Developmental robustness from antagonizing cis-elements

Developmental transitions in plants are tightly regulated by transcriptional networks that require fine-tuned temporal and spatial control, with noncoding sequences in gene promoters playing a key role. The conserved transcriptional regulator UNUSUAL FLORAL ORGANS (UFO) is essential for floral development. In this study, Lanctot et al. identified highly conserved sequences within the UFO promoter in tomato and Arabidopsis, highlighting their role in cis-regulation. Focusing first on tomato, the authors analyzed the promoter of the UFO ortholog, ANANTHA (AN). They identified conserved noncoding sequences (CNSs) and a chromatin accessibility “hotspot” indicative of cis-regulatory activity. CRISPR editing of this region caused strong phenotypic alterations in inflorescence and floral development. A gain-of-function mutant revealed that the deletion of a transcription factor binding site is associated with AN gain of function, with variability in expressivity suggesting the involvement of both activators and repressors. Biallelic mutant analysis confirmed that a balanced dosage of these factors is crucial for robust floral architecture. Extending their analysis to Arabidopsis, the authors found that while homologous regulatory sequences are more dispersed within the UFO promoter, they maintain similar functional control. However, phenotypic differences in mutant lines suggest species-specific regulatory divergence due to differing UFO expression patterns. This study highlights the complexity of cis-regulatory mechanisms in dynamic developmental genes, demonstrating that short, conserved sequences recruit both activators and repressors to maintain developmental robustness across species. (Summary by Elisa De Meo, www.linkedin.com/in/elisa-de-meo-25415a20b) PNAS,  10.1073/pnas.2421990122