Extracellular silica nanocoat formed by layer-by-layer (LBL) self-assembly confers aluminum resistance in root border cells of pea (Pisum sativum)

Abstract

Background Soil acidity (and associated Al toxicity) is a major factor limiting crop production worldwide and threatening global food security. Electrostatic layer-by-layer (LBL) self-assembly provides a convenient and versatile method to form an extracellular silica nanocoat, which possess the ability to protect cell from the damage of physical stress or toxic substances. In this work, we have tested a hypothesis that extracellular silica nanocoat formed by LBL self-assembly will protect root border cells (RBCs) and enhance their resistance to Al toxicity. Results Scanning electron microscopy (SEM) and X-ray photoelectron spectroscopy (XPS) were used to compare the properties of RBCs surface coated with nanoshells with those that were exposed to Al without coating. The accumulation of Al, reactive oxygen species (ROS) levels, and the activity of mitochondria were detected by a laser-scanning confocal microscopy. We found that a crystal-like layer of silica nanoparticles on the surface of RBCs functions as an extracellular Al-proof coat by immobilizing Al in the apoplast and preventing its accumulation in the cytosol. The silica nanoshells on the RBCs had a positive impact on maintaining the integrity of the plasma and mitochondrial membranes, preventing ROS burst and ensuring higher mitochondria activity and cell viability under Al toxicity. Conclusions The study provides evidence that silica nanoshells confers RBCs Al resistance by restraining of Al in the silica-coat, suggesting that this method can be used an efficient tool to prevent multibillion-dollar losses caused by Al toxicity to agricultural crop production. Electronic supplementary material The online version of this article (10.1186/s12951-019-0486-y) contains supplementary material, which is available to authorized users.

Interactions of Silicon With Essential and Beneficial Elements in Plants

“…Moreover, an interesting study by Feng et al (2019) involving the root border cells of pea, showed that these cells were coated with extracellular silica layers, and therefore were able to adsorb Al on their surfaces preventing Al transport into the cells. Very recently, Xiao et al (2021) reported involvement of Si in decreasing Al accumulation (i.e., non exchangeable Al fraction) in the cell wall of rice root apex by decreasing hemicellulose content, which is a main binding site for Al in the cell wall without affecting its cation exchange capacity.…”

Aluminium–silicon interactions in higher plants: an update

“…Until recently, the only example of Al and Si co-deposition in roots that we are aware of outside the grasses was from Norway spruce ( Hodson and Wilkins, 1991 ) where the phenomenon was observed in the cortical cell walls. One slightly unusual example of Al and Si co-deposition comes from the work of Feng et al (2019) working on the root border cells of pea. They were able to produce an extracellular silica nanocoat formed by layer-by-layer self-assembly on the surface of these cells.…”

Root Border Cells as a Convenient Single Cell System to Study Plant-Environmental Interactions: A Case Study for Aluminum Tolerance

“…When RBCs are generated from the root cap, they build a biological interface between the root surface and soil, and play many functions, such as directly affecting the rhizosphere microecosystem, inhibiting the invasion of the pathogen, reducing root mechanical resistance and protecting the root tip (4,7,8,10,(12)(13)(14)(15)(16)(17)(18). It has been reported that RBCs can quickly release antibiotics, specific enzymes, sugars, and other chemicals to regulate the growth of bacteria, fungi, viruses, and nematodes around the rhizosphere by changing gene expression under stress (18)(19)(20).…”

“…Therefore, RBCs are considered to be the front of plant response and defense to stresses. Considering RBCs are easier to be harvested in large quantities and easily purified, they are widely used in studies on Al toxicity (7,8,15,39,52). Of specific interest is pea (Pisum sativum) -Mendel's model genetic material that are capable to produce up to 10,000 RBCs from one root tip (8).…”