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

<p>Abstract</p> <p>Background</p> <p>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...

Full description

Bibliographic Details
Main Authors: Fiore Alessia, Dall'Osto Luca, Cazzaniga Stefano, Diretto Gianfranco, Giuliano Giovanni, Bassi Roberto
Format: Article
Language:English
Published: BMC 2012-04-01
Series:BMC Plant Biology
Online Access:http://www.biomedcentral.com/1471-2229/12/50
_version_ 1818833265428004864
author Fiore Alessia
Dall'Osto Luca
Cazzaniga Stefano
Diretto Gianfranco
Giuliano Giovanni
Bassi Roberto
author_facet Fiore Alessia
Dall'Osto Luca
Cazzaniga Stefano
Diretto Gianfranco
Giuliano Giovanni
Bassi Roberto
author_sort Fiore Alessia
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>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 <it>chy1chy2lut5 </it>mutant is almost completely depleted in β-xanthophylls.</p> <p>Results</p> <p>Here we report on the quadruple <it>chy1chy2lut2lut5 </it>mutant, additionally carrying the <it>lut2 </it>mutation (affecting lycopene ε-cyclase). This genotype lacks lutein and yet it shows a compensatory increase in β-xanthophylls with respect to <it>chy1chy2lut5 </it>mutant. Mutant plants show an even stronger photosensitivity than <it>chy1chy2lut5</it>, 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 <it>chy1chy2lut2lut5 </it>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.</p> <p>Conclusions</p> <p>The physiological and biochemical phenotype of the <it>chy1chy2lut2lut5 </it>mutant shows that (i) LUT1/CYP97C1 protein reveals a major β-carotene hydroxylase activity <it>in vivo </it>when depleted in its preferred substrate α-carotene; (ii) xanthophylls are needed for normal level of Photosystem I and LHCII accumulation.</p>
first_indexed 2024-12-19T02:16:11Z
format Article
id doaj.art-670a345550b44749bf7b95224e8cda24
institution Directory Open Access Journal
issn 1471-2229
language English
last_indexed 2024-12-19T02:16:11Z
publishDate 2012-04-01
publisher BMC
record_format Article
series BMC Plant Biology
spelling doaj.art-670a345550b44749bf7b95224e8cda242022-12-21T20:40:24ZengBMCBMC Plant Biology1471-22292012-04-011215010.1186/1471-2229-12-50A 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 ratioFiore AlessiaDall'Osto LucaCazzaniga StefanoDiretto GianfrancoGiuliano GiovanniBassi Roberto<p>Abstract</p> <p>Background</p> <p>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 <it>chy1chy2lut5 </it>mutant is almost completely depleted in β-xanthophylls.</p> <p>Results</p> <p>Here we report on the quadruple <it>chy1chy2lut2lut5 </it>mutant, additionally carrying the <it>lut2 </it>mutation (affecting lycopene ε-cyclase). This genotype lacks lutein and yet it shows a compensatory increase in β-xanthophylls with respect to <it>chy1chy2lut5 </it>mutant. Mutant plants show an even stronger photosensitivity than <it>chy1chy2lut5</it>, 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 <it>chy1chy2lut2lut5 </it>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.</p> <p>Conclusions</p> <p>The physiological and biochemical phenotype of the <it>chy1chy2lut2lut5 </it>mutant shows that (i) LUT1/CYP97C1 protein reveals a major β-carotene hydroxylase activity <it>in vivo </it>when depleted in its preferred substrate α-carotene; (ii) xanthophylls are needed for normal level of Photosystem I and LHCII accumulation.</p>http://www.biomedcentral.com/1471-2229/12/50
spellingShingle Fiore Alessia
Dall'Osto Luca
Cazzaniga Stefano
Diretto Gianfranco
Giuliano Giovanni
Bassi Roberto
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
BMC Plant Biology
title 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
title_full 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
title_fullStr 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
title_full_unstemmed 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
title_short 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
title_sort 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
url http://www.biomedcentral.com/1471-2229/12/50
work_keys_str_mv AT fiorealessia aquadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio
AT dallostoluca aquadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio
AT cazzanigastefano aquadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio
AT direttogianfranco aquadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio
AT giulianogiovanni aquadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio
AT bassiroberto aquadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio
AT fiorealessia quadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio
AT dallostoluca quadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio
AT cazzanigastefano quadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio
AT direttogianfranco quadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio
AT giulianogiovanni quadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio
AT bassiroberto quadruplemutantofarabidopsisrevealsabcarotenehydroxylationactivityforlut1cyp97c1andaregulatoryroleofxanthophyllsondeterminationofthepsipsiiratio