Apocarotenoid signaling regulates meristem activity and shapes shoot and root lateral organ formation in Arabidopsis

Plant carotenoids are precursors to phytohormones and signaling molecules, playing critical roles in plant development, an emerging area of research. This study investigates the function of the undefined apocarotenoid ACS1 signal in modulating plant development, particularly its impact on the morphologenesis of lateral organs and apical meristems. By modulating ACS1 levels under varying light conditions, we demonstrate its dynamic role in leaf and root development. Notably the characteristic radial leaf morphology of the clb5 mutant reverts to normal even days post-germination, demonstrating that ACS1 is not a toxic signal but rather a key component of a biogenic retrograde signaling pathway. Transcriptomic analysis of clb5 seedlings at different post-germination stages underscores the critical role of ACS1 during specific developmental window. The expression profile of this mutant correlates with a proplastid stage, where even the expression of most of the genes involved in plastid biogenesis are downregulated. Furthermore, ACS1 disrupts the expression of diverse developmentally important genes, including those participating in auxin transport and signaling, leading to impaired meristem maintenance and inhibiting leaf expansion. The effects of ACS1 extends beyond photosynthetic tissues, impacting shoot and apical root meristem organization. In particular, ACS1 affects columella cell pattering, disrupting normal gravitropic responses. These findings demonstrate that ACS1 dynamically regulates both leaf and root development, as well as meristem activity. This study provides new insights into the role of cis-carotenoids as retrograde signals, functioning very early in the plastid differentiation and emphasizes the significance of plastid retrograde signaling in plant growth and development.