Extracellular ATP Signaling Is Mediated by H2O2 and Cytosolic Ca2+ in the Salt Response of Populus euphratica Cells

Sun, Jian; Zhang, Xuan; Deng, Shumin; Zhang, Chunlan; Wang, Meijuan; Ding, Mingquan; Zhao, Rui; Shen, Xin; Zhou, Xin; Lu, Cunfu; Chen, Shao Liang

doi:10.1371/journal.pone.0053136

Cited by 74 publications

(100 citation statements)

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“…Suppression of apyrase significantly altered the expression of genes involved in biotic stress responses (Lim et al, 2014). Additionally, our previous finding suggested that apyrase contributed to salt tolerance in P. euphratica (Sun et al, 2012b). NaCl shock elicited a significant rise in ATP in the ECM, but the eATP levels returned to basal levels after 20 min of salt treatment (Sun et al, 2012b).…”

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confidence: 78%

“…Additionally, our previous finding suggested that apyrase contributed to salt tolerance in P. euphratica (Sun et al, 2012b). NaCl shock elicited a significant rise in ATP in the ECM, but the eATP levels returned to basal levels after 20 min of salt treatment (Sun et al, 2012b). This was presumably due to ATP hydrolysis by ectoapyrase, which enabled P. euphratica to maintain low levels of eATP in a prolonged duration of salinity and, thus, prevent eATPinduced cell death (Sun et al, 2012a).…”

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confidence: 92%

“…The cold-elicited release of ATP through disrupted membranes and the buildup of ATP in the ECM may cause a reduction in cell viability. eATP also plays a fundamental role in mediating plant responses to environmental stresses, such as pathogens (Chivasa et al, 2009), wounds (Cao et al, 2014), high salt (Sun et al, 2012b), and osmotic stress (Jeter et al, 2004;Kim et al, 2009); however, the link between eATP and cold tolerance has not been fully established.…”

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confidence: 99%

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Populus euphratica APYRASE2 Enhances Cold Tolerance by Modulating Vesicular Trafficking and Extracellular ATP in Arabidopsis Plants

et al. 2015

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Apyrase and extracellular ATP play crucial roles in mediating plant growth and defense responses. In the cold-tolerant poplar, Populus euphratica, low temperatures up-regulate APYRASE2 (PeAPY2) expression in callus cells. We investigated the biochemical characteristics of PeAPY2 and its role in cold tolerance. We found that PeAPY2 predominantly localized to the plasma membrane, but punctate signals also appeared in the endoplasmic reticulum and Golgi apparatus. PeAPY2 exhibited broad substrate specificity, but it most efficiently hydrolyzed purine nucleotides, particularly ATP. PeAPY2 preferred Mg 2+ as a cofactor, and it was insensitive to various, specific ATPase inhibitors. When PeAPY2 was ectopically expressed in Arabidopsis (Arabidopsis thaliana), cold tolerance was enhanced, based on root growth measurements and survival rates. Moreover, under cold stress, PeAPY2-transgenic plants maintained plasma membrane integrity and showed reduced cold-elicited electrolyte leakage compared with wild-type plants. These responses probably resulted from efficient plasma membrane repair via vesicular trafficking. Indeed, transgenic plants showed accelerated endocytosis and exocytosis during cold stress and recovery. We found that low doses of extracellular ATP accelerated vesicular trafficking, but high extracellular ATP inhibited trafficking and reduced cell viability. Cold stress caused significant increases in root medium extracellular ATP. However, under these conditions, PeAPY2-transgenic lines showed greater control of extracellular ATP levels than wild-type plants. We conclude that Arabidopsis plants that overexpressed PeAPY2 could increase membrane repair by accelerating vesicular trafficking and hydrolyzing extracellular ATP to avoid excessive, cold-elicited ATP accumulation in the root medium and, thus, reduced ATP-induced inhibition of vesicular trafficking.

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confidence: 78%

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confidence: 92%

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confidence: 99%

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Populus euphratica APYRASE2 Enhances Cold Tolerance by Modulating Vesicular Trafficking and Extracellular ATP in Arabidopsis Plants

et al. 2015

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“…Similarly, some abiotic stress can also affect the release of ATP and the change of eATP level plays important roles in regulating the biotic stress responses. For example, Sun et al (2012b) found that salt shock induced a transient elevation in the eATP level, and eATP regulated a wide range of cellular processes required for salt adaptation. Thus, it seems likely that eATP is a central signal involved in the plant response to a variety of environmental stresses.…”

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confidence: 99%

Extracellular ATP: a potential molecule regulating the defence response of plants to biotic stresses - a review

Jia¹,

Jingyue²,

Dong-Dong³

et al. 2016

Plant Prot. Sci.

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Jia L., Bai J., Guan D., Sun K., Jiao Q., Feng Q. (2016): Extracellular ATP: a potential molecule regulating the defence response of plants to biotic stresses -a review. Plant Protect. Sci., 52: 221-228.Although adenosine 5'-triphosphate (ATP) is commonly considered as an intracellular energy currency molecule, animal, plant, and microbial cells can secrete ATP from the cytosol into the extracellular matrix. In plant cells, extracellular ATP (eATP) is found to play important roles in regulating several physiological processes, such as cell growth, development, and death. Interestingly, recent studies suggest that eATP could be a potential molecule required for the regulation of the defence responses of plants to pathogen infection and herbivore attack. This review article summarises the preliminary studies that have been conducted regarding the possible involvement of eATP in plant defence responses to biotic stress. And, we also attempt to address some speculations and theoretical discussions to aid future research in this area.

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“…A dozen studies showed that extracellular ATP signaling is associated with second messengers-cytosolic calcium (Ca 2+ ), reactive oxygen species (ROS), and nitric oxide (NO; Demidchik et al, 2003;Jeter et al, 2004;Song et al, 2006;Foresi et al, 2007;Wu and Wu, 2008;Reichler et al, 2009;Tanaka et al, 2010b;Tonón et al, 2010;Clark et al, 2011;Sun et al, 2012;Lim et al, 2014). Some of them are suggested to be mediated by cellular components in the plasma membrane, including Ca 2+ channels, heterotrimeric G Proteins, and NADPH oxidase (Song et al, 2006;Demidchik et al, 2009;Weerasinghe et al, 2009;Tanaka et al, 2010b;Hao et al, 2012;Wang et al, 2014).…”

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Extracellular ATP Acts on Jasmonate Signaling to Reinforce Plant Defense

et al. 2017

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Damaged cells send various signals to stimulate defense responses. Recent identification and genetic studies of the plant purinoceptor, P2K1 (also known as DORN1), have demonstrated that extracellular ATP is a signal involved in plant stress responses, including wounding, perhaps to evoke plant defense. However, it remains largely unknown how extracellular ATP induces plant defense responses. Here, we demonstrate that extracellular ATP induces plant defense mediated through activation of the intracellular signaling of jasmonate (JA), a well-characterized defense hormone. In Arabidopsis (Arabidopsis thaliana) leaves, ATP pretreatment induced resistance against the necrotrophic fungus, Botrytis cinerea. The induced resistance was enhanced in the P2K1 receptor overexpression line, but reduced in the receptor mutant, dorn1-3. Mining the transcriptome data revealed that ATP induces a set of JA-induced genes. In addition, the P2K1-associated coexpression network contains defense-related genes, including those encoding jasmonate ZIM-domain (JAZ) proteins, which play key roles as repressors of JA signaling. We examined whether extracellular ATP impacts the stability of JAZ1 in Arabidopsis. The results showed that the JAZ1 stability decreased in response to ATP addition in a proteasome-dependent manner. This reduction required intracellular signaling via second messengers-cytosolic calcium, reactive oxygen species, and nitric oxide. Interestingly, the ATP-induced JAZ1 degradation was attenuated in the JA receptor mutant, coi1, but not in the JA biosynthesis mutant, aos, or upon addition of JA biosynthesis inhibitors. Immunoprecipitation analysis demonstrated that ATP increases the interaction between COI1 and JAZ1, suggesting direct cross talk between extracellular ATP and JA in intracellular signaling events. Taken together, these results suggest that extracellular ATP signaling directly impacts the JA signaling pathway to maximize plant defense responses.

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Extracellular ATP Signaling Is Mediated by H2O2 and Cytosolic Ca2+ in the Salt Response of Populus euphratica Cells

Cited by 74 publications

References 58 publications

Populus euphratica APYRASE2 Enhances Cold Tolerance by Modulating Vesicular Trafficking and Extracellular ATP in Arabidopsis Plants

Populus euphratica APYRASE2 Enhances Cold Tolerance by Modulating Vesicular Trafficking and Extracellular ATP in Arabidopsis Plants

Extracellular ATP: a potential molecule regulating the defence response of plants to biotic stresses - a review

Extracellular ATP Acts on Jasmonate Signaling to Reinforce Plant Defense

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