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

Abstract

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.