Lutein Accumulation in the Absence of Zeaxanthin Restores Nonphotochemical Quenching in the Arabidopsis thaliana npq1 Mutant

Zhirong Li ¹, Tae Kyu Ahn ², Thomas J. Avenson ³, Matteo Ballottari ⁴, Jeffrey A. Cruz ⁵, David M. Kramer ⁵, Roberto Bassi ⁴, Graham R. Fleming ², Jay D. Keasling ⁶, and Krishna K. Niyogi ¹^*

¹ Department of Plant and Microbial Biology, University of California, Berkeley, California 94720-3102; Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720
² Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720; Department of Chemistry, University of California, Berkeley, California 94720-1460
³ Department of Plant and Microbial Biology, University of California, Berkeley, California 94720-3102; Department of Chemistry, University of California, Berkeley, California 94720-1460
⁴ Dipartimento Scientifico e Tecnologico, Università di Verona, I-37134 Verona, Italy
⁵ Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164-6340
⁶ Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720; Department of Chemical Engineering, University of California, Berkeley, California 94720

^* To whom correspondence should be addressed. E-mail: niyogi{at}nature.berkeley.edu.

Plants protect themselves from excess absorbed light energythrough thermal dissipation, which is measured as nonphotochemicalquenching of chlorophyll fluorescence (NPQ). The major componentof NPQ, qE, is induced by high transthylakoid ${Delta}$ pH in excess lightand depends on the xanthophyll cycle, in which violaxanthinand antheraxanthin are deepoxidized to form zeaxanthin. To investigatethe xanthophyll dependence of qE, we identified suppressor ofzeaxanthin-less1 (szl1) as a suppressor of the Arabidopsis thaliananpq1 mutant, which lacks zeaxanthin. szl1 npq1 plants have apartially restored qE but lack zeaxanthin and have low levelsof violaxanthin, antheraxanthin, and neoxanthin. However, theyaccumulate more lutein and ${alpha}$ -carotene than the wild type. szl1contains a point mutation in the lycopene ${beta}$ -cyclase (LCYB) gene.Based on the pigment analysis, LCYB appears to be the majorlycopene ${beta}$ -cyclase and is not involved in neoxanthin synthesis.The Lhcb4 (CP29) and Lhcb5 (CP26) protein levels are reducedby 50% in szl1 npq1 relative to the wild type, whereas otherLhcb proteins are present at wild-type levels. Analysis of carotenoidradical cation formation and leaf absorbance changes stronglysuggest that the higher amount of lutein substitutes for zeaxanthinin qE, implying a direct role in qE, as well as a mechanismthat is weakly sensitive to carotenoid structural properties.

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