Flower-like meristem conditions and spatial constraints shape architecture of floral pseudanthia in Apioideae

Abstract

Background Pseudanthia are multiflowered units that resemble single flowers, frequently by association with pseudocorollas formed by enlarged peripheral florets (ray flowers). Such resemblance is not only superficial, because numerous pseudanthia originate from peculiar reproductive meristems with flower-like characteristics, i.e. floral unit meristems (FUMs). Complex FUM-derived pseudanthia with ray flowers are especially common in Apiaceae, but our knowledge about their patterning is limited. In this paper, we aimed to investigate both the genetic and morphological basis of their development. Results We analysed umbel morphogenesis with SEM in six species representing four clades of Apiaceae subfamily Apioideae with independently acquired floral pseudanthia. Additionally, using in situ hybridization, we investigated expression patterns of LEAFY (LFY), UNUSUAL FLORAL ORGANS (UFO), and CYCLOIDEA (CYC) during umbel development in carrot (Daucus carota subsp. carota). Here, we show that initial differences in size and shape of umbel meristems influence the position of ray flower formation, whereas an interplay between peripheral promotion and spatial constraints in umbellet meristems take part in the establishment of specific patterns of zygomorphy in ray flowers of Apiaceae. This space-dependent patterning results from flower-like morphogenetic traits of the umbel which are also visible at the molecular level. Transcripts of DcLFY are uniformly distributed in the incipient umbel, umbellet and flower meristems, while DcCYC shows divergent expression in central and peripheral florets. Conclusions Our results indicate that umbels develop from determinate reproductive meristems with flower-like characteristics, which supports their recognition as floral units. The great architectural diversity and complexity of pseudanthia in Apiaceae can be explained by the unique conditions of FUMs—an interplay between expression of regulatory genes, specific spatio-temporal ontogenetic constraints and morphogenetic gradients arising during expansion and repetitive fractionation. Alongside Asteraceae, umbellifers constitute an interesting model for investigation of patterning in complex pseudanthia.

The ontogeny of flowers and inflorescences in the andromonoecious annual Iranian endemic Dicyclophora persica (Apiaceae)

“…The development of umbels is not an unstudied subject in Apiaceae. Many studies, however, have been done by light microscopy (Payer 1853, 1857, Jochmann 1854, Sieler 1870, Schuchardt 1881, Schumann 1890, Jurica 1922, Borthwick et al 1931, Saatler 1973) and rarely by scanning electron microscopy (Erbar and Leins 1985, Bull‐Hereñu and Classen‐Bockhoff 2010, 2013, Classen‐Bockhoff 2016, Baczyński et al 2022).…”

“…bulbosum and P. sativa is due to space limitation during development. Such mechanical pressure was found not only in Apiaceae with reduced calyx but also in families with well-developed calyx and dense inflorescences (Ajani et al 2016, Classen-Bockhoff and Arndt 2018, Baczyński et al 2022. In Hydrocotyle vulgaris (formerly in Apiaceae), in contrast, the suppression of sepals is genetically fixed and it has been transferred to Araliaceae Leins 1985, Leins andErbar 2004).…”

“…There are usually temporal overlaps in the initiation of all floral organs except carpels. In Saniculoideae, in contrast, the strictly centripetal sequence of organ initiation has been found (Payer 1853, Jochmann 1854, Sieler 1870, Schuchardt 1881, Schumann 1890, Jurica 1922, Borthwick et al 1931, Saatler 1973, Erbar and Leins 1985, Ajani et al 2016, Baczyński et al 2022.…”

“…Each umbellet includes rings of thickened and hardened pedicellate staminate flowers that are centered on a sessile perfect flower, resulting in a structure that resembles a cage‐shaped lantern (Rechinger 1987, Mozaffarian 2007, Reuther and Classen‐Bockhoff 2010). The enlarged peripheral flowers with ray petals resemble the entire umbel as pseudanthia, i.e., a multi‐flowered unit that looks like a single flower (Baczyński et al 2021, 2022). Considering the unique inflorescence, this tribe has been recognized early as a monophyletic group using molecular data (Drude 1898, Downie et al 2001, Ajani et al 2012).…”

Pseudanthia in angiosperms: a review

“…Consequently, flower primordia are not continuously segregated from the meristem apex, but instead arise by the process of fractionation that subdivides the available meristem until the entire surface of the FUM is used ( Claßen-Bockhoff & Bull-Hereñu, 2013 ; Claßen-Bockhoff, 2016 ). Apart from the difference in size, FUMs share most qualities with flower meristems (FMs), which might explain their numerous flower-like genetic and developmental patterns ( Broholm et al , 2008 ; Carlson et al , 2011 ; Zhao et al , 2016 ; Baczyński et al , 2022 a ).…”