Evolutionary insights into β-cyclocitral signaling in Physcomitrium patens

Abstract

How did a product of photooxidative damage become a signal for stress tolerance? {beta}-cyclocitral ({beta}-cc) promotes acclimation in several angiosperms, yet has detrimental effects in other photosynthetic organisms. We investigated this contrast in the moss Physcomitrium patens to explore the evolution of {beta}-cc signaling. We combined apocarotenoid treatments and excess light exposure with photosynthetic measurements, biochemical analyses and RNA sequencing. Comparative phylogenomics traced the conservation of regulatory and detoxification components associated with {beta}-cc responses. Physcomitrium accumulated {beta}-cc under excess light and mounted a strong transcriptional response to exogenous {beta}-cc, substantially overlapping with its light-stress response. Nevertheless, {beta}-cc impaired photosynthetic performance and provided no protection. At a phylogenetic level, while MBS1 was deeply conserved, the downstream detoxification module showed marked divergence. Notably, ANAC081/ANAC102-like proteins were recovered in terrestrial monocots but not in Physcomitrium or Lemna turionifera, both showing detrimental responses to {beta}-cc. Our findings suggest that the evolution of protective {beta}-cc signaling involved the recruitment of downstream detoxification regulators, with the SCL14/TGAII- and ANAC081/ANAC102-related lineage emerging as a candidate link between an ancient oxidative cue and beneficial acclimation.