Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants

TLDR

Singlet oxygen, produced from triplet‑excited chlorophylls under excess light, is a reactive oxygen species that can be toxic yet also serves as a signaling molecule leading to cell death or acclimation. The study investigates whether light stress induces oxidation of β‑carotene in Arabidopsis, producing volatile derivatives. β‑Cyclocitral, a volatile oxidation product of β‑carotene, triggers expression of many singlet‑oxygen‑responsive genes, has minimal impact on hydrogen‑peroxide markers, and enhances tolerance to photooxidative stress, indicating it functions as a high‑light stress signal in the singlet‑oxygen signaling pathway.

Abstract

(1)O(2) (singlet oxygen) is a reactive O(2) species produced from triplet excited chlorophylls in the chloroplasts, especially when plants are exposed to excess light energy. Similarly to other active O(2) species, (1)O(2) has a dual effect: It is toxic, causing oxidation of biomolecules, and it can act as a signal molecule that leads to cell death or to acclimation. Carotenoids are considered to be the main (1)O(2) quenchers in chloroplasts, and we show here that light stress induces the oxidation of the carotenoid β-carotene in Arabidopsis plants, leading to the accumulation of different volatile derivatives. One such compound, β-cyclocitral, was found to induce changes in the expression of a large set of genes that have been identified as (1)O(2) responsive genes. In contrast, β-cyclocitral had little effect on the expression of H(2)O(2) gene markers. β-Cyclocitral-induced reprogramming of gene expression was associated with an increased tolerance to photooxidative stress. The results indicate that β-cyclocitral is a stress signal produced in high light that is able to induce defense mechanisms and represents a likely messenger involved in the (1)O(2) signaling pathway in plants.