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1.  Specific Duplication and Dorsoventrally Asymmetric Expression Patterns of Cycloidea-Like Genes in Zygomorphic Species of Ranunculaceae 
PLoS ONE  2014;9(4):e95727.
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.
PMCID: PMC3994137  PMID: 24752428
2.  Combining Phylogenetic and Syntenic Analyses for Understanding the Evolution of TCP ECE Genes in Eudicots 
PLoS ONE  2013;8(9):e74803.
TCP ECE genes encode transcription factors which have received much attention for their repeated recruitment in the control of floral symmetry in core eudicots, and more recently in monocots. Major duplications of TCP ECE genes have been described in core eudicots, but the evolutionary history of this gene family is unknown in basal eudicots. Reconstructing the phylogeny of ECE genes in basal eudicots will help set a framework for understanding the functional evolution of these genes. TCP ECE genes were sequenced in all major lineages of basal eudicots and Gunnera which belongs to the sister clade to all other core eudicots. We show that in these lineages they have a complex evolutionary history with repeated duplications. We estimate the timing of the two major duplications already identified in the core eudicots within a timeframe before the divergence of Gunnera and after the divergence of Proteales. We also use a synteny-based approach to examine the extent to which the expansion of TCP ECE genes in diverse eudicot lineages may be due to genome-wide duplications. The three major core-eudicot specific clades share a number of collinear genes, and their common evolutionary history may have originated at the γ event. Genomic comparisons in Arabidopsis thaliana and Solanumlycopersicum highlight their separate polyploid origin, with syntenic fragments with and without TCP ECE genes showing differential gene loss and genomic rearrangements. Comparison between recently available genomes from two basal eudicots Aquilegiacoerulea and Nelumbonucifera suggests that the two TCP ECE paralogs in these species are also derived from large-scale duplications. TCP ECE loci from basal eudicots share many features with the three main core eudicot loci, and allow us to infer the makeup of the ancestral eudicot locus.
PMCID: PMC3760840  PMID: 24019982
3.  Accelerated evolution and coevolution drove the evolutionary history of AGPase sub-units during angiosperm radiation 
Annals of Botany  2012;109(4):693-708.
Background and Aims
ADP-glucose pyrophosphorylase (AGPase) is a key enzyme of starch biosynthesis. In the green plant lineage, it is composed of two large (LSU) and two small (SSU) sub-units encoded by paralogous genes, as a consequence of several rounds of duplication. First, our aim was to detect specific patterns of molecular evolution following duplication events and the divergence between monocotyledons and dicotyledons. Secondly, we investigated coevolution between amino acids both within and between sub-units.
A phylogeny of each AGPase sub-unit was built using all gymnosperm and angiosperm sequences available in databases. Accelerated evolution along specific branches was tested using the ratio of the non-synonymous to the synonymous substitution rate. Coevolution between amino acids was investigated taking into account compensatory changes between co-substitutions.
Key Results
We showed that SSU paralogues evolved under high functional constraints during angiosperm radiation, with a significant level of coevolution between amino acids that participate in SSU major functions. In contrast, in the LSU paralogues, we identified residues under positive selection (1) following the first LSU duplication that gave rise to two paralogues mainly expressed in angiosperm source and sink tissues, respectively; and (2) following the emergence of grass-specific paralogues expressed in the endosperm. Finally, we found coevolution between residues that belong to the interaction domains of both sub-units.
Our results support the view that coevolution among amino acid residues, especially those lying in the interaction domain of each sub-unit, played an important role in AGPase evolution. First, within SSU, coevolution allowed compensating mutations in a highly constrained context. Secondly, the LSU paralogues probably acquired tissue-specific expression and regulatory properties via the coevolution between sub-unit interacting domains. Finally, the pattern we observed during LSU evolution is consistent with repeated sub-functionalization under ‘Escape from Adaptive Conflict’, a model rarely illustrated in the literature.
PMCID: PMC3286274  PMID: 22307567
Angiosperms; monocotyledons; dicotyledons; paralogue genes; molecular evolution; coevolution; neofunctionalization; subfunctionalization; starch synthesis; AGPase
4.  The evolution of flower development: current understanding and future challenges 
Annals of Botany  2011;107(9):1427-1431.
PMCID: PMC3108812  PMID: 21793247
5.  Establishment of zygomorphy on an ontogenic spiral and evolution of perianth in the tribe Delphinieae (Ranunculaceae) 
Annals of Botany  2009;104(5):809-822.
Background and Aims
Ranunculaceae presents both ancestral and derived floral traits for eudicots, and as such is of potential interest to understand key steps involved in the evolution of zygomorphy in eudicots. Zygomorphy evolved once in Ranunculaceae, in the speciose and derived tribe Delphinieae. This tribe consists of two genera (Aconitum and Delphinium s.l.) comprising more than one-quarter of the species of the family. In this paper, the establishment of zygomorphy during development was investigated to cast light on the origin and evolution of this morphological novelty.
The floral developmental sequence of six species of Ranunculaceae, three actinomorphic (Nigella damascena, Aquilegia alpina and Clematis recta) and three zygomorphic (Aconitum napellus, Delphinium staphisagria and D. grandiflorum), was compared. A developmental model was elaborated to break down the successive acquisitions of floral organ identities on the ontogenic spiral (all the species studied except Aquilegia have a spiral phyllotaxis), giving clues to understanding this complex morphogenesis from an evo-devo point of view. In addition, the evolution of symmetry in Ranunculaceae was examined in conjunction with other traits of flowers and with ecological factors.
Key Results
In the species studied, zygomorphy is established after organogenesis is completed, and is late, compared with other zygomorphic eudicot species. Zygomorphy occurs in flowers characterized by a fixed merism and a partially reduced and transformed corolla.
It is suggested that shifts in expression of genes controlling the merism, as well as floral symmetry and organ identity, have played a critical role in the evolution of zygomorphy in Delphinieae, while the presence of pollinators able to exploit the peculiar morphology of the flower has been a key factor for the maintenance and diversification of this trait.
PMCID: PMC2749547  PMID: 19608573
Delphinieae; development; evolution; evo-devo; nectar spurs; ontogenic spiral; Ranunculaceae; zygomorphy
6.  Evolutionary Trends in the Flowers of Asteridae: Is Polyandry an Alternative to Zygomorphy? 
Annals of Botany  2008;102(2):153-165.
Background and Aims
Floral symmetry presents two main states in angiosperms, actinomorphy (polysymmetry or radial symmetry) and zygomorphy (monosymmetry or bilateral symmetry). Transitions from actinomorphy to zygomorphy have occurred repeatedly among flowering plants, possibly in coadaptation with specialized pollinators. In this paper, the rules controlling the evolution of floral symmetry were investigated to determine in which architectural context zygomorphy can evolve.
Floral traits potentially associated with perianth symmetry shifts in Asteridae, one of the major clades of the core eudicots, were selected: namely the perianth merism, the presence and number of spurs, and the androecium organ number. The evolution of these characters was optimized on a composite tree. Correlations between symmetry and the other morphological traits were then examined using a phylogenetic comparative method.
Key Results
The analyses reveal that the evolution of floral symmetry in Asteridae is conditioned by both androecium organ number and perianth merism and that zygomorphy is a prerequisite to the emergence of spurs.
The statistically significant correlation between perianth zygomorphy and oligandry suggests that the evolution of floral symmetry could be canalized by developmental or spatial constraint. Interestingly, the evolution of polyandry in an actinomorphic context appears as an alternative evolutionary pathway to zygomorphy in Asteridae. These results may be interpreted either in terms of plant–pollinator adaptation or in terms of developmental or physical constraints. The results are discussed in relation to current knowledge about the molecular bases underlying floral symmetry.
PMCID: PMC2712368  PMID: 18511411
Floral symmetry; architectural constraints; Asteridae; comparative analysis; composite tree; correlated evolution; evolutionary scenario
7.  Evolution of Perianth and Stamen Characteristics with Respect to Floral Symmetry in Ranunculales 
Annals of Botany  2007;100(3):631-640.
Background and Aims
Floral symmetry presents two main states in angiosperms, namely polysymmetry and monosymmetry. Monosymmetry is thought to have evolved several times independently from polysymmetry, possibly in co-adaptation with specialized pollinators. Monosymmetry commonly refers to the perianth, even though associated androecium modifications have been reported. The evolution of perianth symmetry is examined with respect to traits of flower architecture in the Ranunculales, the sister group to all other eudicots, which present a large diversity of floral forms.
Characters considered were perianth merism, calyx, corolla and androecium symmetry, number of stamens and spurs. Character evolution was optimized on a composite phylogenetic tree of Ranunculales using maximum parsimony.
Key Results
The ancestral state for merism could not be inferred because the basalmost Eupteleaceae lack a perianth and have a variable number of stamens. The Papaveraceae are dimerous, and the five other families share a common trimerous ancestor. Shifts from trimery to dimery (or reverse) are observed. Pentamery evolved in Ranunculaceae. Ranunculales except Eupteleaceae, present a polysymmetric ancestral state. Monosymmetry evolved once within Papaveraceae, Ranunculaceae and Menispermaceae (female flowers only). Oligandry is the ancestral state for all Ranunculales, and polyandry evolved several times independently, in Papaveraceae, Menispermaceae, Berberidaceae and Ranunculaceae, with two reversions to oligandry in the latter. The ancestral state for androecium symmetry is ambiguous for the Ranunculales, while polysymmetry evolved immediately after the divergence of Eupteleaceae. A disymmetric androecium evolved in Papaveraceae. The ancestral state for spurs is none. Multiple spurs evolved in Papaveraceae, Berberidaceae and Ranunculaceae, and single spurs occur in Papaveraceae and Ranunculaceae.
The evolution of symmetry appears disconnected from changes in merism and stamen number, although monosymmetry never evolved in the context of an open ground plan. In bisexual species, monosymmetry evolved coincidently with single spurs, allowing us to propose an evolutionary scenario for Papaveraceae.
PMCID: PMC2533616  PMID: 17428835
Floral symmetry; Ranunculales; perianth; androecium; stamen; spur; merism; evo-devo

Results 1-7 (7)