Abstract

Merosity, indicating the basic number of floral organs such as sepals and petals, has been constrained to specific and stable numbers during the evolution of angiosperms. The ancestral flower is considered to have a spiral arrangement of perianth organs, as in phyllotaxis, the arrangement of leaves. How has the ancestral spiral evolved into flowers with specific merosities? To address this question, we studied perianth organ arrangement in the <em>Anemone</em> genus of the basal eudicot family Ranunculaceae, because various merosities are found in this genus. In three species, <em>A. flaccida</em>, <em>A. scabiosa</em>, and <em>A. nikoensis</em> that are normally pentamerous, we found positional arrangement of the excessive sixth perianth organ indicating the possibility of a transition from pentamerous to trimerous arrangement. Arrangement was intraspecifically stochastic, but constrained to three of five types, where trimerous arrangement was the most frequent in all species except for a form of <em>A. scabiosa</em>. The rank of frequency of the other two types was species-dependent. We connect these observations with classical theories of spiral phyllotaxis. The phyllotaxis model for initiation of the sixth organ showed that the three arrangements occur at a divergence angle <144°, indicating the spiral nature of floral phyllotaxis rather than a perfect penta-radial symmetry of 144°. The model further showed that selective occurrence of trimerous arrangement is mainly regulated by the organ growth rate. Differential organ growth as well as divergence angle may regulate transitions between pentamerous and trimerous flowers in intraspecific variation as well as in species evolution.

Highlights

  • The basic number of floral organs, known as merosity, has been constrained to specific and stable numbers during angiosperm evolution

  • From the ancestral state with an unspecified number of perianth organs, how have flowers evolved whorls with specific merosities? While phyllotaxis studies have shown that transitions between spiral and whorled arrangements (Fig. 1a,b) can be caused by the size or growth speed of meristem [2,3], little is known about developmental mechanisms that determine the specific number of perianth organs

  • Kitazawa and Fujimoto / Variation in floral phyllotaxis in Anemone previously improved phyllotaxis models by showing that tetramerous and pentamerous whorls emerge from spiral initiation of floral organ primordia, as observed in eudicot flower development, and that whorl emergence depends on the rate of organ growth independent of meristem properties [4]

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Summary

Introduction

The basic number of floral organs (e.g., sepals and petals), known as merosity, has been constrained to specific and stable numbers during angiosperm evolution. Most eudicots have multiples of five or four floral organs in pentamerous or tetramerous whorls, meaning that the organs are arranged in concentric circles (Fig. 1a), whereas most monocots and Magnoliids have merosities of three (Fig. 1b). From the ancestral state with an unspecified number of perianth organs, how have flowers evolved whorls with specific merosities? While phyllotaxis studies have shown that transitions between spiral and whorled arrangements (Fig. 1a,b) can be caused by the size or growth speed of meristem [2,3], little is known about developmental mechanisms that determine the specific number of perianth organs. We. Kitazawa and Fujimoto / Variation in floral phyllotaxis in Anemone previously improved phyllotaxis models by showing that tetramerous and pentamerous whorls emerge from spiral initiation of floral organ primordia, as observed in eudicot flower development, and that whorl emergence depends on the rate of organ growth independent of meristem properties [4]. Transitions between pentamerous and trimerous whorls (Fig. 1a,b), remain elusive

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