Interplay between silica deposition and viability during the life span of sorghum silica cells

Abstract

Silica cells are specialized epidermal cells found on both surfaces of grass leaves, with almost the entire lumen filled with solid silica. The mechanism precipitating silicic acid into silica is not known. Here we investigate this process in sorghum (Sorghum bicolor) leaves. Using fluorescent confocal microscopy, we followed silica cells' ontogeny, aiming to understand the fate of vacuoles and nuclei. Correlating the confocal and scanning electron microscopy, we timed the initiation of silica deposition in relation to cell's viability. Contrary to earlier reports, silica cells did not lose their nucleus before silica deposition. Vacuoles in silica cells did not concentrate silicic acid. Instead, postmaturation silicification initiated at the cell periphery in live cells. Less than 1% silica cells showed characteristics of programmed cell death in the cell maturation zone. In fully elongated mature leaves, 2.4% of silica cells were nonsilicified and 1.6% were partially silicified. Silica deposition occurs in the paramural space of live silica cells. The mineral does not kill the cells. Instead, silica cells are genetically programmed to undergo cell death independent of silicification. Fully silicified cells seem to have nonsilicified voids containing membrane remains after the completion of the cell death processes.

Siliplant1 (Slp1) protein precipitates silica in sorghum silica cells

“…Unless indicated otherwise, we used sorghum seedlings of about 2 weeks of age for our studies. Immature, silicifying leaves (L IS ) in our present study is analogous to leaf-2, as reported in our earlier studies (Kumar & Elbaum, 2017, 2018; Kumar et al ., 2017a). The immature leaf was cut into five equal segments.…”

“…Slp1 expression was not detected in roots where silica cells do not form. Furthermore, we could not detect Slp1 expression in mature leaf tissues, in correlation with the absence of viable, active silica cells (Kumar & Elbaum, 2018). This suggests that silica deposition in live silica cells is dependent on Slp1, while silica deposition in cell walls and possibly other locations is governed by other means such as specific cell wall polymers (Fry et al ., 2008; Law & Exley, 2011; Kido et al ., 2015; Brugiére & Exley, 2017; Kulich et al ., 2018).…”

“…The fast silica precipitation over a few hours (Lawton, 1980) in addition to the formation of the mineral at the cell wall, as opposed to the cytoplasm (Kumar et al ., 2017a; Kumar & Elbaum, 2018), point to a factor exported from the cells that induces biogenic silica formation. Our work shows that silica cells express and export the protein Slp1 to the apoplast, timed with silicification in the paramural space (Kumar et al ., 2017a; Kumar & Elbaum, 2018). It is obvious that silica deposition depends on the presence of silicic acid which is absorbed by roots from the soil.…”

“…Within this time period, almost the entire cell lumen is filled with solid silica (Hodson et al ., 1985). Silica cell silicification is immediately followed by cell death (Kumar & Elbaum, 2018) which ceases the silicification process (Markovich et al ., 2015; Kumar et al ., 2017a; Kumar & Elbaum, 2018). Silicification in silica cells is thus different than silicification in macro-hairs and abaxial epidermal cells in lemma where silica deposition takes place in a course of weeks on the thickened cell wall material (Hodson et al ., 1984; Perry et al ., 1984), or in glume prickle hairs and papillae where silica is deposited in the empty lumen of these cells even after cell death (Hodson et al ., 1985).…”

The controversies of silicon's role in plant biology

“…around exodermal and endodermal root cells and leaf epidermal cells; Sangster et al ., ; Gong et al ., ), and cell wall constituents, such as (hemi)cellulose, callose, pectin and lignin, have been demonstrated to interact with Si(OH) 4 as ‘templates’ or ‘scaffolding’ for silicification (Guerriero et al ., ; and references therein). Si can also polymerize in specialized cells and cellular structures of some species (particularly grasses), such as leaf silica and long cells, and spikelet hairs and papillae (Rafi et al ., ), and interesting preliminary evidence for the biological control of this process has emerged (Kumar et al ., ,b; Kumar & Elbaum, ).…”