Evolutionary Insights into β-Cyclocitral Signaling in Physcomitrium patens

Carotenoids are central to plant signaling, serving as precursors to phytohormones like abscisic acid and strigolactones. Among their oxidative derivatives, β-cyclocitral (β-CC) acts as a potent photoxidative stress signal. Produced through β-carotene oxidation in chloroplasts under excessive light (EL), β-CC acts as a retrograde signal and triggers a nuclear detoxification response, protecting cells from oxidative damage. SCL14, a GRAS-domain protein, leads this pathway, activating a cascade of ANAC transcription factors, which in turn induce detoxification enzymes. Yet, β-CC signaling remains cryptic: a volatile, water-soluble molecule with no known receptor and no biosynthetic mutants for functional studies. To tackle its molecular signaling, we explored its evolutionary origins, investigating Physcomitrium patens, a bryophyte that provides a window into early land plant stress responses, offering insights on mechanisms predating vascular plants, which acquired more sofisticated processes to handle photooxidative stress. Using PAM fluorimetry, we tested β-CC effect on P. patens under EL stress. Instead of enhancing protection, β-CC reduced photosynthetic efficiency and increased ROS accumulation. Similarly, the SCL14-regulated detoxification system is incomplete in Physcomitrium and may represent a key transition in β-cyclocitral response across more recent plant lineages. However, its strong transcriptional response, largely overlapping EL repsonse, suggests a conserved but functionally divergent β-CC response in bryophytes, shedding light on the evolutionary trajectory of carotenoid-derived stress signaling. Moreover, we identified a direct and specific effect of β-cyclocitral on photosynthesis, a response absent in Angiosperms. This divergence suggests an early signaling role that may have been reprogrammed in vascular plants as a proper retrograde signaling to optimize oxidative stress resilience. Further investigation will clarify how this pathway evolved and its broader implications for plant adaptation to terrestrial environments.