Thomas A. DeFalco
Wolfgang Moeder
Keiko Yoshioka- 1Department of Biology, Western University, London, ON, Canada
- 2Department of Cell & Systems Biology, University of Toronto, Toronto, ON, Canada
Editorial on the Research Topic
Ca2+ signalling in plant biotic interactions
Calcium ions (Ca2+) serve as a universal second messenger across eukaryotes (Clapham, 2007). In the paradigm of Ca2+ signalling, stimuli trigger rapid changes in free Ca2+ concentration via the coordinated activities of Ca2+-permeable channels, pumps, and antiporters (‘encoding’) (McAinsh and Pittman, 2009). These signals can occur across cellular compartments (Resentini et al., 2021) where they are sensed via suites of Ca2+-binding sensor proteins (‘decoding’), which in turn regulate numerous downstream cellular processes, ultimately eliciting stimulus-appropriate physiological responses (DeFalco et al., 2010). Great progress has been made in the past decade in the development and deployment of new tools to monitor and visualize in vivo calcium signals (Grenzi et al., 2021), spurring a renaissance in the field of plant Ca2+ signalling.
In keeping with its evolutionarily-conserved and universal role, Ca2+ signalling is central to diverse aspects of plant development as well as responses to environmental perturbations (Kudla et al., 2018), including, notably, biotic stimuli (Tian et al., 2020; Köster et al., 2022; Xu et al., 2022). Ca2+ fluxes are among the earliest detectable responses to the perception of pathogens and pests (Yu et al., 2017; DeFalco and Zipfel, 2021) as well as symbiotic microbes (Tian et al., 2020), and as such have been a major area of focus in molecular plant biotic interaction research in recent years. Such work has led to key recent discoveries in the field of biotic interactions, including the identification of numerous Ca2+ channels playing roles in both cell surface and intracellular immunity (Bi et al., 2021; Bjornson et al., 2021; Jacob et al., 2021; Köster et al., 2022; Xu et al., 2022).
In this Research Topic issue, several important aspects of Ca2+ signalling in the context of plant biotic interactions have been advanced. Ca2+ signalling is a central component of many stress response pathways in plants, and Patra et al provide an overview of Ca2+ signalling networks in both abiotic and biotic stress contexts. One of the key downstream effectors of Ca2+ signalling in immunity is the transcriptional regulator CAMTA3/AtSR1, which is regulated by the central Ca2+ sensor calmodulin (CaM) and acts as an executor of the general stress response (Bjornson et al., 2021). Here, Yuan et al provide a detailed summary of the functions of this transcription factor in immunity, its regulation by CaM and phosphorylation, and its guarding by intracellular immune receptors.
While Ca2+ signalling is one of the early hallmarks in response to immune elicitors such as the bacterial flagellin-derived epitope flg22, whether such signals are altered in the context of immune priming was unknown. Eichstadt et al developed an approach to examine Ca2+ signals in both local and systemic leaves upon immune elicitation using the ratiometric fluorescent calcium indicator R-GECO1-mTurquoise, which allowed them to determine that immune priming does not alter rapid Ca2+ signalling dynamics in distal tissues.
Many Ca2+-permeable channels have been implicated in plant biotic responses, including members of the cyclic nucleotide-gated channel (CNGC) family (DeFalco et al., 2016). Sun et al report that CNGC2, a well-studied member of this family, contributes to the Ca2+ signal induced by extracellular ATP (eATP), which acts as an immune elicitor upon cellular damage in plants. Finally, while most signalling work has been performed using model plants such as Arabidopsis, Zhou et al have examined how Ca2+ signalling and transporters contribute to flagellin-induced immune responses in cotton (Gossypium hirsutum), identifying a Ca2+ efflux transporter as a potential regulator of defenses to Verticillium wilt.
The tools available to researchers that allow for monitoring of in planta Ca2+ dynamics continue to expand and improve (Waadt et al., 2021), allowing for ever-more complex and detailed study of Ca2+ signals, from organelles to single cells to whole plants. Recent insights have also expanded our understanding of the repertoire of Ca2+-permeable channels in plants and their potential functions in plant immunity (Köster et al., 2022; Xu et al., 2022). Such breakthroughs have opened key questions for the field, which is poised for fundamental discoveries in coming years.
Author contributions
All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.
Funding
Research in the authors’ laboratories is generously funded by Western University (start-up funding and a Western Strategic Support NSERC-Seed Grant to TAD) and a Discovery Grant from the National Science and Engineering Research Council (NSERC, PGPIN-2019-05832) to KY.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
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References
Bi, G., Su, M., Li, N., Liang, Y., Dang, S., Xu, J., et al. (2021). The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling. Cell 184, 3528–3541.e12. doi: 10.1016/j.cell.2021.05.003
Bjornson, M., Pimprikar, P., Nürnberger, T., Zipfel, C. (2021). The transcriptional landscape of arabidopsis thaliana pattern-triggered immunity. Nat. Plants 7, 579–586. doi: 10.1038/s41477-021-00874-5
DeFalco, T. A., Bender, K. W., Snedden, W. A. (2010). Breaking the code: Ca2+ sensors in plant signalling. Biochem. J. 425, 27–40. doi: 10.1042/BJ20091147
DeFalco, T. A., Moeder, W., Yoshioka, K. (2016). Opening the gates: Insights into cyclic nucleotide-gated channel-mediated signaling. Trends Plant Sci. 21, 903–906. doi: 10.1016/j.tplants.2016.08.011
DeFalco, T. A., Zipfel, C. (2021). Molecular mechanisms of early plant pattern-triggered immune signaling. Mol. Cell 81, 3449–3467. doi: 10.1016/j.molcel.2021.07.029
Grenzi, M., Resentini, F., Vanneste, S., Zottini, M., Bassi, A., Costa, A. (2021). Illuminating the hidden world of calcium ions in plants with a universe of indicators. Plant Physiol. 187, 550–571. doi: 10.1093/plphys/kiab339
Jacob, P., Kim, N. H., Wu, F., El-Kasmi, F., Chi, Y., Walton, W. G., et al. (2021). Plant “helper” immune receptors are Ca2+-permeable nonselective cation channels. Science 373, 420–425. doi: 10.1126/science.abg7917
Köster, P., DeFalco, T. A., Zipfel, C. (2022). Ca 2+ signals in plant immunity. EMBO J. 41, e110741. doi: 10.15252/embj.2022110741
Kudla, J., Becker, D., Grill, E., Hedrich, R., Hippler, M., Kummer, U., et al. (2018). Advances and current challenges in calcium signaling. New Phytol. 218, 414–431. doi: 10.1111/nph.14966
McAinsh, M. R., Pittman, J. K. (2009). Shaping the calcium signature. New Phytol. 181, 275–294. doi: 10.1111/j.1469-8137.2008.02682.x
Resentini, F., Ruberti, C., Grenzi, M., Bonza, M. C., Costa, A. (2021). The signatures of organellar calcium. Plant Physiol. 187, 1985–2004. doi: 10.1093/plphys/kiab189
Tian, W., Wang, C., Gao, Q., Li, L., Luan, S. (2020). Calcium spikes, waves and oscillations in plant development and biotic interactions. Nat. Plants 6, 750–759. doi: 10.1038/s41477-020-0667-6
Waadt, R., Kudla, J., Kollist, H. (2021). Multiparameter in vivo imaging in plants using genetically encoded fluorescent indicator multiplexing. Plant Physiol. 187, 537–549. doi: 10.1093/plphys/kiab399
Xu, G., Moeder, W., Yoshioka, K., Shan, L. (2022). A tale of many families: Calcium channels in plant immunity. Plant Cell 34, 1551–1567. doi: 10.1093/plcell/koac033
Keywords: calcium, ion channels, biotic interaction, immunity, PTI
Citation: DeFalco TA, Moeder W and Yoshioka K (2023) Editorial: Ca2+ signalling in plant biotic interactions. Front. Plant Sci. 14:1137001. doi: 10.3389/fpls.2023.1137001
Received: 03 January 2023; Accepted: 16 January 2023;
Published: 20 January 2023.
Edited and Reviewed by:
Brigitte Mauch-Mani, Université de Neuchâtel, SwitzerlandCopyright © 2023 DeFalco, Moeder and Yoshioka. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Wolfgang Moeder, d21vZWRlckBnbWFpbC5jb20=; Thomas A. DeFalco, dGRlZmFsY0B1d28uY2E=; Keiko Yoshioka, a2Vpa28ueW9zaGlva2FAdXRvcm9udG8uY2E=