Antioxidant and Signaling Role of Plastid-Derived Isoprenoid Quinones and Chromanols

Abstract

Plant prenyllipids, especially isoprenoid chromanols and quinols, are very efficient low-molecular-weight lipophilic antioxidants, protecting membranes and storage lipids from reactive oxygen species (ROS). ROS are byproducts of aerobic metabolism that can damage cell components, they are also known to play a role in signaling. Plants are particularly prone to oxidative damage because oxygenic photosynthesis results in O₂ formation in their green tissues. In addition, the photosynthetic electron transfer chain is an important source of ROS. Therefore, chloroplasts are the main site of ROS generation in plant cells during the light reactions of photosynthesis, and plastidic antioxidants are crucial to prevent oxidative stress, which occurs when plants are exposed to various types of stress factors, both biotic and abiotic. The increase in antioxidant content during stress acclimation is a common phenomenon. In the present review, we describe the mechanisms of ROS (singlet oxygen, superoxide, hydrogen peroxide and hydroxyl radical) production in chloroplasts in general and during exposure to abiotic stress factors, such as high light, low temperature, drought and salinity. We highlight the dual role of their presence: negative (i.e., lipid peroxidation, pigment and protein oxidation) and positive (i.e., contribution in redox-based physiological processes). Then we provide a summary of current knowledge concerning plastidic prenyllipid antioxidants belonging to isoprenoid chromanols and quinols, as well as their structure, occurrence, biosynthesis and function both in ROS detoxification and signaling.

Keywords: antioxidants; lipid peroxidation; oxidative stress; plastochromanol; quinols; reactive oxygen species; signaling pathways; tocochromanols; tocopherols.

Figure 1

The types of ROS generated within the thylakoid membrane and place of action of the selected antioxidants. (SOD, superoxide dismutase; Fd, ferredoxin; FNR, ferredoxin–NADP⁺ reductase; PC, plastocyanin; cyt b₆f, cytochrome b₆f).

Figure 2

Plant isoprenoid chromanols. The more common compounds are shown in color, while the examples of rare forms are shown in black. The table depicts the substituents configuration in α-, β-, γ- and δ-forms of tocopherols and tocoenols. PC-8, plastochromanol; PC-OH, hydroxy-plastochromanol; T₁, tocomonoenols; T₂, tocodienols; T₃, tocotrienols.

Figure 3

Plant isoprenoid quinones. The common compounds are shown in color, while the examples of rare forms are shown in black. For plastoquinone-9, its reduced, quinol form also is shown. PQ-9, plastoquinone-9; PQ B, plastoquinone B; PQ C, plastoquinone C; PQH₂-9, plastoquinol-9; R, fatty acid hydrocarbon tail; α-TQ, α-tocopherol quinone; UQ-10, ubiquinone-10.

Figure 4

Synthesis of tocopherols, plastoquinone and plastochromanol-8 in higher plants. The mutants of genes encoding enzymes of Arabidopsis are given in italics. DMPBQ, 2,3-dimethyl-6-phytyl-1,4-benzoquinone; HGA, homogentisic acid; HPP, p-hydroxyphenylpyruvate; HPPD, p-hydroxyphenylpyruvate dioxygenase; HPT, homogentisate phytyltransferase; HST, homogentisate solanesyl transferase; MPBQ, 2-methyl-6-phytyl-1,4-benzoquinone; MPBQ MT, 2-methyl-6-phytyl-1,4-benzoquinone methyltransferase; MSBQ, 2-methyl-6-solanesyl-1,4-benzoquinone; PC-8, plastochromanol-8; PQ-9, plastoquinone-9; PQH₂-9, plastoquinol-9; PPP, phytyl pyrophosphate; SPP, solanesyl pyrophosphate; TAT, tyrosine aminotransferase; TC, tocopherol cyclase; γ-TMT, γ-tocopherol methyltransferase; α-Toc, α-tocopherol; β-Toc, β-tocopherol; γ-Toc, γ-tocopherol; δ-Toc, δ-tocopherol; Tyr, tyrosine.

Figure 5

Scheme illustrating the functions of tocochromanols and PQ/PQH₂-9 in the regulation of different cellular processes. Orange boxes concern tocochromanol functions, blue boxes concern PQ/PQH₂ functions and yellow boxes concern processes in which both tocochromanols and PQ/PQH_2, are engaged.