On the molecular pathways supporting the development of structurally coloured cuticle in Hibiscus trionum

Evolving from a single ancestor that appeared between 250 and 125 million years ago, flowering plants are the most diverse group of plants with about 78% of plant species. The staggering diversity of flowering plants is often correlated with their capacity of adaptation to the diversity of niche space offered by numerous different animal pollinators displaying many different sensory and behavioural traits. In response to selective pressure to attract pollinators, flowers have developed many strategies such as the production of volatile compounds, thermal patterns, visual cues, and rewards amongst others. In 2009, observations of the proximal adaxial part of Hibiscus trionum petals revealed the presence of structural colours. They are mainly characterised by the specific reflection of blue and UV-light in an angle dependant manner (also known as iridescence). Further observations of the cuticle showed the presence of nano-scaled striations acting as a grating like surface responsible for the diffraction of light. Computational modelling, and existing knowledge in material physics, suggests that the development of such a structure is induced by the buckling of the petal cuticle. In this PhD, the molecular pathways and mechanisms underpinning the production of nanoscaled petal ridges were investigated in Hibiscus trionum. Liquid extraction surface analyses coupled with mass spectrometry were conducted on striated and non-striated tissues, allowing us to highlight the importance of the cuticle chemistry in the development of nano-scaled ridges. The abundance of a specific cutin monomer and the reticulation of the cutin network appeared to be crucial for the buckling of the cuticle. Further investigation using transcriptomic analyses of distal and proximal petal tissues before and after the development of striations revealed the importance of SHN3 and DEWAX transcription factors in the modulation of the cuticle chemistry of the petals. The upregulation of SHN3 and DEWAX expression in the proximal petal region suggested that cuticle buckling could be enabled by a relative abundance of cutin and a decrease in the wax content of the cuticle. Further transcriptomic III analyses revealed the up regulation of numerous genes involved in pectin catabolism in the proximal petal region, consistently with the production of a compliant, softer cell wall for the development of striations. Mutant screen experiments identified 2 mutant lines characterised by the presence of smooth patches of cells and the presence of conical cells in one of them. Further characterisation of the mutant phenotypes suggested the importance of the cell shape and the thickness of the cuticle to achieve proper bucking. Finally, the adhesion properties of structurally coloured cuticle were briefly studied by testing the gripping capacity of Leptinotarsa decemlineata on replicas of the structurally coloured cuticle of Paeonia mascula petals. Wettability was also investigated by measuring the contact angle of water droplets on similar replicas. Together, these results demonstrate that structurally coloured cuticle resulting from nano-scaled striation decreases the grip ability of L. decemlineata, potentially by a decrease in the contact surface between the setose pads and the cuticle.

The European Commission: Marie Skłodowska Curie Actions: Plant inspired Material and Surfaces (PLAMATSU) Innovative training network (ITN).