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.

Highlights

  • During their life plants face a vast set of environmental challenges: extreme changes in ambient illumination, temperature, and humidity, differences in soil salinity, attack by pathogens and herbivores, mechanical wounding, etc

  • The sensu stricto retrograde signaling can be regarded as a part of a larger network where apoplastic signals induce the generation of reactive oxygen species (ROS) in the chloroplast, which in turn leads to regulation of nuclear gene expression by several still uncharacterized, but at least partially chloroplast-derived, ROS-dependent retrograde signals

  • It is propelled by accumulation of ROS in the apoplast and by – still unidentified – symplastic signals, one of which might be ROS production in chloroplasts: results by Joo et al (2005) suggest that chloroplastic ROS is required for intercellular ROS signaling

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Summary

INTRODUCTION

During their life plants face a vast set of environmental challenges: extreme changes in ambient illumination, temperature, and humidity, differences in soil salinity, attack by pathogens and herbivores, mechanical wounding, etc To withstand all these challenges, plants have developed a repertoire of signaling pathways that is unparalleled in its complexity among living organisms. )r,adsuicpael r(oxOidHe)(Oar2e−u)n, ahvyodidroagbelen peroxide (H2O2), and by-products of aerobic metabolism (Imlay, 2003, 2008; Ogilby, 2010) which have traditionally been regarded mainly as damaging cytotoxic agents In line with this view, life has developed a plethora of ROS scavenging systems including the low-molecular weight compounds ascorbic acid and glutathione (Foyer and Noctor, 2011) as well as different classes of antioxidant enzymes (Apel and Hirt, 2004). The sensu stricto retrograde signaling (from chloroplast to nucleus) can be regarded as a part of a larger network where apoplastic signals induce the generation of ROS in the chloroplast, which in turn leads to regulation of nuclear gene expression by several still uncharacterized, but at least partially chloroplast-derived, ROS-dependent retrograde signals

Systemic signaling
ETC response AQP?
CHLOROPLASTIC ROS AS SIGNALS
THE FRUSTRATING COMPLEXITY OF ROS RESPONSES
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