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Moyroud, E.

Publications and source records attributed to Moyroud, E..

6 recordsLinked to original sources

Recurrent Emergence of Boundary Cell Types During Evolution of Floral Bullseye Patterns

Petal patterns play an important role in the reproductive success of flowering plants by attracting pollinators and protecting reproductive organs from environmental factors. Some transcription factors (TFs) that control pigment production and cuticle elaboration in petal epidermal cells have been identified. However, little is known about the upstream developmental processes that pre-pattern the petal surface to first establish the different domains where these regulators will later be expressed. Here, we developed a computational model of the evolution and development of petal patterns to investigate this early pre-patterning phase. We selected for gene regulatory networks (GRNs) that could divide the petal surface into proximal and distal domains to create a bullseye, a very common type of petal pattern across the angiosperms. The evolved GRNs showed robust patterning dynamics and could generate a variety of bullseye proportions. We found that the evolution of bullseye patterns was often accompanied by the spontaneous emergence of a third cell type with a unique gene expression profile at the boundary between the proximal and distal regions. These bullseye boundary cells appeared in most simulations despite not being explicitly selected for, and we validated their presence experimentally in Hibiscus trionum, a model system whose flowers display a bullseye pattern. Although boundary cell types emerged spontaneously in our simulations, they evolved more often and were more important for pattern formation when gene expression was modelled as a noisy process. This suggests that GRNs producing this emergent cell type may support reproducible bullseye formation by buffering against developmental variability. Altogether, the results from our evolutionary simulations illuminate the early steps of petal pattern formation and demonstrate that novel cell types can arise spontaneously and repeatedly from selection on other cell types when developmental robustness is considered.

systems biology↗

The genetic basis of replicated bullseye pattern reduction across the Trionum Complex

Angiosperm flowers exhibit a wide diversity of colorful motifs on their petals. Such patterns fulfill both biotic and abiotic functions, mediating plant-pollinator communication and providing protection against damaging UV rays or desiccation. These motifs are often evolutionary labile, varying in size, shape and hue between closely related species and constitute excellent systems to illuminate the evolutionary processes that generate morphological diversity or instead lead to the repetitive emergence of similar forms. Hibiscus trionum flowers have a prominent bullseye pattern combining a purple center contrasting against a white margin. H. trionum belongs to a small clade of Hibiscus known as the Trionum Complex that displays a range of petal patterns within and between species. Here, we integrate phylogenomic approaches, molecular techniques and genetic manipulation to solve species relationships across the Trionum Complex, identify key genes involved in the production of bullseye pigmentation, and reveal molecular events underpinning pattern variation during the evolution of the group. We find that repetitive bullseye reduction events primarily occur through independent modifications of a single genetic locus encoding BERRY1, an R2R3 MYB that regulates anthocyanin pigment production in petals. Moreover, we demonstrate that buff-tailed bumblebees (Bombus terrestris) discriminate against flowers with smaller bullseye sizes suggesting that a reduction in bullseye proportions potentially impacts plant fitness and contributes to trait distribution across the group. Collectively, our results demonstrate how repeated mutations in a single locus led to morphological variation in petal patterning, a trait that contributes to angiosperm reproductive isolation and speciation.

plant biology↗

Hibiscus bullseyes reveal mechanisms controlling petal pattern proportions that influence plant-pollinator interactions

Colourful patterns on flower corollas are key signals to attract pollinators. The formation of such motifs relies on the establishment of developmental boundaries that partition the growing petal epidermis into different subdomains, where cells can produce specific pigments and acquire distinctive cell shapes and textures. While some of the transcription factors and biosynthetic pathways producing these characteristics as cell differentiate have been extensively studied, the upstream processes restricting the activities of molecular players to specific regions of the petal epidermis remain enigmatic. Here, we unveil that the petal surface of Hibiscus trionum, an emerging model system featuring a bullseye on its corolla, is pre-patterned as the position of the bullseye boundary is specified long before the motif becomes visible to the human eye. Using a 1-D computational model, we explore how a boundary established at such an early stage can be maintained throughout development. Reciprocally, by exploiting transgenic lines and natural variants, we show that plants can regulate the relative position of the boundary during the pre-patterning phase or modulate division and growth on either side of this boundary at later developmental stages to yield variations in final bullseye proportions. Finally, we provide evidence that such modifications in bullseye size have functional significance as buff-tailed bumblebees (Bombus terrestris) can reliably identify a food source based on the size of its bullseye. Notably, we found that individuals exhibit a clear preference for the larger bullseye of H. trionum over the smaller pattern of its close relative, H. richardsonii.

plant biology↗

Investigating Phylogenetic Conflict using Homolog Trees reveals the Genetic Basis of Phenotypic Convergence in Carnivorous Sundews

Phenotypic convergence is found across the tree of life, and morphological similarities in distantly related species are often presumed to have evolved independently. However, clarifying the origins of traits has recently highlighted the complex nature of evolution, as apparent convergent features often share similar genetic foundations. Hence, the tree topology of genes that underlie such traits frequently conflicts with the overall history of species relationships. This conflict creates both a challenge for systematists and an exciting opportunity to investigate the rich, complex network of information that connects molecular trajectories with trait evolution. Here we present a novel conflict identification program named CAnDI (Conflict And Duplication Identifier), which enables the analysis of conflict in homologous gene trees rather than inferred orthologs. We demonstrate that the analysis of conflicts in homologous trees using CAnDI yields more comparisons than in ortholog trees in six datasets from across the eukaryotic tree of life. Using the carnivorous trap of Caryophyllales, a charismatic group of flowering plants, as a case study we demonstrate that analysing conflict on entire homolog trees can aid in inferring the genetic basis of trait evolution: by dissecting all gene relationships within homolog trees, we find genomic evidence that the molecular basis of the pleisiomorphic mucilaginous sticky trap was likely present in the ancestor of all carnivorous Caryophyllales. We also show that many genes whose evolutionary trajectories group species with similar trap devices code for proteins contributing to plant carnivory and identify a LATERAL ORGAN BOUNDARY DOMAIN transcription factor as a possible candidate for regulating sticky trap development.

evolutionary biology↗

Complex petal spot formation in the Beetle Daisy (Gorteria diffusa) relies on spot-specific accumulation of malonylated anthocyanin regulated by paralogous GdMYBSG6 transcription factors

Gorteria diffusa has elaborate petal spots that attract male bee-fly pollinators through sexual deception but the genetic basis of G. diffusa petal spot development is currently unknown. Here we investigate the regulation of pigmentation during spot formation. We used UHPLC-MS/MS to determine the anthocyanin composition of spots and background pigmentation in G. diffusa. Combining gene expression analysis with protein interaction assays we characterised three R2R3-MYB genes regulating anthocyanin production in G. diffusa spots. We found that cyanidin 3-glucoside pigments G. diffusa ray floret petals. Unlike other petal regions, spots contain a high proportion of malonylated anthocyanin. We identified three paralogous subgroup 6 R2R3-MYB transcription factors that activate the production of petal spot pigmentation. The corresponding genes are upregulated in developing spots and induce ectopic anthocyanin production upon heterologous expression in tobacco. EMSAs and dual luciferase assays suggest that these transcription factors regulate genes encoding three anthocyanin synthesis enzymes: anthocyanidin synthase (GdANS), dihydroflavonol reductase (GdDFR) and malonyl transferase (GdMAT1), accounting for the spot-specific production of malonylated pigments. Here we provide the first molecular characterisation of G. diffusa spot development, showing that the elaboration of complex spots begins with accumulation of malonylated pigments at the base of ray floret petals, positively regulated by three subgroup 6 R2R3-MYB transcription factors.

plant biology↗

Disentangling biological and analytical factors that give rise to outlier genes in phylogenomic matrices

The genomic data revolution has enabled biologists to develop innovative ways to infer key episodes in the history of life. Whether genome-scale data will eventually resolve all branches of the Tree of Life remains uncertain. However, through novel means of interrogating data, some explanations for why evolutionary relationships remain recalcitrant are emerging. Here, we provide four biological and analytical factors that explain why certain genes may exhibit "outlier" behavior, namely, rate of molecular evolution, alignment length, misidentified orthology, and errors in modeling. Using empirical and simulated data we show how excluding genes based on their likelihood or inferring processes from the topology they support in a supermatrix can mislead biological inference of conflict. We next show alignment length accounts for the high influence of two genes reported in empirical datasets. Finally, we also reiterate the impact misidentified orthology and short alignments have on likelihoods in large scale phylogenetics. We suggest that researchers should systematically investigate and describe the source of influential genes, as opposed to discarding them as outliers. Disentangling whether analytical or biological factors are the source of outliers will help uncover new patterns and processes that are shaping the Tree of Life.

evolutionary biology↗