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

Department of Plant and Microbial Biology, University of California, Berkeley, California 94720-3102, USA.
The Plant Cell (Impact Factor: 9.34). 07/2009; 21(6):1798-812. DOI: 10.1105/tpc.109.066571
Source: PubMed


Plants protect themselves from excess absorbed light energy through thermal dissipation, which is measured as nonphotochemical quenching of chlorophyll fluorescence (NPQ). The major component of NPQ, qE, is induced by high transthylakoid DeltapH in excess light and depends on the xanthophyll cycle, in which violaxanthin and antheraxanthin are deepoxidized to form zeaxanthin. To investigate the xanthophyll dependence of qE, we identified suppressor of zeaxanthin-less1 (szl1) as a suppressor of the Arabidopsis thaliana npq1 mutant, which lacks zeaxanthin. szl1 npq1 plants have a partially restored qE but lack zeaxanthin and have low levels of violaxanthin, antheraxanthin, and neoxanthin. However, they accumulate more lutein and alpha-carotene than the wild type. szl1 contains a point mutation in the lycopene beta-cyclase (LCYB) gene. Based on the pigment analysis, LCYB appears to be the major lycopene beta-cyclase and is not involved in neoxanthin synthesis. The Lhcb4 (CP29) and Lhcb5 (CP26) protein levels are reduced by 50% in szl1 npq1 relative to the wild type, whereas other Lhcb proteins are present at wild-type levels. Analysis of carotenoid radical cation formation and leaf absorbance changes strongly suggest that the higher amount of lutein substitutes for zeaxanthin in qE, implying a direct role in qE, as well as a mechanism that is weakly sensitive to carotenoid structural properties.

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    • "The other carotenoids (referred to as xanthophylls, as they contain oxygen in their structure) are always bound to antenna proteins (Fig. 1). Among them, Lut, the most common, is required for the correct folding of light-harvesting proteins (Formaggio et al., 2001), but also as a quencher of singlet oxygen and Chl triplets (Dall'Osto et al., 2006; Kalituho et al., 2007), and probably as a modulator of photoprotective thermal dissipation (Keasling & Niyogi, 2009; Li et al., 2009; Esteban et al., 2010). However, Neo is the only carotenoid that occurs regularly in chloroplasts in a cis-configuration and, as a result, is almost exclusively bound to the so-called N1 binding site of light-harvesting proteins of photosystem II (PSII) (Formaggio et al., 2001) (Fig. 1). "
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    ABSTRACT: Photosynthetic pigment composition has been a major study target in plant ecophysiology during the last three decades. Although more than 2000 papers have been published, a com- prehensive evaluation of the responses of photosynthetic pigment composition to environ- mental conditions is not yet available. � After an extensive survey, we compiled data from 525 papers including 809 species (sub- kingdom Viridiplantae) in which pigment composition was described. A meta-analysis was then conducted to assess the ranges of photosynthetic pigment content. � Calculated frequency distributions of pigments were compared with those expected from the theoretical pigment composition. Responses to environmental factors were also analysed. The results revealed that lutein and xanthophyll cycle pigments (VAZ) were highly responsive to the environment, emphasizing the high phenotypic plasticity of VAZ, whereas neoxanthin was very stable. � The present meta-analysis supports the existence of relatively narrow limits for pigment ratios and also supports the presence of a pool of free ‘unbound’ VAZ. Results from this study provide highly reliable ranges of photosynthetic pigment contents as a framework for future research on plant pigments.
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    • "In the NPQ model of Horton and co-workers (Horton et al., 2005) the pH is the main driving force of the LHCIIb aggregation, which itself is further enhanced by the presence of Zx. Additionally, it has been reported that lutein can substitute Zx as a quencher in the charge transfer quenching model (Avenson et al., 2008; Li et al., 2009). "
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    ABSTRACT: In the present study the non-photochemical quenching (NPQ) of four biofilm-forming and two planktonic green algae was investigated by fluorescence measurements, determinations of the light-driven proton gradient and determination of the violaxanthin cycle activity by pigment analysis. It was observed that, despite the common need for efficient photoprotection, the structural basis of NPQ was heterogeneous in the different species. Three species, namely Chlorella saccharophila, Chlorella vulgaris and Bracteacoccus minor, exhibited a zeaxanthin-dependent NPQ, while in the three other species, Tetracystis aeria, Pedinomonas minor and Chlamydomonas reinhardtii violaxanthin de-epoxidation was absent or unrelated to the establishment of NPQ. Acclimation of the algae to high light conditions induced an increase of the NPQ activity, suggesting that a significant part of the overall NPQ was rather inducible than constitutively present in the green algae. Comparing the differences in the NPQ mechanisms with the phylogenetic position of the six algal species led to the conclusion that the NPQ heterogeneity observed in the present study was not related to the phylogeny of the algae but to the environmental selection pressure. Finally, the difference in the NPQ mechanisms in the different species is discussed within the frame of the current NPQ models.
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    • "Although zeaxanthin is mainly responsible for the energydependent component of NPQ (qE), lutein contributes to the residual qE in Arabidopsis thaliana (Muller et al., 2001; Niyogi et al., 2001). Plants lacking zeaxanthin accumulate lutein instead, which partially restores NPQ (Li et al., 2009). The observed increase in lutein and b–carotene levels in the abc1k1/pgr6 mutant may therefore reflect an adaptive strategy to acclimate to HL intensity. "
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