Wounding not only induces the expression of damage-responsive genes, but also initiates physiological changes, such as tissue repair, vascular reconnection, and de novo organogenesis in locally damaged tissues. Wound-induced signals also propagate from the site of wounding to distal organs to elicit a systemic response. Electrical signaling, which is the most conserved type of systemic signaling in eukaryotes, is triggered by wound-induced membrane potential changes. Changes in membrane potential spread toward systemic tissues in synergy with chemical and hydraulic signals. Here, we review current knowledge on wound-induced local and systemic responses in plants. We focus particularly on how wound-activated plasma membrane-localized ion channels and pumps propagate systemic information about wounding to induce downstream molecular responses in distal tissues. Finally, we propose future studies that could lead to a better understanding of plant electrical signals and their role in physiological responses to wounding.

Wound-Induced Systemic Responses and Their Coordination by Electrical Signals

• Herbivory severely affects plant growth, posing a threat to crop production. Calcium ion (Ca2+ ) signaling and accumulation of jasmonates (JAs) are activated in plant response to herbivore attack leading to the expression of defense pathways. However, little is known about how the Ca2+ signal modulates JA biosynthesis. • We used diverse techniques, including CRISPR/Cas9, UPLC-MS/MS, and molecular biology methods to explore the role of ETHYLENE RESPONSE FACTOR 16 in Ca2+ signals-triggered JA burst during herbivore defenses in tomato. • Here we show that simulated herbivory induces GLUTAMATE RECEPTOR LIKE3.3/ 3.5 (GLR3.3/3.5)-dependent increases in electrical activity, Ca2+ influx and increases the levels of CALMODULIN2 (CaM2) and ERF16 transcripts in tomato. The interaction between CaM2 and ERF16 promotes JA biosynthesis by enhancing the transcriptional activity of ERF16, which increases the activation of ERF16 expression, and causes expression of LIPOXYGENASE D (LOXD), AOC, and 12-OXO-PHYTODIENOIC ACID REDUCTASE 3 (OPR3), the key genes in JA biosynthesis. Mutation of CaM2 results in decreased JA accumulation, together with the expression of JA biosynthesis-related genes leading to reduced resistance to the cotton bollworm Helicoverpa armigera. • These findings reveal a molecular mechanism underpinning the Ca2+ signals-initiated systemic JA burst and emphasize the pivotal role of Ca2+ signals/ ERF16 crosstalk in herbivore defenses.

Herbivore-induced Ca2+ signals trigger a jasmonate burst by activating ERF16-mediated expression in tomato.

Plant glutamate receptor-like channels (GLRs) are homologs of animal ionotropic glutamate receptors. GLRs are critical in various plant biological functions, yet their genomic features and functions in disease resistance remain largely unknown in many crop species. Here, we report the results on a thorough genome-wide study of the GLR family in oilseed rape (Brassica napus) and their role in resistance to the fungal pathogen Sclerotinia sclerotiorum. A total of 61 GLRs were identified in oilseed rape. They comprised three groups, as in Arabidopsis thaliana. Detailed computational analyses, including prediction of domain and motifs, cellular localization, cis-acting elements, PTM sites, and amino acid ligands and their binding pockets in BnGLR proteins, unveiled a set of group-specific characteristics of the BnGLR family, which included chromosomal distribution, motif composition, intron number and size, and methylation sites. Functional dissection employing virus-induced gene silencing of BnGLRs in oilseed rape and Arabidopsis mutants of BnGLR homologs demonstrated that BnGLR35/AtGLR2.5 positively, while BnGLR12/AtGLR1.2 and BnGLR53/AtGLR3.2 negatively, regulated plant resistance to S. sclerotiorum, indicating that GLR genes were differentially involved in this resistance. Our findings reveal the complex involvement of GLRs in B. napus resistance to S. sclerotiorum and provide clues for further functional characterization of BnGLRs.

Glutamate Receptor-like (GLR) Family in Brassica napus: Genome-Wide Identification and Functional Analysis in Resistance to Sclerotinia sclerotiorum

ABSTRACT Glutamate receptor-like genes (GLRs) are essential for plant growth and development and for coping with environmental (biological and non-biological) stresses. In this study, 13 GLR members were identified in the Vanilla planifolia genome and attributed to two subgroups (Clade I and Clade III) based on their physical relationships. Cis-acting element analysis and Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) annotations indicated the GLR gene regulation’s complexity and their functional diversity. Expression analysis revealed a relatively higher and more general expression pattern of Clade III members compared to the Clade I subgroup in tissues. Most GLRs showed significant differences in expression during Fusarium oxysporum infection. This suggested that GLRs play a critical role in the response of V. planifolia to pathogenic infection. These results provide helpful information for further functional research and crop improvement of VpGLRs.

https://doi.org/10.1080/15592324.2023.2204654

Genome-wide identification of the glutamate receptor-like gene family in Vanilla planifolia and their response to Fusarium oxysporum infection

Rapid systemic responses to herbivory.

Plant glutamate-like receptor genes (GLRs) are homologous to mammalian ionotropic glutamate receptors genes (iGluRs). Although GLRs have been implicated in plant defenses to biotic stress, the relationship between GLR-mediated plant immunity against fungal pathogens and electrical signals remains poorly understood. Here, we found that pretreatment with a GLR inhibitor, 6,7-dinitriquinoxaline-2,3-dione (DNQX), increased the susceptibility of tomato plants to the necrotrophic fungal pathogen Botrytis cinerea. Assessment of the glr3.3, glr3.5 and glr3.3/glr3.5 double-mutants upon B. cinerea infection showed that tomato GLR3.3 and GLR3.5 are essential for plant immunity against B. cinerea, wherein GLR3.3 plays the main role. Analysis of the membrane potential changes induced by glutamate (Glu) or glycine (Gly) revealed that amplitude was significantly reduced by knocking out GLR3.3 in tomato. While treatment with Glu or Gly significantly increased immunity against B. cinerea in wild-type plants, this effect was significantly attenuated in glr3.3 mutants. Thus, our data demonstrate that GLR3.3- and GLR3.5-mediated plant immunity against B. cinerea is associated with electrical signals in tomato plants.

The Glutamate Receptor Plays a Role in Defense against Botrytis cinerea through Electrical Signaling in Tomato

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The Glutamate Receptor Plays a Role in Defense against Botrytis cinerea through Electrical Signaling in Tomato