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Evolution of an atypical de-epoxidase for photoprotection in the green lineage

Abstract

Plants, algae and cyanobacteria need to regulate photosynthetic light harvesting in response to the constantly changing light environment. Rapid adjustments are required to maintain fitness because of a trade-off between efficient solar energy conversion and photoprotection. The xanthophyll cycle, in which the carotenoid pigment violaxanthin is reversibly converted into zeaxanthin, is ubiquitous among green algae and plants and is necessary for the regulation of light harvesting, protection from oxidative stress and adaptation to different light conditions1,2. Violaxanthin de-epoxidase (VDE) is the key enzyme responsible for zeaxanthin synthesis from violaxanthin under excess light. Here we show that the Chlorophycean VDE (CVDE) gene from the model green alga Chlamydomonas reinhardtii encodes an atypical VDE. This protein is not homologous to the VDE found in plants and is instead related to a lycopene cyclase from photosynthetic bacteria3. Unlike the plant-type VDE that is located in the thylakoid lumen, the Chlamydomonas CVDE protein is located on the stromal side of the thylakoid membrane. Phylogenetic analysis suggests that CVDE evolved from an ancient de-epoxidase that was present in the common ancestor of green algae and plants, providing evidence of unexpected diversity in photoprotection in the green lineage.

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Figure 1: Molecular analysis and complementation of npq1 mutation in Chlamydomonas.
Figure 2: Functional complementation of Arabidopsis vde1 mutant by expression of the Chlamydomonas CVDE protein.
Figure 3: Subcellular localization of CrCVDE proteins expressed in Chlamydomonas and Arabidopsis.

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Acknowledgements

We thank J. García-Cerdán and R. Calderon for helpful discussion of Chlamydomonas subcellular localization. This work was supported by the US Department of Energy, Office of Science, Basic Energy Sciences, Chemical Sciences, Geosciences and Biosciences Division under field work proposal 449B. K.K.N. is an investigator of the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through Grant GBMF3070).

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Z.L., G.P., R.M.D., Y.B., W.A., S.Y.Y. and L.L. performed research; Z.L., G.P., R.M.D. and K.K.N. designed research; Z.L., G.P. and K.K.N. analysed data and wrote the paper; all authors discussed the results and commented on the manuscript.

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Correspondence to Krishna K. Niyogi.

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The authors declare no competing financial interests.

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Li, Z., Peers, G., Dent, R. et al. Evolution of an atypical de-epoxidase for photoprotection in the green lineage. Nature Plants 2, 16140 (2016). https://doi.org/10.1038/nplants.2016.140

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