β-cyclocitral elicits rapid signaling distinct from the excess-light response in Arabidopsis

Abstract

{beta}-Cyclocitral ({beta}-cc), a {beta}-carotene oxidation product, has been proposed as an early retrograde signal that primes protection against photooxidative stress. Its temporal relationship with photosynthetic acclimation, however, remains unresolved. Exogenous {beta}-cc elicited cytosolic calcium changes within minutes and induced the {beta}-cc-responsive pAER::LUC detoxification reporter within 40 min. We exposed Arabidopsis thaliana plants to 1500 mol photons m-2 s-1 under ventilation creating a high-irradiance regime without concomitant heat stress and with a relatively mild photooxidative outcome (RT-EL). Non-photochemical quenching increased, whereas PSII maximum quantum yield progressively decreased during RT-EL, with both responses approaching a plateau by 16 h. Volatile {beta}-cc pretreatment did not improve photosynthetic performance or NPQ dynamics, whereas endogenous {beta}-cc and {beta}-cyclocitric acid accumulated only after prolonged RT-EL exposure (16 h). By contrast, hormone profiling and RNA-seq revealed extensive {beta}-cc-dependent reprogramming that was largely opposite to the RT-EL transcriptional response. Together, these results reveal a kinetic separation between rapid {beta}-cc signaling and its endogenous production. Under RT-EL major photosynthetic adjustments precede detectable {beta}-cc accumulation, whereas {beta}-cc triggers cellular responses within minutes once present. We therefore propose that the timing of {beta}-cc action during excess light is determined primarily by the onset of substantial {beta}-carotene oxidation.