Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding

Abstract

Background: Photosynthetic electron transport is performed by a chain of redox components that are electrochemically connected in series. Its efficiency depends on the balanced action of the photosystems and on the interaction with the dark reaction. Plants are sessile and cannot escape from environmental conditions such as fluctuating illumination, limitation of CO(2) fixation by low temperatures, salinity, or low nutrient or water availability, which disturb the homeostasis of the photosynthetic process. Photosynthetic organisms, therefore, have developed various molecular acclimation mechanisms that maintain or restore photosynthetic efficiency under adverse conditions and counteract abiotic stresses. Recent studies indicate that redox signals from photosynthetic electron transport and reactive oxygen species (ROS) or ROS-scavenging molecules play a central role in the regulation of acclimation and stress responses.

Scope: The underlying signalling network of photosynthetic redox control is largely unknown, but it is already apparent that gene regulation by redox signals is of major importance for plants. Signalling cascades controlling the expression of chloroplast and nuclear genes have been identified and dissection of the different pathways is advancing. Because of the direction of information flow, photosynthetic redox signals can be defined as a distinct class of retrograde signals in addition to signals from organellar gene expression or pigment biosynthesis. They represent a vital signal of mature chloroplasts that report their present functional state to the nucleus. Here we describe possible problems in the elucidation of redox signalling networks and discuss some aspects of plant cell biology that are important for developing suitable experimental approaches.

Conclusions: The photosynthetic function of chloroplasts represents an important sensor that integrates various abiotic changes in the environment into corresponding molecular signals, which, in turn, regulate cellular activities to counterbalance the environmental changes or stresses.

Fig. 1.

Principle approaches to identify the nature and origin of photosynthetic redox signals. The photosynthetic electron transport chain is depicted schematically. Site-specific inhibitors act at different sites of the chain. Various light regimes can be used to manipulate the electron flow through the chain [PSII-light and high-light conditions lead to preferential or excess excitation of PSII and reduction of plastoquinone (PQH₂); PSI-light leads to presumed excitation of PSI and oxidation of the PQ pool]. Mutations may interrupt or affect the electron flow and generate redox signals (reduction of components before the genetic defect and oxidation after it). Combinations of these approaches can help to define the nature and origin of a redox signal. Negative effects are indicated by bars.

Fig. 2.

Possible signal transduction pathways of photosynthetic redox signals. The three plant cell compartments are depicted schematically: chloroplast (light green), cytosol (light yellow) and nucleus (blue). Redox signals generated within the electron transport chain (dark green) or by generation of ROS initiate signalling pathways that activate or repress specific target genes in the nucleus (for details see text). Thin black arrows represent electron transport. ROS are generated as by-products of photosynthesis, e.g. by transfer of electrons from PSI or reduced ferredoxin (Fd) to oxygen-generating superoxide (Mehler reaction). This is detoxified by superoxide dismutase (SOD) to hydrogen peroxide (H₂O₂). Hydrogen peroxide can be reduced to water by ascorbate peroxidases using ascorbate as the electron donor, and requiring glutathione (GSH) to restore the electron donor. Unscavenged H₂O₂ is able to diffuse across the chloroplast envelope and is thought to start MAP kinase cascades in the cytosol. Electrons from PSI are also transferred to thioredoxin (Trx), which can affect LHCII phosphorylation (state transitions) and plastid gene expression and possibly also nuclear gene expression. Glutathione synthesis might be another pathway by which stress signals can directly leave the plastid. Another ROS, singlet oxygen (¹O₂), is generated at PSII. Because of its short half-life it requires additional signalling components, Executer 1 and 2 (EX1, EX2). The plastoquinone pool is the origin for at least two redox signalling pathways that are active under low or high light and which are targeted to plastid and nuclear gene expression machineries. Perception of the redox signal requires a proposed redox responsive factor (RRF). An important sensor for the PQ redox state represents the thylakoid kinase STN7 (possibly in conjunction with STN8). Present data point to the involvement of a phosphorylation cascade in PQ redox signal transduction. Red arrows, redox signals by components that directly leave the plastid; black arrows, redox signals that are mediated by unknown components. Proteins are indicated by orange.

Fig. 3.

Model of integration of various signals in a plant cell. A plant cell and its environment including neighbouring cells are shown. Various environmental influences that are detected by cytosolic receptors (circle marked ‘R’) or photosynthesis in different chloroplasts are represented by white arrows. Due to their different positions in the cell, the impact on the plastids may vary (plastid 1 and 2). The perceiving systems have different impacts (black arrows of different thickness) on the intracellular signalling network (represented as black dots connected by lines), which integrates these signals as well as signals from other cells, resulting in integrated signals (hatched arrows) that affect gene expression events. The ‘gene-copy-number-problem’ is indicated by the numerous ovals within the plastids, representing multiple copies of the plastome (see text for details).