Mg<sup>2+</sup> is a Missing Link in Plant Cell Ca<sup>2+</sup> Signalling and Homeostasis—A Study on <i>Vicia faba</i> Guard Cells
Hyperpolarization-activated calcium channels (HACCs) are found in the plasma membrane and tonoplast of many plant cell types, where they have an important role in Ca<sup>2+</sup>-dependent signalling. The unusual gating properties of HACCs in plants, i.e., activation by membrane hyperpol...
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MDPI AG
2020-05-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/21/11/3771 |
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| author | Fouad Lemtiri-Chlieh Stefan T. Arold Chris Gehring |
| author_facet | Fouad Lemtiri-Chlieh Stefan T. Arold Chris Gehring |
| author_sort | Fouad Lemtiri-Chlieh |
| collection | DOAJ |
| description | Hyperpolarization-activated calcium channels (HACCs) are found in the plasma membrane and tonoplast of many plant cell types, where they have an important role in Ca<sup>2+</sup>-dependent signalling. The unusual gating properties of HACCs in plants, i.e., activation by membrane hyperpolarization rather than depolarization, dictates that HACCs are normally open in the physiological hyperpolarized resting membrane potential state (the so-called pump or P-state); thus, if not regulated, they would continuously leak Ca<sup>2+</sup> into cells. HACCs are permeable to Ca<sup>2+</sup>, Ba<sup>2+</sup>, and Mg<sup>2+</sup>; activated by H<sub>2</sub>O<sub>2</sub> and the plant hormone abscisic acid (ABA); and their activity in guard cells is greatly reduced by increasing amounts of free cytosolic Ca<sup>2+</sup> ([Ca<sup>2+</sup>]<sub>Cyt</sub>), and hence closes during [Ca<sup>2+</sup>]<sub>Cyt</sub> surges. Here, we demonstrate that the presence of the commonly used Mg-ATP inside the guard cell greatly reduces HACC activity, especially at voltages ≤ −200 mV, and that Mg<sup>2+</sup> causes this block. Therefore, we firstly conclude that physiological cytosolic Mg<sup>2+</sup> levels affect HACC gating and that channel opening requires either high negative voltages (≥−200 mV) or displacement of Mg<sup>2+</sup> away from the immediate vicinity of the channel. Secondly, based on structural comparisons with a Mg<sup>2+</sup>-sensitive animal inward-rectifying K<sup>+</sup> channel, we propose that the likely candidate HACCs described here are cyclic nucleotide gated channels (CNGCs), many of which also contain a conserved diacidic Mg<sup>2+</sup> binding motif within their pores. This conclusion is consistent with the electrophysiological data. Finally, we propose that Mg<sup>2+</sup>, much like in animal cells, is an important component in Ca<sup>2+</sup> signalling and homeostasis in plants. |
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| language | English |
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| spelling | doaj.art-f9f2e485823a4bf7a1e6bd64c88996c62023-11-20T01:51:37ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-05-012111377110.3390/ijms21113771Mg<sup>2+</sup> is a Missing Link in Plant Cell Ca<sup>2+</sup> Signalling and Homeostasis—A Study on <i>Vicia faba</i> Guard CellsFouad Lemtiri-Chlieh0Stefan T. Arold1Chris Gehring2King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering (BESE), Thuwal 23955-6900, Saudi ArabiaKing Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering (BESE), Thuwal 23955-6900, Saudi ArabiaKing Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering (BESE), Thuwal 23955-6900, Saudi ArabiaHyperpolarization-activated calcium channels (HACCs) are found in the plasma membrane and tonoplast of many plant cell types, where they have an important role in Ca<sup>2+</sup>-dependent signalling. The unusual gating properties of HACCs in plants, i.e., activation by membrane hyperpolarization rather than depolarization, dictates that HACCs are normally open in the physiological hyperpolarized resting membrane potential state (the so-called pump or P-state); thus, if not regulated, they would continuously leak Ca<sup>2+</sup> into cells. HACCs are permeable to Ca<sup>2+</sup>, Ba<sup>2+</sup>, and Mg<sup>2+</sup>; activated by H<sub>2</sub>O<sub>2</sub> and the plant hormone abscisic acid (ABA); and their activity in guard cells is greatly reduced by increasing amounts of free cytosolic Ca<sup>2+</sup> ([Ca<sup>2+</sup>]<sub>Cyt</sub>), and hence closes during [Ca<sup>2+</sup>]<sub>Cyt</sub> surges. Here, we demonstrate that the presence of the commonly used Mg-ATP inside the guard cell greatly reduces HACC activity, especially at voltages ≤ −200 mV, and that Mg<sup>2+</sup> causes this block. Therefore, we firstly conclude that physiological cytosolic Mg<sup>2+</sup> levels affect HACC gating and that channel opening requires either high negative voltages (≥−200 mV) or displacement of Mg<sup>2+</sup> away from the immediate vicinity of the channel. Secondly, based on structural comparisons with a Mg<sup>2+</sup>-sensitive animal inward-rectifying K<sup>+</sup> channel, we propose that the likely candidate HACCs described here are cyclic nucleotide gated channels (CNGCs), many of which also contain a conserved diacidic Mg<sup>2+</sup> binding motif within their pores. This conclusion is consistent with the electrophysiological data. Finally, we propose that Mg<sup>2+</sup>, much like in animal cells, is an important component in Ca<sup>2+</sup> signalling and homeostasis in plants.https://www.mdpi.com/1422-0067/21/11/3771hyperpolarization-activated calcium channelsHACCscyclic nucleotides-activated channelsCNGCsmagnesiumcalcium |
| spellingShingle | Fouad Lemtiri-Chlieh Stefan T. Arold Chris Gehring Mg<sup>2+</sup> is a Missing Link in Plant Cell Ca<sup>2+</sup> Signalling and Homeostasis—A Study on <i>Vicia faba</i> Guard Cells International Journal of Molecular Sciences hyperpolarization-activated calcium channels HACCs cyclic nucleotides-activated channels CNGCs magnesium calcium |
| title | Mg<sup>2+</sup> is a Missing Link in Plant Cell Ca<sup>2+</sup> Signalling and Homeostasis—A Study on <i>Vicia faba</i> Guard Cells |
| title_full | Mg<sup>2+</sup> is a Missing Link in Plant Cell Ca<sup>2+</sup> Signalling and Homeostasis—A Study on <i>Vicia faba</i> Guard Cells |
| title_fullStr | Mg<sup>2+</sup> is a Missing Link in Plant Cell Ca<sup>2+</sup> Signalling and Homeostasis—A Study on <i>Vicia faba</i> Guard Cells |
| title_full_unstemmed | Mg<sup>2+</sup> is a Missing Link in Plant Cell Ca<sup>2+</sup> Signalling and Homeostasis—A Study on <i>Vicia faba</i> Guard Cells |
| title_short | Mg<sup>2+</sup> is a Missing Link in Plant Cell Ca<sup>2+</sup> Signalling and Homeostasis—A Study on <i>Vicia faba</i> Guard Cells |
| title_sort | mg sup 2 sup is a missing link in plant cell ca sup 2 sup signalling and homeostasis a study on i vicia faba i guard cells |
| topic | hyperpolarization-activated calcium channels HACCs cyclic nucleotides-activated channels CNGCs magnesium calcium |
| url | https://www.mdpi.com/1422-0067/21/11/3771 |
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