Bound by Fate: The Role of Reactive Oxygen Species in Receptor-Like Kinase Signaling

Abstract

In plants, receptor-like kinases (RLKs) and extracellular reactive oxygen species (ROS) contribute to the communication between the environment and the interior of the cell. Apoplastic ROS production is a frequent result of RLK signaling in a multitude of cellular processes; thus, by their nature, these two signaling components are inherently linked. However, it is as yet unclear how ROS signaling downstream of receptor activation is executed. In this review, we provide a broad view of the intricate connections between RLKs and ROS signaling and describe the regulatory events that control and coordinate extracellular ROS production. We propose that concurrent initiation of ROS-dependent and -independent signaling linked to RLKs might be a critical element in establishing cellular responses. Furthermore, we discuss the possible ROS sensing mechanisms in the context of the biochemical environment in the apoplast. We suggest that RLK-dependent modulation of apoplastic and intracellular conditions facilitates ROS perception and signaling. Based on data from plant and animal models, we argue that specific RLKs could be components of the ROS sensing machinery or ROS sensors. The importance of the crosstalk between RLK and ROS signaling is discussed in the context of stomatal immunity. Finally, we highlight challenges in the understanding of these signaling processes and provide perspectives for future research.

Thioredoxin-Mediated ROS Homeostasis Explains Natural Variation in Plant Regeneration

“…Reactive oxygen species (ROS) are crucial signaling molecules that can alter their target proteins 86 activity by oxidative posttranslational modifications (Waszczak et al, 2015 are redox sensitive to ROS (Waszczak et al, 2015;Kimura et al, 2017). Altered levels of ROS lead 89 to change the activity of these target proteins and affect various developmental processes (Schippers 90 et al, 2016).…”

Redox Control of Aphid Resistance through Altered Cell Wall Composition and Nutritional Quality

“…Apoplastic hydrogen peroxide has been shown to exert a strong influence on phenolic metabolism in Norway spruce (Picea abies) cell cultures and to modify lignin formation and polymerization (Laitinen et al, 2017). The ROS burst that occurs upon the perception of a physical or chemical signal triggers redox signaling pathways that regulate plant growth as well as defense Foyer et al, 2017;Kimura et al, 2017;Tang et al, 2017). ROS signaling transmits information locally through plasma membrane receptor-like kinases that modify metabolism and gene expression and systemically through processes called systemic acquired resistance and systemic acquired acclimation on environmental stress Kimura et al, 2017;Tang et al, 2017).…”

“…The ROS burst that occurs upon the perception of a physical or chemical signal triggers redox signaling pathways that regulate plant growth as well as defense Foyer et al, 2017;Kimura et al, 2017;Tang et al, 2017). ROS signaling transmits information locally through plasma membrane receptor-like kinases that modify metabolism and gene expression and systemically through processes called systemic acquired resistance and systemic acquired acclimation on environmental stress Kimura et al, 2017;Tang et al, 2017). Since the apoplast has few antioxidants, ROS are likely to have a longer lifetime in this compartment than they would have inside the cell Parsons and Fry, 2012;Noctor and Foyer, 2016).…”

“…Since the apoplast has few antioxidants, ROS are likely to have a longer lifetime in this compartment than they would have inside the cell Parsons and Fry, 2012;Noctor and Foyer, 2016). While the roles of ROS in the apoplast have been studied extensively in relation to fungal and bacterial pathogens (Mittler, 2017;Kimura et al, 2017), relatively little is known about the roles of apoplastic ascorbate and ascorbate oxidase (AO) in this process. Moreover, relatively few studies have concerned the role of oxidation of the apoplast in the plant response to aphid infestation.…”

The Plant Cell Reviews Plant Immunity: Receptor-Like Kinases, ROS-RLK Crosstalk, Quantitative Resistance, and the Growth/Defense Trade-Off

“…Kimura et al (2017) review the role of ROS in RLK signaling and how the regulation of ROS-RLK crosstalk may be a critical component of communication between the cell interior and the environment. The authors discuss the importance of the apoplast as an arena for ROS production and the initiation of ROS-RLK crosstalk, the role of oxidative posttranslational modifications in ROS perception, and a potential role for RLK-dependent modulation of apoplastic and intracellular conditions in facilitating ROS perception and signaling.…”