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

Abstract

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 (O) and hydrogen peroxide (HO), initiate distinct signalling pathways when photosynthesis is perturbed. O, because of its potent reactivity means that it initiates but does not transduce signalling. In contrast, the lower reactivity of HO means that it can also be a mobile messenger in a spatially-defined signalling pathway. How plants translate a HO 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.

Retrograde signalling as an informant of circadian timing

“…Such environmental stressors are often sufficient to induce metabolic imbalances, causing oxidative stress in mitochondria and chloroplasts and leading to changes to the energy status of the cell (Chan et al ., ). Such disruption of metabolism additionally perturbs hormone biosynthesis and signalling, alters calcium signalling and induces the accumulation of metabolic intermediaries that can subsequently be transported from the mitochondria or chloroplasts to the nucleus (Chan et al ., ; Mullineaux et al ., ). With regard to circadian rhythmicity, high temperatures are sufficient to slow the circadian oscillator, and the circadian system is also delayed by osmotic stress (Gil et al ., ; Litthauer et al ., ).…”

“…Tansley insight New Phytologist intermediaries that can subsequently be transported from the mitochondria or chloroplasts to the nucleus (Chan et al, 2016b;Mullineaux et al, 2018). With regard to circadian rhythmicity, high temperatures are sufficient to slow the circadian oscillator, and the circadian system is also delayed by osmotic stress (Gil et al, 2017;Litthauer et al, 2018).…”

“…Both H 2 O 2 accumulation and the oxidation state of peroxiredoxins (a ubiquitous family of enzymes that serve as antioxidants and regulatory proteins) vary with the circadian rhythm, suggesting that ROS generation is influenced by the circadian system (Edgar et al, 2012;Lai et al, 2012). Although ROS are produced as a consequence of the normal functioning of photosynthesis and respiration, their accumulation increases during suboptimal conditions, when environmental stresses, such as high light, induce an imbalance between photosynthetic and respiratory pathways (Mullineaux et al, 2018). Under these stressful conditions, an increase in ROS production causes significant damage to the metabolic machinery, inducing photoinhibition and a generalized damage response (Mullineaux et al, 2018).…”

“…Although ROS are produced as a consequence of the normal functioning of photosynthesis and respiration, their accumulation increases during suboptimal conditions, when environmental stresses, such as high light, induce an imbalance between photosynthetic and respiratory pathways (Mullineaux et al, 2018). Under these stressful conditions, an increase in ROS production causes significant damage to the metabolic machinery, inducing photoinhibition and a generalized damage response (Mullineaux et al, 2018). ROS, such as H 2 O 2 , can be transferred directly to the nucleus from the chloroplast (Exposito-Rodriguez et al, 2017), where it is likely that the activity of redox-sensitive transcription factors is modulated.…”

“…However, it remains unknown how these factors contribute to circadian timing. By contrast, shorter lived ROS, such as 1 O 2 , are likely to initiate signalling pathways by oxidizing carotenoids or polyunsaturated fatty acids (Mullineaux et al, 2018). One such signalling trigger is b-cyclocitral, which is an oxidized derivative of b-carotene that accumulates as a consequence of 1 O 2 production and induces gene expression in response to high light (Ramel et al, 2012).…”