Evolution of a SHOOTMERISTEMLESS transcription factor binding site promotes fruit shape determination

In animals and plants, organ shape is primarily determined during primordium development by carefully coordinated growth and cell division1–3. Rare examples of post-primordial change in morphology (reshaping) exist that offer tractable systems for the study of mechanisms required for organ shape determination and diversification. One such example is morphogenesis in Capsella fruits whose heart-shaped appearance emerges by reshaping of the ovate spheroid gynoecium upon fertilization4. Here we use whole-organ live-cell imaging and single-cell RNA sequencing (scRNA-seq) analysis to show that Capsella fruit shape determination is based on dynamic changes in cell growth and cell division coupled with local maintenance of meristematic identity. At the molecular level, we reveal an auxin-induced mechanism that is required for morphological alteration and ultimately determined by a single cis-regulatory element. This element resides in the promoter of the Capsella rubella SHOOTMERISTEMLESS5 (CrSTM) gene. The CrSTM meristem identity factor positively regulates its own expression through binding to this element, thereby providing a feed-forward loop at the position and time of protrusion emergence to form the heart. Independent evolution of the STM-binding element in STM promoters across Brassicaceae species correlates with those undergoing a gynoecium-to-fruit shape change. Accordingly, genetic and phenotypic studies show that the STM-binding element is required to facilitate the shape transition and suggest a conserved molecular mechanism for organ morphogenesis. This study identifies a molecular mechanism promoting fruit shape variation. Local meristem identity is maintained through autoregulatory activation of the STM gene to allow post-fertilization changes in fruit morphology.