Then There Were Plenty-Ring Meristems Giving Rise to Many Stamen Whorls

Abstract

Floral meristems are dynamic systems that generate floral organ primordia at their flanks and, in most species, terminate while giving rise to the gynoecium primordia. However, we find species with floral meristems that generate additional ring meristems repeatedly throughout angiosperm history. Ring meristems produce only stamen primordia, resulting in polystemous flowers (having stamen numbers more than double that of petals or sepals), and act independently of the floral meristem activity. Most of our knowledge on floral meristem regulation is derived from molecular genetic studies of Arabidopsis thaliana, a species with a fixed number of floral organs and, as such of only limited value for understanding ring meristem function, regulation, and ecological value. This review provides an overview of the main molecular players regulating floral meristem activity in A. thaliana and summarizes our knowledge of ring primordia morphology and occurrence in dicots. Our work provides a first step toward understanding the significance and molecular genetics of ring meristem regulation and evolution.

Keywords: evo–devo; floral meristem; numerous stamens; polystemony; ring meristem.

Figure 1

Flowers with ring meristems: (A) closed ring meristem and (B) fragmented ring meristem; the ring meristem is shown in orange. Black arrows indicate the direction of stamen primordia initiation. (C–E) Ring meristem of Eschscholzia californica forming stamen primordia. (C) Bud of a late stage 4 flower in which the floral dome separates from the ring meristem (indicated by a blurred orange line). (D) Stage 5 bud showing the continuous formation of stamen primordia while the gynoecium has already initiated. (E) Stage 6 bud showing the formation of new stamen primordia (white arrow) at the time when the early stamens already form a flat surface for microsporangia initiation. The sepals were removed in all images, and staging was done according to Becker et al. (2005) [44]. Abbreviations: b, bidirectional; cp, centripetal; cf, centrifugal; FD, floral dome; FM, floral meristem; G, gynoecium; P, petal; RM, ring meristem; SE, sepal; SP, stamen primordium; S, stamen. Scale bar in C = 86 µm, in D = 100 µm, in E = 120 µm ((A,B) modified from Endress, 2011; (C–E) from Becker, 2016 with permission) [7,43].

Figure 2

Distribution and types of ring meristems across eudicots. On the left, a simplified phylogeny shows only orders and families with ring meristem occurrence. Numbers in brackets next to the orders indicate the number of families in the respective order. On the right, the type of ring meristem is indicated. Numbers below summarize occurrences of morphological traits. Based on [43,45,47,48,49,50,51,52,53,54,55,56,57].