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Diffusion and bulk flow of amino acids mediate calcium waves in plants

ABSTRACT: In plants, a variety of stimuli trigger long-range calcium signals that travel rapidly along the vasculature to distal tissues via poorly understood mechanisms. Here, we use quantitative imaging and analysis to demonstrate that travelling calcium waves are mediated by diffusion and bulk flow of amino acid chemical messengers. Wounding triggers release of amino acids that diffuse locally through the apoplast, activating the calcium permeable channel GLUTAMATE-LIKE RECEPTOR3.3 as they pass. Over long distances through the vasculature, the wound-triggered dynamics of a fluorescent tracer show that calcium waves are likely driven by bulk flow of a channel activating chemical. We observed that multiple stimuli trigger calcium waves with similar dynamics, but calcium waves alone cannot initiate all systemic defence responses, suggesting that mobile chemical messengers are a core component of complex systemic signalling in plants. We present time-lapse images of whole leaves or plants, collected from plants (wild-type and a range of mutants) expressing calcium and glutamate reporters. We used these images to define the dynamics of calcium and glutamate waves that emanate from the sites at which different stimuli were triggered. These images are available as .czi and the scripts we used to analyse them are available via zenodo as described in the links.

ORGANISM(S): Arabidopsis thaliana (thale cress)

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PROVIDER: S-BIAD464 | bioimages |

REPOSITORIES: bioimages

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Project description:BackgroundIn vertebrates and invertebrates, sensory neurons adapt to variable ambient conditions, such as the duration or repetition of a stimulus, a physiological mechanism considered as a simple form of non-associative learning and neuronal plasticity. Although various signaling pathways, as cAMP, cGMP, and the inositol 1,4,5-triphosphate receptor (InsP3R) play a role in adaptation, their precise mechanisms of action at the cellular level remain incompletely understood. Recently, in Drosophila, we reported that odor-induced Ca2+-response in axon terminals of olfactory receptor neurons (ORNs) is related to odor duration. In particular, a relatively long odor stimulus (such as 5 s) triggers the induction of a second component involving intracellular Ca2+-stores.ResultsWe used a recently developed in-vivo bioluminescence imaging approach to quantify the odor-induced Ca2+-activity in the axon terminals of ORNs. Using either a genetic approach to target specific RNAs, or a pharmacological approach, we show that the second component, relying on the intracellular Ca2+-stores, is responsible for the adaptation to repetitive stimuli. In the antennal lobes (a region analogous to the vertebrate olfactory bulb) ORNs make synaptic contacts with second-order neurons, the projection neurons (PNs). These synapses are modulated by GABA, through either GABAergic local interneurons (LNs) and/or some GABAergic PNs. Application of GABAergic receptor antagonists, both GABAA or GABAB, abolishes the adaptation, while RNAi targeting the GABABR (a metabotropic receptor) within the ORNs, blocks the Ca2+-store dependent component, and consequently disrupts the adaptation. These results indicate that GABA exerts a feedback control. Finally, at the behavioral level, using an olfactory test, genetically impairing the GABABR or its signaling pathway specifically in the ORNs disrupts olfactory adapted behavior.ConclusionTaken together, our results indicate that a relatively long lasting form of adaptation occurs within the axon terminals of the ORNs in the antennal lobes, which depends on intracellular Ca2+-stores, attributable to a positive feedback through the GABAergic synapses.

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Diffusion and bulk flow of amino acids mediate calcium waves in plants

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