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

Proc Natl Acad Sci U S A. 2012 Jul 3;109(27):E1888-97. doi: 10.1073/pnas.1206002109. Epub 2012 Jun 15.

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.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Arabidopsis / enzymology
  • Arabidopsis / genetics
  • Carotenoids / metabolism
  • Chlorobium / enzymology
  • Chlorobium / genetics
  • Chloroplasts / enzymology*
  • Chloroplasts / genetics
  • Cold Temperature
  • Cyanobacteria / enzymology
  • Cyanobacteria / genetics
  • Escherichia coli / enzymology
  • Intramolecular Lyases / genetics*
  • Intramolecular Lyases / metabolism
  • Photosynthesis / physiology*
  • Phylogeny
  • Polycyclic Sesquiterpenes
  • Reactive Oxygen Species / metabolism*
  • Sesquiterpenes / metabolism
  • Stress, Physiological / physiology
  • Synechococcus / enzymology*
  • Synechococcus / genetics
  • Zea mays / enzymology
  • Zea mays / genetics

Substances

  • Polycyclic Sesquiterpenes
  • Reactive Oxygen Species
  • Sesquiterpenes
  • Carotenoids
  • caryophyllene
  • Intramolecular Lyases
  • lycopene cyclase-isomerase