Specific duplication and dorsoventrally asymmetric expression patterns of Cycloidea-like genes in zygomorphic species of Ranunculaceae

PLoS One. 2014 Apr 21;9(4):e95727. doi: 10.1371/journal.pone.0095727. eCollection 2014.

Abstract

Floral bilateral symmetry (zygomorphy) has evolved several times independently in angiosperms from radially symmetrical (actinomorphic) ancestral states. Homologs of the Antirrhinum majus Cycloidea gene (Cyc) have been shown to control floral symmetry in diverse groups in core eudicots. In the basal eudicot family Ranunculaceae, there is a single evolutionary transition from actinomorphy to zygomorphy in the stem lineage of the tribe Delphinieae. We characterized Cyc homologs in 18 genera of Ranunculaceae, including the four genera of Delphinieae, in a sampling that represents the floral morphological diversity of this tribe, and reconstructed the evolutionary history of this gene family in Ranunculaceae. Within each of the two RanaCyL (Ranunculaceae Cycloidea-like) lineages previously identified, an additional duplication possibly predating the emergence of the Delphinieae was found, resulting in up to four gene copies in zygomorphic species. Expression analyses indicate that the RanaCyL paralogs are expressed early in floral buds and that the duration of their expression varies between species and paralog class. At most one RanaCyL paralog was expressed during the late stages of floral development in the actinomorphic species studied whereas all paralogs from the zygomorphic species were expressed, composing a species-specific identity code for perianth organs. The contrasted asymmetric patterns of expression observed in the two zygomorphic species is discussed in relation to their distinct perianth architecture.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Flowers / genetics
  • Gene Duplication / genetics
  • Gene Expression Regulation, Plant / genetics
  • Gene Expression Regulation, Plant / physiology
  • Phylogeny
  • Ranunculaceae / genetics*

Grants and funding

FJ was supported by a PhD fellowship from the Ministère de l'Enseignement Supérieur et de la Recherche, France. FJ's postdoc lab work in Munich, Germany, was supported by the German Science Foundation (DFG) grant No. RE 603/12-1. This work was supported in 2007 by a grant from IFR 87 ‘La Plante et son Environnement’, and the Agence Nationale de la Recherche through the ANR-07-BLAN-0112 grant. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.