Triplet-driven chemical reactivity of β-carotene and its biological implications.

The endoperoxides of β-carotene (βCar-EPOs) are regarded as main products of the chemical deactivation of 1 O 2 by β-carotene, one of the most important antioxidants, following a concerted singlet-singlet reaction. Here we challenge this view by showing that βCar-EPOs are formed in the absence of 1 O 2 in a non-concerted triplet-triplet reaction: 3 O 2  +  3 β-carotene → βCar-EPOs, in which 3 β-carotene manifests a strong biradical character. Thus, the reactivity of β-carotene towards oxygen is governed by its excited triplet state. βCar-EPOs, while being stable in the dark, are photochemically labile, and are a rare example of nonaromatic endoperoxides that release 1 O 2 , again not in a concerted reaction. Their light-induced breakdown triggers an avalanche of free radicals, which accounts for the pro-oxidant activity of β-carotene and the puzzling swap from its anti- to pro-oxidant features. Furthermore, we show that βCar-EPOs, and carotenoids in general, weakly sensitize 1 O 2 . These findings underlie the key role of the triplet state in determining the chemical and photophysical features of β-carotene. They shake up the prevailing models of carotenoid photophysics, the anti-oxidant functioning of β-carotene, and the role of 1 O 2 in chemical signaling in biological photosynthetic systems. βCar-EPOs and their degradation products are not markers of 1 O 2 and oxidative stress but of the overproduction of extremely hazardous chlorophyll triplets in photosystems. Hence, the chemical signaling of overexcitation of the photosynthetic apparatus is based on a 3 chlorophyll- 3 β-carotene relay, rather than on extremely short-lived 1 O 2 .