Xanthophyll cycle--a mechanism protecting plants against oxidative stress

Abstract

Six different xanthophyll cycles have been described in photosynthetic organisms. All of them protect the photosynthetic apparatus from photodamage caused by light-induced oxidative stress. Overexcitation conditions lead, in the chloroplast, to the over-reduction of the NADP pool and production of superoxide, which can subsequently be metabolized to hydrogen peroxide or a hydroxyl radical, other reactive oxygen species (ROS). On the other hand, overexcitation of photosystems leads to an increased lifetime of the chlorophyll excited state, increasing the probability of chlorophyll triplet formation which reacts with triplet oxygen forming single oxygen, another ROS. The products of the light-dependent phase of xanthophyll cycles play an important role in the protection against oxidative stress generated not only by an excess of light but also by other ROS-generating factors such as drought, chilling, heat, senescence, or salinity stress. Four, mainly hypothetical, mechanisms explaining the protective role of xanthophyll cycles in oxidative stress are presented. One of them is the direct quenching of overexcitation by products of the light phase of xanthophyll cycles and three others are based on the indirect participation of xanthophyll cycle carotenoids in the process of photoprotection. They include: (1) indirect quenching of overexcitation by aggregation-dependent light-harvesting complexes (LHCII) quenching; (2) light-driven mechanisms in LHCII; and (3) a model based on charge transfer quenching between Chl a and Zx. Moreover, results of the studies on the antioxidant properties of xanthophyll cycle pigments in model systems are also presented.

Figure 1.

The response of plants to different abiotic and biotic stresses. The antioxidant system (enzymatic and non-enzymatic scavengers) enables plants to regulate ROS level and influence on ROS-dependent signal induction. High ROS generation and weak interaction of the antioxidant system cause cell death. Domination of antioxidant system over ROS generation allows defence response or increase in stress tolerance.

Figure 2.

Routes of generation of ROS during the light phase of photosynthesis. ³Chl* on account of increasing chlorophyll excited state (¹Chl*) in incomplete photochemical quenching, reacts with oxygen (³O₂) to form ¹O₂. Over-reduction of the NADP pool causes O₂⁻ production by Mehler's reaction (A). The photoprotective mechanism of excess energy dissipation through NPQ, blocking generation of ROS (B).

Figure 3.

Energy-level diagram. The localization of the S₁ and S₂ energy levels of chlorophyll a (Chl a) and S₁ energy levels of carotenoids. The energies of Chl a: S₂(Qx) 16 000/cm and S₁(Qy) 14 700/cm. The energies of the S₁ state of xanthophylls: violaxanthin (Vx, 15 290/cm), diadinoxanthin (Ddx, 15 130/cm), antheraxanthin and lutein (Ax/L, 14 720/cm), diatoxanthin (Dtx, 14 485/cm), and zeaxanthin (Zx, 14 170/cm).²⁸ Arrows from left to right represent forward energy transfer (light-harvesting); arrows from right to left – reverse energy transfer (NPQ).

Figure 4.

Aggregation-dependent indirect quenching of overexcitation by LHCII. The conformation change produces energy transfer from Chl a to a lutein.

Figure 5.

Model of light-induced transformation of the antenna complex LHCII. Illumination in physiological conditions results in Vx all-trans to Vx cis isomerisation, which causes dissociation of LHCII trimers to monomers, resulting in increased thermal energy dissipation.

Figure 6.

Model of charge transfer quenching between Chl a and Zx. This mechanism involves energy transfer from chl to Chl–Zx heterodimer.