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).