Plant apocarotenoid metabolism utilizes defense mechanisms against reactive carbonyl species and xenobiotics

Carotenoid levels in plant tissues depend on the relative rates of synthesis and degradation of the molecules in the pathway. While plant carotenoid biosynthesis has been extensively characterized, research on carotenoid degradation and catabolism into apocarotenoids is a relatively novel field. To identify apocarotenoid metabolic processes, we characterized the transcriptome of transgenic Arabidopsis (Arabidopsis thaliana) roots accumulating high levels of beta-carotene and, consequently, beta-apocarotenoids. Transcriptome analysis revealed feedback regulation on carotenogenic gene transcripts suitable for reducing beta-carotene levels, suggesting involvement of specific apocarotenoid signaling molecules originating directly from beta-carotene degradation or after secondary enzymatic derivatizations. Enzymes implicated in apocarotenoid modification reactions overlapped with detoxification enzymes of xenobiotics and reactive carbonyl species (RCS), while metabolite analysis excluded lipid stress response, a potential secondary effect of carotenoid accumulation. In agreement with structural similarities between RCS and beta-apocarotenoids, RCS detoxification enzymes also converted apocarotenoids derived from beta-carotene and from xanthophylls into apocarotenols and apocarotenoic acids in vitro. Moreover, glycosylation and glutathionylation-related processes and translocators were induced. In view of similarities to mechanisms found in crocin biosynthesis and cellular deposition in saffron (Crocus sativus), our data suggest apocarotenoid metabolization, derivatization and compartmentalization as key processes in (apo)carotenoid metabolism in plants.

Automated summary

This study characterized the transcriptome of transgenic Arabidopsis roots accumulating high levels of beta-carotene and beta-apocarotenoids, shedding light on the feedback regulation and metabolic processes involved in carotenoid degradation. The research suggests that apocarotenoid metabolization, derivatization, and compartmentalization play key roles in (apo)carotenoid metabolism in plants, with implications for detoxification enzymes and cellular deposition mechanisms.