Lsi2: A black box in plant silicon transport

Abstract

Background: Silicon (Si) is widely considered a non-essential but beneficial element for higher plants, providing broad protection against various environmental stresses (both biotic and abiotic), particularly in species that can readily absorb the element. Two plasma-membrane proteins are known to coordinate the radial transport of Si (in the form of Si(OH)₄) from soil to xylem within roots: the influx channel Lsi1 and the efflux transporter Lsi2. From a structural and mechanistic perspective, much more is known about Lsi1 (a member of the NIP-III subgroup of the Major Intrinsic Proteins) compared to Lsi2 (a putative Si(OH)₄/H⁺ antiporter, with some homology to bacterial anion transporters).

Scope: Here, we critically review the current state of understanding regarding the physiological role and molecular characteristics of Lsi2. We demonstrate that the structure-function relationship of Lsi2 is largely uncharted and that the standing transport model requires much better supportive evidence. We also provide (to our knowledge) the most current and extensive phylogenetic analysis of Lsi2 from all fully sequenced higher-plant genomes. We end by suggesting research directions and hypotheses to elucidate the properties of Lsi2.

Conclusions: Given that Lsi2 is proposed to mediate xylem Si loading and thus root-to-shoot translocation and biosilicification, it is imperative that the field of Si transport focus its efforts on a better understanding of this important topic. With this review, we aim to stimulate and advance research in the field of Si transport and thus better exploit Si to improve crop resilience and agricultural output.

Supplementary information: The online version contains supplementary material available at 10.1007/s11104-021-05061-1.

Keywords: Efflux; Lsi2; Membrane transport; Root-to-shoot translocation; Silicon; Xylem loading.

Fig. 1

The standing Si-transport model in the roots of rice (Oryza sativa). Lsi1 and Lsi2 are expressed in the distal and proximal ends, respectively, of the exodermis and endodermis. Lsi1 mediates the thermodynamically passive uniport of Si(OH)₄, whereas Lsi2 is thought to mediate the secondary active transport of Si(OH)₄ in antiport with H⁺ (the electrochemical gradient of which is generated by the plasma-membrane H⁺-ATPase). Redrawn from Ma and Yamaji (2008)

Fig. 2

Taxonomical distribution of genome-sequenced plant species obtained from the PLAZA 4.5 database (Van Bel et al. 2018). Numbers in parentheses denote the number of Lsi2 homologs identified in each species (sequences provided in Supplementary Table S4

Fig. 3

Phylogenetic distribution of Lsi2 homologs identified in Fig. 2, as well as those found in the species Cucumis sativus, Cucurbita moschata, and Equisetum arvense (which were not available in the PLAZA 4.5 database). To date, only seven sequences have been functionally characterized for Si transport (as denoted by the black circles; see text for details). The tree was developed using the maximum-likelihood method provided in MEGA 7. Only proteins > 400 amino acids were considered in the analysis. Sequences fell into three distinct clades, highlighted by blue, red, and black branches. Gene identifications can be found in Supplementary Table S3 and sequences are provided in Supplementary Table S4

Fig. 4

Predicted secondary structure of OsLsi2 from rice (Oryza sativa). Transmembrane domains have been labeled in Roman numerals. Highlighted red, the residues that show similarity to the GXQ motifs thought to underlie the Si-selectivity of diatomic SIT transporters (Knight et al. ; see text for details; see also Supplementary Fig. S3). Note, no evidence currently exists to support their involvement in Lsi2-mediated Si transport. Highlighted yellow, residues predicted to be able to be phosphorylated; see Supplementary Fig. S4 for details). Structure prediction based on the SOSUI algorithm (http://harrier.nagahama-i-bio.ac.jp/sosui/sosui_submit.html)

Fig. 5

Sequence alignment of six Lsi2 proteins (OsLsi2, ZmLsi2, HvLsi2, CmLsi2-1, CsLsi2, and EaLsi2, from rice (Oryza sativa), maize (Zea mays), barley (Hordeum vulgare), pumpkin (Curcurbita moschata), cucumber (Cucumis sativus), and horsetail (Equisetum arvense), respectively) that have, to date, been functionally verified to transport Si (in the Xenopus oocyte system; see text for details). In red, the 11 predicted transmembrane (TM) domains

Fig. 5

Sequence alignment of six Lsi2 proteins (OsLsi2, ZmLsi2, HvLsi2, CmLsi2-1, CsLsi2, and EaLsi2, from rice (Oryza sativa), maize (Zea mays), barley (Hordeum vulgare), pumpkin (Curcurbita moschata), cucumber (Cucumis sativus), and horsetail (Equisetum arvense), respectively) that have, to date, been functionally verified to transport Si (in the Xenopus oocyte system; see text for details). In red, the 11 predicted transmembrane (TM) domains