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.
Highlights
When exposed to high light, plants produce reactive oxygen species (ROS)
Processes that dissipate energy in excess of that used by the photosynthetic electron-transport chain are collectively known as nonphotochemical quenching (NPQ) mechanisms, and their induction is thought to reduce damage to the photosynthetic apparatus caused by synthesis of ROS [13, 15]
Representative images of Fv′/Fm′ over this time course indicated that responses of the photosynthetic apparatus to high light were relatively homogenous across the leaf (Fig. 1D)
Summary
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 Arabidopsis, ROS have been implicated in rapid systemic signaling responses initiated after various abiotic and biotic stresses including high light, heat, wounding, and pathogen attack [21] Such ROSmediated systemic signaling from a locally perturbed leaf can lead to stomatal aperture being altered in distant leaves, is associated with the hormones abscisic and jasmonic acid, and is dependent on the plasma membrane–localized NADPH oxidase (AtRBOHD and AtRBOHF) in cells of the phloem and xylem [22,23,24,25,26]. The ability of plants to initiate systemic responses to local biotic and abiotic stress is well known One such example takes place after exposure to high-light episodes and involves an initial, local accumulation of reactive oxygen species (ROS) in the region exposed to excessive light. J.K. is a guest editor invited by the Editorial Board
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