Prenylipids in Plastids: Carotenoids, Tocopherols, and Quinones Explained

Prenyllipids occupy a significant place among the biochemical components of plant plastids, playing an important structural and functional role in organizing membranes and other formations. The prenyllipids of plastids are represented by two groups of organic substances.

Simple prenyllipids consist only of isoprenoid compounds (for example, carotenoids), whereas in mixed prenyllipids the lateral isoprenoid chain is linked to a non-terpenoid nucleus (prenylquinones, chlorophyll). The following prenyllipids have been found in isolated chromoplasts and in various subfractions of these organelles:

• carotenoids;
• α-tocopherol;
• plastoquinone-9;
• plastohydroquinone;
• α-tocoquinone;
• phylloquinone (vitamin K1).

The structures of the principal chromoplast prenyllipids are shown in Figure 1. Figure 1 — Final stages of α-tocopherol synthesis in the chromoplasts of annual pepper (Capsicum annuum).

During the transformation of chloroplasts into chromoplasts, significant changes occur in the quantitative content of prenyllipid compounds.

The content of plastoquinone-9 and α-tocopherol in the chromoplasts of annual pepper fruit was considerably higher than in the chloroplasts. This agrees with the data obtained by H. Lichtenthaler, which indicate an increase in α-tocopherol content during the ripening of this plant.

Phylloquinone (vitamin K₁), according to current understanding, plays an important role in photosynthesis and is located in the chloroplasts of green fruit. However, the plastids of red fruit do not contain this component in appreciable amounts. Figure 2 — Final stages of phylloquinone synthesis.

At the same time, phylloquinone was detected in the plastoglobuli of the formed chromoplasts in the flowers of scotch broom (Sarothamnus scoparius). The most substantial changes during the transformation of chloroplasts into chromoplasts, however, affect the pigments — especially chlorophyll, which disappears completely in mature chromoplasts. α-Tocopherol is currently regarded as a compound that prevents the oxidation of membrane lipids and therefore delays the ageing of cells.

This is especially important for chromoplasts, which are characterized by a high content of polyunsaturated lipids. It has been shown that during the conversion of chloroplasts into chromoplasts the content of α-tocopherol in the membrane fraction of chromoplasts increases more than fourfold. At the same time, α-tocopherol was absent from the stroma of the organelles and was found in highly purified plastoglobuli of scotch broom chromoplasts.

Studies on plant tissues established that α-tocopherol is formed from 2,3-dimethyl-phytylquinol, with tocopherol acting as an intermediate compound (Figure 1). When isolated chromoplasts were incubated in the presence of labelled S-adenosyl-[methyl-¹⁴C]-methionine and dimethylphytylquinone, α-tocopherol was formed, indicating the ability of the organelles under study to carry out the final stages of synthesis of this compound.

The activity of chromoplasts in synthesizing α-tocopherol (0.06 picomole per minute per 1 mg of protein) was considerably higher than the activity of spinach chloroplasts.

Chromoplasts are also a site of phylloquinone synthesis (Figure 2). It was shown that isolated plastids from green and ripe fruit of annual pepper are able to incorporate the label of S-adenosyl-[methyl-¹⁴C]-methionine. Experiments with phytyl pyrophosphate, α-naphthoquinone, dihydro-α-naphthoquinone, 1,4-dihydroxy-2-naphthoic acid, and demethylphylloquinone showed that these substances can be precursors in phylloquinone synthesis.

In addition, it was established that the enzymes participating in the synthesis of vitamin K₁ (1,4-dihydroxy-2-naphthoate prenyltransferase and S-adenosyl-methionine methyltransferase) are localized in the membranes of chromoplasts and chloroplasts. J.-P. Gaudillière found a higher activity of annual pepper chromoplasts in vitamin K₁ synthesis compared with chloroplasts, even though the chromoplasts did not contain appreciable amounts of this compound. To the above it should be added that chromoplasts also retain chlorophyll-synthetase activity, despite the fact that chlorophyll is absent in them.

It is known that phytyl pyrophosphate and the other terpenoid side chains of prenyllipids are formed from geranylgeranyl pyrophosphate (GGPP). GGPP has been shown to be synthesized in chromoplasts. The chloroplasts of photosynthesizing tissues synthesize phytyl pyrophosphate and the other side chains of mixed prenyllipids from GGPP. Chromoplasts apparently can also carry out these reactions; however, the site of synthesis of the non-terpenoid nuclei has not yet been established.