Redox-mediated signalling
An intrinsic feature of both PAMP and MAMP triggered responses, as well as physical and chemical perturbations to the plant plasma membrane, is the propagation of waves of ROS and cytoplasmic calcium ([Ca2+]cyt) accumulation from the cell perceiving the signal to all cells throughout the plant (Fig. 2B). Together with fluctuations in electric wave potentials, the ROS wave triggers long-distance systemic defense signaling cascades that induce IR throughout the plant. The ROS wave is an essential systemic signaling system in plants, that contributes to plant-to-plant communication (Szechyńska-Hebda et al., 2022) and plant-to-microorganism interactions (Y. Zhou et al., 2019). Moreover, this signaling system has now been reported in a wide range of organisms (in microorganisms, plants, and mammalian cells) and cell communities (Fichman, Rowland, Oliver, & Mittler, 2023). This universal cell-to-cell communication mechanism probably evolved as part of the stress- or quorum-sensing mechanisms, is a fundamental link between different organisms within a given environment or ecosystem. The “one health” concept is based on accumulating evidence that humans, animals, plants, microbiomes, and the environment are inseparably interlinked and impact each other constantly.
ROS signaling plays an important role in plant and animal interactions with microorganisms. The ROS wave is triggered by the oxidative burst, which occurs as a result of the activation of plasma membrane-bound NADPH oxidases (Respiratory Burst Oxidase Homolgues: Rboh) and cell wall peroxidases. These enzymes generate superoxide in the apoplastic space i.e. the external space around the cell walls, which stores water and nutrients. The oxidative burst is one of the earliest plant responses to infection by microbes such as endophytes (Sahu et al., 2022). The apoplast has a low antioxidant capacity but it is rich in antifreeze proteins and pathogen-related proteins (PR-proteins) such as proteinase inhibitors, defensins, thionins, and lipid transfer proteins that together represent 23–33% of the total apoplastic fluid proteins (Farvardin et al., 2020).
In the case of pathogens, the prolonged activation of Rboh and other ROS-producing enzymes results in the hypersensitive response (HR) that prevents the spread of the pathogen from the attacked cell to neighboring cells. Endophyte-triggered ROS generation does not lead to HR but in contrast, triggers systemic signaling leading to defense gene expression (Sahu et al., 2022) and wide-ranging enhanced protection against biotic and abiotic stresses (Godara & Ramakrishna, 2023). The oxidative burst facilitates the oxidation of secondary compounds in the apoplast/cell wall environment, such as the conversion of sesquiterpenoids to oxygenous sesquiterpenoids through chemical oxidation and differing degrees of oxidation. Endophytes also activate the expression of genes encoding key enzymes involved in secondary metabolism, such as those involved in sesquiterpenoid biosynthesis, creating an array of sesquiterpenoid hydrocarbon scaffolds (J.-Y. Zhou, Yuan, Li, Ning, & Dai, 2016). For example, the microbe-induced oxidative burst and oxygenous sesquiterpenoid accumulation occur synchronously upon colonization of the medicinal plantAtractylodeslancea  by Pseudomonas fluorescens  ALEB7B.  Sesquiterpenoids such as hinesol, β-eudesmol, atractylone, and caryophyllene oxide have medicinal properties protecting against rheumatic diseases, digestive disorders, night blindness, and influenza (J.-Y. Zhou et al., 2016).