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ROS-talk - How the Apoplast, the Chloroplast, and the Nucleus Get the Message Through

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ROS-talk - How the Apoplast, the Chloroplast, and the Nucleus Get the Message Through

Alexey Shapiguzov et al. Front Plant Sci.

Abstract

The production of reactive oxygen species (ROS) in different plant subcellular compartments is the hallmark of the response to many stress stimuli and developmental cues. The past two decades have seen a transition from regarding ROS as exclusively cytotoxic agents to being considered as reactive compounds which participate in elaborate signaling networks connecting various aspects of plant life. We have now arrived at a stage where it has become increasingly difficult to disregard the communication between different types and pools of ROS. Production of ROS in the extracellular space, the apoplast, can influence their generation in the chloroplast and both can regulate nuclear gene expression. In spite of existing information on these signaling events, we can still barely grasp the mechanisms of ROS signaling and communication between the organelles. In this review, we summarize evidence that supports the mutual influence of extracellular and chloroplastic ROS production on nuclear gene regulation and how this interaction might occur. We also reflect on how, and via which routes signals might reach the nucleus where they are ultimately integrated for transcriptional reprogramming. New ideas and approaches will be needed in the future to address the pressing questions of how ROS as signaling molecules can participate in the coordination of stress adaptation and development and how they are involved in the chatter of the organelles.

Keywords: Arabidopsis thaliana; ROS signaling; apoplast; chloroplasts; retrograde signaling.

Figures

FIGURE 1
FIGURE 1
Reactive oxygen species (ROS)-talk in plant cells. Biotic and abiotic stimuli lead to the generation of ROS in the apoplast which is subsequently communicated to the inside of the cell where the signal leads to an increase in chloroplastic ROS production. The chloroplast can further amplify the signal and transmit it to the nucleus via various cytosolic signaling networks. Apoplastic ROS signaling can also reach the nucleus through cytosolic pathways directly. Yellow arrows demonstrate intracellular transmission of apoplastic and chloroplastic ROS-induced signals where they connect neighboring cells (local signaling) or participate in long-distance (“systemic”) signaling throughout the plant (red arrows).
FIGURE 2
FIGURE 2
Reactive oxygen species (ROS) signaling networks connecting apoplast, chloroplast and nucleus. Apoplastic ROS are produced by extracellular peroxidases (hydrogen peroxide; H2O2) and plasma membrane-bound NADPH oxidases, Rboh. Superoxide (O2) is then converted to H2O2. H2O2 (and possibly O2) might enter the cell through plasma membrane channels (aquaporins, AQP) and/or react with extracellular (apoplastic protein, AP) or transmembrane sensor proteins (e.g., receptor-like kinases, RLKs) ultimately resulting in changes in gene expression through intracellular signaling pathways, involving, for example, MAPKs (mitogen-activated protein kinases). Extracellular ROS production is sensed via yet unknown mechanisms in the chloroplast where ROS generation by the electron transfer chain (ETC) subsequently increases. Singlet oxygen (1O2) and O2/H2O22O here should be changed to H2O2. are produced in different domains of ETC. Elevated ROS inside the chloroplast results in transcriptional reprogramming through identified (e.g., EXECUTER1/2, EX1/EX2, rupture of chloroplast envelope) and unknown components of the retrograde signaling but also through hormone signaling, e.g., increased production of the stress hormone salicylic acid (SA). Channel proteins (AQP) might also allow ROS leak from the chloroplast to the cytoplasm. Calcium (Ca2+) is involved in the regulation of ROS production in the apoplast and the chloroplast. In the latter case it acts through the sensory protein CALCIUM-SENSING RECEPTOR (CAS) but the mechanisms are still unclear.

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