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The Plasma Membrane Purinoreceptor P2K1/DORN1 Is Essential in Stomatal Closure Evoked by Extracellular Diadenosine Tetraphosphate (Ap₄A) in Arabidopsis thaliana.

ABSTRACT: Dinucleoside polyphosphates (Np_nNs) are considered novel signalling molecules involved in the induction of plant defence mechanisms. However, Np_nN signal recognition and transduction are still enigmatic. Therefore, the aim of our research was the identification of the Np_nN receptor and signal transduction pathways evoked by these nucleotides. Earlier, we proved that purine and pyrimidine Np_nNs differentially affect the phenylpropanoid pathway in Vitis vinifera suspension-cultured cells. Here, we report, for the first time, that both diadenosine tetraphosphate (Ap₄A) and dicytidine tetraphosphate (Cp₄C)-induced stomatal closure in Arabidopsis thaliana. Moreover, we showed that plasma membrane purinoreceptor P2K1/DORN1 (does not respond to nucleotide 1) is essential for Ap₄A-induced stomata movements but not for Cp₄C. Wild-type Col-0 and the dorn1-3 A. thaliana knockout mutant were used. Examination of the leaf epidermis dorn1-3 mutant provided evidence that P2K1/DORN1 is a part of the signal transduction pathway in stomatal closure evoked by extracellular Ap₄A but not by Cp₄C. Reactive oxygen species (ROS) are involved in signal transduction caused by Ap₄A and Cp₄C, leading to stomatal closure. Ap₄A induced and Cp₄C suppressed the transcriptional response in wild-type plants. Moreover, in dorn1-3 leaves, the effect of Ap₄A on gene expression was impaired. The interaction between P2K1/DORN1 and Ap₄A leads to changes in the transcription of signalling hubs in signal transduction pathways.

SUBMITTER: Dobrogojski J

PROVIDER: S-EPMC10706190 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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The Plasma Membrane Purinoreceptor P2K1/DORN1 Is Essential in Stomatal Closure Evoked by Extracellular Diadenosine Tetraphosphate (Ap4A) in Arabidopsis thaliana.

Dobrogojski Jędrzej J Nguyen Van Hai VH Kowalska Joanna J Borek Sławomir S Pietrowska-Borek Małgorzata M

International journal of molecular sciences 20231124 23

Dinucleoside polyphosphates (NpnNs) are considered novel signalling molecules involved in the induction of plant defence mechanisms. However, NpnN signal recognition and transduction are still enigmatic. Therefore, the aim of our research was the identification of the NpnN receptor and signal transduction pathways evoked by these nucleotides. Earlier, we proved that purine and pyrimidine NpnNs differentially affect the phenylpropanoid pathway in Vit ...[more]

PMID: 38069010

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Project description:The opportunistic bacterial pathogen Pseudomonas aeruginosa causes a wide range of infections that are difficult to treat, largely because of the spread of antibiotic-resistant isolates. Antivirulence therapy, í.e. the use of drugs that inhibit the expression or activity of virulence factors, is currently considered an attractive strategy to reduce P. aeruginosa pathogenicity and complement antibiotic treatments. Because of the multifactorial nature of P. aeruginosa virulence and the broad arsenal of virulence factors this bacterium can produce, the regulatory networks that control the expression of multiple virulence traits have been extensively explored as potential targets for antivirulence drug development. The intracellular signaling molecule diadenosine tetraphosphate (Ap4A) has been reported to control stress resistance and virulence-related traits in some bacteria, but its role has not been investigated in P. aeruginosa so far. To fill this gap, we generated a mutant of the reference strain P. aeruginosa PAO1 that lacks the Ap4A-hydrolysing enzyme ApaH and, consequently, accumulates high intracellular levels of Ap4A. Phenotypic and transcriptomic analyses revealed that the lack of ApaH causes a drastic reduction in the expression of several virulence factors, including extracellular proteases, elastases, siderophores, and quorum sensing signal molecules. Accordingly, infection assays in plant and animal models demonstrated that ApaH-deficient cells are significantly impaired in infectivity and persistence in different hosts, including mice. Finally, deletion of apaH in P. aeruginosa clinical isolates demonstrated that the positive effect of ApaH on the production of virulence-related traits and on infectivity is conserved in P. aeruginosa. This study provides the first evidence that the Ap4A-hydrolysing enzyme ApaH is important for P. aeruginosa virulence, highlighting this protein as a novel potential target for antivirulence therapies against P. aeruginosa.

Dataset Information

The Plasma Membrane Purinoreceptor P2K1/DORN1 Is Essential in Stomatal Closure Evoked by Extracellular Diadenosine Tetraphosphate (Ap₄A) in Arabidopsis thaliana.

Publications

The Plasma Membrane Purinoreceptor P2K1/DORN1 Is Essential in Stomatal Closure Evoked by Extracellular Diadenosine Tetraphosphate (Ap<sub>4</sub>A) in <i>Arabidopsis thaliana</i>.

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