Research ArticlePlant biology

Plasmodesmata-localized proteins and ROS orchestrate light-induced rapid systemic signaling in Arabidopsis

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Science Signaling  23 Feb 2021:
Vol. 14, Issue 671, eabf0322
DOI: 10.1126/scisignal.abf0322

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Orchestrating systemic ROS signaling in plants

Localized abiotic stresses induce systemic responses that protect plants from subsequent occurrences of the stress. Fichman et al. found that systemic acclimation to light stress in Arabidopsis thaliana required the enzyme RBOHD locally at sites of high light stress to generate reactive oxygen species (ROS) as well as throughout the plant to propagate a wave of systemic ROS signaling. Light stress–induced systemic ROS signaling depended on proteins localized to plasmodesmata, which are structures that connect the cytoplasm of adjacent plant cells, and was associated with increases in plasmodesmata pore size. Aquaporins and various Ca2+-permeable ion channels facilitated systemic ROS signaling by amplifying the ROS signal in each cell along the path of the ROS wave. Together, these findings demonstrate the importance of cell-to-cell transport mechanisms for generating, amplifying, and propagating systemic ROS signaling in response to high light stress in Arabidopsis.

Abstract

Systemic signaling and systemic acquired acclimation (SAA) are key to the survival of plants during episodes of abiotic stress. These processes depend on a continuous chain of cell-to-cell signaling events that extends from the initial tissue that senses the stress (the local tissue) to the entire plant (systemic tissues). Reactive oxygen species (ROS) and Ca2+ are key signaling molecules thought to be involved in this cell-to-cell mechanism. Here, we report that the systemic response of Arabidopsis thaliana to a local treatment of high light stress, which resulted in local ROS accumulation, required ROS generated by respiratory burst oxidase homolog D (RBOHD). ROS increased cell-to-cell transport and plasmodesmata (PD) pore size in a manner dependent on PD-localized protein 1 (PDLP1) and PDLP5, and this process was required for the propagation of the systemic ROS signals and SAA. Furthermore, aquaporins and several Ca2+-permeable channels in the glutamate receptor–like (GLR), mechanosensitive small conductance–like (MSL), and cyclic nucleotide–gated (CNGC) families were involved in this systemic signaling process. However, we determined that these channels were required primarily to amplify the systemic signal in each cell along the path of the systemic ROS wave, as well as to establish local and systemic acclimation. Thus, PD and RBOHD-generated ROS orchestrate light stress–induced rapid cell-to-cell spread of systemic signals in Arabidopsis.

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