegre, RS, Brazil 2Laboratory of Design and Material Selection LdSM, Federal University of Rio Grande do Sul (UFRGS), Av. Osvaldo Aranha 99/604, 90033-190, Porto Alegre, RS, Brazil 3Universidad de Buenos Aires, Facultad de Agronomía, Cátedra de Botánica Sistemática, Avenida San Martín 4453, C1417DSE, Buenos Aires, Argentina 4Applied Nuclear Physics Laboratory, Londrina State University (UEL), Rod. Celso Garcia Cid, Km 380, Londrina, PR, Brazil Received 8 March 2017; revised 30 May 2017; accepted for publication 11 August 2017 In Nidularium, inflorescence branches are subtended by large floral bracts, in which water accumulates. The branch- ing pattern is obscured because their internodes remain short, hampering their interpretation. This study focuses on the development of the inflorescence in N. innocentii, combining different approaches in order to understand its architecture and summarize it in a three-dimensional (3D) model. We also present the interpretation of tank- inflorescence development, recognizing the processes that have taken place in the evolution of this structure in this group. The inflorescence was typified based on Troll’s and Weberling’s systems. Development was studied using light microscopy and X-ray microcomputed tomography. The system is polytelic; the main axis ends in the main flores- cence and bears lateral paraclades with coflorescences. Each lateral branch develops in the axil of a bract, which is large and displays alternate arrangement. No prophylls were observed in the system. In the 3D reconstruction, the volume of the model was calculated. The volume of the empty region is c. 2.4 times higher than the plant material. Tank-inflorescence development seems to have occurred by the combination of three processes: bract disposition and its overgrowth; failure in internode elongation; and paraclade flattening. The tank-inflorescence evolved in a few groups of core bromelioids, and may be associated with floral protection. ADDITIONAL KEYWORDS: Bromelioideae – nidularioids – inflorescence architecture - X-ray microcomputed tomography (μCT). INTRODUCTION structures is frequently insufficient for a proper under- standing of inflorescence morphology, resulting in a An inflorescence is usually defined as a shoot system in problem that requires more sophisticated analytical which flowers develop (Troll, 1964). A wide diversity of tools. Comparative typological analysis has proved to inflorescence patterns is exhibited by the angiosperms be a powerful approach for generating primary homol- (Weberling, 1965) as a result of different combinations ogy hypotheses. In this sense, descriptions based on of developmental events. Simple observation of mature Troll’s (1964, 1969) and Weberling’s (1989) systems, which consider the branch systems and the position of each structural unit within the inflorescence as a whole (Weberling, 1965), are accurate and reliable *Corresponding author. E-mail: [email protected] © 2017 The Linnean Society of London, Botanical Journal of the Linnean Society, 2017, 185, 413–424 413 414 F. M. NOGUEIRA ET AL. for examining, describing and naming morphologi- system and the subtending bracts and calculation of cal features of inflorescences and drawing homology the retained water volume, leading to an accurate mor- statements that can drive future evolutionary devel- phological and functional interpretation in virtually opmental research (Rua, 2003; Tortosa, Rua & Bartoli, any plane (Staedler, Masson & Schönenberger, 2013). 2004; Acosta et al., 2009; Stützel & Trovó, 2013). The nidular inflorescence shared by some nidulari- In Bromeliaceae subfamily Bromelioideae, the so- oids brings up some questions, especially when and called ‘nidularioid genera’ (Silvestro, Zizka & Schulte, why this particular morphology has evolved. Is it pos- 2014; Evans et al., 2015; Heller et al., 2015; Santos- sible that this structure evolved in tankless ancestors Silva et al., 2017) comprise an assemblage of genera acting as a water-impounding tank? Could water cap- that mostly occupy humid forest habitats, typical ture in floral bracts make an important contribution of the Brazilian Atlantic Forest. They share a set of to the water balance of floral development? This study morphological traits, which includes a particular focuses on the development of the inflorescence in inflorescence morphology (Leme, 1997, 1998, 2000; N. innocentii, combining different approaches in order Santos-Silva et al., 2017). Otherwise, the relationship to understand the architecture and summarize it in a among these genera is poorly understood, and the 3D model. We also discuss the interpretation of tank- inflorescence arrangement probably does not reflect inflorescence development, describing the processes a synapomorphy for this group (Santos-Silva et al., that may have occurred in the evolution of this struc- 2017). Nidularium Lem., one of the nidularioid gen- ture and its biological consequences. era, is widely distributed in the Neotropics, from the Brazilian states of Bahia to Rio Grande do Sul, occur- ring not only in the Atlantic Forest but also in con- MATERIAL AND METHODS trasting biomes such as caatinga (Leme, 2000; Flora do Brasil, 2020). Nidularium can be distinguished BOTANICAL MATERIAL from related genera [e.g. Canistropsis (Mez) Leme, Specimens of N. innocentii were collected in the field Wittrockia Lindm. and Edmundoa Leme] especially and maintained in the Living Collection of Plant with regard to inflorescence architecture, as it has Anatomy Laboratory (LAVeg) at the Universidade large floral bracts in which water accumulates. This Federal do Rio Grande do Sul (UFRGS), Porto Alegre, strategy might be associated with floral protection Brazil. Forty-nine individuals were analysed at dif- (Leme, 2000). Water-storage bract systems in inflo- ferent developmental stages: 28 at anthesis and 21 in rescences resemble the water-impounding foliage of early stages of development, 18 of which were studied Bromeliaceae and can accumulate up to 100 mL in with light microscopy and three with µCT. A voucher N. innocentii Lem. (Leme, 2000). specimen was deposited at ICN (ICN 190905). The inflorescence of Nidularium consists of a com- plex branched system, with large floral bracts, referred to as ‘nidular inflorescences’ by some authors (Benzing, DESCRIPTIVE BACKGROUND 2000; Leme, 2000). The inflorescence has short inter- Inflorescences were analysed and described using a nodes, causing difficulty in its interpretation. Studies typology-based comparative approach (Troll, 1964, in the genus have not followed any typological criteria 1969; Weberling, 1965, 1989), to allow further compari- in describing inflorescences and have applied terms sons with other genera of Bromeliaceae in a coherent such as compound, cyathium or corymb, preventing framework. comparative morphological studies (Mez, 1934–1935; Smith & Downs, 1979; Leme, 2000). The enhancement of non-invasive methods, such as PREPARATION FOR LIGHT MICROSCOPY X-ray microcomputed tomography (μCT), is providing Inflorescences in early stages of development were new interpretations of structural and morphological collected and dissected. Inflorescence fragments were plant organization (Stuppy et al., 2003; Dhondt et al., fixed in 1% glutaraldehyde and 4% formaldehyde in 2010; Oskolski et al., 2015; Palombini et al., 2016). 0.1 M sodium phosphate buffer, pH 7.2 (McDowell & Through this method, thousands of two-dimensional Trump, 1976), and washed in 0.1 M sodium phosphate (2D), high-resolution radiographic projections are gen- buffer, pH 7.2. Material was dehydrated in an ethanol erated from a single sample and are later combined series (10−100%) and embedded in hydroxyethylmeth- and reconstructed in three dimensions by a computer acrylate (Gerrits & Smid, 1983). Thin sections (4 µm algorithm (Stock, 2009). The three-dimensional (3D) thick) were mounted
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