Silica deposition in plants: scaffolding the mineralization

Abstract

Background: Silicon and aluminium oxides make the bulk of agricultural soils. Plants absorb dissolved silicon as silicic acid into their bodies through their roots. The silicic acid moves with transpiration to target tissues in the plant body, where it polymerizes into biogenic silica. Mostly, the mineral forms on a matrix of cell wall polymers to create a composite material. Historically, silica deposition (silicification) was supposed to occur once water evaporated from the plant surface, leaving behind an increased concentration of silicic acid within plant tissues. However, recent publications indicate that certain cell wall polymers and proteins initiate and control the extent of plant silicification.

Scope: Here we review recent publications on the polymers that scaffold the formation of biogenic plant silica, and propose a paradigm shift from spontaneous polymerization of silicic acid to dedicated active metabolic processes that control both the location and the extent of the mineralization.

Conclusion: Protein activity concentrates silicic acid beyond its saturation level. Polymeric structures at the cell wall stabilize the supersaturated silicic acid and allow its flow with the transpiration stream, or bind it and allow its initial condensation. Silica nucleation and further polymerization are enabled on a polymeric scaffold, which is embedded within the mineral. Deposition is terminated once free silicic acid is consumed or the chemical moieties for its binding are saturated.

Keywords: Cell wall; Siliplant1; lignin; phytoliths; silica; silicic acid.

Fig. 1.

Silica deposited in tomato, which is a Si non-accumulator. Scanning back-scattered electron micrograph showing in high brightness features containing high concentrations of silicon. Leaf margin (A; indicated by arrow) and epidermal trichomes (B; indicated by arrowheads) are mineralized by silica (courtesy of G. Haint).

Fig. 2.

Silica formation from silicic acid solution. (A) Nucleophilic attack of an ionized silanol (siloxyl) on a silicic acid molecule resulting in disilicic acid. The reaction is slow under neutral pH even under supersaturation. The rate of similar condensation reactions is increased in polysilicic acid, which stabilizes the siloxyl group. Further condensation leads to cyclic structures that evolve to silica colloids. (B) The condensation reaction may be catalyzed by positively charged amine residues that stabilize transition states in the condensation. (C) Cell wall polymers may catalyse the condensation and also template the forming mineral. Schematic representation of different silica–polymer composites. (a) Long polymeric chain stabilizes siliceous particle. (b–d) Relatively short polymeric chains that give multiparticle aggregates, soluble (b) or insoluble (c and d). Reproduced from Annenkov et al. (2017) with permission from the Royal Society of Chemistry.

Fig. 3.

Activity of Siliplant1 at the apoplast of sorghum leaves. (A) Silica cell at the active silicification zone. Left to right: Siliplant1 (purple) is exported to the apoplastic space (inset), catalysing the polymerization of the supersaturated silicic acid and forming a silica secondary cell wall (grey) that reduces the cytoplasmic volume (green) and nucleus (red). Finally, silica cells undergo programmed cell death. (B) Ectopic silica deposition in sorghum leaf overexpressing Siliplant1. Arrows point to rows of normal silica cells that are silicified similar to wild-type plants. Arrowheads point to epidermal regions silicified under the activity of transiently overexpressed Siliplant1. All epidermal cell types are heavily silicified. Reproduced with permission from Kumar et al. (2020).

Fig. 4.

Silica aggregates at the endodermis of sorghum adventitious root. (Left) Diagram demonstrating root cortex (Co; blue), endodermis (En; red) and stele (St; green). (Right) Silica aggregates (white particles, arrowheads) form at the endodermis (cell layer between two arrows). Inset: close-up of an endodermis cell showing the aggregate (arrowhead) being an integral part of the inner tangential cell wall.

Fig. 5.

Micro-imaging of silica formation in sorghum primary roots demonstrating the patterning of modified lignin that patterns silica aggregation. (A) SEM imaging of silica aggregates (white) on the background of the endodermis inter-tangential cell wall (dark background). (B) Similar SEM imaging taken from roots of Si-deprived plants. Autofluorescence of the endodermis cell wall of roots grown (C) with and (D) without Si supplementation. Silica aggregates in (C) fluoresce in blue, while silica nucleation sites deprived of Si in (D) fluoresce in green. This shift in fluorescence hints at a change in the chemistry of cell wall phenolic materials following silicification. (E) Raman spectroscopy of the endodermis cell wall of roots deprived of Si. Mapping of the spectral signal at 1660–1775 cm⁻¹, assigned to aromatic carbonyls, recreates the spotted pattern of Si nucleation sites and suggests that lignin modification by carbonyl groups may nucleate silica deposition. All scale bars represent 10 µm. The figure is reproduced with permission from Zexer and Elbaum (2020, 2022).

Fig. 6.

Time course of Si aggregate formation over 24 h using SEM and EDX. Roots grown in Si-deprived medium were transferred to Si-rich medium and Si aggregation was monitored by (A) SEM backscattered electrons and (B) EDX. Before exposure to Si, bright structures can be identified by SEM (0 h, A). These structures contain no measurable Si (0 h, B). After 2 h, first signs of Si aggregation are detected using both SEM and EDX. Silicification continues until reaching saturation after 24 h. Scale bar represents 10 µm. Τhe figure is reproduced with permission from Zexer and Elbaum (2020).

Fig. 7.

Suggested model to explain supersaturation and deposition of silicic acid in the apoplast. (A) Stability of silicic acid (black) at supersaturation may be established through H-bonding to hydroxyl groups of a cell wall polymer (blue), as suggested for polyethylene glycol (Preari et al., 2014). (B) Once chemical moieties carrying positive charge (red) are introduced, silica deposition (grey) could be catalysed. Positive charge may originate from proteins similar to Siliplant1.