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Revista mexicana de ciencias agrícolas

versión impresa ISSN 2007-0934

Rev. Mex. Cienc. Agríc vol.7 no.5 Texcoco jun./ago. 2016



Biomanufacturing of metal nanoparticles using plant cells or plant extracts

América Berenice Morales-Díaz1 

Antonio Juárez-Maldonado2 

Álvaro Morelos-Moreno3 

Susana González-Morales3 

Adalberto Benavides-Mendoza4  § 

1Robótica y Manufactura Avanzada-Centro de Investigación y de Estudios Avanzados, IPN- Unidad Saltillo. Avenida Industria Metalúrgica 1062, C. P. 25900, Parque Industrial, Ramos Arizpe, Coahuila.

2Departamento de Botánica de la Universidad Autónoma Agraria Antonio Narro.

3Cátedras CONACYT-Universidad Autónoma Agraria Antonio Narro.

4Departamento de Horticultura de la Universidad Autónoma Agraria Antonio Narro, Calzada Antonio Narro 1923. C. P. 25315. Saltillo, Coahuila, México. (;;;


A review is presented on the biomanufacturing of nanoparticles (NPs) of metals using plant extracts, cell organ cultures or live plants. The two methods of manufacturing green nanoparticles are described: the biochemical process extracts and biological process involving living cells. The redox mechanism biomanufacturing of NPs is discussed, emphasizing those points that require further clarification in order to standardize processes to adapt to an industrial production system. It also describes what is known about the fate of NPs biomanufacturing in living cells, highlighting the process of extra- and intracellular as well as between different tissues and organs of the plant mobilization. Finally the factors discussed that regulate the rate of biomanufacturing of nanoparticles in living cells and tissues, directing attention to what you need to master to obtain bio-factories for the production of NPs where the variability in size, shape and reactivity fit to industry standards.

Keywords: balance redox; bioproduction; bioreduction metal; green chemical synthesis


Se presenta una revisión acerca de la biofabricación de nanopartículas (NPs) de metales usando extractos vegetales, cultivos celulares de órganos o bien plantas vivas. Se describen los dos métodos de biofabricación verde de nanopartículas: el proceso bioquímico con extractos y el proceso biológico que involucra células vivas. Se discute el mecanismo redox de biofabricación de NPs, haciendo énfasis en aquellos puntos que requieren mayor dilucidación con el propósito de estandarizar los procesos para adaptarlos a un sistema industrial de producción. Se describe igualmente lo que se conoce acerca del destino de las NPs biofabricadas en células vivas, remarcando el proceso de movilización extra- e intracelular así como entre diferentes tejidos y órganos de la planta. Se discuten por último los factores que regulan la tasa de biofabricación de nanopartículas en las células y tejidos vivos, dirigiendo la atención hacia aquello que se necesita dominar para obtener biofábricas para la producción de NPs en donde la variabilidad de tamaño, forma y reactividad se ajusten a estándares industriales.

Palabras clave: balance redox; bioproducción; bioreducción de metales; síntesis química verde


The nanotechnology has become promise of improvement and rapid change in thinking, designing and making technology. The definition of nanoscience is "research and technological development at a scale of 1 to 100 nm using atoms, molecules or macromolecules" (EPA 2007). Chemical elements in nanometric form or nanoparticles (NPs) show different properties that are manifested in the macroscopic scale or micro or when in ionic form (Hochella et al., 2008). The metal NPs exhibit properties unique electrical, magnetic, catalytic and optical, differing from those undergoing the same bulk material (Gericke and Pinches, 2006). These new emergent properties are value added, is per se manifest in the nanoparticles and depend mainly on a high ratio surface/volume (Nie et al., 2010), which grows significantly with decreasing the size of the NPs (Karlsson et al., 2009), reaching values above 60 m2 cm-3 (E. C. 2011).

In this review the progress described in a specific sector of nanotechnology is the biomanufacturing of NPs using as a tool the living plant cells or plant extracts. These green techniques called allow the manufacture of NPs with an environmental cost much less than the physicochemical techniques (Zhang et al., 2011), however, despite this advantage has not yet been established processes green biomanufacturing of NPs in levels pilot plant or industrial scale. The test objective is to highlight the advances in biochemical and physiological understanding of the phenomenon of biomanufacturing of NPs with plants or extracts, indicating the factors that may result in increased production capacity of NPs in production systems located in laboratories, industrial reactors or greenhouses.

Nanoparticles biomanufacturing

The different manufacturing methods NPs, nanomaterials and nanodevices (EPA, 2007) are known, but in particular the use of metabolites, plant extracts, cells, tissues, seeds or structures for vegetative reproduction, organs and whole organisms for biomanufacturing of NPs is an area of great scientific dynamism (Iravani, 2011; Kuppusamy et al., 2014). The number of publications is very large and most of the studies refer to the biosynthesis of metal NPs, but also found results about the biosynthesis of nanomaterials such as graphene (Gurunathan et al., 2014). It has a series of reviews of literature that indicate many specific cases, including plant species used for biomanufacturing of NPs, as well as elements transformed to NPs (Iravani, 2011; Baker et al., 2013; Rai and Yadav, 2013; PardhaSaradhi et al., 2014b; Ahmed and Ikram, 2015; Keat et al., 2015).

Biomanufacturing methods nanoparticles. They can be classified into (i) biochemical and (ii) biological. Both types have been termed "green" because unlike physico-chemical methods do not generate polluting by-products (Kharissova et al., 2013) and among other advantages come at a lower cost because they do not require much infrastructure, reagents and energy expenditure (Li et al., 2011).

For the biochemical production of NPs nonliving things are used, but the fresh or dried extracts from roots, leaves, stems, flowers or fruits of different plant species (Mittal et al., 2013; Borovaya et al., 2014) or seeds (Rajasekharreddy and Rani, 2014) of the remaining biomass of bio-industrial processes or biosolids (Sarkar et al., 2014; Dauthal and Mukhopadhyay, 2015) or biopolymers, carbohydrates, gums and latex (Hortigüela et al., 2011; Iravani, 2011) which are contacted with a solution containing from 1 to 5 mM of metal ions to the reducing potential of the compounds contained in the extract or biochemical compound to carry out the reaction shown in equation (1).

Metal cation + reducing compound metal with zero valent + oxidized compound 1)

Moreover for biological production of NPs can use cultures of bacteria or cyanobacteria (Patel et al., 2015), fungi (Ahmad et al., 2003), microalgae (Patel et al., 2015) or cell cultures or plant organs (Al-Shalabi and Doran 2013), whole plants (Mittal et al., 2014) or structures such outbreaks (Gardea-Torresdey et al., 2003), flowers and stems (Kuppusamy et al., 2014) or roots (PardhaSaradhi et al., 2014b). The manufacturing process may occur biological intracellularly (Haverkamp and Marshall 2008), extracellular (Li et al., 2011) or even ex plant via root exudates (Pardha-Saradhi et al., 2014A). Basically what is done for the biomanufacturing of NPs is to put a solution with 1 to 2 mM of a metal ion with a cell culture, organ, seed or entire plant, so contact the reductive process develops indicated in equation (1). The lowest concentration indicated would be used for elements with high toxicity as Cu and highest for elements such as Au.

The mechanism biomanufacturing nanoparticles. Biochemical or biological synthesis of NPs metal is a redox reaction occurs because to the reducing capacity of the cell or extracellular components such as proteins, carbohydrates, organic acids, phenols and other metabolites (Haverkamp and Marshall, 2008; Juárez-Maldonado et al., 2013; Rai and Yadav, 2013; Kumar et al., 2013), which provide electrons to the metal cations taking them to a metallic form with zero load and nanometer scale. In general for NPs of metals such as Cu, Ag, Pd, Au, Ni, Ce, among others, the process is as shown in the following equation (2):

Cu+2 + reducing compound  cu0 + oxidized compound 2)

The reducing compound in equations (1) and (2) indicates a single metabolite or chemical compound or an assembly of several of them from a vegetable extract or living cells. Functional groups which have been reported involved in the biosynthesis of NPs are alcohols, aldehydes, amines, carboxyls, ketones, hydroxyls, sulfhydryls (Baker et al., 2013; Rai and Yadav, 2013; Huang et al., 2015), so it can be assumed that virtually any biological compound to provide such groups is usable to convert metal ions in NPs. However, Rai and Yadav (2013) indicated that some compounds like terpenoids, flavonoids, various heterocyclic, polyphenols, reducing sugars, glutathione and ascorbate are directly involved in biosynthesis, while others such as proteins function as stabilizing agents, forming by adsorbing an organic cover called crown.

The Cu zero valent (Cu0) indicated in equation (2) was obtained with the reduction in two steps from Cu+2, first Cu+ and then Cu0 (Kitching et al., 2014) which forms complexes with other atoms of Cu0 resulting aggregation to a nanoparticle can be crystalline or amorphous and will have a certain size and specific geometry, this chemical environment dependent reaction and where compounds provide reducing potential occurs (Bashir et al., 2015; Metz et al., 2015). The magnitude of nanometric NPs results in a high ratio surface/volume, generating a plasma exposure electronic metal with very small amounts of mass. This increases by several orders of magnitude the amount of electrostatic and kinetic energy of the electronic plasma available for interaction (for example with electromagnetic radiation or metabolites and proteins forming the crown) per unit mass of nanoelement (Noguez, 2007; Lynch and Dawson, 2008). Precisely therein lies much of the biological reactivity of NPs and what turns them on one side in a very effective microbicide but on the other hand, also becomes an inducing agent of cellular stress for other organisms such as plants, animals and humans.

Additional factors to the ratio surface/volume, as the geometry of the NPs and type of organic coating also modify the interaction with cellular components (Karlsson et al., 2009). This partially explain the existence of conflicting reports concerning the positive and negative effects of different types of NPs (Rivera-Gil et al., 2013), since the specific activity of NPs of an element depend on the surface interaction with different metabolites and proteins present (Metz et al., 2015). In fact it states that the crown formed by the adsorption of proteins and various metabolites to the surface of the NPs, is the signal that the cells perceive and signaled to modify their physiological behavior and gene expression (Lynch and Dawson, 2008). Moreover, it is possible that different methods of synthesis, physical chemistry, biochemistry and biological lead to NPs with the same ranges in diameter but with differences in geometry and therefore in its ratio surface/volume and in organic cover or crown, which would result in the NPs of the same element and the same diameter class exert different effects when applying for certain uses or to interact with living beings or ecological systems.

The question arises as to why the living cells NPs manufactured in the presence of metal ions has been shown that when these are very reactive and can induce oxidative stress and other cellular disorders (Navarro et al., 2008). You may simply try an automatic response of the biochemical system that has a certain antioxidant capacity. Or perhaps the answer is related to the greater facility to keep the NPs in specific cellular locations with lower energy costs compared with metal ions in solution (Karlsson et al., 2009).

Faced with a stress-induced excess metal ions plants respond to various defense mechanisms such as lower income and increase the excretion of these elements by the root, complexation with metabolites, proteins or cell wall, accumulation of antioxidants and complexation and transport into the vacuole (Shahid et al., 2014). All these responses are induced and require time and energy expenditure for functional implementation. The advantage of the formation of NPs is occurring rapidly, it depends only on the existing antioxidant potential at the time and works as an expedited response that would later be supplemented by the aforementioned adjustments that would lead to finer control and effective concentration metal ions.

It seems then that the synthesis of NPs would be the first defensive responses of plants to stress induced by excess metal ions. It is therefore expected that the production capacity of NPs of a biological system to respond in part to the contribution of metal ions in concentrations above the right and on the other hand, the system's ability to biotransform ions in NPs. The latter obey the global antioxidant capacity provided by the metabolites and other compounds located in the plant extract or living cells (Huang et al., 2015; Valko et al., 2015).

The NPs biosynthesis occurs spontaneously in nature, both in its abiotic components and biotic (Hochella et al., 2008). However, the literature shows an information bias, in the sense that published studies are mainly directed towards the biomanufacturing of NPs as well as the effects of artificially manufactured NPs and their ecological destination. There is little information about NPs generated under natural conditions. What effects on organisms causing ecological functions and develop natural NPs? The issue seems relevant not only for metal NPs but also for NPs clay, various mineral and biological components.

The biosynthesis NPs is observed even human cells (Anshup et al., 2005; El-Said et al., 2014), and generally in biochemical systems derived from living things, that is, systems that exhibit reducing ability as example fresh or dried extracts obtained from plant organisms (Mittal et al., 2013; Kumar et al., 2013; Huang et al., 2015), honey (Venu et al., 2011), wine (Mittal et al., 2014), or to the material obtained from cell lysis (El-Said et al., 2014). The NPs obtained can form oxides (Haverkamp and Marshall, 2008) or complex hydrated (Petit et al., 2015), but what usually happens is the NPs acquire an organic coating adsorbed on the surface of the NPs, which increases its stability and decreases aggregation (Iravani, 2011); i.e., biological agents develop a double function as reducing agents and as coating.

It is not yet clear whether the biotransformation is mainly dependent on one or a few types of metabolites or if what matters is the overall reduction potential, that is, the sum of the reducing capabilities of all biomolecules found in the system (Anshup et al., 2005). None reported any limitation as to the transformation of ions NPs to be performed by some kind of specific compound (El-Said et at., 2014), while some authors point out specific metabolites as responsible for biotransformation (Shukla et al., 2014; Huang et al., 2015), but without providing elements to totally exclude the action of other biomolecules. If what is required is the presence of a few different reducing metabolites lot transgenic organisms or plant extracts (Hong-Bo et al., 2010) or hyperaccumulators with innate ability to build the element to be used for would be used the biosynthesis of NPs (Iravani, 2011). On the other hand if you need a great general reducing capacity from many different metabolites then genetic selection, environmental manipulation or agronomic management could be applied (Ortega-Ortiz et al., 2007).

Fate of nanoparticles in the cell or tissue. Once the NPs are formed in cells or living tissues from the element ions of interest, what happens to them? It is known that NPs have intracellular and apoplastic mobility (Larue et al., 2014), can enter organelles such as chloroplasts (Miralles et al., 2012), the vacuole and the core (Kurepa et al., 2010) at which may be distributed throughout the cell. It has been further shown that several elements NPs not greater than 100 nm are mobilized between different organs of the plant through the phloem (Rico et al., 2011; Wang et al., 2013).

It is also possible that NPs are transformed back to the element in ionic form, then resulting in ongoing replacement element status NPs ion and therefore check in the case of the Ag forming NPs unstable (Larue et al., 2014), while the NPs with greater stability would be those elements such as Ce, which cumulatively cause damage by mechanical interference with the pores of the cell walls (Asli and Neumann., 2009), by interaction with proteins modifying the conformation and functionality (Mahmoudi et al., 2011), or by interference with the cytoskeleton or oxidative stress (Wang et al., 2011). The phenotypic changes observed in cells or whole organisms in the presence of NPs possibly come from the aforementioned interactions occurring in the genomic, epigenomic, biochemical and metabolic areas. The general scenario that is obtained is high mobility between organs of plants, both in terms of NPs intact and its replacement to the ionic form of the element and vice versa. This must be considered for their potential environmental impact and for food purposes use of plants that interact with NPs.

Factors regulating biomanufacturing nanoparticles in plant cells and tissues. According to Haverkamp and Marshall (2008) there are several limitations for biochemical and biological synthesis NPs from ions in solution:

In the case of biochemical manufacturing plant extracts finite volume of compounds that provide reduction potential in the system.

The ability to restore or maintain the gearhead potential, which in the case of biological production depends on photosynthesis and respiration of carbon stocks of plants, plant cells or organs.

For the redox potential biological transformation (potential standard electrochemical reduction) of the transformation ion of the element to form zero-valent (eg Cu+2 to Cu0) is a factor, being limited by the authors to values greater than 0 Volts (V) (electrochemical potential relative to a standard hydrogen electrode) and therefore includes only elements such as Au, Ag, Cu, Se, Pd, Ir, Pt, Cr, Ru and Rh. The greater the positive value of the redox potential easier biotransformation occurs, i.e., there will be a higher percentage of recovery element in its nanoparticulate form. Other elements such as Zn, Ni, Pb, Tl and Cd having lower potentials redox to 0 V for the transformation of its common ionic form to the form with zero valent not appear to be susceptible to becoming NPs using cells, organs or whole plants but if by biochemical means, using for example plant extracts (Kuppusamy et al., 2014).

The chemical form of the element in solution, whether in ionic form is as Ag+ or in the form of an ionic complex as Ag(NH3)2 + or Ag(S2O3)2 3- also has an impact on the biotransformation process when it occurs intracellularly in cultured cells or microorganisms or plants intra somatically. It is not known with certainty why it occurs so but obtained ion NPs are larger to those obtained from ionic complexes (Haverkamp and Marshall, 2008). This difference could be related to the ease of diffusion or transport (Anshup et al., 2005), which in turn is associated with ease of transport elements in ionic form (usually cations) by conveyors energized by proton pumps (Guerinot, 2000) vs ionic complex (which will normally be anions) and mobilized more slowly (Wright and Diamond, 1977). No reported special conveyors for elements which become NPs into cells, such as Ag and Au, but this occurs by means of the carrier proteins used to mobilize other elements such as Fe (Jain et al., 2014) or directly through the lipid bilayer of cells or organelles apparently by vesicular transport (Serag et al., 2012).

The concentration of the elements also impacts biosynthesis NPs since the rise salinity becomes less effective transport of ions into the cell or its different compartments (Grattan and Grieve 1998), also increase the toxic effect of some elements, especially non-essential, when they are above a certain threshold concentration (Poschenrieder et al., 2013). Additionally the changes in the concentration and chemical species in solution modify the redox potential of the system, which impacts both the ability to biotransform ions in NPs and the size of such NPs finally obtained (Haverkamp and Marshall, 2008).

After the reaction biotransformation of ions NPs reducing potential of smaller magnitude would biochemical system. In the case of a live system reducing potential could be equal or greater depending on the metabolic capacity and inductive effect of the element itself in ionic or their NPs which in some cases leads to increased antioxidant capacity in the biological system (Juarez-Maldonado et al., 2013). The concentration of ions of the element or elements subject to biotransformation decreases more or less depending on the element concerned, of its chemical form and capacity reduction system (Haverkamp and Marshall, 2008) and found to efficiency biotransformation microorganisms can be as high as 88% of the initial concentration of the metal in ionic form or complex (Suresh et al., 2011). In the case of the use of live plants for biomanufacturing of NPs it found that species such as Brassica juncea and Medicago sativa can earn up to 3% of its dry weight in the form of silver nanoparticles, in times of 24-72 h, using a hydroponic solution containing 1 000 to 10 000 mg L-1 of AgNO3 (Harris y Bali, 2007).

Escalation of nanoparticles biomanufacturing plants

A possible limitation in the larger scale use methods biotransformation with plants or their derivatives is that the reducing capacity of the system (whether it is a biological product such as honey, humic acids, a fresh extract or a set of living cells) it will be dependent on its composition (Iravani, 2011; Kharissova et al., 2013), being complicated standardization principle since each specific combination of environment-organism will result in a different composition (Starnes et al., 2010). Likewise the identity and reactivity of the crown of the NPs will differ depending on the composition of cells or extracts (Metz et al., 2015). In the case of the use of plants for the biomanufacturing of NPs the result will be different depending on the species or variety, growth conditions (Jain et al., 2014), the element in question of biotransformed and concentration so and the way it is applied to the plant is the root (López-Moreno et al., 2010) or by foliar spraying (Juárez-Maldonado et al., 2013).

If the system is not standardized biochemically then it is difficult to obtain NPs with certain standards (Starnes et al., 2010), especially size, geometry and composition of the crown. Standardization provides certainty about the effectiveness of NPs. Many studies report obtaining NPs by biochemical or biological means, but studies on one occasion, with a kind and specific individuals, leaving unanswered the reproducibility of the phenomenon in terms of the characteristics of NPs.

Indeed, if we think of a process with crops in greenhouses and shade houses, where either through the nutrient solution or by foliar spraying the item you are looking biotransformed then apply the way to increase production of NPs would be based on the same techniques or processes used to:

  1. To improve absorption of elements in agricultural production conditions in poor soils or saline soils including the use of zeolites, organic acids, mycorrhizal and rhizobacteria.

  2. Allow growth in situations where natural or artificial plants are subjected to certain chemicals above a certain concentration. An example would be to use soils with high natural concentration of an element such as Se, Zn, Mg, Na, or soils contaminated by mining (mine lands) or wastewater with Cr, Pb, Hg, Cd, etc.

  3. Achieve the accumulation of a particular element with a technique to promote biofortification or hyperaccumulation.

  4. Get a greater capacity reduction and renewal capacity reduction which correlates with the growth and biomass accumulation. Is need to increase photosynthetic rate and storage of carbon compounds in the roots and stems so that the metabolic capacity to generate reducing potential increases.

As it is difficult for the production of NPs using whole plants compete with other systems (microorganisms or plant organs in bioreactors) in terms of ease of implementation, then it would be necessary to think about systems biomanufacturing of NPs dual purpose: an example would be the production hydroponic green fodder, a system designed for the production of biomass optimizing water use. If the ions to biotransformed, such as Cu+2 or Ag+, we introduce in the nutrient solution (Haverkamp and Marshall, 2008) using the concentrations reported in the literature the biotransformation process will occur using the reducing potential obtained from the photosynthetic activity and respiratory the plants. Upon completion of the cultivation and before harvesting the NPs they will be harvested by grinding and centrifugation and fresh pasta remnant, which is expected to further reducing capacity by the inductive effect of the applied element (Juárez-Maldonado et al., 2013), could use for making compost or even for livestock feed, putting the due care to avoid the trophic transfer of NPs to animals and human bodies. It is obvious that the development of a system of this kind require multiple tests to verify its safety regarding the release of NPs ecosystems and food chains.

Processes expected to occur in this system bioproduction of NPs coupled to the production of hydroponic green fodder are the same as naturally occur during mineral nutrition of plants or during a bioremediation of land with native plants, that is: ion complexation, absorption, assimilation and transport, use and storage or in cases of excess excretion (Haverkamp and Marshall, 2008; Jain et al., 2014).


Biomanufacturing of nanoparticles (NPs) of metals using biochemical methods with fresh or dried plant extracts, or biological methods with cell cultures, organ cultures, seeds or whole plants is an area of study still developing with great potential for industrial production of NPs.

The mechanism redox in the transformation of metals is based on ionic form your form of NPs is reasonably well understood, but a lot still to research and develop in the control and standardization of reductive capabilities extracts or live cells of vegetables, subject to obtaining necessary industrial scale systems that will generate NPs functionality standards required by the medical, industrial and other applications.

Another area that requires further research is referring to the fate of NPs in living cells. These NPs suffer mobilization between cellular compartments and organs, in addition to remobilization of NPs stores to its ionic form. Greater understanding of these phenomena support in the implementation of techniques that maximize the production of NPs.

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Received: March 2016; Accepted: May 2016

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