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A novel single-domain Na+-selective voltage-gated channel in photosynthetic eukaryotes

A novel single-domain Na+-selective voltage-gated channel in photosynthetic eukaryotes
A novel single-domain Na+-selective voltage-gated channel in photosynthetic eukaryotes
The evolution of Na+-selective four-domain voltage-gated channels (4D-Navs) in animals allowed rapid Na+-dependent electrical excitability, and enabled the development of sophisticated systems for rapid and long-range signaling. While bacteria encode single-domain Na+-selective voltage-gated channels (BacNav), they typically exhibit much slower kinetics than 4D-Navs, and are not thought to have crossed the prokaryote–eukaryote boundary. As such, the capacity for rapid Na+-selective signaling is considered to be confined to certain animal taxa, and absent from photosynthetic eukaryotes. Certainly, in land plants, such as the Venus flytrap (Dionaea muscipula) where fast electrical excitability has been described, this is most likely based on fast anion channels. Here, we report a unique class of eukaryotic Na+-selective, single-domain channels (EukCatBs) that are present primarily in haptophyte algae, including the ecologically important calcifying coccolithophores, Emiliania huxleyi and Scyphosphaera apsteinii. The EukCatB channels exhibit very rapid voltage-dependent activation and inactivation kinetics, and isoform-specific sensitivity to the highly selective 4D-Nav blocker tetrodotoxin. The results demonstrate that the capacity for rapid Na+-based signaling in eukaryotes is not restricted to animals or to the presence of 4D-Navs. The EukCatB channels therefore represent an independent evolution of fast Na+-based electrical signaling in eukaryotes that likely contribute to sophisticated cellular control mechanisms operating on very short time scales in unicellular algae.
0032-0889
1674-1683
Helliwell, Katherine E.
514f8174-da3f-46c8-be0d-3bcd92ee8189
Chrachri, Abdul
4c8a3ca0-7e80-42f4-a3be-dd2dae8583ba
Koester, Julie A.
b667b66c-d284-4be5-bedf-338a27be02a9
Wharam, Susan
1d37eedf-556e-4b1e-94d5-465e2a3e6e01
Taylor, Alison R.
a20791ff-9a08-4fb9-b484-2e39368f7789
Wheeler, Glen L.
80ee477b-ceb3-4051-923c-399098bb746a
Brownlee, Colin
2af37c1c-b2bf-4832-8370-d9c35e7b3385
Helliwell, Katherine E.
514f8174-da3f-46c8-be0d-3bcd92ee8189
Chrachri, Abdul
4c8a3ca0-7e80-42f4-a3be-dd2dae8583ba
Koester, Julie A.
b667b66c-d284-4be5-bedf-338a27be02a9
Wharam, Susan
1d37eedf-556e-4b1e-94d5-465e2a3e6e01
Taylor, Alison R.
a20791ff-9a08-4fb9-b484-2e39368f7789
Wheeler, Glen L.
80ee477b-ceb3-4051-923c-399098bb746a
Brownlee, Colin
2af37c1c-b2bf-4832-8370-d9c35e7b3385

Helliwell, Katherine E., Chrachri, Abdul, Koester, Julie A., Wharam, Susan, Taylor, Alison R., Wheeler, Glen L. and Brownlee, Colin (2020) A novel single-domain Na+-selective voltage-gated channel in photosynthetic eukaryotes. Plant Physiology, 184 (4), 1674-1683. (doi:10.1104/pp.20.00889).

Record type: Article

Abstract

The evolution of Na+-selective four-domain voltage-gated channels (4D-Navs) in animals allowed rapid Na+-dependent electrical excitability, and enabled the development of sophisticated systems for rapid and long-range signaling. While bacteria encode single-domain Na+-selective voltage-gated channels (BacNav), they typically exhibit much slower kinetics than 4D-Navs, and are not thought to have crossed the prokaryote–eukaryote boundary. As such, the capacity for rapid Na+-selective signaling is considered to be confined to certain animal taxa, and absent from photosynthetic eukaryotes. Certainly, in land plants, such as the Venus flytrap (Dionaea muscipula) where fast electrical excitability has been described, this is most likely based on fast anion channels. Here, we report a unique class of eukaryotic Na+-selective, single-domain channels (EukCatBs) that are present primarily in haptophyte algae, including the ecologically important calcifying coccolithophores, Emiliania huxleyi and Scyphosphaera apsteinii. The EukCatB channels exhibit very rapid voltage-dependent activation and inactivation kinetics, and isoform-specific sensitivity to the highly selective 4D-Nav blocker tetrodotoxin. The results demonstrate that the capacity for rapid Na+-based signaling in eukaryotes is not restricted to animals or to the presence of 4D-Navs. The EukCatB channels therefore represent an independent evolution of fast Na+-based electrical signaling in eukaryotes that likely contribute to sophisticated cellular control mechanisms operating on very short time scales in unicellular algae.

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More information

Accepted/In Press date: 15 September 2020
e-pub ahead of print date: 1 October 2020
Published date: 1 December 2020

Identifiers

Local EPrints ID: 447773
URI: http://eprints.soton.ac.uk/id/eprint/447773
ISSN: 0032-0889
PURE UUID: bd1938c9-43cc-4115-8807-0efb66f56341

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Date deposited: 19 Mar 2021 17:37
Last modified: 16 Mar 2024 10:41

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Contributors

Author: Katherine E. Helliwell
Author: Abdul Chrachri
Author: Julie A. Koester
Author: Susan Wharam
Author: Alison R. Taylor
Author: Glen L. Wheeler
Author: Colin Brownlee

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