The plant uptake of nanoparticles is affected by several factors related to the nature of the nanoparticle itself, but also with the plant physiology and the interaction of the nanomaterials with the environment (Figure 1).

It is clear that nanoparticle traits will greatly influence its behavior, and hence if the plant will be able to absorb it. Size seems to be one of the main restrictions for penetration into plant tissues, and there are some reports about the maximum dimensions that plants allow for nanoparticles to move and accumulate inside the cells, usually with 40–50 nm as a size exclusion limit (González-Melendi et al., 2008; Corredor et al., 2009; Sabo-Attwood et al., 2012; Taylor et al., 2014). Additionally, the type of nanoparticle and its chemical composition is another factor influencing the uptake (Ma et al., 2010; Rico et al., 2011), whereas morphology has also been demonstrated as determinant in some cases (Raliya et al., 2016). Functionalization and coating of the nanomaterial surface can greatly change and alter the properties for its absorption and accumulation by the plant (Judy et al., 2012).

Plant species can differ in their physiology, and such differences result in variations regarding uptake of nanoparticles, as reported for example by Cifuentes et al. (2010), Larue et al. (2012), and Zhu et al. (2012). These works showed how crops species belonging to different botanical families, and exposed to either magnetic carbon-coated, titanium dioxide or gold nanoparticles respectively, presented diverse absorption and accumulation patterns inside the plants. But the ways of application are also crucial in order to determine how effectively a plant will internalize the nanomaterials: roots are specialized in absorption of nutrients and water, whereas leaves are developed for gas exchange and present a cuticle which hampers penetration of substances (Schwab et al., 2015).

But nanoparticles interact with other components of the environment, and it can affect their properties and their traits for being assimilated by plants (Figure 1). For example, humic acids and other organic matter present in the soil can lead to an improved stability and hence a better bioavailability of nanomaterials, whereas salt ions might induce precipitation and trigger a contrary effect (Navarro et al., 2008). Even more, the presence of other organisms, such as bacteria and fungi, influences the plant uptake of nanoparticles, mainly if those microorganisms establish symbiosis with plants as in the case of mycorrhizal fungi (Feng et al., 2013; Wang et al., 2016).

Once the nanoparticles penetrate into the plant, there are two ways for them to move through tissues: the apoplast and the symplast (Figure 1). Apoplastic transport takes place outside the plasma membrane through the extracellular spaces, cell walls of adjacent cells and xylem vessels (Sattelmacher, 2001), whereas symplastic transport involves movement of water and substances between the cytoplasm of adjacent cells through specialized structures called plasmodesmata (Roberts and Oparka, 2003) and sieve plates. The apoplastic pathway is important for radial movement within plant tissues, and allows nanomaterials to reach the root central cylinder and the vascular tissues, for further movement upwards the aerial part (González-Melendi et al., 2008; Larue et al., 2012; Zhao et al., 2012; Sun et al., 2014). Once inside the central cylinder, nanoparticles can move toward the aerial part though the xylem, following the transpiration stream (Cifuentes et al., 2010; Larue et al., 2012; Wang et al., 2012; Sun et al., 2014). Nevertheless, reaching the xylem through the root implies crossing a barrier to the apoplastic pathway, the Casparian strip, which must be done following a symplastic way (Robards and Robb, 1972) via endodermal cells. Indeed, some nanomaterials can be stopped and accumulated at the Casparian strip (Larue et al., 2012; Sun et al., 2014; Lv et al., 2015). Another important symplastic transport is possible too, using the sieve tube elements in the phloem, and allowing distribution toward non-photosynthetic tissues and organs (Wang et al., 2012; Raliya et al., 2016). In the case of foliar applications, nanomaterials must cross the barrier the cuticle presents, following the lipophilic or the hydrophilic pathway (Schönherr, 2002). The lipophilic one involves diffusion through cuticular waxes, whereas the hydrophilic pathway is accomplished through polar aqueous pores presented in the cuticle and/or stomata (Eichert and Goldbach, 2008; Eichert et al., 2008). Because the diameter of cuticular pores has been estimated around 2 nm (Eichert and Goldbach, 2008), the stomatal pathway appears as the most likely route for nanoparticle penetration, with a size exclusion limit above 10 nm (Eichert et al., 2008).

The way nanomaterials move inside plants is really important, because it can give indications about what parts of the plant they can reach, and where they might end and accumulate. For example, if a kind of nanoparticles are transported mainly through the xylem and not the phloem, they will likely move mainly from root to shoot and leaves, and not downwards, so they should be applied to the roots in order to get a good distribution in the plant. On the contrary, if the nanoparticles show a good translocation through the phloem, application should be done via foliar spraying. In addition, nanomaterials moving along the phloem will likely accumulate in plant organs acting as sink, such as fruits and grains, so that is another important consideration when trying to avoid further human or animal ingestion of nanomaterials. However, translocation is not necessarily restricted to a specific cell type, and lateral movement of nanomaterials between xylem and phloem is possible (Pate, 1975).

The characteristics and nature of the nanomaterials, in addition to the plant species, will greatly influence translocation and accumulation in plant tissues. For example, for the same kind of nanoparticle, differences in translocation and accumulation in different plant species have been observed (Cifuentes et al., 2010; Zhu et al., 2012), whereas slight differences in similar nanoparticles lead to different results within the same plant (Zhu et al., 2012). Cifuentes et al. (2010) reported higher accumulation of carbon-coated iron nanoparticles in the roots of pea compared with sunflower and wheat, and faster translocation to the aerial parts in pea and wheat compared with sunflower and tomato. On the other hand, Zhu et al. (2012) found that radish and ryegrass roots accumulated higher amounts of gold nanoparticles than rice and pumpkin, and that positively charged gold nanoparticles were taken up faster by the roots than negatively charged one, whereas these last ones were more efficiently translocated to the aerial parts. This phenomenon was explained by the negative charge present in the plant cell walls, favoring accumulation of positively charged nanoparticles in the tissues, and hampering its movement through the plant.

But, where do the nanomaterials go after being translocated to other parts? Typically, nanoparticles will accumulate in certain tissues and organs, in the same way it happens with animals (Varna et al., 2012). As commented above, plant organs acting as strong sinks for sap and nutrients are likely to accumulate nanomaterials traveling through the vascular system, mainly fruits (Servin et al., 2013), grains (Lin et al., 2009), flowers, and young leaves (Cifuentes et al., 2010; Koo et al., 2015). That is something to be used in our advantage when deciding the role of the nanomaterial we want to test. Do we need to deliver a plant hormone during flower development? Or an inhibitor for undesirable substances in the fruit? Perhaps a herbicide against a parasitic plant (Pérez-de-Luque and Rubiales, 2009)? It is also crucial to know the final fate of the nanomaterials if we do not want they to persist for human or animal consumption after the treatment. Some nanoparticles could be transformed or degraded by the plant after some time (Wang et al., 2012; Zhang et al., 2012; Lv et al., 2015), or simply being stored in tissues that will not be used after harvesting. In this last case, could they be recovered and recycled for further use (Liu et al., 2017)?

In order to enter the symplastic pathway, nanomaterials must be internalized by the plant cell and cross the plasma membrane (Figure 1). There are several ways for nanoparticles to achieve this, although such mechanisms are better studied in animal cells and less known in plants (Rico et al., 2011; Schwab et al., 2015):

– Endocytosis: The nanoparticles are incorporated into the cell by invagination of the plasma membrane, originating a vesicle that can travel to different compartments of the cell (Etxeberria et al., 2006).

How nanoparticles are internalized in the cells is another key question, because it will again influence the practical application of the nanomaterials. If we want to deliver chemicals inside specific cell organelles, then endocytosis appears as the most suitable way. On the contrary, for delivery in the cytosol, pore formation should be the most direct way for it. Additionally, we could be interested in nanomaterials that do not penetrate inside the plant cell but in other organisms, such as bacteria or fungi, in order to treat crop systemic diseases and infections (Rispail et al., 2014).

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.