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

Plastids synthesize signals crucial for plant development, including carotenoid-derived molecules with hormonal and retrograde signaling functions that regulate nuclear gene expression, which is an emerging research area. Here we investigate the function of the plastid-derived apocarotenoid signal 1 (ACS1), whose accumulation disrupts plastid biogenesis, affects lateral organ formation, and compromises apical meristem maintenance. By modulating ACS1 levels in Arabidopsis (Arabidopsis thaliana) through different light conditions, we show its reversible and dynamic role in leaf and root development. Notably, the characteristic morphological defects of ACS1-accumulating mutants revert under conditions that limit its synthesis, even several days post-germination. This indicates that ACS1 does not cause irreversible damage but rather acts as a signal produced under specific tissues and conditions that associates with the cell-specific expression of its biosynthetic enzymes. Transcriptomic analysis of ACS1-accumulating mutants shows a critical developmental window during which ACS1 affects the expression of numerous plastid-housekeeping genes, correlating with an early block in plastid biogenesis after DNA replication and before transcriptional activation. This disruption affects chloroplast biogenesis and amyloplast starch accumulation. ACS1 accumulation also alters the expression of key developmental regulators, including genes involved in auxin signaling and transport, leading to compromised meristem maintenance and leaf expansion. Beyond photosynthetic tissues, ACS1 also disrupts root apical meristem organization, notably altering columella cell patterning and gravitropic responses. Overall, our findings establish ACS1 as a dynamic conditionally active plastid-derived signal that modulates plastid differentiation, meristem activity, and lateral organ development, underscoring the broader role of cis-carotenoid-derived signals in coordinating plastid function with plant growth and development.