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A Design Principle for Floral Organ Number and Arrangement in Flowers with Bilateral Symmetry Aiko Nakagawa1,*, Miho S

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A Design Principle for Floral Organ Number and Arrangement in Flowers with Bilateral Symmetry Aiko Nakagawa1,*, Miho S © 2020. Published by The Company of Biologists Ltd | Development (2020) 147, dev182907. doi:10.1242/dev.182907 RESEARCH ARTICLE A design principle for floral organ number and arrangement in flowers with bilateral symmetry Aiko Nakagawa1,*, Miho S. Kitazawa1,2,*,‡ and Koichi Fujimoto1,‡ ABSTRACT Some flowers have achieved this regulation of pollen attachment The bilateral symmetry of flowers is a striking morphological position by modifying floral organ number, positioning and form. achievement during floral evolution, providing high adaptation In particular, zygomorphic (or bilateral) flowers, which have dorso- potential for pollinators. The symmetry can appear when floral ventral (also called adaxial-abaxial or DV axis) asymmetry that organ primordia developmentally initiate. Primordia initiation at the corresponds to the DV axis of the pollinator (Fig. 1A,B, lateral ventral and dorsal sides of the floral bud is differentially regulated flower; Endress, 1999), have developed in many plant species in by several factors, including external organs of the flower and various clades adapted to a variety of pollinator species, resulting in CYCLOIDEA (CYC) gene homologues, which are expressed the diversification of floral morphologies (Sargent, 2004). asymmetrically on the dorso-ventral axis. It remains unclear how In the early stages of floral development, the first indication of these factors control the diversity in the number and bilateral perianth diversity appears in the number and arrangement of the arrangement of floral organs. Here, we propose a mathematical floral organs, the sepals and the petals. The perianth of a flower model demonstrating that the relative strength of the dorsal-to-ventral typically consists of two circles or whorls of floral organs, and each inhibitions and the size of the floral stem cell region (meristem) whorl contains the same number of floral organs. Merosity determines the number and positions of the sepal and petal describes the common organ number of perianth whorls and is primordia. The simulations reproduced the diversity of monocots usually clade specific (Fig. 1C; Ronse De Craene, 2010; Smyth, and eudicots, including snapdragon Antirrhinum majus and its cyc 2018). In eudicots, the largest clade of flowering plants, the mutant, with respect to organ number, arrangement and initiation common number is usually four or five, whereas in monocots, the patterns, which were dependent on the inhibition strength. These sister clade to eudicots, it is three (Ronse De Craene and theoretical results suggest that diversity in floral symmetry is primarily Brockington, 2013; Endress, 2010; Remizowa et al., 2010). regulated by the dorso-ventral inhibitory field and meristem size Lateral flowers that bloom as the lateral branch of the main stem during developmental evolution. have two types of floral organ arrangements for each organ number with respect to the DV axis of the flower (Fig. 1C, upper panel). The KEY WORDS: CYCLOIDEA, Bilateral symmetry, Flower development, arrangements along the DV axis are recognized by dividing the Floral evolution, Phyllotaxis, Organ positioning floral bud into three regions from the position closest to the main axis: dorsal, lateral and ventral regions (Fig. 1A,B). The model plant INTRODUCTION Arabidopsis thaliana exhibits tetramerous flowers with four sepals Spatial positioning and number of organs (e.g. eyes, ears, nose and and four petals, and the sepal arrangement along the DV axis has mouth in animals; carpels, stamens, petals and sepals in plants) two sepals in the lateral region and one each in the dorsal and ventral represent one of the most fundamental differences among species. regions (type 4A; Fig. 1C; Smyth et al., 1990). The other type of In flowering plants (angiosperms), the forms of flowers exhibit tetramerous arrangement (type 4B) is also found in certain plants, enormous diversity. Floral symmetry is an important example including those in the genus Veronica (Plantaginaceae). Regarding of this diversity, which affects the success of sexual reproduction pentamerous flowers, the majority of eudicot flowers have one via pollination, i.e. pollen transfer from male to female organs dorsal, two lateral and two ventral sepals (type 5A), whereas flowers (Wozniaḱ and Sicard, 2018). Because plants are immobile, these in several clades have reversed arrangements with two dorsal, two organisms entrust the transport of pollen to wind, water or, in the lateral and one ventral sepal (type 5B; e.g. the subfamily majority of flowering plants, to animals. A recent study suggested Papilionoideae or Fabaceae). The trimerous flowers in monocots that approximately 87.5% of flowering plants are pollinated by typically have one inner and two outer tepals (perianth organs) in animals, such as insects and birds (Ollerton et al., 2011); therefore, the dorsal region, and one outer and two inner tepals in the ventral plant floral forms have evolved to attract and control pollinators. region (type 3B; Rudall and Bateman, 2004). On the other hand, the One mechanism to ensure the success of pollination is to fix reversed arrangement is a representative phenotype in several orders the position of pollen attachment on the body of the pollinator. of monocots (type 3A; Ronse De Craene, 2010; Tobe et al., 2018). Additionally, dimerous flowers appear in several families in 1Department of Biological Sciences, Graduate School of Science, Osaka monocots and eudicots, and have two lateral sepals (outer tepals; University, Toyonaka, 560-0043, Japan. 2Center for Education in Liberal Arts and type 2B). The developmental mechanisms that produce the clade- Sciences, Osaka University, Toyonaka, 560-0043, Japan. specific diversity of organ number and positioning along the DV *These authors contributed equally to this work axis have not been thoroughly elucidated. ‡Authors for correspondence ([email protected]; The number and positioning of floral organs are mainly [email protected]) determined when the floral organ primordia initiate (Endress, M.S.K., 0000-0001-9468-8018; K.F., 0000-0001-6473-7990 1999; Tucker, 1999; Spencer and Kim, 2018). The simplest case occurs when several primordia that make up a whorl (i.e. organs, Received 22 July 2019; Accepted 7 January 2020 such as petals, with the same identity) in a concentric circle initiate DEVELOPMENT 1 RESEARCH ARTICLE Development (2020) 147, dev182907. doi:10.1242/dev.182907 Fig. 1. Structure and symmetry of flowers. (A) Schematic diagram of an inflorescence. Each lateral flower has a DV axis with respect to the main axis and a bract. (B) DV axis in an Antirrhinum majus lateral flower, corresponding to the DV axis of the pollinators. (C) Upper: typical arrangements of the outermost floral organs (sepals or outer tepals) with respect to the DV axis. Bottom: clade-specific number and arrangement of the outer organs (sepals and petals) with respect to the main axis (black circle) in a phylogenetic tree modified from APG IV (The Angiosperm Phylogeny Group, 2016). Monocots exhibit either dimery or trimery. Most trimerous species show the same arrangement (3B), although their initiating orders are not identical. For example, in Orchidaceae, the outer perianth initiates from the dorsal side (Pabón-Mora and González, 2008). The exceptionally opposite positioning of the trimerous perianth organs along the DV axis (3A) is found specifically in the order Dioscoreales and the family Smilacaceae (Liliales; Ronse De Craene, 2010), which exhibit sequential initiation for both inner and outer perianth organs. A dimerous arrangement with two lateral external tepals, one ventral tepal and one dorsal internal tepal, is found in several clades, including the genus Paepalanthus (Eriocaulaceae and Poales; de Lima Silva et al., 2016), but rarely in orchids [a few Japanese Dendrobium cultivars, abnormal flowers in Cattleya (Harshberger, 1907) and Cypripedium (Masters, 1887)]. The pentamerous and tetramerous flowers co-exist in many eudicot families, such as Plantaginaceae (e.g. 5A in A. majus and 4B in Veronica) and Fabaceae (e.g. 5A, 5B and 4A). at once; however, this is not the case in many flowering plants, as Floral symmetry depends on the position in the inflorescence early floral development is associated with non-synchronous (Fig. 1A). The lateral flowers are zygomorphic, whereas terminal initiation of the sepal primordia. The initiating order in the sepal flowers are actinomorphic (radially symmetric) in some peloria whorl differs among species. The zygomorphic initiation patterns, mutants of Lamiaceae (Rudall and Bateman, 2003). The merosity of such as unidirectional initiation along the DV axis and bidirectional lateral and terminal flowers can also be different with pentamery and initiation (Tucker, 2003), are unique to floral organ initiation in tetramery, respectively, occurring in Adoxa (Adoxaceae, asterids; contrast to the spiral initiation sequence, which is also observed Roels and Smets, 1994) or the opposite case for Ruta (Rutaceae, in phyllotaxis (the arrangement of leaves along the stem) as rosids; Wei et al., 2012), where the organ initiation is zygomorphic well as floral organs. Although the developmental mechanisms in lateral flowers. Such differences between lateral and terminal underlying the diversity of the initiation sequence, as well as the flowers suggest that lateral floral bud polarity (Thoma and number and positioning of the floral organs, have been proposed for Chandler, 2015) affects zygomorphy. The relative
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