The calcium ion (Ca2+) is a universal signal in all eukaryotic cells. A fundamental question is how Ca2+, a simple cation, encodes complex information with high specificity. Extensive research has established a two-step process (encoding and decoding) that governs the specificity of Ca2+ signals. While the encoding mechanism entails a complex array of channels and transporters, the decoding process features a number of Ca2+ sensors and effectors that convert Ca2+ signals into cellular effects. Along this general paradigm, some signalling components may be highly conserved, but others are divergent among different organisms. In plant cells, Ca2+ participates in numerous signalling processes, and here we focus on the latest discoveries on Ca2+-encoding mechanisms in development and biotic interactions. In particular, we use examples such as polarized cell growth of pollen tube and root hair in which tip-focused Ca2+ oscillations specify the signalling events for rapid cell elongation. In plant–microbe interactions, Ca2+ spiking and oscillations hold the key to signalling specificity: while pathogens elicit cytoplasmic spiking, symbiotic microorganisms trigger nuclear Ca2+ oscillations. Herbivore attacks or mechanical wounding can trigger Ca2+ waves traveling a long distance to transmit and convert the local signal to a systemic defence program in the whole plant. What channels and transporters work together to carve out the spatial and temporal patterns of the Ca2+ fluctuations? This question has remained enigmatic for decades until recent studies uncovered Ca2+ channels that orchestrate specific Ca2+ signatures in each of these processes. Future work will further expand the toolkit for Ca2+-encoding mechanisms and place Ca2+ signalling steps into larger signalling networks.
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Berridge, M. J., Lipp, P. & Bootman, M. D. The versatility and universality of calcium signaling. Nat. Rev. Mol. Cell Biol. 1, 11–21 (2000).
Demidchik, V. et al. Calcium transport across plant membranes: mechanisms and functions. New Phytol. 220, 49–69 (2018).
McAinsh, M. R. & Pittman, J. K. Shaping the calcium signature. New Phytol. 181, 275–294 (2009).
Webb, A. A. R., McAinsh, M. R., Taylor, J. E. & Hetherington, A. M. Calcium ions as intracellular second messengers in higher plants. Adv. Bot. Res. 22, 45–96 (1996).
Plieth, C. Calcium, metaphors, and zeitgeist in plant sciences. Plant Physiol. 171, 1790–1793 (2016).
Marcec, M. J., Gilroy, S., Poovaiah, B. W. & Tanaka, K. Mutual interplay of Ca2+ and ROS signaling in plant immune response. Plant Sci. 283, 343–354 (2019).
Tang, R. & Luan, S. Regulation of calcium and magnesium homeostasis in plants: from transporters to signaling network. Curr. Opin. Plant Biol. 39, 97–105 (2017).
Edel, K. H., Marchadier, E., Brownlee, C., Kudla, J. & Hetherington, A. M. The evolution of calcium-based signaling in plants. Curr. Biol. 27, R667–R679 (2017).
DeFalco, T. A., Bender, K. W. & Snedden, W. A. Breaking the code: Ca2+ sensors in plant signaling. Biochem. J. 425, 27–40 (2010).
Zhu, J. Abiotic stress signaling and responses in plants. Cell 167, 313–324 (2016).
Yang, Z. Cell polarity signaling in Arabidopsis. Annu. Rev. Cell Dev. Biol. 24, 551–575 (2008).
Bascom, C. S., Hepler, P. K. & Bezanilla, M. Interplay between ions, the cytoskeleton, and cell wall properties during tip growth. Plant Physiol. 176, 28–40 (2018).
Iwano, M. et al. Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth. Plant Physiol. 150, 1322–1334 (2009).
Hepler, P. K., Kunkel, J. G., Rounds, C. M. & Winship, L. J. Calcium entry into pollen tubes. Trends Plant Sci. 17, 32–38 (2012).
Damineli, D. S., Portes, M. T. & Feijó, J. A. Oscillatory signatures underlie growth regimes in Arabidopsis pollen tubes: computational methods to estimate tip location, periodicity, and synchronization in growing cells. J. Exp. Bot. 68, 3267–3281 (2017).
Konrad, K. R., Wudick, M. M. & Feijó, J. A. Calcium regulation of tip growth: new genes for old mechanisms. Curr. Opin. Plant Biol. 14, 721–730 (2011).
Frietsch, S. et al. A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc. Natl Acad. Sci. USA 104, 14531–14536 (2007).
Tunc-Ozdemir, M. et al. Cyclic nucleotide gated channels 7 and 8 are essential for male reproductive fertility. PLoS ONE 8, e55277 (2013).
Tunc-Ozdemir, M. et al. A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development. Plant Physiol. 161, 1010–1020 (2013).
Pan, Y. et al. Dynamic interactions of plant CNGC subunits and calmodulins drive oscillatory Ca2+ channel activities. Dev. Cell 48, 710–725 (2019).
Gao, Q., Fei, C., Dong, J., Gu, L. & Wang, Y. Arabidopsis CNGC18 is a Ca2+-permeable channel. Mol. Plant 7, 739–743 (2014).
Gao, Q. et al. Cyclic nucleotide-gated channel 18 is an essential Ca2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis. Proc. Natl Acad. Sci. USA 113, 3096–3101 (2016).
Landoni, M., De Francesco, A., Galbiati, M. & Tonelli, C. A loss-of-function mutation in Calmodulin2 gene affects pollen germination in Arabidopsis thaliana. Plant Mol. Biol. 74, 235–247 (2010).
Pina, C., Pinto, F., Feijó, J. A. & Becker, J. D. Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control and gene expression regulation. Plant Physiol. 138, 744–756 (2005).
Michard, E. et al. Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-Serine. Science 332, 434–437 (2011).
Wudick, M. M. et al. CORNICHON sorting and regulation of GLR channels underlie pollen tube Ca2+ homeostasis. Science 360, 533–536 (2018).
Johnson, M. A., Harper, J. F. & Palanivelu, R. A fruitful journey: pollen tube navigation from germination to fertilization. Annu. Rev. Plant Biol. 70, 809–837 (2019).
Monshausen, G. B., Messerli, M. A. & Gilroy, S. Imaging of the Yellow Cameleon 3.6 indicator reveals that elevations in cytosolic Ca2+ follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiol. 147, 1690–1698 (2008).
Kiegle, E., Gilliham, M., Haseloff, J. & Tester, M. Hyperpolarisation-activated calcium currents found only in cells from the elongation zone of Arabidopsis thaliana roots. Plant J. 21, 225–229 (2000).
Véry, A. A. & Davies, J. M. Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs. Proc. Natl Acad. Sci. USA 97, 9801–9806 (2000).
Demidchik, V. et al. Arabidopsis thaliana root non-selective cation channels mediate calcium uptake and are involved in growth. Plant J. 32, 799–808 (2002).
Miedema, H. et al. Two voltage-dependent calcium channels co-exist in the apical plasma membrane of Arabidopsis thaliana root hairs. New Phytol. 179, 378–385 (2008).
Foreman, J. et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446 (2003).
Zhang, S. et al. Arabidopsis CNGC14 mediates calcium influx required for tip growth in root hairs. Mol. Plant 10, 1004–1006 (2017).
Brost, C. et al. Multiple cyclic nucleotide-gated channels coordinate calcium oscillations and polar growth of root hairs. Plant J. 99, 910–923 (2019).
Tan, Y. et al. Three CNGC family members, CNGC5, CNGC6, and CNGC9, are required for constitutive growth of Arabidopsis root hairs as Ca2+-permeable channels. Plant Commun. 1, 100001 (2019).
Zeb, Q. et al. The interaction of CaM7 and CNGC14 regulates root hair growth in Arabidopsis. J. Integr. Plant Biol. https://doi.org/10.1111/jipb.12890 (2019).
Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323 (2006).
Felix, G., Duran, J. D., Volko, S. & Boller, T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265–276 (1999).
Zipfel, C. & Oldroyd, G. Plant signaling in symbiosis and immunity. Nature 543, 328–336 (2017).
Yuan, P., Jauregui, E., Du, L., Tanaka, K. & Poovaiah, B. W. Signatures and signaling events orchestrate plant-microbe interactions. Curr. Opin. Plant Biol. 38, 173–183 (2017).
Kwaaitaal, M., Huisman, R., Maintz, J., Reinstadler, A. & Panstruga, R. Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana. Biochem. J. 440, 355–365 (2011).
Ranf, S., Eschen-Lippold, L., Pecher, P., Lee, J. & Scheel, D. Interplay between calcium signaling and early signaling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J. 68, 100–113 (2011).
Maintz, J. et al. Comparative analysis of MAMP-induced calcium influx in Arabidopsis seedlings and protoplasts. Plant Cell Physiol. 55, 1813–1825 (2014).
Keinath, N. F. et al. Live cell imaging with R-GECO1 sheds light on flg22- and chitin-induced transient [Ca2+]cyt patterns in Arabidopsis. Mol. Plant 8, 1188–1200 (2015).
Tian, W. et al. A calmodulin-gated calcium channel links pathogen patterns to plant immunity. Nature 572, 131–135 (2019).
Yu, I. C., Parker, J. & Bent, A. F. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc. Natl Acad. Sci. USA 95, 7819–7824 (1998).
Clough, S. J. et al. The Arabidopsis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc. Natl Acad. Sci. USA 97, 9323–9328 (2000).
Balagué, C. et al. HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15, 365–379 (2003).
Jurkowski, G. I. et al. Arabidopsis DND2, a second cyclic nucleotide-gated ion channel gene for which mutation causes the “defense, no death” phenotype. Mol. Plant Microbe Interact. 17, 511–520 (2004).
Yoshioka, K. et al. Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis. Plant J. 26, 447–459 (2001).
Yoshioka, K. et al. The chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 activates multiple pathogen resistance responses. Plant Cell 18, 747–763 (2006).
Baxter, J. et al. Identification of a functionally essential amino acid for Arabidopsis cyclic nucleotide gated ion channels using the chimeric AtCNGC11/12 gene. Plant J. 56, 457–469 (2008).
Urquhart, W. et al. The chimeric cyclic nucleotide-gated ion channel ATCNGC11/12 constitutively induces programmed cell death in a Ca2+ dependent manner. Plant Mol. Biol. 65, 747–761 (2007).
Defalco, T. A. et al. Using GCaMP3 to study Ca2+ signaling in Nicotiana species. Plant Cell Physiol. 58, 1173–1184 (2017).
Zhang, Z., Hou, C., Tian, W., Li, L. & Zhu, H. Electrophysiological studies revealed CaM1-mediated regulation of the Arabidopsis calcium channel CNGC12. Front. Plant Sci. 10, 1090 (2019).
Ali, R. et al. Death don’t have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell 19, 1081–1095 (2007).
Ma, Y., Walker, R. K., Zhao, Y. & Berkowitz, G. A. Linking ligand perception by PEPR pattern recognition receptors to cytosolic Ca2+ elevation and downstream immune signaling in plants. Proc. Natl Acad. Sci. USA 109, 19852–19857 (2012).
Wu, F. et al. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 578, 577–581 (2020).
Wang, J. et al. A cyclic nucleotide-gated channel mediates cytoplasmic calcium elevation and disease resistance in rice. Cell Res. 29, 820–831 (2019).
Yu, X. et al. The receptor kinase BAK1/SERK4 regulate Ca2+ channel-mediated cellular homeostasis for cell death containment. Curr. Biol. 29, 1–13 (2019).
Li, F. et al. Glutamate receptor-like channel3.3 is involved in mediating glutathione-triggered cytosolic calcium transients, transcriptional changes, and innate immunity responses in Arabidopsis. Plant Physiol. 162, 1497–1509 (2013).
Manzoor, H. et al. Involvement of the glutamate receptor AtGLR3.3 in plant defense signaling and resistance to Hyaloperonospora arabidopsidis. Plant J. 76, 466–480 (2013).
Hou, S., Liu, Z., Shen, H. & Wu, D. Damage-associated molecular pattern-triggered immunity in plants. Front. Plant Sci. 10, 646 (2019).
Frei dit Frey, N. et al. Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development. Plant Physiol. 159, 798–809 (2012).
Yu, H., Yan, J., Du, X. & Hua, J. Overlapping and differential roles of plasma membrane calcium ATPases in Arabidopsis growth and environmental responses. J. Exp. Bot. 69, 2693–2703 (2018).
Hirschi, K. D., Zhen, R. G., Cunningham, K. W., Rea, P. A. & Fink, G. R. CAX1, an H+/ Ca2+ antiporter from Arabidopsis. Proc. Natl Acad. Sci. USA 93, 8782–8786 (1996).
Cheng, N. H. et al. Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol. 138, 2048–2060 (2005).
Wang, Y. et al. CNGC2 is a Ca2+ influx channel that prevents accumulation of apoplastic Ca2+ in the leaf. Plant Physiol. 173, 1342–1354 (2017).
Wang, B. & Qiu, Y. L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363 (2006).
Heckman, D. S. et al. Molecular evidence for the early colonization of land by fungi and plants. Science 293, 1129–1133 (2001).
Kistner, C. & Parniske, M. Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci. 7, 511–518 (2002).
Svistoonoff, S., Hocher, V. & Gherbi, H. Actinorhizal root nodule symbioses: what is signaling telling on the origins of nodulation? Curr. Opin. Plant Boil. 20, 11–18 (2014).
Martin, F. M., Uroz, S. & Barker, D. G. Ancestral alliances: Plant mutualistic symbioses with fungi and bacteria. Science 356, eaad4501 (2017).
Oldroyd, G. E. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252–263 (2013).
Gherbi, H. et al. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc. Natl Acad. Sci. USA 105, 4928–4932 (2008).
Granqvist, E. et al. Bacterial-induced calcium oscillations are common to nitrogen-fixing associations of nodulating legumes and nonlegumes. New Phytol. 207, 551–558 (2015).
Barker, D. G., Chabaud, M., Russo, G. & Genre, A. Nuclear Ca2+ signalling in arbuscular mycorrhizal and actinorhizal endosymbioses: on the trail of novel underground signals. New Phytol. 214, 533–538 (2017).
Chabaud, M. et al. Chitinase-resistant hydrophilic symbiotic factors secreted by Frankia activate both Ca2+ spiking and NIN gene expression in the actinorhizal plant Casuarina glauca. New Phytol. 209, 86–93 (2016).
Endre, G. et al. A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962–966 (2002).
Stracke, S. et al. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959–962 (2002).
Kevei, Z. et al. 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19, 3974–3989 (2007).
Venkateshwaran, M. et al. A role for the mevalonate pathway in early plant symbiotic signaling. Proc. Natl Acad. Sci. USA 112, 9781–9786 (2015).
Ane, J. M. et al. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364–1367 (2004).
Imaizumi-Anraku, H. et al. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433, 527–531 (2005).
Charpentier, M. et al. Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20, 3467–3479 (2008).
Charpentier, M. et al. Nuclear-localized cyclic nucleotide-gated channels mediate symbiotic calcium oscillations. Science 352, 1102–1105 (2016).
Capoen, W. et al. Nuclear membranes control symbiotic calcium signaling of legumes. Proc. Natl Acad. Sci. USA 108, 14348–14353 (2011).
Peiter, E. et al. The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol. 145, 192–203 (2007).
Granqvist, E. et al. Buffering capacity explains signal variation in symbiotic calcium oscillations. Plant Physiol. 160, 2300–2310 (2012).
Kim, S. et al. Ca2+-regulated Ca2+ channels with an RCK gating ring control plant symbiotic associations. Nature Commun. 10, 3703 (2019).
Levy, J. et al. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361–1364 (2004).
Gleason, C. et al. Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441, 1149–1152 (2006).
Tirichine, L. et al. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441, 1153–1156 (2006).
Yano, K. et al. CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl Acad. Sci. USA 105, 20540–20545 (2008).
Ovchinnikova, E. et al. IPD3 controls the formation of nitrogen-fixing symbiosomes in pea and Medicago Spp. Mol. Plant Microbe Interact. 24, 1333–1344 (2011).
Singh, S., Katzer, K., Lambert, J., Cerri, M. & Parniske, M. CYCLOPS, A DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 15, 139–152 (2014).
Pimprikar, P. et al. A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching. Curr. Biol. 26, 987–998 (2016).
Groth, M. et al. NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22, 2509–2526 (2010).
Kanamori, N. et al. A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc. Natl Acad. Sci. USA 103, 359–364 (2006).
Saito, K. et al. NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19, 610–624 (2007).
Zuleger, N., Korfali, N. & Schirmer, E. C. Inner nuclear membrane protein transport is mediated by multiple mechanisms. Biochem. Soc. Trans. 36, 1373–1377 (2008).
Shaw, S. L. & Long, S. R. Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiol. 131, 976–984 (2003).
Miwa, H., Sun, J., Oldroyd, G. E. & Downie, J. A. Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol. Plant Microbe Interact. 19, 914–923 (2006).
Seidl, A. H. Regulation of conduction time along axons. Neuroscience 276, 126–134 (2014).
Hilleary, R. & Gilroy, S. Systemic signaling in response to wounding and pathogens. Curr. Opin. Plant Biol. 43, 57–62 (2018).
Yan, C. et al. Injury activates Ca2+/calmodulin-dependent phosphorylation of JAV1-JAZ8-WRKY51 complex for jasmonate biosynthesis. Mol. Cell 70, 136–149 (2018).
Toyota, M. et al. Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361, 1112–1115 (2018).
Mousavi, S. A., Chauvin, A., Pascaud, F., Kellenberger, S. & Farmer, E. E. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signaling. Nature 500, 422–426 (2013).
Nguyen, C. T., Kurenda, A., Stolz, S., Chételat, A. & Farmer, E. E. Identification of cell populations necessary for leaf-to-leaf electrical signaling in a wounded plant. Proc. Natl Acad. Sci. USA 115, 10178–10183 (2018).
Kumari, A., Chételat, A., Nguyen, C. T. & Farmer, E. E. Arabidopsis H+-ATPase AHA1 controls slow wave potential duration and wound-response jasmonate pathway activation. Proc. Natl Acad. Sci. USA 116, 20226–20231 (2019).
Shao, Q., Gao, Q, Lhamo, D., Zhang, H. & Luan, S. Two glutamate- and pH-regulated calcium channels required for systemic wound signaling in Arabidopsis. Sci. Signal. (in the press).
Meena, M. K. et al. Cyclic nucleotide gated channel 19 (CNGC19) is an important Ca2+ channel regulating Arabidopsis defense against Spodoptera herbivory. Plant Cell 31, 1539–1562 (2019).
Vincent, T. R. et al. Interplay of plasma membrane and vacuolar ion channels, together with BAK1, elicits rapid cytosolic calcium elevations in Arabidopsis during aphid feeding. Plant Cell 29, 1460–1479 (2017).
Gilroy, S. et al. ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol. 171, 1606–1615 (2016).
Kaupp, U. B. & Seifert, R. Cyclic nucleotide-gated ion channels. Physiol. Rev. 82, 769–824 (2002).
Traynelis, S. F. et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405–496 (2010).
Vincill, E. D., Clarin, A. E., Molenda, J. N. & Spalding, E. P. Interacting glutamate receptor-like proteins in phloem regulate lateral root initiation. Plant Cell 25, 1304–1313 (2013).
Hou, C. et al. DUF221 proteins are a family of osmosensitive calcium permeable cation channels conserved across eukaryotes. Cell Res. 24, 632–635 (2014).
Yuan, F. et al. OSCA1 mediates osmotic stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514, 367–371 (2014).
Leng, Q., Mercier, R. W., Hua, B.-G., Fromm, H. & Berkowitz, G. A. Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels. Plant Physiol. 128, 400–410 (2002).
Ma, W. et al. Ca2+, cAMP, and transduction of non-self perception during plant immune responses. Proc. Natl Acad. Sci. USA 106, 20995–21000 (2009).
Chin, K., DeFalco, T. A., Moeder, W. & Yoshioka, K. The Arabidopsis cyclic nucleotide-gated ion channels AtCNGC2 and AtCNGC4 work in the same signaling pathway to regulate pathogen defense and floral transition. Plant Physiol. 163, 611–624 (2013).
DeFalco, T. A., Moeder, W. & Yoshioka, K. Opening the gates: insights into cyclic nucleotide-gated channel-mediated signaling. Trends Plant Sci. 21, 903–906 (2016).
Qi, Z., Stephens, N. R. & Spalding, E. P. Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiol. 142, 963–971 (2006).
Stephens, N. R., Qi, Z. & Spalding, E. P. Glutamate receptor subtypes evidenced by differences in desensitization and dependence on the GLR3.3 and GLR3.4 genes. Plant Physiol. 146, 529–538 (2008).
Roy, S. J. et al. Investigating glutamate receptor-like gene co-expression in Arabidopsis thaliana. Plant Cell Environ. 31, 861–871 (2008).
Vincill, E. D., Bieck, A. M. & Spalding, E. P. Ca2+ conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiol. 159, 40–46 (2012).
Tapken, D. et al. A plant homolog of animal glutamate receptors is an ion channel gated by multiple hydrophobic amino acids. Sci. Signal. 6, ra47 (2013).
Ortiz-ramírez, C. et al. Glutamate receptor-like channels are essential for chemotaxis and reproduction in mosses. Nature 549, 91–95 (2017).
Alfieri, A. et al. The structural bases for agonist diversity in an Arabidopsis thaliana glutamate receptor-like channel. Proc. Natl Acad. Sci. USA 117, 752–760 (2020).
Yu, F., Tian, W. & Luan, S. From receptor-like kinases to calcium spikes: what are the missing links? Mol. Plant 7, 1501–1504 (2014).
Choi, J. et al. Identification of a plant receptor for extracellular ATP. Science 343, 290–294 (2014).
Chen, D. et al. Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture. Nat. Commun. 8, 2265 (2017).
Haruta, M., Sabat, G., Stecker, K., Minkoff, B. B. & Sussman, M. R. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343, 408–411 (2014).
Research in authors’ laboratories is supported by National Key Research and Development Program of China (grant YFD0300102-3 to L.L.), National Natural Science Foundation of China (grants 31930010 and 31872170 to L.L.), the National Science Foundation (grant 1714795 to S.L.), and a grant from the Innovative Genomics Institute of California (to S.L.). C.W. is supported by Tang Distinguished Scholarship, University of California at Berkeley.
The authors declare no competing interests.
Peer review information Nature Plants thanks Jean-Philippe Galaud, Kiwamu Tanaka and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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Tian, W., Wang, C., Gao, Q. et al. Calcium spikes, waves and oscillations in plant development and biotic interactions. Nat. Plants 6, 750–759 (2020). https://doi.org/10.1038/s41477-020-0667-6
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