Comparison of Floral Structure and Ontogeny in Monoecious and Dioecious Species of the Palm Tribe Chamaedoreeae (Arecaceae; Arecoideae)
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Int. J. Plant Sci. 177(3):000–000. 2016. q 2016 by The University of Chicago. All rights reserved. 1058-5893/2015/17703-00XX$15.00 DOI: 10.1086/684262 COMPARISON OF FLORAL STRUCTURE AND ONTOGENY IN MONOECIOUS AND DIOECIOUS SPECIES OF THE PALM TRIBE CHAMAEDOREEAE (ARECACEAE; ARECOIDEAE) Felipe Castaño,* Xavier Marquínez,† Michèle Crèvecoeur,‡ Myriam Collin,* Fred W. Stauffer,§ and James W. Tregear1,* *Institut de Recherche pour le Développement (IRD), Unité Mixte de Recherche–Diversité, Adaptation, et Développement des Plantes, Centre IRD Montpellier, BP 64501, 911, avenue Agropolis, cedex 5, 34394 Montpellier, France; †Departamento de Biología, Universidad Nacional de q1 Colombia, sede Bogotá, Carrera 30 45-03, Edificio 421, Bogotá, Colombia; ‡Université de Genève, Faculté des Sciences, Département de Botanique et Biologie Végétale, quai Ernest Ansermet 30, 1211 Genève 4, Switzerland and §Conservatoire et Jardin Botaniques de la Ville de Genève, Université de Genève, Laboratoire de Systématique Végétale et Biodiversité, CP 60, CH-1292 Chambésy, Switzerland Editor: Bruce K. Kirchoff Premise of research. The sexuality of flowers is an important reproductive character in angiosperms. An insight into the evolutionary events that led to the appearance of monoecious and dioecious species can be gained by comparing closely related groups with contrasting characters. For this study, we focused on the tribe Chamaedoreeae, within which dioecy appears to have evolved twice from a monoecious ancestor. Methodology. To improve our knowledge of flower structure and ontogeny in this group, SEM and an- atomical sectioning were performed on inflorescences and flowers of the dioecious species Chamaedorea tepejilote and the monoecious species Hyophorbe lagenicaulis at different developmental stages. Pivotal results. Our data highlighted that the higher degree of spatial sexual separation seen in the dioe- cious C. tepejilote, compared to the monoecious H. lagenicaulis, is accompanied by a more accentuated di- morphism between male and female flowers. More specifically, in the case of C. tepejilote, the vestigial repro- ductive organs (staminodes of the female flower and pistillode of the male flower) are more rudimentary structures, in terms of their developmental differentiation, than their homologs in H. lagenicaulis. Conclusions. Our data suggest that the unisexual flowers already present in the monoecious ancestor of the Chamaedoreeae underwent further modifications either shortly before or since the appearance of dioecy in the genus Chamaedorea. These structural changes were presumably the result of genomic mutations causing earlier developmental arrest of the vestigial reproductive organs and are likely, in turn, to have conferred en- hanced resource-allocation efficiency. Keywords: flower development, Chamaedoreeae, Hyophorbe, Chamaedorea, monoecy, dioecy. Introduction duction in the possible negative consequences of hermaphro- ditism (e.g., gamete wastage), collectively referred to as sexual Flowers are the complex reproductive structures produced interference (Barrett 2002). Second, unisexual flowers provide by angiosperms and are considered to have played a central role a means to favor outbreeding and therefore heterosis or hybrid in the evolutionary success of this group (Endress 1994). They vigor (Freeman et al. 1997). Male and female flowers may be contain the organs necessary to produce pollen and ovules for produced on either the same plant (monoecious species) or sep- seed production. Depending on the species, male and female arate plants (dioecious species). Dioecy is a mechanism that reproductive organs may be separated in different ways in time ensures total outbreeding but can also be considered in some and space. In contrast to the situation in animals, plants are respects as inefficient in that only about half of the population mostly hermaphrodites. However, some species, representing bears seeds (Richards 1997). In monoecious species, the tempo- approximately 10% of flowering plants, produce unisexual ral separation of male and female functions, a condition known male or female flowers (Ainsworth 2000). Sexual separation be- as dichogamy, has also been interpreted as a mechanism to re- tween pistillate (female) and staminate (male) flowers is consid- duce self-fertilization (Bertin and Newman 1993). ered to confer several advantages. First, the diversification of Sexual differentiation and breeding systems are important roles between male flowers devoted to pollen production and factors in the formation of fruits and seeds, which are the most female flowers producing ovules and seeds results in a more common products harvested from crop plants. Moreover, sex- efficient use of available resources and, more generally, a re- ual systems are of key importance in population genetics and evolution. In the case of dioecy, a number of observations have 1 Author for correspondence; e-mail: [email protected]. been made regarding its geographical and phylogenetic distri- Manuscript received May 2015; revised manuscript received September 2015; bution. Examples of general tendencies observed for dioecious electronically published February XX, 2016. clades include tropical distribution, inconspicuous flower or 000 42822.proof.3d 1 Achorn International 01/13/16 01:35 000 INTERNATIONAL JOURNAL OF PLANT SCIENCES inflorescence production, lower species richness, and wind pol- appear to have evolved independently on numerous occasions lination (Heilbuth 2000). Dioecy has evolved numerous times in various different lineages within the family (Weiblen et al. in plants, and more than one evolutionary mechanism can ex- 2000). It is estimated that dioecy appeared at least nine times plain how it may originate from hermaphroditism (Weiblen during the radiation of the Arecaceae, from monoecious or her- et al. 2000). Once dioecy evolves from gender monomorphism, maphrodite ancestors. These multiple transitions make palms an the sexual morphs have different roles and are often observed ideal model to study the evolutionary pathways of sexual sys- to diverge in their characteristics, resulting in sexual dimor- tems at a morphological and a molecular level; however, at pres- phism (Barrett and Hough 2013). It has been suggested that ent, little is known about the molecular processes that reg- the most common evolutionary pathways involve an interme- ulate the sex of palm flowers. There is considerable interest in diate stage where plants are gynodioecious (separate female characterizing these pathways, however, since this would fa- and hermaphrodite plants) or monoecious (Barrett 2013). cilitate the genetic improvement of cultivated species and the Although plant sexuality has been studied for relatively few understanding of the population dynamics of wild ones, many species at the molecular genetic level, much progress has been of which are threatened. The best characterized species at the made in understanding the wider process of flower development molecular level are the monoecious African oil palm (Elaeis in recent years. The availability of whole-genome sequences for guineensis) and the dioecious date palm (Phoenix dactylifera), some model plants has allowed detailed studies of the molecular genome sequences having been obtained for both (Al-Dous determination of their flower structure. The ABC model, pro- et al. 2011; Al-Mssallem et al. 2013; Singh et al. 2013). Studies posed to explain the interaction of homeotic genes to control of flowerstructureandsexdeterminationhavealsobeencar- floral organ determination (Coen and Meyerowitz 1991) and ried out on both of these species (Adam et al. 2007, 2011; Daher later modified to include additional functions (Gutierrez and et al. 2010; Cherif et al. 2013). Davies 2000; Pelaz et al. 2000) has been fundamental for the This study focuses on two members of the tribe Chamae- understanding of floral development in angiosperms. The ma- doreeae, belonging to the almost entirely monoecious subfamily jority of genes implicated in the ABC model encode members Arecoideae (Asmussen et al. 2000, 2006; Asmussen and Chase of the MADS-box family of transcription factors (Becker and 2001; Lewis and Doyle 2002). The tribe Chamaedoreeae has Theissen 2003), the latter being involved in most aspects of been resolved as monophyletic in several phylogenetic analyses the plant’s life cycle (Gramzow and Theissen 2010). In spite using both morphological and molecular data (Thomas et al. of the considerable progress made in understanding the molec- 2006; Cuenca and Asmussen 2007; Cuenca et al. 2008, 2009). ular basis of flower development in monocots, attention has The key synapomorphy that defines the tribe is the arrange- tended to focus on the Poaceae (Poales), since the latter group ment of flowers in distinctive clusters called acervuli (Cuenca contains several model species such as maize and rice that are et al. 2009). These structures are considered to be a reversed easily accessible to genetic studies and also have major economic cincinnus adnate to the rachilla (Uhl and Moore 1978; Uhl importance. Among the other monocot orders, the largely trop- and Dransfield 1987; Ortega and Stauffer 2011). ical palm family (Arecaceae), which forms the order Arecales on The Chamaedoreeae are composed of five genera (Hender- its own, is of great interest as a case study to investigate the evo- son et al. 1995; Dransfield et al. 2008), two of which are dioe- lution of reproductive morphology and sexual differentiation. It cious: Chamaedorea Willd., the richest