Ricca’s factors as mobile proteinaceous effectors of electrical signaling

Gao, Yong‐Qiang; Jiménez‐Sandoval, Pedro; Tiwari, Satyam; Stolz, Stéphanie; Wang, Jing; Glauser, Gaëtan; Santiago, Julia; Farmer, Edward E.

doi:10.1016/j.cell.2023.02.006

Cited by 31 publications

(35 citation statements)

References 52 publications

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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%

“…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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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Rapid systemic responses of Arabidopsis to waterlogging stress

Peláez-Vico

Tukuli

Singh

et al. 2023

Preprint

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“…The latter two glutamate receptor type Ca 2+ channels are required for long‐distance Ca 2+ ‐electrical signalling in Arabidopsis (Mousavi et al ., 2013; Toyota et al ., 2018). That the APs and wounding‐induced SWPs (Mousavi et al ., 2013; Gao et al ., 2023) travel along the phloem does not come as a surprise, since the interconnected sieve tubes without a vacuole, nucleus and chloroplast provide for a perfect cable (Hedrich et al ., 2016).…”

Section: Ap Is a Feature Of All Fast‐moving Plantsmentioning

confidence: 99%

“…This ‘Ricca's factor’ hypothesis was later used to explain wound‐induced, long‐distance, electrical waves. Very recently, the Ted Farmer laboratory found that in Arabidopsis, the SWP in response to wounding is associated with a xylem‐traveling ‘Ricca's factor’ identified as myrosinase/glucosinolate‐derived aglucone moiety (Gao et al ., 2023; Hedrich & Roelfsema, 2023). It is possible that Ricca's factor provides the interface between xylem and phloem by facilitation of tissue‐dependent glutamate release.…”

Section: Ap Is a Feature Of All Fast‐moving Plantsmentioning

confidence: 99%

Demystifying the Venus flytrap action potential

Hedrich

Kreuzer

2023

New Phytologist

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SummaryAll plants are electrically excitable, but only few are known to fire a well‐defined, all‐or‐nothing action potential (AP). The Venus flytrap Dionaea muscipula displays APs with an extraordinarily high firing frequency and speed, enabling the capture organ of this carnivorous plant to catch small animals as fast as flies. The number of APs triggered by the prey is counted and serves as the basis for decisions within the flytrap's hunting cycle. The archetypical Dionaea AP lasts 1 s and consists of five phases: Starting from the resting state, an initial cytosolic Ca2+ transient is followed by depolarization, repolarization and a transient hyperpolarization (overshoot) before the original membrane potential is finally recovered. When the flytrap matures and becomes excitable, a distinct set of ion channels, pumps and carriers is expressed, each mastering a distinct AP phase.

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“…Leaf infiltration with the benzoxazinoid DIMBOA, on the other hand, induces callose deposition in wild type maize (Ahmad et al, 2011) and wheat ( Triticum aestivum ) (Li et al, 2018). Glucosinolate breakdown products have further been shown to: i) inhibit root growth, presumably via competitive binding of auxin receptor TIR1 (Katz et al, 2015); ii) regulate stomatal aperture via ROS signaling (Zhao et al, 2008; Khokon et al, 2011; Hossain et al, 2013; Salehin et al, 2019), and; iii) elicit membrane depolarizations, calcium fluxes and jasmonate responses in distal leaves upon a local wounding event (Gao et al, 2023). Whether benzoxazinoid breakdown products also act as defense regulators is unknown, although it is likely given their abundance and reactivity.…”

Section: Introductionmentioning

confidence: 99%

The benzoxazinoid breakdown product 5-Methoxy-2-Nitrophenol has a dual function in maize defense against herbivory

Schimmel,

Escobar-Bravo,

Mateo

et al. 2023

Preprint

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Catabolism of plant secondary metabolites can yield bioactive breakdown products. However, these compounds often remain poorly characterized. Here, we report on the discovery, biosynthesis, and biological relevance of 5 Methoxy-2-Nitrophenol (5M2NP), a secondary metabolite breakdown product which accumulates in damaged maize tissues. We used mutant plants, biochemical complementation, and metabolomic analyses to determine the biosynthetic origin of 5M2NP. Additionally, we assessed 5M2NP′s role in plant defense against herbivores. For this, we surveyed defense-associated responses (gene expression, phytohormones, volatile organic compounds) in wounded, 5M2NP-supplemented maize leaves, and performed bioassays with herbivorous insects. We found that 5M2NP accumulation upon tissue disruption is contingent upon a functional benzoxazinoid biosynthesis pathway. Labeling experiments demonstrated that 5M2NP is derived from DIMBOA. Physiological doses of exogenous 5M2NP increased the wound-induced expression of defense genes and emission of terpenoids. Additionally, 5M2NP exhibited antibiotic and antixenotic activities towards both generalist and specialist herbivores in nano- to micromolar quantities. We conclude that 5M2NP, which represents a novel class of plant-derived compounds, can act as a direct defense and a defense modulator. 5M2NP thus expands the functional repertoire of benzoxazinoids and likely contributes to their protective function against insect herbivores. The discovery of 5M2NP highlights the multifunctionality of plant secondary metabolites and their breakdown products.

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Ricca’s factors as mobile proteinaceous effectors of electrical signaling

Cited by 31 publications

References 52 publications

Rapid systemic responses of Arabidopsis to waterlogging stress

Rapid systemic responses of Arabidopsis to waterlogging stress

Demystifying the Venus flytrap action potential

The benzoxazinoid breakdown product 5-Methoxy-2-Nitrophenol has a dual function in maize defense against herbivory

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