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Originally published In Press as doi:10.1074/jbc.M704729200 on October 3, 2007

J. Biol. Chem., Vol. 282, Issue 48, 35056-35068, November 30, 2007
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Different Roles of {alpha}- and β-Branch Xanthophylls in Photosystem Assembly and Photoprotection*Formula

Luca Dall'Osto{ddagger}1, Alessia Fiore§12, Stefano Cazzaniga{ddagger}, Giovanni Giuliano§, and Roberto Bassi{ddagger}3

From the {ddagger}Dipartimento Scientifico e Tecnologico, Università di Verona, Strada Le Grazie 15, 37134 Verona, Italy and the §Ente per le Nuove Tecnologie, l'Energia e l'Ambiente, Dipartimento Biotecnologie, Centro Ricerche Casaccia, C.P. 2400, Rome 00100, Italy

Xanthophylls (oxygenated carotenoids) are essential components of the plant photosynthetic apparatus, where they act in photosystem assembly, light harvesting, and photoprotection. Nevertheless, the specific function of individual xanthophyll species awaits complete elucidation. In this work, we analyze the photosynthetic phenotypes of two newly isolated Arabidopsis mutants in carotenoid biosynthesis containing exclusively {alpha}-branch (chy1chy2lut5) or β-branch (chy1chy2lut2) xanthophylls. Both mutants show complete lack of qE, the rapidly reversible component of nonphotochemical quenching, and high levels of photoinhibition and lipid peroxidation under photooxidative stress. Both mutants are much more photosensitive than npq1lut2, which contains high levels of viola- and neoxanthin and a higher stoichiometry of light-harvesting proteins with respect to photosystem II core complexes, suggesting that the content in light-harvesting complexes plays an important role in photoprotection. In addition, chy1chy2lut5, which has lutein as the only xanthophyll, shows unprecedented photosensitivity even in low light conditions, reduced electron transport rate, enhanced photobleaching of isolated LHCII complexes, and a selective loss of CP26 with respect to chy1chy2lut2, highlighting a specific role of β-branch xanthophylls in photoprotection and in qE mechanism. The stronger photosystem II photoinhibition of both mutants correlates with the higher rate of singlet oxygen production from thylakoids and isolated light-harvesting complexes, whereas carotenoid composition of photosystem II core complex was not influential. In depth analysis of the mutant phenotypes suggests that {alpha}-branch (lutein) and β-branch (zeaxanthin, violaxanthin, and neoxanthin) xanthophylls have distinct and complementary roles in antenna protein assembly and in the mechanisms of photoprotection.


Received for publication, June 8, 2007 , and in revised form, September 27, 2007.

* This work was supported by the Italian Ministry of Research Special Fund for Basic Research Grant FIRB RBLA0345SF_002 and Provincia Autonoma di Trento Grant SAMBAx2. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Formula The on-line version of this article (available at http://www.jbc.org) contains supplemental Table a1 and Figs. a1-a3.

1 Both authors contributed equally to this work.

2 Supervised by Prof. Laura Spano' (University of L'Aquila) for doctoral work.

3 To whom correspondence should be addressed: Dipt. Scientifico e Tecnologico, Università di Verona, Strada Le Grazie 15, 37134 Verona, Italy. Tel.: 39-045-8027916; Fax: 39-045-8027929/8027035; E-mail: bassi{at}sci.univr.it.


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