Nano-enabled agriculture: How do nanoparticles cross barriers in plants?

Abstract

Nano-enabled agriculture is a topic of intense research interest. However, our knowledge of how nanoparticles enter plants, plant cells, and organelles is still insufficient. Here, we discuss the barriers that limit the efficient delivery of nanoparticles at the whole-plant and single-cell levels. Some commonly overlooked factors, such as light conditions and surface tension of applied nano-formulations, are discussed. Knowledge gaps regarding plant cell uptake of nanoparticles, such as the effect of electrochemical gradients across organelle membranes on nanoparticle delivery, are analyzed and discussed. The importance of controlling factors such as size, charge, stability, and dispersibility when properly designing nanomaterials for plants is outlined. We mainly focus on understanding how nanoparticles travel across barriers in plants and plant cells and the major factors that limit the efficient delivery of nanoparticles, promoting a better understanding of nanoparticle-plant interactions. We also provide suggestions on the design of nanomaterials for nano-enabled agriculture.

Keywords: barriers; cell membranes; cell wall; efficient delivery; electrochemical gradients; nanoparticles.

Figure 1

Phenotypes of plants subjected directly to a growth light after foliar application of NPs. (A) Four days later, compared with a control plant (foliar spray with 0.05% Silwet L-77). Obvious phytotoxicity symptoms were observed in cotton plants subjected directly to growth light conditions after foliar application of 0.09 mM polyacrylic acid-coated nanoceria (PNC; ∼10 nm, approximately −18 mV). (B) Five days later, compared with a control plant (leaf laminar infiltration with 10 mM 2-(N-morpholino)ethanesulfonic acid (MES) + 10 mM MgCl₂). Obvious phytotoxicity spots were observed in Arabidopsis plants subjected directly to growth light conditions after leaf laminar infiltration of 0.05 mg/l AuNPs (∼16 nm, ∼36 mV). White arrows indicate the damaged spots in NP-infiltrated plants without proper room light incubation.

Figure 2

Main factors that limit delivery efficiency of nanoparticles to plants. Interfacing NPs to plants in the field is done mainly through foliar delivery or root application. For foliar delivery, the status of stomata (open or closed), thickness of the cuticle, leaf cell wall porosity, sieve plate pore size in the phloem, surface tension of nanoformulations, sap composition, and sap flow rate are the main factors that affect the delivery efficiency of foliar NPs. For root application, interactions between NPs and soil or root exudates need to be considered. After NPs interface with roots, root cell wall porosity, transpiration, pore size of pit membranes, sap composition, and sap flow rate are the main factors that affect the delivery efficiency of root-applied NPs.

Figure 3

A proposed model showing cell barriers faced by NPs and possible mechanisms by which NPs pass through these barriers. The cell wall, plasma membrane, and organelle membrane are the main barriers that limit the delivery efficiency of NPs into a cell. In foliar application, NPs can pass through the leaf barrier via the stomatal or cuticular pathway. The latter applies only to small NPs (less than ∼2.4 nm). Unlike the stomatal and cuticular pathways in foliar application, root-applied NPs directly interface with root cells. Cells located at the root meristem zone, which is in an actively dividing state, may be able to deliver large NPs. Three mechanisms are proposed by which NPs may cross the plasma membrane. As in animal cells, NPs might enter plant cells by endocytosis. Channels like mechanosensitive channels, which can deliver cargo about 4 nm in size, could be a possible means of plant cell NP uptake. A well-established model, lipid exchange envelope penetration, applies more to high-aspect-ratio nanomaterials. Some NPs may form a pore on the membrane to allow entry of NPs. The electrical gradient across cell membranes could be an important factor that affects NP delivery. It is mostly unknown how NPs cross organelle membranes. More efforts are needed on this topic.

Figure 4

The importance of properly designing nanomaterials for crop production enhancement. Different areas of the cycles represent the proposed priority of factors that should be considered during the design and synthesis of nanomaterials for crops.