Recent Progress in Understanding the Role of Reactive Oxygen Species in Plant Cell Signaling

Abstract

The significance and often centrality of reactive oxygen species (ROS)- and redox-related signaling are now established for most processes in plant development and acclimation. Each cell possesses a redox regulatory network whose state is adjusted by ROS and virtually controls all processes such as gene expression and translation, metabolism, and turnover. Recent years have witnessed significant advancements in understanding the cross talk between organelles in orchestrating the cellular redox state temporally and spatially. ROS function as oxidants of proteins altering their function and of lipids releasing signal-active compounds. This Focus Issue combines 18 publications that either summarize recent advances in the format of topical Focus Reviews or provide novel insight into ROS-associated processes. Our most detailed knowledge of ROS functions still comes from work with photosynthesizing leaves; therefore, the majority of reports in this special issue focus on leaf processes. Other contributions address ROS-dependent regulation of flower senescence (Rogers and Munné-Bosch, 2016), polar growth of pollen and root hairs (Mangano et al., 2016), and other root processes, including root architecture formation (Evans et al., 2016; Liu et al., 2016). In vivo ROS imaging in cells and tissues has contributed significantly to many of the recent advances in understanding ROS signaling. Historically, 3,3′-diaminobenzidine for H2O2 and nitroblue tetrazolium for O2 •− were used as the main workhorses for in situ imaging. Both dyes provided preliminary indications for ROS accumulation, but in most cases, more sensitive and less invasive probes should be used nowadays. Thus, the majority of studies presented in this Focus Issue employed fluorescein-based probes such as the 1O2 sensory fluorescein anthracene Singlet Oxygen Sensor Green (Koh et al., 2016) or the H2O2 probe OxyBurst Green (2′,7′-dichlorodihydrofluorescein diacetate; Evans et al., 2016; Zhang et al., 2016). These newer probes offer sensitive and more reliable readouts but are difficult to apply to some tissues like leaves, and their specificity is still disputed (Winterbourn, 2014). Genetically encoded sensors such as the ratiometric HyPer and HyPerRed were also used for ROS and redox detection in previous studies (Chiu et al., 2014; Ermakova et al., 2014). A major advantage for future plant ROS research would be to standardize protocols for in vivo cell imaging. Standardization would enable comparing ROS images and measurements between different studies and different labs. ROS are conditionally generated in various subcellular compartments and cellular environments (Fig. 1). The spatial and temporal pattern of ROS in combination with their reaction specificity is exploited for specific sensing and signaling in the cell. Chloroplasts (Dietz et al., 2016; Takagi et al., 2016), mitochondria (Huang et al., 2016), peroxisomes (Kerchev et al., 2016; Rodriguez-Serrano et al., 2016), and plasma membrane-associated NADPH oxidases (Respiratory burst oxidase homologs, RBOH; Gilroy et al., 2016) and the ROS-dependent dynamics of organellar shape are addressed in this Focus Issue. Some of the multiple regulatory roles of ROS in plants addressed in this Focus Issue. Subcellular sites of ROS generation, e.g. in the chloroplast or mitochondrion, determine processes such as gene expression, cellular damage, and cell death. Progress has been made in understanding intracellular ROS transfer; formation of protrusions such as stromules, peroxules, and matrixules; and the ROS network of cells. ROS play a profound role in intercellular and long-distance communication in plants. In addition to their roles in environmental acclimation, ROS are receiving increasing awareness for their function in developmental processes such as the regulation of root architecture, polar growth, and organ senescence. Abbreviations not defined in the text: AOX, alternative oxidase; GO, glycolate oxidase; PTOX, plastid terminal oxidase. Redox interactions between intracellular compartments are key to stress responses and developmental processes. Organelles such as chloroplasts, mitochondria, and peroxisomes are powerful generators of ROS and other redox signals through core processes such as photosynthesis, photorespiration, and respiration. Coordination of gene expression between the three genomes of the plant cell requires monitoring of chloroplast and mitochondrial status, to allow appropriate retrograde signaling to the nucleus (Kleine and Leister, 2016). In this issue, the latest developments in understanding ROS and redox signals originating in chloroplasts and mitochondria are discussed by Dietz et al. (2016) and Huang et al. (2016). An outstanding question is how such signals are transmitted between compartments. This question is discussed by Noctor and Foyer (2016) in light of recent advances such as the identification of chloroplast envelope ascorbate transporters (Miyaji et al., 2015) and