Natural variation in Arabidopsis uncouples leaf and flower development and reveals massive transcriptomic heterochrony.
Plant development is a sequence of precisely timed and spatially coordinated events that produce organs such as leaves and flowers. In Arabidopsis thaliana, for example, the development of leaves (called bracts in the inflorescence) halts once the first flower forms. Understanding how this transition is regulated is key for decoding how developmental programmes are coordinated during the floral transition. In this study, we investigated a natural phenotypic variation that uncouples bract repression from flower initiation. We discovered that the continued formation of bracts after the floral transition involves complex genetic interactions across at least four loci. Interestingly, none of these loci included known floral identity genes previously linked to bract repression, pointing to novel regulators in the coordination of bract and flower development. Using time-series transcriptomics and curve registration, we found that differences in gene expression levels when bracts persist are mainly driven by a massive desynchronization of gene dynamics. This affects a wide range of biological processes beyond those associated with leaf identity. These findings align with the ‘inverse hourglass’ model, which proposes that transcriptomic divergence at transitional stages contributes to morphological variation. Our results suggest that this model may also explain trait variability within species, highlighting how transcriptome dynamics shape phenotypic robustness during developmental transitions.