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 tradeoff 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 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.

Regulation of Oxygenic Photosynthesis during Trophic Transitions in the Green Alga Chromochloris zofingiensis

“…Beta-carotene hydroxylase (CHYB1) and beta-ketolase (BKT)1, which are critical for the production of astaxanthin in C. zofingiensis (Li et al, 2008;Roth et al, 2017), were upregulated in Glc-treated cells, consistent with the increase in ketocarotenoids (Figures 1B and 2F; Supplemental Figure 1D). Moreover, expression of the gene encoding the chlorophycean violaxanthin de-epoxidase (CVDE1), which converts violaxanthin to zeaxanthin (Li et al, 2016), was upregulated, while zeaxanthin epoxidase (ZEP1), the gene responsible for the reverse reaction, was downregulated. These expression changes correlated with an increase in the proportion of zeaxanthin to violaxanthin ( Figure 2F; Supplemental Figure 1D).…”

Changing Form and Function through Carotenoids and Synthetic Biology

“…For example, excess light at the reaction center leads to nonenzymatic formation of b-carotene epoxides and consequential harmful reactive oxygen species. The repair of b-carotene epoxide has been postulated to be controlled by CruP, an enzyme that likely evolved from a carotenoid biosynthetic enzyme, lycopene cyclase (Bradbury et al, 2012;Li et al, 2016). Overexpression of maize CruP in Arabidopsis reduced the formation of b-carotene epoxides and reactive oxygen species, and produced cold-tolerant and anoxia-tolerant plants (Bradbury et al, 2012).…”

Transcriptomic responses associated with carbon and energy flows under high salinity stress suggest the overflow of acetyl-CoA from glycolysis and NADPH co-factor induces high lipid accumulation and halotolerance inChlorellasp. HS2

“…Zeaxanthin, however, is known to be associated with several types of photoprotection events of the PSII reaction center (Dall’Osto et al, 2012); therefore, VDE upregulation has been acknowledged as one of common algal responses under high oxidative stress (Z. Li et al, 2016). Given that the relative amount of carotenoid pigments in HS2 was increased under high salinity stress (Yun et al, 2019), enhancing the content of zeaxanthin by either upregulating VDE or downregulating ZEP may further enhance the halotolerance of HS2.…”