Photosynthesis-independent production of reactive oxygen species in the rice bundle sheath during high light is mediated by NADPH oxidase

Abstract

When exposed to high light, plants produce reactive oxygen species (ROS). In Arabidopsis thaliana, local stress such as excess heat or light initiates a systemic ROS wave in phloem and xylem cells dependent on NADPH oxidase/respiratory burst oxidase homolog (RBOH) proteins. In the case of excess light, although the initial local accumulation of ROS preferentially takes place in bundle-sheath strands, little is known about how this response takes place. Using rice and the ROS probes diaminobenzidine and 2′,7′-dichlorodihydrofluorescein diacetate, we found that, after exposure to high light, ROS were produced more rapidly in bundle-sheath strands than mesophyll cells. This response was not affected either by CO2 supply or photorespiration. Consistent with these findings, deep sequencing of messenger RNA (mRNA) isolated from mesophyll or bundle-sheath strands indicated balanced accumulation of transcripts encoding all major components of the photosynthetic apparatus. However, transcripts encoding several isoforms of the superoxide/H2O2-producing enzyme NADPH oxidase were more abundant in bundle-sheath strands than mesophyll cells. ROS production in bundle-sheath strands was decreased in mutant alleles of the bundle-sheath strand preferential isoform of OsRBOHA and increased when it was overexpressed. Despite the plethora of pathways able to generate ROS in response to excess light, NADPH oxidase–mediated accumulation of ROS in the rice bundle-sheath strand was detected in etiolated leaves lacking chlorophyll. We conclude that photosynthesis is not necessary for the local ROS response to high light but is in part mediated by NADPH oxidase activity.

Salicylic acid alleviates the water stress on photochemical apparatus and quality of Schinus terebinthifolia seedlings

“…Since these pigments are responsible for light interception and electron transfer excitation processes, their degradation decreased the photochemical activity of PSII (F v /F m ). The decreased PSII activity leads to increased excitation energy, resulting in excessive energy, ROS production, and lipid peroxidation (Santos et al, 2021;Zhao et al, 2021), thus inhibiting NADPH oxidation and electron transfer to the reaction centers (Xiong et al, 2021).…”

Plants’ Physio-Biochemical and Phyto-Hormonal Responses to Alleviate the Adverse Effects of Drought Stress: A Comprehensive Review

“…Droughttolerant genotypes have a better antioxidant capability, which results in less oxidative damage [78,91]. Wheat crop (Triticum aestivum L.) responses vary by tissue type, duration, the severity of stress, and developmental stage, demonstrating the intricacy of ROS generation and detoxifying pathways and the impact of ROS on antioxidant systems [137].…”

ROS production and signalling in chloroplasts: cornerstones and evolving concepts

“…Little is known about how chloroplast ROS production participates in such long‐distance signalling pathways but a growing body of evidence supports the hypothesis that they play an important role, particularly as environmental sensors (Yi et al., 2015; Guo et al., 2016; Wang et al., 2018a; Wang et al., 2018b; Zhou et al., 2019). Similarly, photosynthesis is not necessary for local ROS responses to high light conditions, which are, at least in part, mediated by RBOH activity (Xiong et al., 2021), and CO 2 signalling pathways can modify immunity in ways that are largely independent of photosynthesis (Hu et al., 2021). The signalling network that incorporates ROS to transmit local and long‐distance signals is highly complex and requires much more intensive research in years to come, in order to target these processes for sustainable crop production under climate change.…”