Early Extracellular ATP Signaling in Arabidopsis Root Epidermis: A Multi-Conductance Process

Wang, Limin; Stacey, Gary; Leblanc‐Fournier, Nathalie; Legué, Valérie; Moulia, Bruno; Davies, Julia M.

doi:10.3389/fpls.2019.01064

Cited by 13 publications

(26 citation statements)

References 81 publications

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“…Although the present study demonstrated the utility of the method in a microbiological setting, it is important to highlight that it is not limited to the use in prokaryotic organisms. Aside from roles in bacterial physiology, numerous studies reported different roles of eATP in eukaryotic organisms including human and plant physiology [ 17 , 39 , 47 ]. As a universal molecule of all living beings, eATP plays important roles in bacterial, animal and plant kingdoms, thus we believe that this method will allow elucidating the role and dynamics of eATP in different organisms.…”

Section: Discussionmentioning

confidence: 99%

Real-time monitoring of extracellular ATP in bacterial cultures using thermostable luciferase

Ihssen¹,

Jovanović

Širec³

et al. 2021

PLoS ONE

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Adenosine triphosphate (ATP) is one of the most important indicators of cell viability. Extracellular ATP (eATP) is commonly detected in cultures of both eukaryotic and prokaryotic cells but is not the focus of current scientific research. Although ATP release has traditionally been considered to mainly occur as a consequence of cell destruction, current evidence indicates that ATP leakage also occurs during the growth phase of diverse bacterial species and may play an important role in bacterial physiology. ATP can be conveniently measured with high sensitivity in luciferase-based bioluminescence assays. However, wild-type luciferases suffer from low stability, which limit their use. Here we demonstrate that an engineered, thermostable luciferase is suitable for real-time monitoring of ATP release by bacteria, both in broth culture and on agar surfaces. Different bacterial species show distinct patterns of eATP accumulation and decline. Real-time monitoring of eATP allows for the estimation of viable cell number by relating luminescence onset time to initial cell concentration. Furthermore, the method is able to rapidly detect the effect of antibiotics on bacterial cultures as Ampicillin sensitive strains challenged with beta lactam antibiotics showed strongly increased accumulation of eATP even in the absence of growth, as determined by optical density. Patterns of eATP determined by real-time luminescence measurement could be used to infer the minimal inhibitory concentration of Ampicillin. Compared to conventional antibiotic susceptibility testing, the method presented here is faster and more sensitive, which is essential for better treatment outcomes and reducing the risk of inducing antibiotic resistance. Real-time eATP bioluminescence assays are suitable for different cell types, either prokaryotic or eukaryotic, thus, permitting their application in diverse fields of research. It can be used for example in the study of the role of eATP in physiology and pathophysiology, for monitoring microbial contamination or for antimicrobial susceptibility testing in clinical diagnostics.

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Section: Discussionmentioning

confidence: 99%

Real-time monitoring of extracellular ATP in bacterial cultures using thermostable luciferase

Ihssen¹,

Jovanović

Širec³

et al. 2021

PLoS ONE

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“…It is known that eATP-induced [Ca 2+ ] cyt increase in Arabidopsis roots requires plasma membrane Ca 2+ influx channels but the molecular identities of these channels remain unknown, as is also the case for other organs [ 9 , 11 , 14 , 21 , 22 , 23 ]. It has been hypothesized that the Arabidopsis annexin 1 protein (AtANN1) could be involved in mediating plasma membrane Ca 2+ influx [ 5 , 24 ] and recently AtANN4 was found to mediate eATP-induced [Ca 2+ ] cyt increase when expressed in Xenopus oocytes [ 25 ].…”

Section: Introductionmentioning

confidence: 99%

Annexin 1 Is a Component of eATP-Induced Cytosolic Calcium Elevation in Arabidopsis thaliana Roots

Mohammad-Sidik

Sun

Shin

et al. 2021

IJMS

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Extracellular ATP (eATP) has long been established in animals as an important signalling molecule but this is less understood in plants. The identification of Arabidopsis thaliana DORN1 (Does Not Respond to Nucleotides) as the first plant eATP receptor has shown that it is fundamental to the elevation of cytosolic free Ca2+ ([Ca2+]cyt) as a possible second messenger. eATP causes other downstream responses such as increase in reactive oxygen species (ROS) and nitric oxide, plus changes in gene expression. The plasma membrane Ca2+ influx channels involved in eATP-induced [Ca2+]cyt increase remain unknown at the genetic level. Arabidopsis thaliana Annexin 1 has been found to mediate ROS-activated Ca2+ influx in root epidermis, consistent with its operating as a transport pathway. In this study, the loss of function Annexin 1 mutant was found to have impaired [Ca2+]cyt elevation in roots in response to eATP or eADP. Additionally, this annexin was implicated in modulating eATP-induced intracellular ROS accumulation in roots as well as expression of eATP-responsive genes.

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“…Two lectin receptor kinases, P2K1 and P2K2, were identified to be eATP receptors in Arabidopsis thaliana [ 19 , 20 ] involved in eATP-induced immune responses [ 13 , 14 , 21 ]. Signal transducers in the plasma membrane (PM), including heterotrimeric G proteins [ 12 , 22 ], NADPH oxidase [ 23 , 24 ], and Ca 2+ channels [ 6 , 23 , 25 , 26 ], were reported to be involved in eATP signal transduction. Several secondary messengers, e.g., ROS, H 2 O 2 , NO, and Ca 2+ may be responsible for the eATP-induced intracellular responses that eventually alter plant growth and development [ 6 , 17 , 26 , 27 , 28 , 29 ].…”

Section: Introductionmentioning

confidence: 99%

P2K1 Receptor, Heterotrimeric Gα Protein and CNGC2/4 Are Involved in Extracellular ATP-Promoted Ion Influx in the Pollen of Arabidopsis thaliana

Yin

et al. 2021

Plants

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As an apoplastic signal, extracellular ATP (eATP) is involved in plant growth and development. eATP promotes tobacco pollen germination (PG) and pollen tube growth (PTG) by stimulating Ca2+ or K+ absorption. Nevertheless, the mechanisms underlying eATP-stimulated ion uptake and their role in PG and PTG are still unclear. Here, ATP addition was found to modulate PG and PTG in 34 plant species and showed a promoting effect in most of these species. Furthermore, by using Arabidopsis thaliana as a model, the role of several signaling components involved in eATP-promoted ion (Ca2+, K+) uptake, PG, and PTG were investigated. ATP stimulated while apyrase inhibited PG and PTG. Patch-clamping results showed that ATP promoted K+ and Ca2+ influx into pollen protoplasts. In loss-of-function mutants of P2K1 (dorn1-1 and dorn1-3), heterotrimeric G protein α subunit (gpa1-1, gpa1-2), or cyclic nucleotide gated ion channel (cngc2, cngc4), eATP-stimulated PG, PTG, and ion influx were all impaired. Our results suggest that these signaling components may be involved in eATP-promoted PG and PTG by regulating Ca2+ or K+ influx in Arabidopsis pollen grains.

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Early Extracellular ATP Signaling in Arabidopsis Root Epidermis: A Multi-Conductance Process

Cited by 13 publications

References 81 publications

Real-time monitoring of extracellular ATP in bacterial cultures using thermostable luciferase

Real-time monitoring of extracellular ATP in bacterial cultures using thermostable luciferase

Annexin 1 Is a Component of eATP-Induced Cytosolic Calcium Elevation in Arabidopsis thaliana Roots

P2K1 Receptor, Heterotrimeric Gα Protein and CNGC2/4 Are Involved in Extracellular ATP-Promoted Ion Influx in the Pollen of Arabidopsis thaliana

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