Dataset Information

Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture

ABSTRACT: A multibillion dollar pharmaceutical industry targets purinergic signaling pathways in humans. However, in contrast, little is known about purinergic signaling in plants. Extracellular adenosine-5’-triphosphate (eATP) acts as a damage-associated molecular pattern (DAMP) in both animals and plants. The first plant eATP receptor, DORN1, was identified in Arabidopsis, defining a new kinase family (P2K) of purinoceptors. Stomates are leaf pores that control gas exchange and, therefore, impact critical functions such as photosynthesis and drought tolerance. Stomates are also the prefer entry point for leaf pathogens. The addition of ATP led to the rapid closure of Arabidopsis leaf stomates resulting in enhanced resistance to the bacterial pathogen Psuedomonas syringae. The data indicate that this response is mediated by eATP recognition by DORN1 followed by direct phosphorylation of the NADPH oxidase RBOHD, resulting in elevated production of reactive oxygen species and stomatal closure. Mutation of the DORN1 phosphorylation sites on RBOHD eliminated the ability of eATP to induce stomatal closure. To date, in contrast to work in animals, purinergic signaling in plants has been viewed as a curiosity without any direct, mechanistic connection to key plant processes. The data presented clearly demonstrates eATP as an important signal controlling stomatal aperture with important implications for the control of plant photosynthesis, water homeostasis, pathogen resistance and ultimately yield.

INSTRUMENT(S): LTQ Orbitrap

ORGANISM(S): Arabidopsis Thaliana (mouse-ear Cress)

SUBMITTER: Nagib Ahsan

LAB HEAD: Nagib Ahsan

PROVIDER: PXD006678 | Pride | 2018-10-24

REPOSITORIES: Pride

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Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture.

Chen Dongqin D Cao Yangrong Y Li Hong H Kim Daewon D Ahsan Nagib N Thelen Jay J Stacey Gary G

Nature communications 20171222 1

In addition to acting as a cellular energy source, ATP can also act as a damage-associated molecular pattern in both animals and plants. Stomata are leaf pores that control gas exchange and, therefore, impact critical functions such as photosynthesis, drought tolerance, and also are the preferred entry point for pathogens. Here we show the addition of ATP leads to the rapid closure of leaf stomata and enhanced resistance to the bacterial pathogen Psuedomonas syringae. This response is mediated b ...[more]

PMID: 29273780

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Project description:Pokhilko2013 - TOC1 signalling in Arabidopsis circadian clock In this model, Pokhilko et al. has incorporated the negative transcriptional regulations of the core clock genes by TOC1 and the up-regulation of TOC1 expression by ABA signalling, to their previous model BIOMD0000000412 This model is described in the article: Modelling the widespread effects of TOC1 signalling on the plant circadian clock and its outputs. Pokhilko A, Mas P, Millar AJ. BMC Syst Biol 2013; 7: 23 Abstract: BACKGROUND: 24-hour biological clocks are intimately connected to the cellular signalling network, which complicates the analysis of clock mechanisms. The transcriptional regulator TOC1 (TIMING OF CAB EXPRESSION 1) is a founding component of the gene circuit in the plant circadian clock. Recent results show that TOC1 suppresses transcription of multiple target genes within the clock circuit, far beyond its previously-described regulation of the morning transcription factors LHY (LATE ELONGATED HYPOCOTYL) and CCA1 (CIRCADIAN CLOCK ASSOCIATED 1). It is unclear how this pervasive effect of TOC1 affects the dynamics of the clock and its outputs. TOC1 also appears to function in a nested feedback loop that includes signalling by the plant hormone Abscisic Acid (ABA), which is upregulated by abiotic stresses, such as drought. ABA treatments both alter TOC1 levels and affect the clock's timing behaviour. Conversely, the clock rhythmically modulates physiological processes induced by ABA, such as the closing of stomata in the leaf epidermis. In order to understand the dynamics of the clock and its outputs under changing environmental conditions, the reciprocal interactions between the clock and other signalling pathways must be integrated. RESULTS: We extended the mathematical model of the plant clock gene circuit by incorporating the repression of multiple clock genes by TOC1, observed experimentally. The revised model more accurately matches the data on the clock's molecular profiles and timing behaviour, explaining the clock's responses in TOC1 over-expression and toc1 mutant plants. A simplified representation of ABA signalling allowed us to investigate the interactions of ABA and circadian pathways. Increased ABA levels lengthen the free-running period of the clock, consistent with the experimental data. Adding stomatal closure to the model, as a key ABA- and clock-regulated downstream process allowed to describe TOC1 effects on the rhythmic gating of stomatal closure. CONCLUSIONS: The integrated model of the circadian clock circuit and ABA-regulated environmental sensing allowed us to explain multiple experimental observations on the timing and stomatal responses to genetic and environmental perturbations. These results crystallise a new role of TOC1 as an environmental sensor, which both affects the pace of the central oscillator and modulates the kinetics of downstream processes. This model is hosted on BioModels Database and identified by: BIOMD0000000445. To cite BioModels Database, please use: BioModels Database: An enhanced, curated and annotated resource for published quantitative kinetic models. To the extent possible under law, all copyright and related or neighbouring rights to this encoded model have been dedicated to the public domain worldwide. Please refer to CC0 Public Domain Dedication for more information.

Project description:Systems responses of mature leaves from 4 reference cultivars of a larger collection of European potato cultivars (Solanum tuberosum L.) are investigated by metabolome profiling and RNA-Sequencing. The chosen reference cultivars, Milva, Alegria, Desiree, and Saturna, vary in ascending order in regard to drought tolerance. Systems analyses are based on 3 independent field trials and 3 paralleled greenhouse trials. Robust responses across all cultivars and conditions to natural seasonal drought stress comprise proline, raffinose, galactinol, arabitol, arabinonic acid, chlorogenic acid, and 102 transcripts which consist to a high proportion of heat shock proteins and genes with signaling or regulatory functions, such as a homolog of abscisic acid receptor PYL4. Constitutive differences of the tolerant cultivars, Desiree and Saturna, compared to the sensitive cultivars include arbutin (hydroquinone-beta-D-glucopyranoside), octopamine (p-hydroxyphenylethanolamine), ribitol and 248 differential transcripts. Many of these transcripts are disease related, receptor kinases, or regulatory genes, for example a homolog of the Arabidopsis FOUR LIPS MYB-regulator of stomatal cell proliferation. Functional enrichment analyses imply that heat stress is a major acclimation component of potato leaves to agronomical relevant drought stress. Enhanced leaf heat stress is a result of drought caused by loss of transpiration cooling. This effect and CO2-limitation are the main dilemmas of drought- or ABA-induced stomatal closure. Constitutive differences between tolerant and sensitive cultivars indicate partially synergistic interactions of drought and biotic stress responses. We suggest that drought tolerance of the potato reference cultivars may be caused by general resistance mechanisms which are part of previously selected pathogen tolerance. Transcriptome profiling by RNA-sequencing of 48 leaf samples from 4 potato cultivars grown under control or drought stress conditions in 6 independent experiments

Dataset Information

Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture

Publications

Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture.

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