Redox- and Reactive Oxygen Species-Dependent Signaling into and out of the Photosynthesizing Chloroplast

Abstract

Photosynthesis is a high-rate redox metabolic process that is subjected to rapid changes in input parameters, particularly light. Rapid transients of photon capture, electron fluxes, and redox potentials during photosynthesis cause reactive oxygen species (ROS) to be released, including singlet oxygen, superoxide anion radicals, and hydrogen peroxide. Thus, the photosynthesizing chloroplast functions as a conditional source of important redox and ROS information, which is exploited to tune processes both inside the chloroplast and, following retrograde release or processing, in the cytosol and nucleus. Analyses of mutants and comparative transcriptome profiling have led to the identification of these processes and associated players and have allowed the specificity and generality of response patterns to be defined. The release of ROS and oxidation products, envelope permeabilization (for larger molecules), and metabolic interference with mitochondria and peroxisomes produce an intricate ROS and redox signature, which controls acclimation processes. This photosynthesis-related ROS and redox information feeds into various pathways (e.g. the mitogen-activated protein kinase and OXI1 signaling pathways) and controls processes such as gene expression and translation.

Figure 1.

Sources of ROS in the photosynthesizing chloroplast. The interplay between photosynthetic redox metabolism (top) and ROS generation and associated signaling (bottom) is shown. Safe redox metabolism allows the overreduction of photosynthetic electron transport (PET) to be avoided by balancing metabolism and efficient redox regulation. Reducing power is exported via the malate valve, and export of dihydroxyacetone phosphate (DHAP) occurs via the triosephosphate phosphate translocator (TPT). Increasing production of ROS also feeds into redox regulation, enables redox and ROS signaling, and ultimately causes oxidative damage. FTR, Ferredoxin-dependent thioredoxin reductase; PQ, plastoquinone; PQH₂, plastohydroquinol.

Figure 2.

Connection between chloroplast redox/ROS generation and cytosolic signaling pathways. The focus is given to the MAPK and OXI1 pathways. The high-energy metabolite DHAP and H₂O₂ are exported and feed into the MAPK pathway. ¹O₂ activates the OXI1-dependent pathway. Both processes induce changes in gene expression for acclimation, defense, and eventual cell death. The MAPK pathway also feeds back into the chloroplast and affects PET. See text for details.

Figure 3.

Scenarios of chloroplast redox/ROS signaling of increasing strength. The scheme illustrates three scenarios of redox/ROS disturbances. A, Under conditions of environmentally induced, moderate metabolic changes, the redox milieu is altered but ROS are still kept in check. Retrograde signaling relies on redox and other mechanisms. B, Under moderate stress, which may include combinatorial stresses, ROS-dependent metabolites such as cyclocitral, the regulatory proteins EXECUTER1 (EX1) and EX2, and ROS themselves are released or activate retrograde signaling. The membrane-anchored transcription factor PTM is shed from the outer envelope. Gene expression and protein translation are altered to enable defense and acclimation. C, Extreme stress alters PET and metabolism, leading to the accumulation of high levels of ROS. β-Cyclocitral participates in extreme light stress signaling, which often is accompanied by the loss of integrity. The envelope is permeabilized and molecules are released to the cytosol. These changes may activate the cell death program.