Style deflection is determined by the handedness of phyllotaxis and differential cell elongation in a species with mirror-image flowers

Abstract

ABSTRACTMany animals and plants show left-right (LR) asymmetry. In some animal systems, handedness has a simple genetic basis, which has allowed identifying how handedness is determined at the molecular level, even if its functional relevance remains unclear. Mirror-image flowers represent an example of LR asymmetry of clear functional significance, with the reciprocal placement of male and female organs in left-versus right-handed flowers promoting cross-pollination. Here, we use the South African geophyteCyanella albato study how handedness of its mirror-image flowers is determined and elaborated during development. Inflorescences ofC. albaproduce flowers with a largely consistent handedness. However, we find that this handedness has no simple genetic basis, and individual plants can switch handedness between years. Rather, it is the direction of the phyllotactic spiral that determines floral handedness. Cellular analysis combined with biophysical modelling demonstrates that style deflection is driven by increased cell expansion in the adaxial carpel facing the next oldest flower compared to the other adaxial carpel. The carpel with greater expansion shows transcriptional signatures of increased auxin signaling and cell-wall modifications compared to the less expanding one. We propose that a recently described inherent LR auxin asymmetry in the initiating organs of spiral phyllotaxis determines handedness inC. alba, representing a conserved non-genetic mechanism for creating a stable floral polymorphism. This mechanism links chirality across different levels of plant development and exploits a developmental constraint in a core patterning process to produce morphological variation of ecological relevance.SIGNIFICANCE STATEMENTSeveral plant species show left-right asymmetry in their flowers, with the female reproductive organ displaced to the left or to the right of the midline, and at least one of the male organs positioned reciprocally. This increases reproductive success by promoting cross-pollination between individuals, yet how the handedness of flowers is established is unknown. Here, we show that mostCyanella albaplants form flowers of only one handedness, but this is not genetically controlled. Rather, left-right determination in flowers builds on a patterning process at the shoot tip that forms leaf and flower primordia in a clockwise or counter-clockwise spiral. Thus, an inbuilt handedness at one level of development is used to establish left-right asymmetry of ecological relevance.