Relationships Between Antioxidant Metabolism and Carotenoids in the Regulation of Photosynthesis

Abstract

SummaryThe large driving forces produced in photosynthesis require precise control and regulation to prevent potentially destructive side reactions involving active oxygen species that damage pigments and proteins. Oxygen can be activated either by energy transfer, yielding singlet oxygen, or by reduction, yielding superoxide or hydrogen peroxide. At Photosystem I, the lifetime of the excited chlorophyll singlet state within the antenna pigment bed is short and little threat is posed by formation of highly reactive singlet oxygen. The situation is completely different in Photosystem II. Here, the lifetime of singlet chlorophyll is sufficiently long to allow significant formation of chlorophyll triplet states able to transfer energy to ground state triplet oxygen, generating singlet oxygen. Carotenoids intervene to control these processes in at least two important ways. First, pigments such as β-carotene are capable of directly quenching both triplet chlorophyll and singlet oxygen states (the so-called triplet valve mechanism). Second, the xanthophyll cycle is involved in lowering the yield of triplet chlorophyll formation by pre-emptive quenching of excited singlet state chlorophyll, a mechanism that can have a high quantum yield value for energy dissipation. The chief difference between these two mechanisms is that the xanthophyll cycle is inducible and subject to regulation, whereas the triplet valve pathway is constitutive and unregulated. Although formation of singlet oxygen must be avoided or controlled, chloroplasts have exploited the potential of oxygen chemistry to drive and regulate metabolism while minimizing the deleterious effects of uncontrolled interactions with oxygen. Hence, while the potential of the chloroplast as a source of oxidative stress is large, in reality this organelle offers minimal risk because of pre-emptive regulation and effective defense. The production of superoxide and hydrogen peroxide by the thylakoid membranes is limited by efficient control of electron transport. This regulation limits the potential for oxidative damage and prevents high rates of electron transport to oxygen. Effective antioxidant defense ensrures rapid elimination of active forms of oxygen further preventing oxidative damage.