Zygomorphy evolved from disymmetry in Fumarioideae (Papaveraceae, Ranunculales): new evidence from an expanded molecular phylogenetic framework

Sauquet, Hervé; Carrive, Laetitia; Poullain, Noëlie; Sannier, Julie; Damerval, Catherine; Nadot, Sophie

doi:10.1093/aob/mcv020

Cited by 34 publications

(49 citation statements)

References 73 publications

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“…In Papaveraceae, Fumarioideae shows a transition to monosymmetry that involves an intermediate disymmetric state (Damerval & Nadot, ; Sauquet et al ., ). In disymmetric flowers (e.g.…”

Section: Discussionmentioning

confidence: 97%

“…In Fumarioideae, there is no evidence of a CYL duplication within Papaveraceae paralog lineages associated with the emergence of zygomorphy in the subfamily, but instead a speciesspecific additional duplication in our zygomorphic model C. vesicaria. In Papaveraceae, Fumarioideae shows a transition to monosymmetry that involves an intermediate disymmetric state (Damerval & Nadot, 2007;Sauquet et al, 2015). In disymmetric flowers (e.g.…”

Section: Evolution Of Zygomorphy In Fumarioideaementioning

confidence: 99%

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Evolutionary diversification of CYC/TB1‐like TCP homologs and their recruitment for the control of branching and floral morphology in Papaveraceae (basal eudicots)

et al. 2018

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Angiosperms possess enormous morphological variation in plant architectures and floral forms. Previous studies in Pentapetalae and monocots have demonstrated the involvement of TCP domain CYCLOIDEA/TEOSINTE BRANCHED1-like (CYC/TB1) genes in the control of floral symmetry and shoot branching. However, how TCP/CYC-like (CYL) genes originated, evolved and functionally diversified remain unclear. We conducted a comparative functional study in Ranunculales, the sister lineage to all other eudicots, between Eschscholzia californica and Cysticapnos vesicaria, two species of Papaveraceae with actinomorphic and zygomorphic flowers, respectively. Phylogenetic analysis indicates that CYL genes in Papaveraceae form two paralogous lineages, PapaCYL1 and PapaCYL2. Papaveraceae CYL genes show highly diversified expression patterns as well as functions. Enhanced branching by silencing of EscaCYL1 suggests that the role of CYC/TB1-like genes in branching control is conserved in Papaveraceae. In contrast to the arrest of stamen development in Pentapetalae, PapaCYL genes promote stamen initiation and growth. In addition, we demonstrate that CyveCYLs are involved in perianth development, specifying sepal and petal identity in Cysticapnos by regulating the B-class floral organ identity genes. Our data also suggest the involvement of CyveCYL genes in the regulation of flower symmetry in Cysticapnos. Our work provides evidence of the importance of TCP/CYC-like genes in the promotion of morphological diversity across angiosperms.

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“…In Papaveraceae, Fumarioideae shows a transition to monosymmetry that involves an intermediate disymmetric state (Damerval & Nadot, ; Sauquet et al ., ). In disymmetric flowers (e.g.…”

Section: Discussionmentioning

confidence: 97%

Section: Evolution Of Zygomorphy In Fumarioideaementioning

confidence: 99%

Evolutionary diversification of CYC/TB1‐like TCP homologs and their recruitment for the control of branching and floral morphology in Papaveraceae (basal eudicots)

et al. 2018

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“…The rjMCMC approach integrates results over the model space and visits models (e.g., equal and unequal transition rate models) and parameters (e.g., RateDev parameter, to get an acceptance rate of changes between 20%–40%) in proportion to their posterior probability. The hyper prior provides a distribution from which values are drawn to seed the exponential prior (Pagel, Meade, & Barker, ; Pagel & Meade, ; see Onstein & Linder, ; Sauquet et al., for empirical examples).…”

Section: Methodsmentioning

confidence: 99%

Which frugivory‐related traits facilitated historical long‐distance dispersal in the custard apple family (Annonaceae)?

Onstein

Kissling

Chatrou

et al. 2019

Journal of Biogeography

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Aim Long‐distance dispersal has contributed to the disjunct biogeographical distribution of rain forest plants—something that has fascinated biogeographers since Humboldt's time. However, the dispersal agent for these tropical plant lineages remains puzzling. Here, we investigate which frugivory‐related traits may have facilitated past intercontinental long‐distance dispersal in the custard apple family (Annonaceae), a major vertebrate‐dispersed tropical plant family. We hypothesize that long‐distance dispersal was associated with the evolution of traits related to dispersal by large‐bodied mammals (e.g., large, dull‐coloured, “megafaunal” fruits) and strong‐flying, ocean‐crossing birds and bats (e.g., dehiscent, moniliform or cauliflorous fruits). Location Global. Taxon Annonaceae. Methods We used a fossil‐calibrated phylogenetic framework to infer the biogeographic history of 234 Annonaceae species (10%, covering nearly all genera) in relation to the evolution of 15 frugivory‐related traits, using maximum likelihood and Bayesian inferences. Furthermore, we used linear and generalized linear models and phylogenetic simulations to test whether ancestral fruit traits during intercontinental dispersal were different from those of other lineages not involved in long‐distance dispersal. Results We inferred the ancestral Annonaceae fruits to be small with a single or few small seeds and a small number of fruitlets. These fruits were most probably apocarpous, indehiscent and/or moniliform (i.e., long beads of fruitlets). Furthermore, most of the long‐distance dispersal events in Annonaceae occurred via the expanded tropical forests in the Early Cenozoic (“geodispersal”), and were significantly associated with large (c. 3 cm long), dull‐coloured fruits and short stipes. Additionally, long‐distance dispersal was also facilitated by dehiscent, moniliform and non‐cauliflorous fruits. Main conclusions We suggest that the evolution of frugivory‐related traits associated with dispersal by frugivores that frequently move across large distances and/or barriers, such as large‐bodied mammals and strong‐flying birds, has contributed to the disjunct tropical biogeographical distribution of Annonaceae, and probably of tropical rain forest plants more generally.

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“…High merism such as in the androecium (polyandry) and/or spiral phyllotaxis may favor organ number variations within species, suggesting that Ranunculales development is flexible, in contrast to most core eudicots and monocots. Polyandry is ancestral in the Papaveraceae and most probably in the Ranunculales (Sauquet et al, 2015). In Eschscholzia californica as in other members of the Papaveraceae, a ring primordium is formed on which the numerous stamen primordia progressively emerge.…”

Section: Floral Diversity In Ranunculalesmentioning

confidence: 99%

Genetics of flower development in Ranunculales – a new, basal eudicot model order for studying flower evolution

Damerval

Becker

2017

New Phytologist

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Contents 361I.361II.362III.363IV.364V.364Acknowledgements365References365 Summary Ranunculales, the sister group to all other eudicots, encompasses species with a remarkable floral diversity, which are currently emerging as new model organisms to address questions relating to the genetic architecture of flower morphology and its evolution. These questions concern either traits only found in members of the Ranunculales or traits that have convergently evolved in other large clades of flowering plants. We present recent results obtained on floral organ identity and number, symmetry evolution and spur formation in Ranunculales species. We discuss benefits and future prospects of evo‐devo studies in Ranunculales, which can provide the opportunity to decipher the genetic architecture of novel floral traits and also to appraise the degree of conservation of genetic mechanisms involved in homoplasious traits.

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Zygomorphy evolved from disymmetry in Fumarioideae (Papaveraceae, Ranunculales): new evidence from an expanded molecular phylogenetic framework

Cited by 34 publications

References 73 publications

Evolutionary diversification of CYC/TB1‐like TCP homologs and their recruitment for the control of branching and floral morphology in Papaveraceae (basal eudicots)

Evolutionary diversification of CYC/TB1‐like TCP homologs and their recruitment for the control of branching and floral morphology in Papaveraceae (basal eudicots)

Which frugivory‐related traits facilitated historical long‐distance dispersal in the custard apple family (Annonaceae)?

Genetics of flower development in Ranunculales – a new, basal eudicot model order for studying flower evolution

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