Damage Signaling by Extracellular Nucleotides: A Role for Cyclic Nucleotides in Elevating Cytosolic Free Calcium?

Abstract

Extracellular ATP (eATP) is now held to be a constitutive damage-associated molecular pattern (DAMP) that is released by wounding, herbivory or pathogen attack. The concentration of eATP must be tightly regulated as either depletion or overload leads to cell death. In Arabidopsis thaliana, sensing of eATP is by two plasma membrane legume-like lectin serine–threonine receptor kinases (P2K1 and P2K2), although other receptors are postulated. The transcriptional response to eATP is dominated by wound- and defense-response genes. Wounding and pathogen attack can involve the cyclic nucleotides cyclic AMP (cAMP) and cyclic GMP (cGMP) which, in common with eATP, can increase cytosolic-free Ca2+ as a second messenger. This perspective on DAMP signaling by eATP considers the possibility that the eATP pathway involves production of cyclic nucleotides to promote opening of cyclic nucleotide-gated channels and so elevates cytosolic-free Ca2+. In silico analysis of P2K1 and P2K2 reveals putative adenylyl and guanylyl kinase sequences that are the hallmarks of “moonlighting” receptors capable of cAMP and cGMP production. Further, an Arabidopsis loss of function cngc mutant was found to have an impaired increase in cytosolic-free Ca2+ in response to eATP. A link between eATP, cyclic nucleotides, and Ca2+ signaling therefore appears credible.

Calcium-Mobilizing Properties of Salvia miltiorrhiza-Derived Carbon Dots Confer Enhanced Environmental Adaptability in Plants

“…LecRK-I.9 (DORN1/P2K1) and LecRK-I.5 (P2K2), two LecRKs that function as extracellular ATP receptors in Arabidopsis, may harbor AC/GC domains and generate cNMPs to activate CNGCs. 59 The conserved sequence that confers GC function was also found in LORE and LecRK-I.8 (Figure S18). Therefore, LORE and LecRK-I.8 may perceive CDs at the extracellular lectin domain and then activate their own GC activity to produce cGMP for CNGC stimulation.…”

“…These results indicated that plant LecRKs might be the receptors of CDs for activating Ca 2+ influx via CNGCs. LecRK-I.9 (DORN1/P2K1) and LecRK-I.5 (P2K2), two LecRKs that function as extracellular ATP receptors in Arabidopsis , may harbor AC/GC domains and generate cNMPs to activate CNGCs . The conserved sequence that confers GC function was also found in LORE and LecRK-I.8 (Figure S18).…”

Advances in chilling injury of postharvest fruit and vegetable: Extracellular ATP aspects

“…Additionally, H 2 S could evoke the endothelial NO synthase, then attenuate the cGMP degradation, and, finally, act as a modulator of the NO‐cGMP pathway (Bełtowski & Jamroz‐Wis̈niewska, 2014). Although eATP could enhance the synthesis of cGMP as an important second messenger (Sun et al., 2021b), it is still unclear about the role of the eATP to induce DAMP signaling pathway under cold temperature stress in plants. It is interesting to note that phytosulfokine (PSK) perception by tomato plasma membrane PSK receptor 1 (PSKR1) elevated cytosolic [Ca 2+ ] cyt to enhance plant immunity against B. cinerae (Yu et al., 2016).…”

“…It is interesting to note that phytosulfokine (PSK) perception by tomato plasma membrane PSK receptor 1 (PSKR1) elevated cytosolic [Ca 2+ ] cyt to enhance plant immunity against B. cinerae (Yu et al., 2016). Increasing [Ca 2+ ] cyt triggered by eATP signaling inhibited kinase activity of Arabidopsis PSK1 (Sun et al., 2021b). The addition of PSK1 enhanced chilling tolerance of loquat fruit during low‐temperature storage by maintaining iATP homeostasis (Song et al., 2017), while exogenous phytosulfokine α (PSKα) alleviated the CI of banana by modulating NO metabolism (Wang et al., 2022).…”

New Horizons in Plant Cell Signaling

“…One such signaling molecule is the cyclic mononucleotide phosphodiesterases (PDEs), which, together with nucleotide cyclases, regulate the cellular concentrations of the second messengers, cyclic nucleotide monophosphates (cNMPs), cAMP and cGMP. While well-defined in bacteria, yeast and animals, the components of cNMP signaling pathways in plants are still poorly characterized [ 22 , 23 , 24 , 25 , 26 ]. The use of manually curated amino acid motifs based only on the catalytic centers of the corresponding enzymes in organisms across species have enabled the identification and concomitantly also the characterization of several novel adenylate cyclases (ACs) and guanylate cyclases (GCs) [ 27 , 28 ].…”