Long-Distance Turgor Pressure Changes Induce Local Activation of Plant Glutamate Receptor-Like Channels

Grenzi, Matteo; Buratti, Stefano; Parmagnani, Ambra S.; Aziz, Ilaria Abdel; Wojcik, Iwona Bernacka; Resentini, Francesca; Šimura, Jan; Doccula, Fabrizio Gandolfo; Alfieri, Andrea; Luoni, Laura; Ljung, Karin; Bonza, Maria Cristina; Stavrinidou, Eleni; Costa, Alex

doi:10.2139/ssrn.4234694

Cited by 8 publications

(22 citation statements)

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“…The nature of this information encoding remains unclear. Recently, in Arabidopsis, it has been shown that upon wounding glucohydrolase, enzymes generate mobile signaling molecules (e.g., Ricca's factors) and that, together with hydraulic pressure changes, they are involved in the electrical signal and Ca 2+ wave propagation (41,42). We can only speculate that, in the VFT, similar mechanisms might be triggered upon AP generation and therefore be involved in the excitability of the trap.…”

Section: Discussionmentioning

confidence: 95%

Plant electrophysiology with conformable organic electronics: Deciphering the propagation of Venus flytrap action potentials

et al. 2023

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Electrical signals in plants are mediators of long-distance signaling and correlate with plant movements and responses to stress. These signals are studied with single surface electrodes that cannot resolve signal propagation and integration, thus impeding their decoding and link to function. Here, we developed a conformable multielectrode array based on organic electronics for large-scale and high-resolution plant electrophysiology. We performed precise spatiotemporal mapping of the action potential (AP) in Venus flytrap and found that the AP actively propagates through the tissue with constant speed and without strong directionality. We also found that spontaneously generated APs can originate from unstimulated hairs and that they correlate with trap movement. Last, we demonstrate that the Venus flytrap circuitry can be activated by cells other than the sensory hairs. Our work reveals key properties of the AP and establishes the capacity of organic bioelectronics for resolving electrical signaling in plants contributing to the mechanistic understanding of long-distance responses in plants.

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Section: Discussionmentioning

confidence: 95%

Plant electrophysiology with conformable organic electronics: Deciphering the propagation of Venus flytrap action potentials

et al. 2023

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“…Plants respond to different treatments that abruptly alter the water pressure in their vascular system with a hydraulic wave ( e.g., wounding; Kloth and Dicke, 2022; Grenzi et al, 2023; Gao et al, 2023). As the sudden application of WLS could potentially activate a hydraulic wave in plants due to an increase in the water pressure around the root system, we measured the systemic hydraulic wave in plants subjected to WLS (Zimmermann et al, 2013; Fichman and Mittler, 2021).…”

Section: Resultsmentioning

confidence: 99%

“…Hydraulic waves are thought to play an important role in the systemic response of plants to different stresses (Kloth and Dicke, 2022; Grenzi et al, 2023). The changes in water pressure propagating through the vascular system of plants were proposed to trigger mechanosensory proteins that translate the hydraulic signal into a calcium signal and subsequently a ROS accumulation response in systemic tissues (Gilroy et al, 2016; Kloth and Dicke, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…The association between the stomatal opening response, ABA, and the hydraulic wave (Figure 3) should also be pursued in future studies as it suggests that the degree of stomatal aperture openness at the time WLS occurs might impact hydraulic waves and other systemic responses to this stress. In this respect, it should be mentioned that hydraulic waves were recently proposed to control glutamic acid release from cells during systemic responses to wounding, controlling the systemic calcium wave (Grenzi et al, 2023), as well as linked to the mobilization of glucohydrolases, which are important for the regulation of electrical signals during wound responses (Gao et al, 2023). Hydraulic waves might therefore play a central role in regulating systemic responses in plants, and elucidating their function requires further studies.…”

Section: Discussionmentioning

confidence: 99%

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Rapid systemic responses of Arabidopsis to waterlogging stress

Peláez-Vico

Tukuli

Singh

et al. 2023

Preprint

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Waterlogging stress (WLS) negatively impacts the growth and yield of crops resulting in heavy losses to agricultural production. Previous studies revealed that WLS induces a systemic response in shoots that is partially dependent on the plant hormones ethylene and abscisic acid. However, the role of rapid cell-to-cell signaling pathways, such as the reactive oxygen species (ROS) and calcium waves, in systemic responses of plants to WLS is unknown at present. Here we reveal that an abrupt WLS treatment of Arabidopsis thaliana plants growing in peat moss triggers systemic ROS and calcium wave responses, and that the WLS-triggered ROS wave response of Arabidopsis is dependent on the ROS generating RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD), calcium-permeable channels GLUTAMATE-LIKE RECEPTOR 3.3 and 3.6 (GLR3.3 and GLR3.6), and aquaporin PLASMA MEMBRANE INTRINSIC PROTEIN 2;1 (PIP2;1) proteins. We further show that WLS is accompanied by a rapid systemic transcriptomic response that is evident as early as 10 min following waterlogging initiation, includes many hypoxia-response transcripts, and is partially dependent on RBOHD. Interestingly, the abrupt WLS of Arabidopsis resulted in the triggering of a rapid hydraulic wave response and the transient opening of stomata on leaves. Taken together, our findings reveal that the initiation of WLS in plants is accompanied by rapid systemic physiological and transcriptomic responses that involve the ROS, calcium, and hydraulic waves. These findings reveal that systemic plant responses to WLS are rapid and at least partially dependent on cell-to-cell signaling mechanisms.

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“…Rapid systemic signals that are mobilized within seconds to minutes of stress sensing by the local tissue, and can transverse the entire plant, include hydraulic, electric, calcium and ROS/redox waves (Choudhury et al, 2018;Fichman & Mittler, 2020Gao et al, 2023;Grenzi et al, 2023;Huber & Bauerle, 2016;Klejchova et al, 2021;Kollist et al, 2019;Peláez-Vico et al, 2022;Toyota et al, 2018). transcription factors (TFs), kinases, phosphatases, and channels (Choudhury et al, 2018;Fichman & Mittler, 2020Gao et al, 2023;Grenzi et al, 2023;Huber & Bauerle, 2016;Klejchova et al, 2021;Kollist et al, 2019;Peláez-Vico et al, 2022;Toyota et al, 2018). Recent studies identified potential links between the different systemic signals and began defining their hierarchy (Figure 2).…”

Section: Systemic and ' Rapid' Systemic Signalling In Plantsmentioning

confidence: 99%

Systemic stomatal responses in plants: Coordinating development, stress, and pathogen defense under a changing climate

Peláez‐Vico,

Zandalinas,

Devireddy

et al. 2024

Plant Cell & Environment

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To successfully survive, develop, grow and reproduce, multicellular organisms must coordinate their molecular, physiological, developmental and metabolic responses among their different cells and tissues. This process is mediated by cell‐to‐cell, vascular and/or volatile communication, and involves electric, chemical and/or hydraulic signals. Within this context, stomata serve a dual role by coordinating their responses to the environment with their neighbouring cells at the epidermis, but also with other stomata present on other parts of the plant. As stomata represent one of the most important conduits between the plant and its above‐ground environment, as well as directly affect photosynthesis, respiration and the hydraulic status of the plant by controlling its gas and vapour exchange with the atmosphere, coordinating the overall response of stomata within and between different leaves and tissues plays a cardinal role in plant growth, development and reproduction. Here, we discuss different examples of local and systemic stomatal coordination, the different signalling pathways that mediate them, and the importance of systemic stomatal coordination to our food supply, ecosystems and weather patterns, under our changing climate. We further discuss the potential biotechnological implications of regulating systemic stomatal responses for enhancing agricultural productivity in a warmer and CO2‐rich environment.

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Long-Distance Turgor Pressure Changes Induce Local Activation of Plant Glutamate Receptor-Like Channels

Cited by 8 publications

References 0 publications

Plant electrophysiology with conformable organic electronics: Deciphering the propagation of Venus flytrap action potentials

Plant electrophysiology with conformable organic electronics: Deciphering the propagation of Venus flytrap action potentials

Rapid systemic responses of Arabidopsis to waterlogging stress

Systemic stomatal responses in plants: Coordinating development, stress, and pathogen defense under a changing climate

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