Carotenoid Biosynthesis and Plastid Development in Plants: The Role of Light

Abstract

Light is an important cue that stimulates both plastid development and biosynthesis of carotenoids in plants. During photomorphogenesis or de-etiolation, photoreceptors are activated and molecular factors for carotenoid and chlorophyll biosynthesis are induced thereof. In fruits, light is absorbed by chloroplasts in the early stages of ripening, which allows a gradual synthesis of carotenoids in the peel and pulp with the onset of chromoplasts' development. In roots, only a fraction of light reaches this tissue, which is not required for carotenoid synthesis, but it is essential for root development. When exposed to light, roots start greening due to chloroplast development. However, the colored taproot of carrot grown underground presents a high carotenoid accumulation together with chromoplast development, similar to citrus fruits during ripening. Interestingly, total carotenoid levels decrease in carrots roots when illuminated and develop chloroplasts, similar to normal roots exposed to light. The recent findings of the effect of light quality upon the induction of molecular factors involved in carotenoid synthesis in leaves, fruit, and roots are discussed, aiming to propose consensus mechanisms in order to contribute to the understanding of carotenoid synthesis regulation by light in plants.

Keywords: carotenoids; chloroplasts; chromoplasts; light signaling; photoreceptors.

Figure 1

Simplified carotenoid synthesis pathway. Methylerythritol phosphate (MEP) pathway leads to the production of geranylgeranyl pyrophosphate (GGPP), the main precursor of carotenoids and chlorophylls synthesis. We highlighted the main enzymes of the pathway and the most accumulated carotenoids in plant models discussed throughout the review, in (a) Star Ruby grapefruits (Citrus paradisi M.), Satsuma mandarin (Citrus unshiu M.) (b) tomato (Solanum lycopersicum L.) in mature green (MG) stage, (c) leaves, (d) tomato in ripening (RR) stage, (e,f) carrot (Daucus carota L.) taproot, (g) leaves, and (h) Star Ruby grapefruits (Citrus paradisi M.). Abbreviations of enzymes: phytoene synthase (PSY), phytoene desaturase (PDS), z-carotene desaturase (ZDS), z-isomerase (Z-ISO), carotenoid isomerase (CRTiso), lycopene β-cyclase (LCYB), lycopene ε-cyclase (LCYE), carotene β-hydroxylase (CHYB), carotene ε-hydroxylase (CHYE), violaxanthin de-epoxidase (VDE), zeaxanthin epoxidase (ZEP).

Figure 2

Regulation in carotenoid synthesis in photosynthetic organs under different light conditions. (a) Plants grown in dark develop etioplasts were the expression of PSY and the synthesis of carotenoids is repressed by phytochrome interacting factors (PIFs) transcription factors. (b) Plants grown in shade exhibit a reduced expression of PSY and carotenoid synthesis in chloroplasts that take place due to the activation of phytochrome A (PHYA). (c) In the presence of white (W) light, a high level of PSY expression and carotenoid synthesis is observed due to phytochrome B (PHYB) activation. See further details in the text.

Figure 3

Effect of light on carotenoid synthesis in different plant organs. (a) Tomato fruit in MG stage exhibits chloroplasts in low R/FR light. (b) Tomato fruit in RR stage presents chromoplasts in high R/FR light. (c) Citrus fruit in the ripening stage accumulates carotenoids in high R/FR light. (d) Grapefruits accumulate more carotenoids in the pericarp in low R/FR light in comparison with high R/FR light. (e) Navel orange (Citrus sinensis O.), Star Ruby grapefruit, and Miyagawa wase (Citrus unshiu M.) are examples in which, at the breaker (B) stage, carotenoids in chromoplasts are produced in the flesh, whereas in the pericarp, which is exposed to high R/FR, carotenoids are produced in chloroplasts. (f) In Arabidopsis (Arabidopsis thaliana L.) seedling, high R/FR light induces photomorphogenesis. (g) In carrots (Daucus carota L.), a high R/FR produces chloroplast development, whilst a low R/FR induces carotenoid accumulation on chromoplasts. Yellow upwards arrows indicate a high R/FR light ratio while downwards arrows indicate a low R/FR light ratio.