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1. Jasmonate Primes Plant Responses to Extracellular ATP

   https://doi.org/10.1101/2024.11.07.622526  

   Jewell, Jeremy B; Carlton, Ashleigh S; Tolley, Jordan P; Bartley, Laura E; Tanaka, Kiwamu (September 2025, The Plant Journal)

   Extracellular ATP (eATP) signaling inArabidopsis thalianais mediated by the purinoceptor P2K1. Previous studies have clarified that the downstream transcriptional responses to eATP involve jasmonate (JA)-based signaling components such as the JA receptor (COI1) and JA-responsive bHLH transcription factors (MYCs). However, the specific contributions of JA signaling itself on eATP signaling are unexplored. Here, we report that JA primes plant responses to eATP through P2K1. Our findings show that JA treatment significantly upregulatesP2K1transcription, corroborating our observation that JA facilitates eATP-induced cytosolic calcium elevation and transcriptional reprogramming in a JA signaling-dependent manner. Additionally, we find that salicylic acid pretreatment represses eATP-induced plant response. These results suggest that JA accumulation during biotic or abiotic stresses may potentiate eATP signaling, enabling plants to better cope with subsequent stress events. Plant hormone jasmonate (JA) enhances plant responses to extracellular ATP (eATP) inArabidopsis thalianathrough a mechanism dependent on the JA receptor COI1 and the eATP receptor P2K1. The reciprocal amplification of these signals provides a mechanistic explanation for how plants effectively respond to different stress events. 

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2. CamelliA-based simultaneous imaging of Ca2+ dynamics in subcellular compartments

   https://doi.org/10.1093/plphys/kiac020  

   Guo, Jingzhe; He, Jiangman; Dehesh, Katayoon; Cui, Xinping; Yang, Zhenbiao (February 2022, Plant Physiology)

   Abstract As a universal second messenger, calcium (Ca2+) transmits specific cellular signals via a spatiotemporal signature generated from its extracellular source and internal stores. Our knowledge of the mechanisms underlying the generation of a Ca2+ signature is hampered by limited tools for simultaneously monitoring dynamic Ca2+ levels in multiple subcellular compartments. To overcome the limitation and to further improve spatiotemporal resolutions, we have assembled a molecular toolset (CamelliA lines) in Arabidopsis (Arabidopsis thaliana) that enables simultaneous and high-resolution monitoring of Ca2+ dynamics in multiple subcellular compartments through imaging different single-colored genetically encoded calcium indicators. We uncovered several Ca2+ signatures in three types of Arabidopsis cells in response to internal and external cues, including rapid oscillations of cytosolic Ca2+ and apical plasma membrane Ca2+ influx in fast-growing Arabidopsis pollen tubes, the spatiotemporal relationship of Ca2+ dynamics in four subcellular compartments of root epidermal cells challenged with salt, and a shockwave-like Ca2+ wave propagating in laser-wounded leaf epidermis. These observations serve as a testimony to the wide applicability of the CamelliA lines for elucidating the subcellular sources contributing to the Ca2+ signatures in plants. 

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3. Extracellular ATP plays an important role in systemic wound response activation

   https://doi.org/10.1093/plphys/kiac148  

   Myers, Jr, Ronald J.; Fichman, Yosef; Stacey, Gary; Mittler, Ron (March 2022, Plant Physiology)

   Abstract Mechanical wounding occurs in plants during biotic or abiotic stresses and is associated with the activation of long-distance signaling pathways that trigger wound responses in systemic tissues. Among the different systemic signals activated by wounding are electric signals, calcium, hydraulic, and reactive oxygen species (ROS) waves. The release of glutamate (Glu) from cells at the wounded tissues was recently proposed to trigger systemic signal transduction pathways via GLU-LIKE RECEPTORs (GLRs). However, the role of another important compound released from cells during wounding (extracellular ATP [eATP]) in triggering systemic responses is not clear. Here, we show in Arabidopsis (Arabidopsis thaliana) that wounding results in the accumulation of nanomolar levels of eATP and that these levels are sufficient to trigger the systemic ROS wave. We further show that the triggering of the ROS wave by eATP during wounding requires the PURINORECEPTOR 2 KINASE (P2K) receptor. Application of eATP to unwounded leaves triggered the ROS wave, and the activation of the ROS wave by wounding or eATP application was suppressed in mutants deficient in P2Ks (e.g. p2k1-3, p2k2, and p2k1-3p2k2). In addition, expression of systemic wound response (SWR) transcripts was suppressed in mutants deficient in P2Ks during wounding. Interestingly, the effect of Glu and eATP application on ROS wave activation was not additive, suggesting that these two compounds function in the same pathway to trigger the ROS wave. Our findings reveal that in addition to sensing Glu via GLRs, eATP sensed by P2Ks plays a key role in the triggering of SWRs in plants. 

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

   https://doi.org/10.1111/nph.17987  

   Wang, Limin; Ning, Youzheng; Sun, Jian; Wilkins, Katie A.; Matthus, Elsa; McNelly, Rose E.; Dark, Adeeba; Rubio, Lourdes; Moeder, Wolfgang; Yoshioka, Keiko; et al (February 2022, New Phytologist)

   Summary Damage can be signalled by extracellular ATP (eATP) using plasma membrane (PM) receptors to effect cytosolic free calcium ion ([Ca²⁺]_cyt) increase as a second messenger. The downstream PM Ca²⁺channels remain enigmatic. Here, theArabidopsis thalianaCa²⁺channel subunit CYCLIC NUCLEOTIDE‐GATED CHANNEL2 (CNGC2) was identified as a critical component linking eATP receptors to downstream [Ca²⁺]_cytsignalling in roots.Extracellular ATP‐induced changes in single epidermal cell PM voltage and conductance were measured electrophysiologically, changes in root [Ca²⁺]_cytwere measured with aequorin, and root transcriptional changes were determined by quantitative real‐time PCR. Twocngc2loss‐of‐function mutants were used:cngc2‐3anddefence not death1(which expresses cytosolic aequorin).Extracellular ATP‐induced transient depolarization of Arabidopsis root elongation zone epidermal PM voltage was Ca²⁺dependent, requiring CNGC2 but not CNGC4 (its channel co‐subunit in immunity signalling). Activation of PM Ca²⁺influx currents also required CNGC2. The eATP‐induced [Ca²⁺]_cytincrease and transcriptional response incngc2roots were significantly impaired.CYCLIC NUCLEOTIDE‐GATED CHANNEL2 is required for eATP‐induced epidermal Ca²⁺influx, causing depolarization leading to [Ca²⁺]_cytincrease and damage‐related transcriptional response. 

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5. Activation of the plant mevalonate pathway by extracellular ATP

   https://doi.org/10.1038/s41467-022-28150-w  

   Cho, Sung-Hwan; Tóth, Katalin; Kim, Daewon; Vo, Phuc H.; Lin, Chung-Ho; Handakumbura, Pubudu P.; Ubach, Albert Rivas; Evans, Sterling; Paša-Tolić, Ljiljana; Stacey, Gary (December 2022, Nature Communications)

   Abstract The mevalonate pathway plays a critical role in multiple cellular processes in both animals and plants. In plants, the products of this pathway impact growth and development, as well as the response to environmental stress. A forward genetic screen of Arabidopsis thaliana using Ca 2+ -imaging identified mevalonate kinase (MVK) as a critical component of plant purinergic signaling. MVK interacts directly with the plant extracellular ATP (eATP) receptor P2K1 and is phosphorylated by P2K1 in response to eATP. Mutation of P2K1-mediated phosphorylation sites in MVK eliminates the ATP-induced cytoplasmic calcium response, MVK enzymatic activity, and suppresses pathogen defense. The data demonstrate that the plasma membrane associated P2K1 directly impacts plant cellular metabolism by phosphorylation of MVK, a key enzyme in the mevalonate pathway. The results underline the importance of purinergic signaling in plants and the ability of eATP to influence the activity of a key metabolite pathway with global effects on plant metabolism. 

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