Abstract

BackgroundXanthophylls are oxygenated carotenoids playing an essential role as structural components of the photosynthetic apparatus. Xanthophylls contribute to the assembly and stability of light-harvesting complex, to light absorbance and to photoprotection. The first step in xanthophyll biosynthesis from α- and β-carotene is the hydroxylation of ε- and β-rings, performed by both non-heme iron oxygenases (CHY1, CHY2) and P450 cytochromes (LUT1/CYP97C1, LUT5/CYP97A3). The Arabidopsis triple chy1chy2lut5 mutant is almost completely depleted in β-xanthophylls.ResultsHere we report on the quadruple chy1chy2lut2lut5 mutant, additionally carrying the lut2 mutation (affecting lycopene ε-cyclase). This genotype lacks lutein and yet it shows a compensatory increase in β-xanthophylls with respect to chy1chy2lut5 mutant. Mutant plants show an even stronger photosensitivity than chy1chy2lut5, a complete lack of qE, the rapidly reversible component of non-photochemical quenching, and a peculiar organization of the pigment binding complexes into thylakoids. Biochemical analysis reveals that the chy1chy2lut2lut5 mutant is depleted in Lhcb subunits and is specifically affected in Photosystem I function, showing a deficiency in PSI-LHCI supercomplexes. Moreover, by analyzing a series of single, double, triple and quadruple Arabidopsis mutants in xanthophyll biosynthesis, we show a hitherto undescribed correlation between xanthophyll levels and the PSI-PSII ratio. The decrease in the xanthophyll/carotenoid ratio causes a proportional decrease in the LHCII and PSI core levels with respect to PSII.ConclusionsThe physiological and biochemical phenotype of the chy1chy2lut2lut5 mutant shows that (i) LUT1/CYP97C1 protein reveals a major β-carotene hydroxylase activity in vivo when depleted in its preferred substrate α-carotene; (ii) xanthophylls are needed for normal level of Photosystem I and LHCII accumulation.

Highlights

  • Xanthophylls are oxygenated carotenoids playing an essential role as structural components of the photosynthetic apparatus

  • In order to further detail the effects of altered xanthophyll composition on the organization of photosynthetic complexes and gain understanding on the regulatory events controlling xanthophyll biosynthesis in Arabidopsis, we have introduced the lut2 mutation in the semi-lethal chy1chy2lut5 background

  • One of the most noticeable results of recent work on the plant carotenoid biosynthesis pathway is the high level of redundancy in carotene hydroxylation, which is found to be catalyzed by 4 different enzymes

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Summary

Introduction

Xanthophylls are oxygenated carotenoids playing an essential role as structural components of the photosynthetic apparatus. The first step in xanthophyll biosynthesis from a- and b-carotene is the hydroxylation of ε- and b-rings, performed by both non-heme iron oxygenases (CHY1, CHY2) and P450 cytochromes (LUT1/CYP97C1, LUT5/CYP97A3). Carotenoids are a group of C40 pigments that contain a conjugated double-bond system, leading to strong absorption of visible light and antioxidant properties They are widely distributed among taxa, ranging from cyanobacteria and fungi to red and green algae and land plants [1]. It has been suggested that a third chloroplast-targeted member of the CYP97 family, CYP97B3 might have a role in carotenoid biosynthesis [14] This hypothesis is in contrast with the complete lack of xanthophylls in the quadruple chy1chy2lut1lut mutant [14], suggesting that CHY1, CHY2, LUT1/ CYP97C1 and LUT5/CYP97A3 are the complete complement of carotene hydroxylases in A. thaliana

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