<i>Arabidopsis thaliana</i> CYCLIC NUCLEOTIDE‐GATED CHANNEL2 mediates extracellular ATP signal transduction in root epidermis

Wang, Limin; Ning, Youzheng; Sun, Jian; Wilkins, Katie A.; Matthus, Elsa; McNelly, Rose E.; Dark, Adeeba; Rubio, Lourdes; Moeder, Wolfgang; Yoshioka, Keiko; Véry, Anne‐Aliénor; Stacey, Gary; Leblanc‐Fournier, Nathalie; Legué, Valérie; Moulia, Bruno; Davies, Julia M.

doi:10.1111/nph.17987

Cited by 19 publications

(19 citation statements)

References 33 publications

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“…As induced above, the potential biological effects or functions of exATP can be revealed by exogenous application of ATP [ 7 , 13 ]. For example, the elevation of cytosolic free calcium ([Ca 2+ ] cyt ) level is usually used as the indicator of the exATP-induced response [ 46 ]. Tanaka et al [ 47 ] revealed that the concentrations of exogenous ATP as higher as 100 μM can trigger the elevation of [Ca 2+ ] cyt level in Arabidopsis seedlings.…”

Section: Discussionmentioning

confidence: 99%

The involvement of extracellular ATP in regulating the stunted growth of Arabidopsis plants by repeated wounding

et al. 2022

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Background Extracellular ATP (exATP) has been shown to act as a signal molecule for regulating growth, development, and responses of plants to the external environment. Results In this study, we investigated the possible involvement of exATP in regulating the stunted growth caused by repeated wounding. The present work showed that the repeated wounding caused the decreases in leaf area, fresh weight, dry weight, and root length of Arabidopsis seedlings, while the exATP level was enhanced by the repeated wounding. Repeated application of exogenous ATP had similar effects on the plant growth, as the repeated wounding. Through the comparison of p2k1-3 mutant (in which T-DNA disrupted the gene coding P2K1, as exATP receptor) and wide type (WT) plants, it was found that the mutation in P2K1 decreased the sensitivity of plant growth to the repeated wounding and exogenous ATP application. Further works showed that the ibuprofen (IBU, an inhibitor of jasmonate biosynthesis) partially rescued the wound-induced growth degradation. In comparison, the P2K1 mutation partly rescued the wound-induced growth degradation, whereas this mutation failed to do so in the wounded seedlings treated with IBU, indicating that the role of exATP in regulating the growth degradation by repeated wounding could be linked to the JA signaling pathway. Conclusions In conclusion, these results indicate that exATP could be a regulator for the stunted growth of plants by repeated wounding.

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Section: Discussionmentioning

confidence: 99%

The involvement of extracellular ATP in regulating the stunted growth of Arabidopsis plants by repeated wounding

et al. 2022

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“…CNGC14 has been tested in Pi-replete conditions and found not to be involved (Shih et al 2015). However, CNGC2, CNGC4 and CNGC6 have since been shown to contribute to the root eATP-induced [Ca 2+ ] cyt elevation in Pi-replete conditions (Duong et al 2022;Wang et al 2022). Among the Glutamate Receptor-Like family (GLR), GLR3.3 and GLR3.6 are involved in leaf wounding and signal propagation (Vincent et al 2017).…”

Section: Discussionmentioning

confidence: 99%

Spatial origin of the extracellular ATP‐induced cytosolic calcium signature in Arabidopsis thaliana roots: wave formation and variation with phosphate nutrition

et al. 2022

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Extracellular ATP (eATP) increases cytosolic free calcium ([Ca 2+ ] cyt ) as a specific second messenger 'signature' through the plasma membrane DORN1/P2K1 receptor. Previous studies revealed a biphasic signature in Arabidopsis thaliana roots that is altered by inorganic phosphate (Pi) deprivation. The relationship between the two phases of the signature and possible wave formation have been tested as a function of Pi nutrition.• The bioluminescent aequorin and intensiometric GCaMP3 reporters were used to resolve the spatial origin of the eATP [Ca 2+ ] cyt signature in Arabidopsis root tips. Application of eATP only to the root apex allowed [Ca 2+ ] cyt wave resolution without the confounding effects of eATP delivery by superfusion.• The first apical millimetre of the root generates the first [Ca 2+ ] cyt increase by eATP, regardless of nutritional status. The second increase occurs sub-apically in the root hair zone, has some autonomy and is significantly reduced in Pi-starved roots. A significant component of the Pi-replete signature does not require DORN1/P2K1, but Pi-starved roots appear to have an absolute requirement for that receptor. Application of eATP specifically to the root apex provides evidence for cell-to-cell propagation of a [Ca 2+ ] cyt wave that diminishes sub-apically.• The apex maintains a robust [Ca 2+ ] cyt increase (even under Pi starvation) that is the basis of a propagative wave, with implications for the ability of the root's eATP signalling systems to signal systemically. Partial autonomy of the sub-apical region may be relevant to the perception of eATP from microbes. eATP-induced [Ca 2+ ] cyt increase may not have always have an obligate requirement for DORN1/P2K1.

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“…Another CNGC, CNGC6, may also be involved in the root’s response ( Duong et al., 2022 ). CNGC2 is also part of the eATP pathway in cotyledons and pollen grain ( Sun et al., 2021 ; Wu et al., 2021 ), although its involvement in roots appears restricted to the epidermis ( Wang et al., 2022a ). CNGC2 may form a connection with PAMP-triggered immunity as it can also operate in flg22 signalling ( Tian et al., 2019 ) and it also works in Jasmonic Acid signalling ( Lu et al., 2016 ).…”

Section: Eatp Signalling Intersects With Multiple Pathwaysmentioning

confidence: 99%

Phosphate-deprivation and damage signalling by extracellular ATP

et al. 2023

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Phosphate deprivation compromises plant productivity and modulates immunity. DAMP signalling by extracellular ATP (eATP) could be compromised under phosphate deprivation by the lowered production of cytosolic ATP and the need to salvage eATP as a nutritional phosphate source. Phosphate-starved roots of Arabidopsis can still sense eATP, indicating robustness in receptor function. However, the resultant cytosolic free Ca2+ signature is impaired, indicating modulation of downstream components. This perspective on DAMP signalling by extracellular ATP (eATP) addresses the salvage of eATP under phosphate deprivation and its promotion of immunity, how Ca2+ signals are generated and how the Ca2+ signalling pathway could be overcome to allow beneficial fungal root colonization to fulfill phosphate demands. Safe passage for an endophytic fungus allowing root colonization could be achieved by its down-regulation of the Ca2+ channels that act downstream of the eATP receptors and by also preventing ROS accumulation, thus further impairing DAMP signalling.

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Arabidopsis thaliana CYCLIC NUCLEOTIDE‐GATED CHANNEL2 mediates extracellular ATP signal transduction in root epidermis

Cited by 19 publications

References 33 publications

The involvement of extracellular ATP in regulating the stunted growth of Arabidopsis plants by repeated wounding

The involvement of extracellular ATP in regulating the stunted growth of Arabidopsis plants by repeated wounding

Spatial origin of the extracellular ATP‐induced cytosolic calcium signature in Arabidopsis thaliana roots: wave formation and variation with phosphate nutrition

Phosphate-deprivation and damage signalling by extracellular ATP

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