Lycopene cyclase paralog CruP protects against reactive oxygen species in oxygenic photosynthetic organisms

Abstract

In photosynthetic organisms, carotenoids serve essential roles in photosynthesis and photoprotection. A previous report designated CruP as a secondary lycopene cyclase involved in carotenoid biosynthesis [Maresca J, et al. (2007) Proc Natl Acad Sci USA 104:11784-11789]. However, we found that cruP KO or cruP overexpression plants do not exhibit correspondingly reduced or increased production of cyclized carotenoids, which would be expected if CruP was a lycopene cyclase. Instead, we show that CruP aids in preventing accumulation of reactive oxygen species (ROS), thereby reducing accumulation of β-carotene-5,6-epoxide, a ROS-catalyzed autoxidation product, and inhibiting accumulation of anthocyanins, which are known chemical indicators of ROS. Plants with a nonfunctional cruP accumulate substantially higher levels of ROS and β-carotene-5,6-epoxide in green tissues. Plants overexpressing cruP show reduced levels of ROS, β-carotene-5,6-epoxide, and anthocyanins. The observed up-regulation of cruP transcripts under photoinhibitory and lipid peroxidation-inducing conditions, such as high light stress, cold stress, anoxia, and low levels of CO 2 , fits with a role for CruP in mitigating the effects of ROS. Phylogenetic distribution of CruP in prokaryotes showed that the gene is only present in cyanobacteria that live in habitats characterized by large variation in temperature and inorganic carbon availability. Therefore, CruP represents a unique target for developing resilient plants and algae needed to supply food and biofuels in the face of global climate change.photoinhibition | stress tolerance | chilling stress | oxygenic photosynthesis

Mechanistic Aspects of Carotenoid Biosynthesis

“…199b C. tepidum CruA has been shown to convert lycopene to γ-carotene in complementation studies 199b,222 and is required for lycopene cyclization in vivo. 199b However, the lycopene cyclization activity and physiological role of the CruP paralog from cyanobacteria and plants is not quite clear.…”

“…199b There is, however, evidence that plant CruP plays a role in the reduction of oxidative stress associated with cold or anoxic conditions. 222 …”

Insights into the Binding Mechanism of Ascorbic Acid and Violaxanthin with Violaxanthin De-Epoxidase (VDE) and Chlorophycean Violaxanthin De-Epoxidase (CVDE) Enzymes: Docking, Molecular Dynamics, and Free Energy Analysis

“…For CVDE, CruP and CruA, there presents a common ancestor. CruA is known to be involved in bacterial carotenoid biosynthesis as a lycopene cyclase, whereas CruP is a paralogue of CruA, widely found in oxygenic photosynthetic living organisms [Bradbury et al, 2012]. Zhirong Li et al hypothesized based on phylogenetic analysis that CVDE evolved by duplication of CruP from the ancestor of green algae and plants.…”

Transcriptome sequencing and annotation of the halophytic microalga Dunaliella salina

“…As the main source for natural β-carotene production, Dunaliella has been developed to accumulate β-carotene through environmental modification (Mogedas et al, 2009). CruP cannot affect the production of cyclized carotenoids under photo-inhibitory stress and protects against reactive oxygen species (ROS) in oxygenic photosynthetic organisms, providing a unique target to develop algae for food and cosmetics (Bradbury et al, 2012). There were four transcripts coding the CruP enzyme (Table S4).…”