Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Calcium spikes, waves and oscillations in plant development and biotic interactions

Abstract

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1: Ca2+ channels required for tip growth of pollen tubes and root hairs.
Fig. 2: Plasma membrane Ca2+ channels encode PAMP-triggered Ca2+ spikes.
Fig. 3: Ca2+ channels and a Ca2+ pump coordinate to encode the nuclear Ca2+ oscillation for symbiosis.

References

  1. Berridge, M. J., Lipp, P. & Bootman, M. D. The versatility and universality of calcium signaling. Nat. Rev. Mol. Cell Biol. 1, 11–21 (2000).

    CAS  PubMed  Google Scholar 

  2. Demidchik, V. et al. Calcium transport across plant membranes: mechanisms and functions. New Phytol. 220, 49–69 (2018).

    CAS  PubMed  Google Scholar 

  3. McAinsh, M. R. & Pittman, J. K. Shaping the calcium signature. New Phytol. 181, 275–294 (2009).

    CAS  PubMed  Google Scholar 

  4. 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).

    CAS  Google Scholar 

  5. Plieth, C. Calcium, metaphors, and zeitgeist in plant sciences. Plant Physiol. 171, 1790–1793 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 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).

    CAS  PubMed  Google Scholar 

  7. 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).

    CAS  PubMed  Google Scholar 

  8. 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).

    CAS  PubMed  Google Scholar 

  9. DeFalco, T. A., Bender, K. W. & Snedden, W. A. Breaking the code: Ca2+ sensors in plant signaling. Biochem. J. 425, 27–40 (2010).

    CAS  Google Scholar 

  10. Zhu, J. Abiotic stress signaling and responses in plants. Cell 167, 313–324 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Yang, Z. Cell polarity signaling in Arabidopsis. Annu. Rev. Cell Dev. Biol. 24, 551–575 (2008).

    PubMed  PubMed Central  Google Scholar 

  12. 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).

    CAS  PubMed  Google Scholar 

  13. Iwano, M. et al. Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth. Plant Physiol. 150, 1322–1334 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Hepler, P. K., Kunkel, J. G., Rounds, C. M. & Winship, L. J. Calcium entry into pollen tubes. Trends Plant Sci. 17, 32–38 (2012).

    CAS  PubMed  Google Scholar 

  15. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 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).

    CAS  PubMed  Google Scholar 

  17. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Tunc-Ozdemir, M. et al. Cyclic nucleotide gated channels 7 and 8 are essential for male reproductive fertility. PLoS ONE 8, e55277 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 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).

    CAS  PubMed  Google Scholar 

  20. Pan, Y. et al. Dynamic interactions of plant CNGC subunits and calmodulins drive oscillatory Ca2+ channel activities. Dev. Cell 48, 710–725 (2019).

    CAS  PubMed  Google Scholar 

  21. Gao, Q., Fei, C., Dong, J., Gu, L. & Wang, Y. Arabidopsis CNGC18 is a Ca2+-permeable channel. Mol. Plant 7, 739–743 (2014).

    CAS  PubMed  Google Scholar 

  22. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 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).

    CAS  PubMed  Google Scholar 

  24. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 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).

    CAS  PubMed  Google Scholar 

  26. Wudick, M. M. et al. CORNICHON sorting and regulation of GLR channels underlie pollen tube Ca2+ homeostasis. Science 360, 533–536 (2018).

    CAS  PubMed  Google Scholar 

  27. 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).

    CAS  PubMed  Google Scholar 

  28. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 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).

    CAS  PubMed  Google Scholar 

  30. 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).

    PubMed  PubMed Central  Google Scholar 

  31. 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).

    CAS  PubMed  Google Scholar 

  32. 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).

    CAS  PubMed  Google Scholar 

  33. Foreman, J. et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446 (2003).

    CAS  PubMed  Google Scholar 

  34. Zhang, S. et al. Arabidopsis CNGC14 mediates calcium influx required for tip growth in root hairs. Mol. Plant 10, 1004–1006 (2017).

    CAS  PubMed  Google Scholar 

  35. Brost, C. et al. Multiple cyclic nucleotide-gated channels coordinate calcium oscillations and polar growth of root hairs. Plant J. 99, 910–923 (2019).

    CAS  PubMed  Google Scholar 

  36. 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).

    PubMed  PubMed Central  Google Scholar 

  37. 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).

  38. Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323 (2006).

    CAS  PubMed  Google Scholar 

  39. 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).

    CAS  PubMed  Google Scholar 

  40. Zipfel, C. & Oldroyd, G. Plant signaling in symbiosis and immunity. Nature 543, 328–336 (2017).

    CAS  PubMed  Google Scholar 

  41. 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).

    CAS  PubMed  Google Scholar 

  42. 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).

    CAS  PubMed  Google Scholar 

  43. 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).

    CAS  PubMed  Google Scholar 

  44. Maintz, J. et al. Comparative analysis of MAMP-induced calcium influx in Arabidopsis seedlings and protoplasts. Plant Cell Physiol. 55, 1813–1825 (2014).

    CAS  PubMed  Google Scholar 

  45. 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).

    CAS  PubMed  Google Scholar 

  46. Tian, W. et al. A calmodulin-gated calcium channel links pathogen patterns to plant immunity. Nature 572, 131–135 (2019).

    CAS  PubMed  Google Scholar 

  47. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 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).

    PubMed  PubMed Central  Google Scholar 

  50. 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).

    CAS  PubMed  Google Scholar 

  51. Yoshioka, K. et al. Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis. Plant J. 26, 447–459 (2001).

    CAS  PubMed  Google Scholar 

  52. Yoshioka, K. et al. The chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 activates multiple pathogen resistance responses. Plant Cell 18, 747–763 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. 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).

    CAS  PubMed  Google Scholar 

  54. 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).

    CAS  PubMed  Google Scholar 

  55. Defalco, T. A. et al. Using GCaMP3 to study Ca2+ signaling in Nicotiana species. Plant Cell Physiol. 58, 1173–1184 (2017).

    CAS  PubMed  Google Scholar 

  56. 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).

    PubMed  PubMed Central  Google Scholar 

  57. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Wu, F. et al. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 578, 577–581 (2020).

    CAS  PubMed  Google Scholar 

  60. Wang, J. et al. A cyclic nucleotide-gated channel mediates cytoplasmic calcium elevation and disease resistance in rice. Cell Res. 29, 820–831 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 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).

    Google Scholar 

  62. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. 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).

    CAS  PubMed  Google Scholar 

  64. Hou, S., Liu, Z., Shen, H. & Wu, D. Damage-associated molecular pattern-triggered immunity in plants. Front. Plant Sci. 10, 646 (2019).

    PubMed  PubMed Central  Google Scholar 

  65. 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).

  66. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 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).

    CAS  PubMed  Google Scholar 

  70. Wang, B. & Qiu, Y. L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363 (2006).

    CAS  PubMed  Google Scholar 

  71. Heckman, D. S. et al. Molecular evidence for the early colonization of land by fungi and plants. Science 293, 1129–1133 (2001).

    CAS  PubMed  Google Scholar 

  72. Kistner, C. & Parniske, M. Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci. 7, 511–518 (2002).

    CAS  PubMed  Google Scholar 

  73. 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).

    Google Scholar 

  74. Martin, F. M., Uroz, S. & Barker, D. G. Ancestral alliances: Plant mutualistic symbioses with fungi and bacteria. Science 356, eaad4501 (2017).

    PubMed  Google Scholar 

  75. Oldroyd, G. E. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252–263 (2013).

    CAS  PubMed  Google Scholar 

  76. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. 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).

    CAS  PubMed  Google Scholar 

  79. 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).

    CAS  PubMed  Google Scholar 

  80. Endre, G. et al. A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962–966 (2002).

    CAS  PubMed  Google Scholar 

  81. Stracke, S. et al. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959–962 (2002).

    CAS  PubMed  Google Scholar 

  82. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Venkateshwaran, M. et al. A role for the mevalonate pathway in early plant symbiotic signaling. Proc. Natl Acad. Sci. USA 112, 9781–9786 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Ane, J. M. et al. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364–1367 (2004).

  85. Imaizumi-Anraku, H. et al. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433, 527–531 (2005).

    CAS  PubMed  Google Scholar 

  86. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Charpentier, M. et al. Nuclear-localized cyclic nucleotide-gated channels mediate symbiotic calcium oscillations. Science 352, 1102–1105 (2016).

    CAS  PubMed  Google Scholar 

  88. Capoen, W. et al. Nuclear membranes control symbiotic calcium signaling of legumes. Proc. Natl Acad. Sci. USA 108, 14348–14353 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Peiter, E. et al. The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol. 145, 192–203 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Granqvist, E. et al. Buffering capacity explains signal variation in symbiotic calcium oscillations. Plant Physiol. 160, 2300–2310 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Kim, S. et al. Ca2+-regulated Ca2+ channels with an RCK gating ring control plant symbiotic associations. Nature Commun. 10, 3703 (2019).

    Google Scholar 

  92. Levy, J. et al. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361–1364 (2004).

    CAS  PubMed  Google Scholar 

  93. Gleason, C. et al. Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441, 1149–1152 (2006).

    CAS  PubMed  Google Scholar 

  94. Tirichine, L. et al. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441, 1153–1156 (2006).

    CAS  PubMed  Google Scholar 

  95. Yano, K. et al. CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl Acad. Sci. USA 105, 20540–20545 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. 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).

    CAS  PubMed  Google Scholar 

  97. 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).

    CAS  PubMed  Google Scholar 

  98. Pimprikar, P. et al. A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching. Curr. Biol. 26, 987–998 (2016).

    CAS  PubMed  Google Scholar 

  99. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Zuleger, N., Korfali, N. & Schirmer, E. C. Inner nuclear membrane protein transport is mediated by multiple mechanisms. Biochem. Soc. Trans. 36, 1373–1377 (2008).

    CAS  PubMed  Google Scholar 

  103. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  104. 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).

    CAS  PubMed  Google Scholar 

  105. Seidl, A. H. Regulation of conduction time along axons. Neuroscience 276, 126–134 (2014).

    CAS  PubMed  Google Scholar 

  106. Hilleary, R. & Gilroy, S. Systemic signaling in response to wounding and pathogens. Curr. Opin. Plant Biol. 43, 57–62 (2018).

    PubMed  Google Scholar 

  107. Yan, C. et al. Injury activates Ca2+/calmodulin-dependent phosphorylation of JAV1-JAZ8-WRKY51 complex for jasmonate biosynthesis. Mol. Cell 70, 136–149 (2018).

    CAS  PubMed  Google Scholar 

  108. Toyota, M. et al. Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361, 1112–1115 (2018).

    CAS  PubMed  Google Scholar 

  109. 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).

    CAS  PubMed  Google Scholar 

  110. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  112. 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).

  113. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Gilroy, S. et al. ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol. 171, 1606–1615 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Kaupp, U. B. & Seifert, R. Cyclic nucleotide-gated ion channels. Physiol. Rev. 82, 769–824 (2002).

    CAS  PubMed  Google Scholar 

  117. Traynelis, S. F. et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405–496 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Hou, C. et al. DUF221 proteins are a family of osmosensitive calcium permeable cation channels conserved across eukaryotes. Cell Res. 24, 632–635 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Yuan, F. et al. OSCA1 mediates osmotic stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514, 367–371 (2014).

    CAS  PubMed  Google Scholar 

  121. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  123. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  124. 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).

    CAS  PubMed  Google Scholar 

  125. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  126. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Roy, S. J. et al. Investigating glutamate receptor-like gene co-expression in Arabidopsis thaliana. Plant Cell Environ. 31, 861–871 (2008).

    CAS  PubMed  Google Scholar 

  128. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  129. 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).

    PubMed  Google Scholar 

  130. Ortiz-ramírez, C. et al. Glutamate receptor-like channels are essential for chemotaxis and reproduction in mosses. Nature 549, 91–95 (2017).

    PubMed  Google Scholar 

  131. 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).

    CAS  PubMed  Google Scholar 

  132. Yu, F., Tian, W. & Luan, S. From receptor-like kinases to calcium spikes: what are the missing links? Mol. Plant 7, 1501–1504 (2014).

    CAS  Google Scholar 

  133. Choi, J. et al. Identification of a plant receptor for extracellular ATP. Science 343, 290–294 (2014).

    CAS  PubMed  Google Scholar 

  134. Chen, D. et al. Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture. Nat. Commun. 8, 2265 (2017).

    PubMed  PubMed Central  Google Scholar 

  135. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Contributions

S.L. designed the outline of the manuscript. W.T., C.W. and S.L. with the help of Q.G. and L.L. wrote the manuscript. C.W. prepared the figures.

Corresponding author

Correspondence to Sheng Luan.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-020-0667-6

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing