Edwige Moyroud

Pointillist structural color in Pollia fruit

Biological communication by means of structural color has existed for at least 500 million years. Structural color is commonly observed in the animal kingdom, but has been little studied in plants. We present a striking example of multilayer-based strong iridescent coloration in plants, in the fruit of Pollia condensata. The color is caused by Bragg reflection of helicoidally stacked cellulose microfibrils that form multilayers in the cell walls of the epicarp. We demonstrate that animals and plants have convergently evolved multilayer-based photonic structures to generate colors using entirely distinct materials. The bright blue coloration of this fruit is more intense than that of any previously described biological material. Uniquely in nature, the reflected color differs from cell to cell, as the layer thicknesses in the multilayer stack vary, giving the fruit a striking pixelated or pointillist appearance. Because the multilayers form with both helicoidicities, optical characterization reveals that the reflected light from every epidermal cell is polarized circularly either to the left or to the right, a feature that has never previously been observed in a single tissue.

Prediction of Regulatory Interactions from Genome Sequences Using a Biophysical Model for the Arabidopsis LEAFY Transcription Factor

This work presents the generation of a predictive model describing the DNA recognition specificity of the LEAFY floral transcription factor. The model is used to predict in vivo regulatory interactions between LEAFY and its target genes from mere inspection of various plant genome sequences. Despite great advances in sequencing technologies, generating functional information for nonmodel organisms remains a challenge. One solution lies in an improved ability to predict genetic circuits based on primary DNA sequence in combination with detailed knowledge of regulatory proteins that have been characterized in model species. Here, we focus on the LEAFY (LFY) transcription factor, a conserved master regulator of floral development. Starting with biochemical and structural information, we built a biophysical model describing LFY DNA binding specificity in vitro that accurately predicts in vivo LFY binding sites in the Arabidopsis thaliana genome. Applying the model to other plant species, we could follow the evolution of the regulatory relationship between LFY and the AGAMOUS (AG) subfamily of MADS box genes and show that this link predates the divergence between monocots and eudicots. Remarkably, our model succeeds in detecting the connection between LFY and AG homologs despite extensive variation in binding sites. This demonstrates that the cis-element fluidity recently observed in animals also exists in plants, but the challenges it poses can be overcome with predictions grounded in a biophysical model. Therefore, our work opens new avenues to deduce the structure of regulatory networks from mere inspection of genomic sequences.

Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins

The LEAFY (LFY) protein is a key regulator of flower development in angiosperms. Its gradually increased expression governs the sharp floral transition, and LFY subsequently controls the patterning of flower meristems by inducing the expression of floral homeotic genes. Despite a wealth of genetic data, how LFY functions at the molecular level is poorly understood. Here, we report crystal structures for the DNA‐binding domain of Arabidopsis thaliana LFY bound to two target promoter elements. LFY adopts a novel seven‐helix fold that binds DNA as a cooperative dimer, forming base‐specific contacts in both the major and minor grooves. Cooperativity is mediated by two basic residues and plausibly accounts for LFYs effectiveness in triggering sharp developmental transitions. Our structure reveals an unexpected similarity between LFY and helix‐turn‐helix proteins, including homeodomain proteins known to regulate morphogenesis in higher eukaryotes. The appearance of flowering plants has been linked to the molecular evolution of LFY. Our study provides a unique framework to elucidate the molecular mechanisms underlying floral development and the evolutionary history of flowering plants.

Analysing photonic structures in plants

The outer layers of a range of plant tissues, including flower petals, leaves and fruits, exhibit an intriguing variation of microscopic structures. Some of these structures include ordered periodic multilayers and diffraction gratings that give rise to interesting optical appearances. The colour arising from such structures is generally brighter than pigment-based colour. Here, we describe the main types of photonic structures found in plants and discuss the experimental approaches that can be used to analyse them. These experimental approaches allow identification of the physical mechanisms producing structural colours with a high degree of confidence.

The LEAFY Floral Regulators in Angiosperms: Conserved Proteins with Diverse Roles

Genetic analyses in model angiosperms have shown that the LEAFY/FLORICAULA transcription factor plays a central role in flower development. In Arabidopsis, LEAFY (LFY) triggers the development of floral meristems and controls their patterning through the activation of floral organ identity genes. Several recent reports enlighten the structure and function of this conserved protein but also illustrate the variety of roles it plays in different angiosperms.

A variant of LEAFY reveals its capacity to stimulate meristem development by inducing RAX1

In indeterminate inflorescences, floral meristems develop on the flanks of the shoot apical meristem, at positions determined by auxin maxima. The floral identity of these meristems is conferred by a handful of genes called floral meristem identity genes, among which the LEAFY (LFY) transcription factor plays a prominent role. However, the molecular mechanism controlling the early emergence of floral meristems remains unknown. A body of evidence indicates that LFY may contribute to this developmental shift, but a direct effect of LFY on meristem emergence has not been demonstrated. We have generated a LFY allele with reduced floral function and revealed its ability to stimulate axillary meristem growth. This role is barely detectable in the lfy single mutant but becomes obvious in several double mutant backgrounds and plants ectopically expressing LFY. We show that this role requires the ability of LFY to bind DNA, and is mediated by direct induction of REGULATOR OF AXILLARY MERISTEMS1 (RAX1) by LFY. We propose that this function unifies the diverse roles described for LFY in multiple angiosperm species, ranging from monocot inflorescence identity to legume leaf development, and that it probably pre-dates the origin of angiosperms.

The flower of Hibiscus trionum is both visibly and measurably iridescent

Living organisms can use minute structures to manipulate the reflection of light and display colours based on interference. There has been debate in recent literature over whether the diffractive optical effects produced by epoxy replicas of petals with folded cuticles persist and induce iridescence in the original flowers when the effects of petal pigment and illumination are taken into account. We explored the optical properties of the petal of Hibiscus trionum by macro-imaging, scanning and transmission electron microscopy, and visible and ultraviolet (UV) angle-resolved spectroscopy of the petal. The flower of Hibiscus trionum is visibly iridescent, and the iridescence can be captured photographically. The iridescence derives from a diffraction grating generated by folds of the cuticle. The iridescence of the petal can be quantitatively characterized by spectrometric measurements with several square-millimetres of sample area illuminated. The flower of Hibiscus trionum has the potential to interact with its pollinators (honeybees, other bees, butterflies and flies) through iridescent signals produced by its cuticular diffraction grating.

Buckling as an origin of ordered cuticular patterns in flower petals.

The optical properties of plant surfaces are strongly determined by the shape of epidermal cells and by the patterning of the cuticle on top of the cells. Combinations of particular cell shapes with particular nanoscale structures can generate a wide range of optical effects. Perhaps most notably, the development of ordered ridges of cuticle on top of flat petal cells can produce diffraction-grating-like structures. A diffraction grating is one of a number of mechanisms known to produce ‘structural colours’, which are more intense and pure than chemical colours and can appear iridescent. We explore the concept that mechanical buckling of the cuticle on the petal epidermis might explain the formation of cuticular ridges, using a theoretical model that accounts for the development of compressive stresses in the cuticle arising from competition between anisotropic expansion of epidermal cells and isotropic cuticle production. Model predictions rationalize cuticle patterns, including those with long-range order having the potential to generate iridescence, for a range of different flower species.

Structural colour from helicoidal cell-wall architecture in fruits of Margaritaria nobilis

The bright and intense blue-green coloration of the fruits of Margaritaria nobilis (Phyllanthaceae) was investigated using polarization-resolved spectroscopy and transmission electron microscopy. Optical measurements of freshly collected fruits revealed a strong circularly polarized reflection of the fruit that originates from a cellulose helicoidal cell wall structure in the pericarp cells. Hyperspectral microscopy was used to capture the iridescent effect at the single-cell level.

How Have Advances in Comparative Floral Development Influenced Our Understanding of Floral Evolution

Evolutionary developmental biology has come to prominence in the past two decades, in both the plant kingdom and the animal kingdom, particularly following the description of homeotic genes linked to key morphological transitions. A primary goal of evolutionary developmental biology (“evo-devo”) is to define how developmental programs are modified to generate novel or labile morphologies. This requires an understanding of the molecular genetic basis of these programs and of the evolutionary changes they have undergone. The past decade has seen the establishment of a common language and common standards, and these changes have greatly improved the integration of evo-devo. Recently, a more comparative approach has been added to mechanistic developmental biology. In this review we attempt to show how, by using this “next-generation evo-devo” approach, insights into both developmental biology and evolutionary biology can be gained. Although the concepts we discuss are more broadly applicable, we have focused our examples on traits of the angiosperm flower, a structure that has undergone enormous morphological and developmental evolution since its relatively recent appearance in the fossil record.