Insights into the ancestral flowers of Ranunculales

Carrive, Laetitia; Domenech, Boris; Sauquet, Hervé; Jabbour, Florian; Damerval, Catherine; Nadot, Sophie

doi:10.1093/botlinnean/boaa031

Cited by 23 publications

(18 citation statements)

References 91 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Thus, reconstruction of the ancestral gynoecium condition in a clade of all angiosperms except Amborella is directly sensitive to the unstable placement of Nuphar . Two families–the apocarpous Eupteleaceae (single genus Euptelea ) and the syncarpous Papaveraceae–are unresolved at the root of the basal eudicot lineage Ranunculales ( Carrive et al, 2020 ). Similarly, two families with contrasting gynoecium morphology (Tofieldiaceae and Araceae) are unresolved at the root of Alismatales, a lineage of basal monocots ( Luo et al, 2016 ; Ross et al, 2016 ; Givnish et al, 2018 ).…”

Section: Methodsmentioning

confidence: 99%

Refined Interpretation of the Pistillate Flower in Ceratophyllum Sheds Fresh Light on Gynoecium Evolution in Angiosperms

Sokoloff

El²,

Pechenyuk³

et al. 2022

Front. Cell Dev. Biol.

View full text Add to dashboard Cite

Molecular phylogenetic analyses have revealed a superclade of mesangiosperms with five extant lineages: monocots, eudicots, magnoliids, Ceratophyllum and Chloranthaceae. Both Ceratophyllum and Chloranthaceae are ancient lineages with a long fossil record; their precise placement within mesangiosperms is uncertain. Morphological studies have suggested that they form a clade together with some Cretaceous fossils, including Canrightia, Montsechia and Pseudoasterophyllites. Apart from Canrightia, members of this clade share unilocular gynoecia commonly interpreted as monomerous with ascidiate carpels. Alternatively, the gynoecium of Ceratophyllum has also been interpreted as syncarpous with a single fertile carpel (pseudomonomerous). We investigate patterns of morphological, anatomical and developmental variation in gynoecia of three Ceratophyllum species to explore the controversial interpretation of its gynoecium as either monomerous or pseudomonomerous. We use an angiosperm-wide morphological data set and contrasting tree topologies to estimate the ancestral gynoecium type in both Ceratophyllum and mesangiosperms. Gynoecia of all three Ceratophyllum species possess a small (sometimes vestigial) glandular appendage on the abaxial side and an occasionally bifurcating apex. The ovary is usually unilocular with two procambium strands, but sometimes bilocular and/or with three strands in C. demersum. None of the possible phylogenetic placements strongly suggest apocarpy in the stem lineage of Ceratophyllum. Rescoring Ceratophyllum as having two united carpels affects broader-scale reconstructions of the ancestral gynoecium in mesangiosperms. Our interpretation of the glandular appendage as a tepal or staminode homologue makes the Ceratophyllum ovary inferior, thus resembling (semi)inferior ovaries of most Chloranthaceae and potentially related fossils Canrightia and Zlatkocarpus. The entire structure of the flower of Ceratophyllum suggests strong reduction following a long and complex evolutionary history. The widely accepted notion that apocarpy is ancestral in mesangiosperms (and angiosperms) lacks robust support, regardless of which modes of carpel fusion are considered. Our study highlights the crucial importance of incorporating fossils into large-scale analyses to understand character evolution.

show abstract

Section: Methodsmentioning

confidence: 99%

Refined Interpretation of the Pistillate Flower in Ceratophyllum Sheds Fresh Light on Gynoecium Evolution in Angiosperms

Sokoloff

El²,

Pechenyuk³

et al. 2022

Front. Cell Dev. Biol.

View full text Add to dashboard Cite

show abstract

“…Jabbour et al unpublished manuscript). Because nectariferous petals originated once within Ranunculaceae (Carrive et al 2020), petals in Nigelleae and Delphinieae are homologous.…”

Section: Samplingmentioning

confidence: 99%

“…In Ranunculales, the earliest-diverging order of eudicots (APG IV 2016), synorganization was briefly reported in the flowers of the tribe Delphinieae, in which the nectar spurs of the dorsal petals are nested within the hollow dorsal sepal (Chartier et al 2016;Chen et al 2018;Jabbour et al in press). The phylogenetic position of Delphinieae within Ranunculaceae, and the floral morphological evolution in the family were both clarified recently (Zhai et al 2019;Carrive et al 2020). Phylogenetic relationships within Delphinieae have been largely clarified as well in the last ten years Renner 2011b, 2012b;Wang et al 2013;Espinosa et al 2017;Hong et al 2017;Xiang et al 2017).…”

Section: Introductionmentioning

confidence: 99%

Floral Organogenesis and Morphogenesis ofStaphisagria(Ranunculaceae): Implications for the Evolution of Synorganized Floral Structures in Delphinieae

Zalko

Frachon

Morel

et al. 2021

International Journal of Plant Sciences

Self Cite

View full text Add to dashboard Cite

Premise of the research. Floral synorganization is a structural feature of many speciose angiosperm taxa, and is considered as a morphological innovation paving the way for evolutionary diversification. Staphisagria is sister to the remaining Delphinieae, the only lineage of Ranunculaceae characterized by zygomorphic flowers. We aim at providing a description of floral organogenesis and morphogenesis in both Staphisagria species, presenting the disparity of Delphinieae hyperorgan in a phylogenetic framework, and proposing a scenario of likely developmental pathways underlying the different types of hyperorgans in Delphinieae. Methodology. We carried out morphological, anatomical, and developmental studies on flowers of Staphisagria macrosperma and S. picta. Pivotal results. Synorganization is complex in Staphisagria and Delphinieae as a whole, and involves flower dorsoventralization, nesting of spurs, postgenital fusion of petals, and the formation of a shared cavity. From a choripetalous ancestor, late and partial postgenital fusion among dorsal petals evolved once or twice in the tribe. Conclusions. Delphinieae flower includes nested spurs and nested floral parlors. These key innovations, unique in angiosperms, probably led to the diversification of this species-rich tribe in the Northern Hemisphere. The length of the inner (nectariferous) spurs and the nested floral parlors determine the range of pollinators able to collect nectar. These traits could be used to revise the circumscription of taxonomic groups within the tribe, and should be taken into account when examining the possible coevolution between Delphinieae flowers and their pollinators. Integrating this new knowledge about the hyperorgan will be essential for future research in taxonomy, evo-devo and pollination ecology in Delphinieae.

show abstract

“…The order Ranunculales is among the most diverse angiosperm lineages with respect to floral organization ( Carrive et al, 2020 ). The flowers display considerable variation in terms of number of floral organs, size, organ shape, and perianth differentiation.…”

Section: Introductionmentioning

confidence: 99%

“…Until recently, petals in Ranunculaceae were considered to have been repeatedly recruited from stamens during the evolutionary history of the family ( Kosuge, 1994 ; Ronse De Craene, 2007 ). This view has recently been challenged by evo-devo studies of ABCE model gene expression in several Ranunculales species (reviewed in Damerval and Becker, 2017 ; Meaders et al, 2020 ) and by the Ranunculales-wide study on flower organization of Carrive et al (2020) . These studies revealed that the ancestral flower of Ranunculaceae likely had petals that were further lost repeatedly in several genera belonging to different tribes ( Anemone, Anemoclema, Enemion, Clematis, Caltha, Glaucidium, Hydrasti s).…”

Section: Introductionmentioning

confidence: 99%

A flat petal as ancestral state for Ranunculaceae

et al. 2022

Self Cite

View full text Add to dashboard Cite

Ranunculaceae comprise ca. 2,500 species (ca. 55 genera) that display a broad range of floral diversity, particularly at the level of the perianth. Petals, when present, are often referred to as “elaborate” because they have a complex morphology. In addition, the petals usually produce and store nectar, which gives them a crucial functional role in the interaction with pollinators. Its morphological diversity and species richness make this family a particularly suitable model group for studying the evolution of complex morphologies. Our aims are (1) to reconstruct the ancestral form of the petal and evolutionary stages at the scale of Ranunculaceae, (2) to test the hypothesis that there are morphogenetic regions on the petal that are common to all species and that interspecific morphological diversity may be due to differences in the relative proportions of these regions during development. We scored and analyzed traits (descriptors) that characterize in detail the complexity of mature petal morphology in 32 genera. Furthermore, we described petal development using high resolution X-Ray computed tomography (HRX-CT) in six species with contrasting petal forms (Ficaria verna, Helleborus orientalis, Staphisagria picta, Aconitum napellus, Nigella damascena, Aquilegia vulgaris). Ancestral state reconstruction was performed using a robust and dated phylogeny of the family, allowing us to produce new hypotheses for petal evolution in Ranunculaceae. Our results suggest a flat ancestral petal with a short claw for the entire family and for the ancestors of all tribes except Adonideae. The elaborate petals that are present in different lineages have evolved independently, and similar morphologies are the result of convergent evolution.

show abstract

Insights into the ancestral flowers of Ranunculales

Cited by 23 publications

References 91 publications

Refined Interpretation of the Pistillate Flower in Ceratophyllum Sheds Fresh Light on Gynoecium Evolution in Angiosperms

Refined Interpretation of the Pistillate Flower in Ceratophyllum Sheds Fresh Light on Gynoecium Evolution in Angiosperms

Floral Organogenesis and Morphogenesis ofStaphisagria(Ranunculaceae): Implications for the Evolution of Synorganized Floral Structures in Delphinieae

A flat petal as ancestral state for Ranunculaceae

Contact Info

Product

Resources

About