ROS-dependent signalling pathways in plants and algae exposed to high light: Comparisons with other eukaryotes

• Published in: Free radical biology & medicine 2018-07, Vol.122, p.52-64
• Main Authors: Mullineaux, Philip M., Exposito-Rodriguez, Marino, Laissue, Pierre Philippe, Smirnoff, Nicholas
• Format: Article
• Language: English
• Subjects: Animal cells; Chloroplast-to-nucleus communication; High light; Hydrogen peroxide; Microdomains; Mitochondria; Peroxisomes; Photosynthesis; Plant cells; Redox relay; Retrograde signalling; ROS-mediated signalling; Singlet oxygen; Thiol peroxidases; Yeast
• ISSN: 0891-5849; 1873-4596
• DOI: 10.1016/j.freeradbiomed.2018.01.033

Like all aerobic organisms, plants and algae co-opt reactive oxygen species (ROS) as signalling molecules to drive cellular responses to changes in their environment. In this respect, there is considerable commonality between all eukaryotes imposed by the constraints of ROS chemistry, similar metabolism in many subcellular compartments, the requirement for a high degree of signal specificity and the deployment of thiol peroxidases as transducers of oxidising equivalents to regulatory proteins. Nevertheless, plants and algae carry out specialised signalling arising from oxygenic photosynthesis in chloroplasts and photoautotropism, which often induce an imbalance between absorption of light energy and the capacity to use it productively. A key means of responding to this imbalance is through communication of chloroplasts with the nucleus to adjust cellular metabolism. Two ROS, singlet oxygen (1O2) and hydrogen peroxide (H2O2), initiate distinct signalling pathways when photosynthesis is perturbed. 1O2, because of its potent reactivity means that it initiates but does not transduce signalling. In contrast, the lower reactivity of H2O2 means that it can also be a mobile messenger in a spatially-defined signalling pathway. How plants translate a H2O2 message to bring about changes in gene expression is unknown and therefore, we draw on information from other eukaryotes to propose a working hypothesis. The role of these ROS generated in other subcellular compartments of plant cells in response to HL is critically considered alongside other eukaryotes. Finally, the responses of animal cells to oxidative stress upon high irradiance exposure is considered for new comparisons between plant and animal cells. Summary of the main features of ROS-initiated chloroplast-to-nucleus retrograde signalling. PAP 3'-phosphoadenosine 5'-phosphate; JA jasmonic acid; EX1/2 EXECUTER 1 and EXECUTER 2. [Display omitted] •Common features of ROS deployed as signalling molecules in eukaryotes.•Chloroplast-nucleus retrograde signalling route initiated by singlet oxygen.•Spatial components of chloroplast-to-nucleus retrograde communication.•H2O2 signal propagation from chloroplast to nucleus or cytosol.•ROS from other subcellular compartments in high light-exposed plant cells.