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BMC Plant Biol. 2012; 12: 50.
Published online Apr 18, 2012. doi:  10.1186/1471-2229-12-50
PMCID: PMC3349566
A quadruple mutant of Arabidopsis reveals a β-carotene hydroxylation activity for LUT1/CYP97C1 and a regulatory role of xanthophylls on determination of the PSI/PSII ratio
Alessia Fiore,#1 Luca Dall'Osto,#2 Stefano Cazzaniga,2 Gianfranco Diretto,1 Giovanni Giuliano,1 and Roberto Bassicorresponding author2,3,4
1Italian National Agency for New Technologies, Energy and Sustainable Development (ENEA), Casaccia Research Center, Via Anguillarese 301, 00123 Rome, Italy
2Dipartimento di Biotecnologie, Università di Verona, Strada Le Grazie 15, 37134 Verona, Italy
3ICG-3: Phytosphäre Forschungszentrum Jülich, 52425 Jülich, Germany
4Dipartimento di Biotecnologie, Università di Verona, Strada Le Grazie 15, 37134 Verona, Italy
corresponding authorCorresponding author.
#Contributed equally.
Alessia Fiore: alessia.fiore/at/enea.it; Luca Dall'Osto: luca.dallosto/at/univr.it; Stefano Cazzaniga: stefano.cazzaniga/at/univr.it; Gianfranco Diretto: gianfranco.diretto/at/enea.it; Giovanni Giuliano: giovanni.giuliano/at/enea.it; Roberto Bassi: roberto.bassi/at/univr.it
Received November 27, 2011; Accepted April 18, 2012.
Abstract
Background
Xanthophylls 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.
Results
Here 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.
Conclusions
The 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.
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