Structural basis for malate-driven, pore lipid-regulated activation of the Arabidopsis vacuolar anion channel ALMT9

Yeongmok Lee, Elsa Demes-Causse, Jaemin Yoo, Seo Young Jang, Seoyeon Jung, Justyna Jaślan, Geum-Sook Hwang, Jejoong Yoo, Alexis Angeli and Sangho Lee ()
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Yeongmok Lee: Sungkyunkwan University
Elsa Demes-Causse: Université Montpellier
Jaemin Yoo: Sungkyunkwan University
Seo Young Jang: Korea Basic Science Institute
Seoyeon Jung: Sungkyunkwan University
Justyna Jaślan: Université Montpellier
Geum-Sook Hwang: Korea Basic Science Institute
Jejoong Yoo: Sungkyunkwan University
Alexis Angeli: Université Montpellier
Sangho Lee: Sungkyunkwan University

Nature Communications, 2025, vol. 16, issue 1, 1-18

Abstract: Abstract In plant cells, ALMTs are key plasma and vacuolar membrane-localized anion channels regulating plant responses to the environment. Vacuolar ALMTs control anion accumulation in plant cells and, in guard cells, they regulate stomata aperture. The activation of vacuolar ALMTs depends on voltage and cytosolic malate, but the underlying molecular mechanisms remain elusive. Here we report the cryo-EM structures of ALMT9 from Arabidopsis thaliana (AtALMT9), a malate-activated vacuolar anion channel, in plugged and unplugged lipid-bound states. In all these states, membrane lipids interact with the ion conduction pathway of AtALMT9. We identify two unplugged states presenting two distinct pore width profiles. Combining structural and functional analysis we identified conserved residues involved in ion conduction and in the pore lipid interaction. Molecular dynamics simulations revealed a peculiar anion conduction mechanism in AtALMT9. We propose a voltage-dependent activation mechanism based on the competition between pore lipids and malate at the cytosolic entrance of the channel.

Date: 2025
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DOI: 10.1038/s41467-025-56940-5

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