Structure and function of a silicic acid channel Lsi1

Abstract

Silicon is a beneficial element for plant growth and production, especially in rice. Plant roots take up silicon in the form of silicic acid. Silicic acid channels, which belong to the NIP subfamily of aquaporins, are responsible for silicic acid uptake. Accumulated experimental results have deepened our understanding of the silicic acid channel for its uptake mechanism, physiological function, localization, and other aspects. However, how the silicic acid channel efficiently and selectively permeates silicic acid remains to be elucidated. Recently reported crystal structures of the silicic acid channel enabled us to discuss the mechanism of silicic acid uptake by plant roots at an atomic level. In this mini-review, we focus on the crystal structures of the silicic acid channel and provide a detailed description of the structural determinants of silicic acid permeation and its transport mechanism, which are crucial for the rational creation of secure and sustainable crops.

Keywords: NIP; aquaporin; channel; crystal structure; rice; silicon; substrate selectivity; transporter.

Figure 1

Localization of silicic acid transporters in rice and crystal structure of Lsi1. (A) Schematic representation of silicic acid absorption and distribution in rice plants. Rice roots take up silicic acid in the soil. Blue arrows indicate silicic acid migration. Silicic acid channel Lsi1 is mainly localized in the roots, and Lsi6 is localized in the nodes. Lsi1 and Lsi6 are involved in silicic acid absorption and distribution, respectively. (B) Schematic cross-section of a rice root. Lsi1, shown in the green line, is localized on the distal side of the cell membrane in the exodermis and endodermis. A silicic acid efflux transporter Lsi2 is shown in the blue line. Lsi2 is localized on the proximal side of the cell membrane in the exodermis and endodermis. Lsi3, shown in the orange line, is localized on the cell membrane in the pericycle. (C) The overall structure of the Lsi1 tetramer is viewed from the FIGURE 1 (Continued)extracellular side (PDB ID: 7CJS). One protomer is shown in a rainbow, while the others are shown in gray. Light blue circles indicate substrate permeation pathways. (D) Side view of the monomeric Lsi1. Numbers indicate TM1~6; B and E indicate short helix B and E, respectively. The grey bars indicate the membrane boundaries. A square in a dashed line indicates the SF region. Panels (C,D) are reproductions from Saitoh et al. (2021).

Figure 2

Structures of Lsi1 and silicic acid permeation model in SF. (A) Superposition of the Lsi1 structures in the open state (PDB 7CJS, cyan) and closed state (PDB 7NL4, magenta). Numbers indicate TM1~6; Alphabets indicate Short helices B and E. The solid and open arrowheads indicate loop D and loop B, respectively. (B) The view from the Intracellular side. Amino acid residues of loop D are shown as stick representations in light blue (open state) and light pink (closed state). Spheres indicate Na⁺ ion (open state, light blue), and Cd²⁺ ion (closed state, light pink). In the closed state, FIGURE 2 (Continued)loop D blocks the channel of Lsi1. Loop B structure in the closed state differs from the open state structure probably due to the crystal packing, Cd²⁺ ion, and interactions with loop D. (C) The SF of Lsi1 is viewed from the extracellular side (PDB ID: 7CJS). (C) Silicic acid molecule was manually placed based on the oxygen atoms of the water molecules in the crystal structure and examined by the QM/MM calculation. The predicted OH groups of silicic acid are indicated. (D) Schematic diagram of silicic acid passing through the SF. The OH groups of silicic acid pass through three crevices in the SF; the first OH group passes between Arg222 and the carbonyl ladder, the second one passes between the carbonyl ladder and Ser207, and the third one passes between Ser207 and a polar face made by waters (Wat3, Wat9). δ− and δ+ indicate bond polarity. (E) Classification of SFs by pore size and hydrophilicity. BtAQP1 (PDB 1J4N), GlpF (PDB 1FX8), and Lsi1 (PDB 7CJS). A question mark indicates that no such SFs have yet been identified. (F) Unique water molecules (Wat3, Wat9, and Wat17) in the Lsi1 channel limit silicic acid permeation. Channel profile along the Lsi1 pore calculated using the program HOLE2 is also shown. The SF and NPA motifs regions are colored in plum and khaki, respectively. Wat17 was observed only in the MD simulation. Panels C and E are reproductions from Saitoh et al. (2021).