Plasmodesmata-localized proteins and reactive oxygen species orchestrate light-induced rapid systemic signaling 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 (local tissue) to the entire plant (systemic tissues). Among the different systemic signaling molecules and processes thought to be involved in this cell-to-cell signaling mechanism are reactive oxygen species (ROS), calcium, electric and hydraulic signals. How these different signals and processes are interlinked, and how they transmit the systemic signal all the way from the local tissue to the entire plant, remain however largely unknown. Here, studying the systemic response of Arabidopsis thaliana to a local treatment of excess light stress, we report that respiratory burst oxidase homolog D (RBOHD)-generated ROS enhance cell-to-cell transport and plasmodesmata (PD) pore size in a process that depends on the function of PD-localized proteins (PDLPs) 1 and 5, promoting the cell-to-cell transport of systemic signals during responses to light stress. We further identify aquaporins, and several different calcium-permeable channels, belonging to the glutamate receptor-like, mechanosensitive small conductance-like, and cyclic nucleotide-gated families, as involved in this process, but determine that their function is primarily required for the maintenance of the signal in each cell along the path of the systemic signal, as well as for the establishment of acclimation at the local and systemic tissues. PD and RBOHD-generated ROS orchestrate therefore light stress-induced rapid cell-to-cell spread of systemic signals in Arabidopsis. One-sentence summaryRespiratory burst oxidase homolog D-generated reactive oxygen species enhance cell-to-cell transport and plasmodesmata (PD) pore size in a process that depends on the function of the PD-localized proteins (PDLPs) 1 and 5, promoting the cell-to-cell transport of rapid systemic signals during the response of Arabidopsis to excess light stress.