Rapid Leaf-to-leaf communication of high light stress in Arabidopsis

Abstract

Two models have recently been proposed to explain systemic abiotic stress signaling in Arabidopsis: the idea of a cell-to-cell autonomous system within an individual leaf, as well as an algorithmic model of intercellular signaling functioning as a whole-plant stress signaling network. Both models assume a universal stress signaling mechanism that acts via plasma membrane-bound NADPH-oxidases to induce apoplastic H2O2 in order to signal to neighbouring cells. These models are problematic, however, as they do not address the idea of stress specificity which is currently believed to be perceived by a plant based on the induction of compartment-specific ROS induced by individual types of stress. They also do not address how, and in what form, a signal can travel from a stressed leaf via the vascular to another leaf within the rosette. Additional problems are that even in studies that focus on a specific stress such as HL, results cannot be consolidated due to experimental differences in light intensity, duration, and tissue sampling. This study focuses on rapid systemic HL signaling, known as Systemic Acquired Acclimation (SAA). The major strategy in studying this signal was to observe the behaviour of the signal from two different points in the pathway: (1) investigation into the initiation of SAA through perception of HL as well as identification of chloroplast to nucleus retrograde signaling pathways, and (2) investigation of what is required for the long distance relay of the signal from leaf-to-leaf. These aims were achieved through spatial and temporal investigation of the immediate HL stress events in local and distal tissue and investigation of compartment-specific ROS production and signaling. Results revealed leaf-age dependant differences in oxidative stress tolerance across the rosette, justifying consistent leaf sampling, and that SAA confers uniform HL tolerance across the rosette for up to 12 h. There was also a strong indication that both H2O2 and 1O2 production in the chloroplast are required for initiation of SAA, and that extracellular H2O2 is necessary for distal induction of SAA responses, as this was blocked in the rbohD/F NADPH-oxidase mutant. While the presence of EX1/2 1O2-specific retrograde signaling appeared to be required for nuclear induction of SAA genes, both antagonistic and synergistic effects of chloroplast-generated ROS were also apparent. This indicates the existence of a highly complex ROS regulatory system within the chloroplast that does not strictly follow the general view that 1O2 promotes cell death, while H2O2 is required for acclimation. This study further improves our understanding of how environmentally-sensed signals can move rapidly through a plant undergoing localised HL stress in order to induce immediate systemic acclimation. Speculative assessment of these new findings alongside other recent publications subsequently reveals further possibilities of investigation into SAA with the hypothesis that rapid volatile signals induce specific distal stress responses, followed by slower more general stress vascular signals through the phloem. Show more