How Extracellular Reactive Oxygen Species Reach Their Intracellular Targets in Plants

Reactive oxygen species (ROS) serve as secondary messengers that regulate various developmental and signal transduction processes, with ROS primarily generated by NADPH OXIDASEs (referred to as RESPIRATORY BURST OXIDASE HOMOLOGs [RBOHs] in plants). However, the types and locations of ROS produced by RBOHs are different from those expected to mediate intracellular signaling. RBOHs produce O2 center dot- rather than H2O2 which is relatively long-lived and able to diffuse through membranes, and this production occurs outside the cell instead of in the cytoplasm, where signaling cascades occur. A widely accepted model explaining this discrepancy proposes that RBOH-produced extracellular O2 center dot- is converted to H2O2 by superoxide dismutase and then imported by aquaporins to reach its cytoplasmic targets. However, this model does not explain how the specificity of ROS targeting is ensured while minimizing unnecessary damage during the bulk translocation of extracellular ROS (eROS). An increasing number of studies have provided clues about eROS action mechanisms, revealing various mechanisms for eROS perception in the apoplast, crosstalk between eROS and reactive nitrogen species, and the contribution of intracellular organelles to cytoplasmic ROS bursts. In this review, we summarize these recent advances, highlight the mechanisms underlying eROS action, and provide an overview of the routes by which eROS-induced changes reach the intracellular space.

Automated summary

Reactive oxygen species (ROS), primarily generated by NADPH oxidases (RBOHs), serve as secondary messengers in developmental and signal transduction processes. However, the types and locations of ROS produced by RBOHs differ from those involved in intracellular signaling. Recent studies have revealed mechanisms underlying extracellular ROS (eROS) action, including perception in the apoplast, crosstalk with reactive nitrogen species, and contributions of intracellular organelles. This review summarizes these advances and provides an overview of the routes by which eROS-induced changes reach the intracellular space.