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Recent developments on nanotechnology in agriculture: plant mineral nutrition, health and interactions with soil microflora Gauri Achari, and Meenal Kowshik J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.8b00691 • Publication Date (Web): 23 Jul 2018 Downloaded from http://pubs.acs.org on July 23, 2018

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Journal of Agricultural and Food Chemistry

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Title: Recent developments on nanotechnology in agriculture: plant mineral nutrition, health and

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interactions with soil microflora

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Gauri A. Achari* and Meenal Kowshik*

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Gauri A. Achari

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Post-Doctoral Fellow

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Department of Biological Sciences, Birla Institute of Technology and Science Pilani,

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KK Birla Goa Campus, Zuarinagar, Goa 403726, India

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*Tel: 0091-832-2580352, Email: [email protected]

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ORCID Id: 0000-0002-7661-0900

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Meenal Kowshik

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Associate Professor

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Department of Biological Sciences, Birla Institute of Technology and Science Pilani,

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KK Birla Goa Campus, Zuarinagar, Goa 403726, India

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*Tel: 0091-832-2580304, Email: [email protected]

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1 ACS Paragon Plus Environment


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Abstract

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Plant mineral nutrition is important for obtaining higher agricultural productivity to meet the

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future demands of the increasing global human population. It is envisaged that nanotechnology

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can provide sustainable solutions by replacing traditional bulk fertilizers with their

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nanoparticulate counterparts possessing superior properties to overcome the current challenges of

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bioavailability and uptake of minerals, increasing crop yield, reducing fertilizer wastage and

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protecting the environment. Recent studies have shown that nanoparticles of essential minerals

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and non-essential elements affect plant growth, physiology and development, depending on their

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size, composition, concentration and mode of application. The current article reviews the recent

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findings on the positive as well as negative effects that nanofertilizers exert on plants when

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applied via foliar and soil routes; their effects on plant associated microorganisms and potential

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for controlling agricultural pests. This review suggests future research needed for the

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development of sustained release nanofertilizers for enhancing food production and

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environmental protection.

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Keywords: Nanotechnology, nanofertilizers, plant mineral nutrition, plant health, plant

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associated microorganisms

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Introduction

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Soils are the main source of macronutrients and micronutrients for plants, and the bioavailability

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of mineral nutrients is influenced by soil characteristics and other environmental factors.1

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Agricultural soils have been cropped over thousands of years. However, the rate of input of soil

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mineral nutrients has remained less than that of removal due to crop uptake. There is a lack of

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synchronization between the release of minerals from bulk ionic fertilizers and uptake by plants,

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wherein efficiencies may be less than 5%.2 In addition, macronutrients mainly nitrogen (N),

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phosphorus (P), potassium (K) and micronutrients such as zinc (Zn), copper (Cu), manganese

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(Mn) etc. can undergo several transformations, form precipitates, and react with clay colloids

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and the organo-mineral matrix in soils.1,3-6 These insoluble forms are unavailable for plant

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uptake. It is therefore important to develop new strategies to overcome macronutrient and

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micronutrient deficiencies in the agricultural soils.

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nanotechnology can provide solutions to the increasing problem of deficiency of nutrient

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availability, due to conversion to biologically unavailable forms.7,8 Nanoparticles (NPs) are

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materials with at least one dimension between 1-100 nm, have shapes which can be 0D, 1D, 2D

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or 3D, exhibit hybrid quantum effects and biological activities which are between those of atoms,

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molecules, and bulk minerals.9,10 It is now also evident that particles with dimensions between 1-

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250 nm can represent the properties similar to those of NPs with dimensions of 1-100 nm.11

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Apart from size and dimensions, the composition, surface structure, core chemistry, crystallinity,

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charge, redox potential, catalytic activity, porosity and aggregation contribute to the ability of the

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NPs to cross biological barriers and bring about biological effects.12-15 NPs have high surface

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area, sorption capacity and serve as reservoirs of functional ions with control over the rate of

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their release.16-19 NPs in the form of nanofertilizers can enhance the efficiency of micronutrient


Recent literature suggests that


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use through mechanisms of controlled release, thereby reducing fertilizer wastage due to

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leaching, degradation and volatilization.17,20,21 Plants are known to take up NPs through cuticular

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pores and stomata on the leaves or through the root epidermis, and transport them to all the plant

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parts.22,23 NPs can also enter in fruits when applied as a spray and may be useful to enhance

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nutrient quality of fruits.24 However, uptake and translocation of NPs is dependent on their

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physiochemical properties and presence of ion transporters as well.13,15,

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plant growth and yield mainly due to increased mineral nutrition, chlorophyll content, increased

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levels of antioxidant enzymes, stimulation of beneficial soil / rhizosphere microflora and

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suppression or induction of resistance to agricultural pests.21, 27-32 The current review summarizes

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the recent developments on the use of NPs of essential minerals and non-essential elements as

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nanofertilizers for plant growth promotion when applied as foliar spray or via soil route, and

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discusses the effects of NPs on soil and rhizosphere microflora and plant pathogens.

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Transport of NPs applied via the foliar route

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Foliar applied NPs enter the leaves through the cuticle or stomata. The cuticle is the primary

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barrier on the leaves and restricts entry of NPs to a size of < 5 nm. Cellular transport of NP > 10

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nm entering through the stomata to the vascular system of the plant can occur via apoplastic or

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symplastic routes.

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route (through the cytoplasm of adjacent cells) whereas translocation of larger NPs (between 50-

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200 nm) occurs via the apoplast (in between the cells).21-23,33 Internalized NPs are transported via

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the phloem sieve tubes along with the sugar flow. As a result of vascular transport through

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phloem, NPs can move bidirectionally and accumulate in the root, stem, fruits, grains and young

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leaves to varying degrees, since these organs act as strong sinks for the sap. 21-23,33 The NP size,

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concentration, application methods and environment, are important factors for successful uptake

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21, 25, 26

NPs enhance

Transport of NPs (between 10-50 nm) is favored through the symplastic


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of NPs after foliar application.22 Leaf morphology and its chemical composition, presence of leaf

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wax and exudates, presence of trichomes are important factors influencing the trapping of NPs

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on the leaf surface.34-35 In addition, phyllosphere microflora, sunlight, humidity, temperature,

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may also influence the fate of foliar NPs and their transformation.35, 36 Coating of NPs on the leaf

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surface after foliar application may also influence the photosynthetic activity.37 Uptake of NPs

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through plant leaves is represented schematically in fig. 1. An overview of the effects of NPs at

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different concentrations, applied through foliar route on plants is provided in table 1.

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Positive effects of NPs applied via the foliar route on plant growth

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Macronutrient NPs

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Foliar application of nanoparticulate formulations of essential mineral nutrients such as calcium

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(Ca), magnesium (Mg) and iron (Fe) have been attempted. Foliar spray of calcium carbonate-

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NPs (CaCO3-NPs) at a concentration of 260 g.L-1 increased the Ca concentration in Citrus

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tankan and controlled infestation by California red scale and Oriental fruit fly in Citrus tankan

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and Zizyphus mauritiana, indirectly promoting growth.38 Mg is an important co-factor in plant

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metabolic processes and also a component of chlorophyll. An increase in absorption of solar

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radiation, uptake of minerals (Fe, Cu, Zn, P and Mg) and activities of the enzymes

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(dehydrogenase, esterase, acid phosphatase, alkaline phosphatase, nitrate reductase) in Triticum

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aestivum L. (wheat) and Vigna unguiculata subsp. unguiculata (black eyed peas) was recorded

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on application of nano-Mg at a concentration ranging from 0.2-0.5 g.L-1.39, 40 Literature suggests

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that there are no studies on foliar application of NPs of N, P and K. Foliar application of bulk

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urea fertilizer causes ‘leaf burns’, desiccation of leaves, accumulation of toxic amounts of urea

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and disruption of carbohydrate metabolism.41,42 However, in absence of these ill effects, foliar

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application of bulk urea fertilizer is reported to enhance yield and can also help to limit the



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loss of N due to certain transformations of urea that occur when applied to soil. Bulk urea

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has been a preferred N source for foliar application over NH4+ and NO3− since they cause

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extensive leaf damage. In addition, urea is nonpolar in nature and readily diffuses through

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the leaf cuticle.43 A positive response on foliar application of bulk N, P and K fertilizers has

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been reported for several crops.43-46 Therefore, research on the development of superior,

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sustained release NPs of N, P and K for foliar application, which can help in overcoming the

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limitations of currently used conventional bulk fertilizers, is needed.

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Micronutrient NPs

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Zn is a cofactor for various enzymes required for chlorophyll synthesis. Biofortification by foliar

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application of Zn fertilizers has been reported to be effective as compared to soil application.47

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Foliar treatment with ZnO-NP stabilizes and protects the plant cell membrane against oxidative

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stress.48 Upon foliar application of zinc oxide NPs (ZnO-NPs), Zn is released in the acidic

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stomatal interior and translocated via the phloem with the highest absorption in the leaves

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followed by the stem, seeds and root.49, 50 The translocation of ZnO-NPs from leaves to Vigna

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radiata (mung bean) roots, resulted in an increase in rhizosphere microbial population,

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nodulation and activity of phosphate mobilizing enzymes (acid phosphatase, alkaline

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phosphatase, phytase and dehydrogenase) when tested at a concentration of 10 mg.L-1.49 ZnO-

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NPs at a concentration of 1000 mg.L-1 enhanced fibre, carbohydrate, fat and ash content in

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Spinacia oleracea (spinach) leaves and increased chlorophyll content, growth parameters and

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yield in V. radiata, Cicer arietinum (chickpea), Pennisetum americanum (pearl millet) and

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Arachis hypogaea (groundnut) grown in pots and/or field conditions.48,49,51-53 In Lycopersicum

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esculentum (tomato), increases in flowering, fruit yield and fruit lycopene content in addition to

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other growth parameters was reported 14 days after application of 250-750 mg.Kg-1 via aerosol


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mediated foliar spray.54 Foliar spray of Zn-chitosan NPs (25 ml, Zn content of 20 mg.g-1) before

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anthesis (60 days post germination) in T. aestivum plants grown in sand and irrigated with Zn

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deficient Hoagland’s nutrient medium, increased Zn content in the grains.50 Fe is majorly located

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in the plant chloroplast and foliar application of Fe-NPs is reported to stimulate synthesis of

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chlorophyll, carbohydrates and growth parameters in plants.55 In Ocimum basilicum (sweet

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basil), the effectiveness of foliar spray of magnetite NPs (Fe3O4-NPs, 1-3 mg.L-1) for increase of

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biomass and essential oil content was reported due to the formation of insoluble complexes of

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Fe3O4 with phytoferritin in leaves, resulting in the persistence of Fe3O4 on the leaf surface,

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allowing prolonged stimulation of chlorophyll synthesis by the Fe ions.56 Spraying of citrate

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coated negatively charged maghemite NPs (γ-Fe2O3-NPs) on the adaxial as well as abaxial leaf

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surfaces of the four and eight trifoliate leaf stages in Glycine max, enhanced the net

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photosynthetic rate, stomatal conductance and transpiration rates due to increase in stomatal

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opening.55 Positive effects of foliar application of Fe2O3-NPs have also been observed in C.

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maxima and V. unguiculata subsp. unguiculata.39,57 However, the concentration of Fe applied

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plays a crucial role on the type of effect on plants. Concentrations of 250-500 mg.L-1 of Fe-NPs

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were optimal for enhancing biomass/chlorophyll content in V. unguiculata subsp. unguiculata.

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However, concentrations as low as 50 mg.L-1 begin to be toxic, and stress responses such as

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increased wax content on leaves to prevent excessive uptake of Fe ions was activated in C.

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maxima.

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content, redox status and yield in Z. mays.58 A combination of foliar spray of SiO2-NPs and

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farmyard manure stimulated canopy spread, and increased the number of achenes in capitulum of

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Carthamus tinctorius L. (safflower) grown in fields.59 In addition, SiO2-NPs were reported to

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alleviate cadmium toxicity in rice when applied to leaves.60 The effects of foliar application for

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Silica NPs (SiO2-NPs) at a concentration of 15 g.L-1 enhanced growth, phenol



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NPs of Mn, Molybdenum (Mo) and Nickel (Ni) have not been investigated. Effectiveness of

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foliar sprays of bulk Mn, Mo, Ni fertilizers for correcting nutrient deficiency and enhancing

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crop yield are well documented.61-63 Although, the effectiveness in case of foliar application

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can be limited due the holding capacity of leaf and the leaf surface area, plants are reported to

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respond faster to foliar fertilization as compared to the soil application approach.64, 65 Therefore,

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development of surface modified micronutrient NPs with hydrophobic/ hydrophilic molecules

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for longer persistence on leaf surface or better absorption through cuticles would be

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advantageous to bring about positive effects in plants. Alternatively, foliar application of certain

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micronutrient NPs which have poor absorption profiles through roots should be encouraged in

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combination with other NPs applied via the soil route.

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NPs of non-essential elements

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Although Ti is a non-essential element for plants, application of titanium dioxide NPs (TiO2-NP)

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is reported to have greater effects in promoting plant growth than bulk TiO2.26,66,67 Under

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nitrogen deficient conditions, foliar application of nano-anatase TiO2 at a dose of 2.5 g.L-1

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(0.25%) causes chemisorption of dinitrogen and its photoreduction to ammonium on exposure to

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sunlight, further leading to conversion of ammonium to organic nitrogen and protein in S.

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oleracea.66 Foliar spray of TiO2-NPs increased growth, chlorophyll content, light absorption and

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total soluble leaf protein in L. esculentum at a concentration of 500-1000 mg per pot.54 Silver

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NPs (Ag-NPs) induced positive growth response in V. unguiculata (cowpea) and Brassica

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juncea (mustard) at a concentration of 50 mg.L-1 and 75 mg.L-1 respectively.68 However, foliar

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application of Ag-NP (100 µg.g-1) exhibited neutral effects on growth of Lactuca sativa (lettuce)

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due to oxidation of Ag-NPs and complexation of Ag by thiol containing molecules, suggesting


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safe use of Ag containing foliar nano-pesticides for disease control in L. sativa.35 Studies using

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gold NPs (Au-NPs) report enhancement of growth, phenol content, redox status and yield in B.

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juncea.69 Ti, Au and Ag are not essential elements since there is no deficiency reported and

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plants can complete their life cycle without these elements. However, there are increasing reports

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documenting the role of NPs of non-essential elements in bringing about positive effects in

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plants, directly through the enhancement of physiological processes or indirectly by disease

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control.26,27,35,69 However, these studies also suggest that these element exhibit hormesis effect on

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plants, which is a dose dependent growth stimulation or retardation. Therefore, determining the

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dose of the NPs of non-essential elements for plant growth promotion is important. In addition,

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exhaustive studies are necessary for ascertaining the exact mechanisms of plant growth

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regulation by NPs of non-essential elements for their promotion as foliar nanofertilizers. Safety

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of NPs towards pollinators such as birds and insects also needs to be carefully evaluated for their

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use for foliar fertilization.

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Positive effects of NPs of other nanomaterials on plant growth on application via the foliar

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route

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Recently, carbon based nanomaterials such as fullerene, fullerenol and carbon nanotubes (CNTs)

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are gaining interest due to their ability to improve plant biomass.70-74 In a greenhouse study,

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foliar application of fullerenol (0.01 nmol mm-2 per leaf area) reduced drought induced oxidative

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stress in Beta vulgaris L. (sugarbeet) mainly by binding water and enhancing the activity of

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antioxidant enzymes (catalase, ascorbate peroxidase and guiacol peroxidase), saccharose content

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and malondialdehyde levels in treated plants.11 The ability of carbon based NPs to traverse the

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cell wall and cell membrane, make them potential delivery vehicles for small molecules and



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DNA75, thus functionalized carbon NPs can have an application for regulating the gene

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expression in plants, by acting as ‘nano-carriers’ of certain DNA regulatory molecules. Findings

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on the plant growth regulation by carbon based NPs in certain plants open new avenues for

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research on understanding the mechanisms underlying the physiological changes and growth

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promotion on uptake of carbon NPs. However, environmental implications and effects on other

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plant species also needs to be considered.

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Transport of NPs applied to the soil and/or the roots

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When applied to soil, NPs usually undergo biotransformation after interaction with organic

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materials and root exudates, which is followed by uptake and translocation to above and below

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ground plant parts.54 Small NPs (diameters ranging from 3-5 nm), are reported to enter plant

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roots due to osmotic pressure, capillary forces or by directly passing through the root epidermal

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cells.76,77 Walls of root epidermal cells are semipermeable due to the presence of pores

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(diameters ranging from 20-50 nm) restricting entry of NPs with larger sizes. Some NPs can

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induce formation of newer and larger pores in the epidermal cell wall facilitating their entry. 76,77

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After crossing the cell walls, NPs are transported through extracellular spaces apoplastically until

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they reach the central vascular cylinder allowing unidirectional upward movement through the

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xylem. However, to enter the central vascular cylinder, NPs must cross the Casparian strip

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barrier symplastically. This occurs by endocytosis, pore formation and transport by binding to

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carrier proteins of the endodermal cell membrane. Aquaporins and ion channels have pore sizes

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< 1 nm and are unlikely to transport NPs, however some studies suggest that carbon nanotubes

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can regulate aquaporin pore size for permeation in plant cells.21,25,33,78,79 Once internalized in the

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cytoplasm, NPs travel from one cell to another through the plasmodesmata.21,33 NPs which are


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not internalized by the endodermal cells, aggregate at the Casparian strip.33 NPs that have

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entered in the xylem are transported to the shoots. Subsequently, NPs can be translocated back to

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the roots from the shoots via the phloem.80 Aggregates of NPs taken up by plants can be located

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inside the cell wall of epidermal cells, cytoplasm of cortical cells and also in the nuclei.80 NPs

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which are not taken up from soil, aggregate on the root surface and may alter nutrient

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absorption.15,81 Direct uptake of NPs can occur in seeds via entry through parenchymatous

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intercellular spaces of the coat followed by diffusion in the cotyledon.21 Natural organic matter

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(NOM), minerals, soil organisms, pH, temperature, redox status of the soil environment are

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important parameters that influence the fate of NPs applied via the soil route. Capping of NPs by

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components of NOM with reactive functional groups such as carboxyl, amino, hydroxyl,

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sulfhydryl; dissolution of NPs and release of ions; complexation and chelation with minerals and

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clays; aggregation of NPs and degradation by soil microflora are some of the widely reported

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transformations of NPs occurring in soil.36,

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naturally formed in soil can contribute towards the effectiveness of NPs as nanofertilizers.36,87

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Rhizodeposits and exudates from plant roots also control other processes such as precipitation

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and detoxification of NPs in the rhizosphere.87 Transport of NPs through roots is represented

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schematically in fig. 1. Summary of the effects of NPs on plants at different doses when applied

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through soil route is provided in table 2.

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Positive effects of NPs on plant growth when applied through the soil

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Macronutrient NPs

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Macronutrient fertilizers are applied in large quantities to enhance crop production.

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Macronutrients especially N and P have low plant uptake efficiency, leading to wastage and

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leaching of fertilizers causing environmental issues.28 Therefore, use of slow release

82-86

Reactions between the applied NPs and NPs



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macronutrient NPK fertilizers is needed to enhance uptake, reduce wastage and control

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environmental problems. It is demonstrated that extruded urea-montmorillonite nanocomposites

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and urea-modified hydroxyapatite NPs encapsulated in Gliricidia sepium wood chips have

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controlled-N release capacity over 30 days.88,89 Sustained release urea-hydroxyapatite-NPs

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(having urea: hydroxyapatite ratio of 6:1 by weight) enhanced rice yield at a 50% lower rate of

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urea fertilizer application, thus reducing N wastage under field conditions.90 Sustained release

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urea-hydroxyapatite-KCl entrapped in montmorillonite and G. sepium wood chips, tested by soil

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leaching test over a period of 60 days, were more effective in enhancing the growth parameters

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in Festuca arundinacea seedlings than conventional NPK fertilizers due to efficient uptake of

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macronutrients by plants.91 Application of carboxy methyl cellulose (CMC) stabilized

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hydroxyapatite-NPs as P source (21.8 mg.L-1 P) enhanced growth rate and seed yield by 32.6%

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and 20.4%, respectively in Glycine max (soybean) plants as compared to the soybean plants

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treated with conventional Ca(H2PO4)2.92 Additional studies suggest that, hydroxyapatite-NPs

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reduce heavy the, reduce the bioavailability and mobility of heavy metals, induce synthesis of

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antioxidant enzymes to combat heavy metal stress and enhance growth of plants in contaminated

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soil.93-95 Although Ca deficiency in soil is rare, application of CaCO3-NPs (160 mg.L−1) in

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combination with humic substances is reported to enhance Ca uptake and growth in A.

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hypogaea.96 Magnesium oxide nanoparticles (MgO-NPs) are recently reported to induce reactive

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oxygen species (ROS) and systemic resistance when applied to roots at a concentration of 7

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mg.L-1, resulting in resistance against Ralstonia solanacearum and development of healthy L.

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esculentum plants.29 Urea is the most abundant N fertilizer applied to soil and is most often

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hydrolyzed to ammonia by soil urease.97 Ammonia is converted to nitrite via hydroxylamine, and

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further to nitrate by the soil nitrifier community. In waterlogged conditions such as during paddy


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cultivation, nitrates are lost to the atmosphere on conversion to N2 by the action of denitrifiers,

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which also generate greenhouse gases such as N2O in the process.97 Ill-effects of presence of

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excessive N fertilizers on seed germination and seedling growth are well documented.42,98 These

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reports necessitate application of sustained released N fertilizers to soil. However, currently there

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are limited studies on the development and efficacy of N based sustained release

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nanofertilizers.88-91 Development of newer multi-macronutrient NPs responsive to plant signals

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and exhibiting controlled release profile is the need of the hour for enhancing the macronutrient

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uptake efficiency in plants. Certainly, testing these novel and ‘smart’ NPs under greenhouse/field

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conditions will be necessary for determining their macronutrient release efficiency and uptake in

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plants under natural environmental conditions.

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Micronutrient NPs

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Zn is one of the major cationic micronutrients required by plants, and crops easily respond to Zn

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fertilization in soil. Zn deficiency causes stunted growth, chlorosis, reduced yield and poor

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nutritional quality.99-100 ZnO-NPs are reported to be less toxic to some plants as compared to

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bulk Zn fertilizers when applied to roots, indicating their potential use as nanofertilizers.101,102

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ZnO-NPs enhanced growth parameters and antioxidant status in L. esculentum and Gossypium

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hirsutum L. (cotton).103,104 Laboratory scale germination tests, hydroponic studies and pot based

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experiments have shown that ZnO-NPs enhance germination and growth in Zea mays (maize), C.

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arietinum and A. hypogaea at various concentrations (Table 2).52,105-107 In Cucumis sativus

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(cucumber), ZnO-NPs increased starch and protein content, which suggests that fertilization of

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soil with ZnO-NPs (800 mg.Kg-1) is beneficial for enhancing nutritional and caloric vsalue of C.

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sativus.108 ZnO-NPs also alleviate copper oxide NPs (CuO-NPs) induced toxicity in Phaseolus



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vulagris (common bean) and salt stress in L. esculentum.109-110 Iron is a part of cellular redox

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reactions and essential for the synthesis of chloroplast, and its deficiency results in whitening of

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leaves and chlorosis.17 Non-toxic nature of Fe-NPs towards L. sativa, radish and C. sativus is

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reported.111 Role of hematite NPs (α-Fe2O3-NPs) and ferrihydrite (5Fe2O3.9H2O) NPs in

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increasing chlorophyll content in hydroponically grown Z. mays and G. max seedlings is

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reported.112,113 Fe2O3-NPs (2-50 mg.L-1) applied to roots were transported to foliar parts and

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played a role in enhancing seed germination, seedling growth, and antioxidant enzymes in

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Citrullus lanatus (watermelon).114 Fe2O3-NPs increased abscisic acid, indole-3-acetic acid and

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malondialdehyde levels in transgenic and non-transgenic rice and enhanced growth in A.

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hypogaea grown in pot based experiments.115,116 Increase in growth, glycoprotein and protein

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concentration in leaves of A. hypogea was observed on seed priming and soil amendment with

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Fe3O4-NPs at a concentration of 4000 mg.L-1.117 Copper (Cu) plays an important role in

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photosynthesis, respiration, and plant growth.118 Although CuO-NPs are reported to induce

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oxidative stress in plants, a recent study has shown that a combination of Cu-Zn NPs enhanced

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redox status, photosynthetic pigments and leaf area in T. aestivum during drought stress.119 CuO-

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NPs enhanced germination and growth in L. sativa (concentration of 0.26 g.L-1) and were

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nontoxic at a concentration ranging from 0.25 -5 mg.L-1 to Elodea desnsa P. as compared to

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bulk CuSO4.120,121 Polyethylene glycol encapsulated CuO-NPs with chain like morphology

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exhibited reduced toxicity and effectively enhanced photosynthetic parameters, N and C

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assimilation in V. radiata at a dose of 0.05 to 1 mg.L-1.118 Seed priming with Cu-chitosan NPs

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resulted in improved vigor, synthesis and mobilization of starch and proteins in germinating Z.

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mays seedlings.122 Cu-NPs in chitosan hydrogels amended in potting medium boosted nutritional

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characteristics, biomass, lycopene content and yield in L. esculentum.123 Manganese is an


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essential plant micronutrient and its deficiency in plants results in chlorosis.17 Manganese

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nanoparticles (Mn-NPs) have been suggested as excellent fertilizers for L. sativa cultivation at

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low concentrations (50 mg.L-1).124 Mn-NPs (0.05 mg.L-1) enhanced growth, levels of

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photosynthetic and accessory pigments, and O2 uptake during the light reaction in the chloroplast

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of V. radiata seedlings, possibly due to translocation of NPs from roots to the shoots via xylem.30

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Mo is a cofactor of plant enzymes involved in N assimilation and rhizobial N fixation.17 A recent

321

study demonstrated that a combination of Mo-NPs (0.8 mg.g-1) and Ryzobofitom (Rhizobium

322

biofertilizer containing 8 Log CFU.ml-1 cells) improved antioxidant activity in C. arietinum

323

allowing better stress adaptation.125 Si is a normal component of soil and is deposited mainly in

324

endoplasmic reticulum, cell wall, intercellular spaces of plant cells and helps alleviate biotic and

325

abiotic stress.126,127 SiO2-NPs are reported to be nontoxic to growth of Oryza sativa (rice), Z.

326

mays and L. esculentum.127-129 Si accumulation after application of SiO2-NPs is reported to

327

contribute to drought tolerance in Z. mays and L. esculentum. 127-130 SiO2-NPs enhanced leaf area,

328

photosynthetic activity, proteins, phenols and population of beneficial rhizobacteria (phosphate

329

solubilizing bacteria, nitrogen fixers and silicate solubilizing bacteria) in Z. mays.58,130,131 All

330

these studies are indicative of the rapid progress in the

331

micronutrient NPs and assessment of their effect on plant growth and physiology. However, the

332

growth stimulatory effect of NPs is not a universal property as the response of plants may differ

333

based on the type of NPs and the plant species. Moreover, the positive effects of micronutrient

334

NPs on plant growth will also be governed by the type of environment under which the study has

335

been carried out. Presently, most of the testing has been carried out under laboratory conditions

336

or using hydroponic systems. However, under the influence of the natural environmental

337

conditions, the behavior of NPs as growth promoting agents may differ. For concrete


development of diverse types of


338

conclusions, subsequent to laboratory experimentation, confirmation of the growth stimulating

339

effects by NPs under field conditions is important. One has to also consider the effects of the

340

engineered NPs on the flora and fauna during field application. Multifaceted experimentations

341

may thus be required for ascertaining the role of micronutrient NPs as positive effectors for

342

plants with no consequences to animals/ microbes before labelling them as micronutrient

343

fertilizers.

344 345

NPs of non-essential elements

346

NPs of elements which are non-essential for plant growth have enormous industrial applications

347

and their effects on plants and the environment is recently gaining attention due to continuous

348

release in the environment.132,133 C. sativus and L. esculentum plants grown in soil supplemented

349

with rutile (0.5 g,L-1) and anatase (250-750 mg.Kg-1) TiO2-NPs increased levels of chlorophyll

350

and P content.134,135 L. sativa plants grown in soil containing TiO2-NPs (250 mg.kg-1) exhibited

351

higher biomass, cysteine, and methionine contents.136 In addition to higher biomass, B. juncea

352

and L. esculentum plants grown in Hoagland’s nutrient solution with TiO2-NPs had increased

353

levels of ROS scavengers (proline, malondialdehyde and antioxidant enzymes), indicating that

354

TiO2-NPs can help alleviate stress in plants.135,137 Ag-NPs exhibit excellent antimicrobial

355

properties as compared to bulk silver compounds and have proven beneficial as

356

nanopesticides.138 Ag-NP (100 mg.L-1) treated Bacopa monnieri plants had higher seedling

357

vigour, higher levels of protein and carbohydrate; and lower levels of total phenols, catalase and

358

peroxidase, in comparison to the plants treated with silver nitrate.139 Shape and charge on NPs is

359

an important parameter determining its effect on plant growth. Triangular (47 nm) and

360

decahedral (45 nm) Ag-NPs enhanced root growth and lowered oxidative stress in Arabidopsis,


Page 16 of 50

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361

whereas spherical Ag-NPs (8 nm) caused inhibition of cotyledon growth and increased the

362

oxidative stress. Treatment of Arabidopsis with triangular and decahedral Ag-NPs increased

363

accumulation of proteins involved in photosynthesis and hormone signaling. The study indicated

364

that the smaller size and higher ROS generation by spherical Ag-NPs induced negative effects in

365

Arabidopsis.140 To study specifically the shape based effects, Ag-NP nanospheres, nanocubes

366

and nanowires with similar mass based dose, particle concentration, and surface area were tested

367

on Lolium multiflorum seedlings and also on other soil organisms mainly Caenorhabditis

368

elegans, Escherichia coli, Bacillus cereus and Pseudomonas aeruginosa. As compared to the

369

Ag-NP nanospheres, Ag-NP nanocubes and nanowires were less toxic to the roots and the shoots

370

of germinating L. multiflorum seedlings, however, little differences in shape based toxicity

371

towards other soil organisms was recorded. Shape based toxicity differences could be due to

372

increased uptake of NPs of certain shapes by plants, and differences in their stability or

373

dissolution patterns in soil.141,142 Au-NPs (10 µg.mL-1) increased seed yield, growth parameters

374

and free radical scavenging activity in the seedlings of model plant Arabidopsis thaliana in

375

laboratory conditions, indicating that Au-NPs released in environment may have positive effects

376

on other related fodder crop species as well.143 NPs of other non-essential plant element, Cerium

377

(Ce) in the form of CeO2-NPs increased the content of globulin and flavoring compounds,

378

antioxidant capacity and fresh weight in soil grown C. sativus plants, indicating that the CeO2-

379

NPs released from industries can impact nutritive quality of fruits.108 Alumina nanoparticles

380

(Al2O3-NPs) at 0.3 g.L-1 enhanced the efficiency of light reactions in photosynthesis thereby

381

stimulating biomass increase in aquatic hydrophytic plant Lemna minor.144 This finding suggests

382

that Al2O3-NPs can play a role in growth stimulation in related terrestrial plant species as well.

383

These studies targeted on determining the effects of NPs of non-essential elements on plant



384

growth and physiology have revealed that TiO2-NPs, Ag-NPs, Au-NPs and Al2O3-NPs may

385

follow similar mechanisms for plant growth improvement as that of the essential elements; for

386

instance the ability to enhance photosynthetic light reactions, alleviation of stress, enhancement

387

of the levels of antioxidant enzymes and inhibition of plant pathogens.138,144. However, there are

388

limited observations on the long term effects of continuous exposure of non-essential elements

389

on plants, microbes and animals. Studies have shown that there is direct uptake and accumulation

390

of ions and NPs in above and below ground plant parts.22,23 Accumulation, concentration and

391

bio-magnification of NPs transported to the different plant organs over time can pose serious

392

ecological consequences. Therefore, long term monitoring of the effects of NPs of non-essential

393

elements is of utmost importance for their use as plant growth stimulants.

394 395

NPs of carbon based materials

396

Carbon based nanomaterials such as Fullerene-Multi-walled coated nanotubes (MWCNT) in

397

combination with natural organic matter are easily taken up by O. sativa seedlings.145 CNTs are

398

reported to penetrate the tomato seed coat and roots, generate new pores or regulate aquaporins

399

thereby increasing the water permeation inside the seeds, resulting in faster germination of seeds

400

and enhanced biomass.78,79 Uptake and accumulation of fullerol in Momordica charantia (bitter

401

gourd) seedlings resulted in heightened expression of anticancer compounds (cucurbitacin-B and

402

lycopene) and antidiabetic compounds (charantin and insulin) in the fruits; in addition to increase

403

in biomass, water content and fruit numbers.146 Although it was observed that industrial grade

404

MWCNTs (2560 mg.L-1) aggregated on the root surface and there was no uptake, an increase in

405

the root length was noted in Medicago sativa (alfalfa) and T. aestivum seedlings exposed to

406

MWCNTs.146 Chitosan NPs exhibit phytoimmunogenic properties, due to their ability to


Page 18 of 50

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407

upregulate defense enzymes (peroxidase, polyphenol oxidase, phenylalanine ammonia lyase, β -

408

1, 3-glucanase, nitric oxide, thaumatin like protein) in excised Camellia sinensis (tea) leaves in

409

comparison to bulk chitosan.147 Despite of the above positive effects of carbon based NPs,

410

contrasting effects such as formation of ROS and facilitation of uptake of toxic heavy metals and

411

metalloids in the plant system have been reported.148 However, the mechanism of action of

412

carbon based NPs in bringing about these manifestations are unclear warranting the need for

413

exhaustive and conclusive experimentation for the use of carbon based NPs as fertilizers.

414

Interactions of plant beneficial microflora with NPs

415

Plant health relies on colonization of its rhizosphere by plant beneficial microflora.149 NPs of

416

essential minerals enhance colonization of plants by beneficial microflora due to improved

417

adhesion of microbial cells on plant surfaces, stimulation in enzyme activity and enhancement in

418

synthesis of secondary metabolites, exopolysaccharides and antibiotics essential for rhizosphere

419

competence.28,31,150 On supplementation of ZnO-NPs at a concentration of 8 mg.L-1 in the growth

420

medium, rhizosphere colonizing Bacillus subtilis strain JCT1 produced 6-7 times more

421

exopolysaccharides with better soil aggregation and moisture retention properties useful for

422

agriculture in arid regions, whereas ZnO-NPs (18 mg.Kg-1) enhanced siderophore production by

423

17% in plant beneficial Pseudomonas chloraraphis strain PcO6.28,150,151 Fe3O4-NPs stimulated

424

colonization of G. max rhizosphere by Arbuscular mycorrhiza and rhizobia under greenhouse

425

conditions.

426

amyloliquefaciens 5113 to Brassica napus (oilseed rape) rhizosphere, thereby allowing better

427

colonization and pathogen control.31 Single application of Mo-NPs (8 mg.L-1) brought about two

428

fold increase in nodulation by Bradyrhizobium japonicum in C. arietinum grown under

429

greenhouse conditions and also increased population of other plant beneficial bacteria

152

TiO2-NPs enhanced adhesion of plant growth promoting strain of Bacillus



430

(actinomycetes, oligotrophic bacteria and bacteria involved in C, N and P cycles), thereby

431

promoting agronomically valuable microflora.153 Endophytic bacteria are also hypothesized to be

432

involved in control of dissolution and aggregation patterns of CuO-NPs and ZnO-NPs in T.

433

aestivum roots.154 Colonization of Glomus sp. helped to alleviate ZnO-NPs and Ag-NPs induced

434

toxicity in Z. mays and Trifolium repens (clover) seedlings respectively, possibly by reducing NP

435

induced stress.155,156 In turn, plants are reported to protect their rhizosphere mutualists

436

(arbuscular mycorrhiza and rhizobia) from toxicity of NPs of Zn, Fe and Ti.152,157 These studies

437

highlight that NPs of plant essential and non-essential elements act via diverse mechanisms for

438

eliciting plant beneficial activity in microbes, and in turn plant beneficial microbes participate in

439

NP transformations in rhizosphere/soil and in mitigating toxic effects which certain NPs have on

440

plants. However, stimulatory action of NPs is nonspecific and thus can also benefit pathogenic

441

microbes in plant rhizosphere, assisting in disease incidence. Therefore, suppression of

442

pathogens by other biocontrol mechanisms in combination with NP application can be deployed

443

for targeting the stimulatory action of NPs towards plant beneficial microbes. NPs functionalized

444

with molecules involved in ‘bio-stimulation’ of beneficial microbes can be alternatively tested.

445 446

NPs for control of agricultural pests

447

Metal NPs are potential candidates as nano-pesticides since they exhibit properties such as small

448

size, large surface area, permeability, thermal stability, solubility, and biodegradability.27 Nano-

449

pesticides comprising of metal NPs can target the pathogens through several mechanisms such as

450

generation of ROS, binding to metabolites and penetration of cells and spores.158 Other indirect

451

mechanisms include stimulation of plants to produce enzymes and compounds to combat

452

pathogen and induction of systemic resistance.29 In vitro antifungal activity of Cu-Chitosan


Page 20 of 50

Page 21 of 50


453

nanoconjugates, ZnO-NPs and Ag-NPs against plant pathogenic Alternaria sp., Fusarium sp.,

454

Pythium sp.; strains of Macrophomina phaseolina, Sclerotinia sclerotiorum, Botrytis cinerea,

455

Curvularia lunata, Bipolaris sorokiniana, Magnaporthe grisea and Rhizoctonia solani are

456

reported.151,159-163 In pot based assays using soil amendment, Cu-Chitosan nanoconjugates

457

(0.12%, 10 ml per plant) were effective in prevention of Alternaria early blight and Fusarium

458

wilt in L. esculentum.162 On addition to solid and liquid growth medium at a concentration of 500

459

mg.L-1, fungistatic action of ZnO-NPs and CuO-NPs reduced the production siderophore like

460

metabolites by plant pathogenic Pythium sp., thus interfering in the Fe uptake mechanisms which

461

are necessary for fungal growth.163 Foliar spray of CuO-NPs exhibited superior efficacy at

462

concentrations lower than four other commercial copper based fungicides in controlling

463

Phytophtora infestans late blight symptoms of L. esculentum leaves and were non-toxic to

464

seedlings when tested under field conditions.164 There are limited studies on effect of NPs

465

against bacterial plant pathogens. A recent study reports activation of salicylic acid, jasmonic

466

acid and ethylene signaling pathways, accumulation of β-1,3-glucanase and tyloses on

467

application of Mg-NPs (1% suspension) to L. esculentum roots, which was useful to prevent R.

468

solanacearum infection.29 Most of the studies using NPs are targeted towards fungal plant

469

pathogens. Development of effective nanopesticides against bacterial plant pathogen needs to be

470

explored. One potential approach is to use nanoconjugates with bacterial quorum sensing

471

inhibitors for specifically controlling the plant pathogens, since such strategies have been

472

successfully applied for animal pathogens.165,166 It is also uncertain, if the NPs used for fungal

473

pest control would affect plant beneficial association between mycorrhiza and other beneficial

474

fungal strains such as Trichoderma sp. All these aspects need to be researched for determining

475

suitability of NPs for dual purpose of biocontrol and plant growth promotion.



476

Negative effects of nanoparticles on plants

477

NPs applied via foliar route

478

Studies on long term effects of foliar application of 100 ppm Fe3O4-NPs have demonstrated that

479

NP application enhanced growth and physiological parameters in Z. mays only in the first

480

generation, whereas repeated application of NPs in the subsequent generations resulted in

481

reduction in growth and physiological parameters, mainly chlorophyll content, photosynthesis,

482

ferritin, Ca and Fe contents. Observed effects can be attributed to the Fe inherited in seedlings of

483

the second generation which was sufficient for the growth and any additional treatment with NP

484

caused toxicity and altered the growth in Z. mays.167 At doses above 26%, CaCO3-NP induces K

485

deficiency because of the reduction in K uptake in C. tankan.38 Foliar application of γ-Fe2O3-NPs

486

in C. maxima above 100 mg.L-1 can cause toxic effects.57 CuO-NPs reduce photosynthetic

487

activity, induce chlorosis, stunting, necrosis, deformation of stomata indicating oxidative stress

488

in Brassica oleracea var. capitata (cabbage) and L. sativa plants, in comparison to control plants

489

without any treatment. However, it is difficult to comment whether the negative effects were due

490

to the nanoparticulate nature of CuO or exclusively due to ion toxicity, since the study did not

491

have bulk CuO as a control in the foliar treatment. The Cu content in L. sativa and Brassica

492

oleracea var. capitata were 2-45 times higher than the Tolerable Daily Intake as set by the US

493

Environment Protection Agency, indicating that foliar application of CuO-NPs can cause

494

contamination of vegetables.168 Ce nanoparticles can be taken up and stored in plants and pose a

495

threat to the environment and humans. In addition, Ce generates ROS which damages the plant

496

cells.169 No negative effects on foliar application of ZnO-NPs and Zn-Chitosan nanoconjugates

497

are reported. Negative effects after foliar application of NPs containing P, C, Ti, Ag, Au, Al and

498

Si as active elements are not reported. Toxicity of NPs is dependent on dose and environmental 22 ACS Paragon Plus Environment

Page 22 of 50

Page 23 of 50


499

conditions.25, 87, 133 Studies indicate that the dose for toxicity of NPs differs with respect to the

500

host plant. For example, γ-Fe2O3-NPs above the concentration of 100 mg.L-1 were toxic to C.

501

maxima, whereas a concentration of 500-1000 mg/L was necessary for growth stimulatory

502

effects in G. max.55,

503

confines our understanding about potential risks of NPs applied through this route. A recent

504

study indicates that it is important to determine the long term effects of NP application on plants,

505

as indicated by the risk associated with of accumulation of toxic levels of ions in maize kernels

506

over generations.167 The negative effects of some of NPs on animals are well documented.170

507

Similarly, thorough nano-toxicological studies in plant models and the establishment of standard

508

test procedures for safe use of NPs as nanofertilizers is an urgent need.

57

There are limited studies reporting foliar application of NPs, which

509 510

NPs applied through soil

511

Hydroxyapatite-NPs (30 nm, 1-5 mg.L-1) inhibited hypocotyl elongation in V. radiata bean

512

sprouts by entering cells and increasing the intracellular Ca+2 concentrations leading to activation

513

of Ca2+-dependent endonucleases and apoptosis.171 At concentrations between 5-10 mg.L-1

514

hydroxyapatite-NPs aggregated forming bigger particles affecting entry in the cells and

515

alleviating inhibition. In addition, uptake of hydroxyapatite-NPs caused excessive movement of

516

microtubules leading to exhaustion of cell ATP levels and hampered mitochondrial function.170

517

ZnO-NPs prevented root and shoot growth, reduced biomass and chlorophyll content in A.

518

thaliana, Z. mays, O. sativa and T. aestivum.16,77,129,156,172 Ill effects of ZnO-NPs are attributed to

519

aggregation of NPs on roots and release of Zn+2 ions from ZnO-NP to soil.77,155 In Lolium

520

perenne (ryegrass), ZnO-NPs generated holes and increased the permeability of plant cell walls,

521

damaging the epidermal, cortical, endodermal and vascular cells causing growth inhibition. Zn+2



522

ions or ZnO-NPs at a concentration above 50 mg/L, caused shoots to turn yellow, whereas a

523

concentration of 1000 mg/L was completely lethal to the L. perenne seedlings. Toxicity of ZnO-

524

NPs was also dependent on growth-stage with the older L. perenne seedlings being less sensitive

525

to three times higher concentration of ZnO-NPs, than the newly germinated seedlings of the

526

same plant species.76 However, concentration of ZnO-NPs ranging from 750-1000 mg/L

527

stimulated growth and nutritional value in other plants such as A. hypogaea, C. sativus and

528

Spinacia oleracea (spinach), indicating that the level of NP toxicity can be dependent on plant

529

species.51,52, 108 At concentrations of 32 mg.kg-1, FeO-NPs caused growth retardation in T. repens

530

and reduced biomass and glomalin levels in mycorrhiza Glomus caledonium.155 The exposure to

531

CuO-NPs and Ag-NPs hampered mineral uptake and growth in P. vulgaris and Raphanus sativus

532

(radish) respectively.109,173 In O. sativa and B. juncea, CuO-NPs caused reduction in

533

photosynthesis, and an increase in anti-oxidative enzymes, whereas in transgenic G. hirsutum,

534

inhibition of phytohormone production (indole acetic acid, abcisic acid, giberllic acid and

535

transzeatinriboside) was observed.108,174,175 TiO2-NPs when applied at a concentration of 4307.5

536

mg.Kg-1 aggregated on root periderm and reduced biomass in T. aestivum, as well as soil enzyme

537

activities.77 Al2O3, Co and Ni-NPs treatments posed deleterious effect on biomass in above and

538

below ground tissues of L. esculentum and Z. mays.129,176 Uptake of CNTs (400 mg.L-1) in xylem

539

vessels of rice affected nutrient and water uptake resulting in delayed flowering and seed

540

setting.145 The currently available information clearly shows that toxicity of NPs is dose, particle

541

size, host plant and plant growth-stage dependent. At higher doses, metal oxide NPs aggregate

542

on root/ seed surface due to physical attachment, electrostatic attraction and hydrophobic

543

interactions, causing local accumulation of ions released from the NPs to toxic levels.111 On the

544

other hand, studies have also reported that aggregates of NP with larger sizes are not taken up to


Page 24 of 50

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545

the shoot, thereby eliminating the toxicity or restricting it to the root surface.76,171 The negative

546

effects of NPs containing Au, Ce, Si upon soil application have not been studied well, and needs

547

to be evaluated due to their extensive use in commercial products, drug delivery systems and

548

industries can lead to increased release in the soil environment. Studies have indicated that that

549

NPs containing Ca, Mo, Mg and mineral nanoconjugates of chitosan and montmorillonite

550

exhibited limited negative effects on plants after soil application.29,88,96,125

551

Negative effect of NPs on plant beneficial microflora

552

The soil bacterial taxa sensitive to TiO2-NP (2 mg.g-1) and ZnO-NP (0.5 mg.g-1) exposure

553

include those involved in N2 fixation, methane oxidation, and organic matter decomposition;

554

indicating that these ecosystem processes are sensitive to the presence of NPs in soil.177 TiO2-

555

NPs reduced the population of Arbuscular mycorrhiza in endorhizosphere of G. max, in contrast

556

to Fe-NP treatment which enhanced the population of Arbuscular mycorrhiza, however none of

557

the NPs (100-200 mg.Kg-1 soil) affected colonization of G. max by Arbuscular mycorrhiza.152

558

ZnO-NPs reduced biofilm formation and activity of enzymes involved in nitrification, urea and

559

starch degradation in two soil bacteria P. aeruginosa and B. subtilis above the concentration

560

range of 50 -200 ppm.178,179 Toxic effect of the NPs in microbes are due to the uptake of NPs by

561

the microbial cells, its chemical nature and concentration in the soil and within the plant roots,

562

interactions of ions released from the NPs with DNA and other cellular biomolecules, changes

563

brought about by the NP in protein expression, cell membrane stability, metabolism of other

564

nutrients and disruption of quorum sensing.165,178-180 It is clear that NPs can negatively regulate

565

several soil enzyme activities, microbial physiological processes and beneficial plant-microbe

566

associations. The ‘side effects’ on soil microbial communities can be controlled by using

567

biodegradable polymer coated NPs, which would release metal ions in response to microbial



568

degradation at a sustained rate. However, inhibitory action of NPs against microbial processes

569

such as denitrification and nitrification can be advantageous to control nitrogen losses and

570

production of greenhouse gases from agricultural soils.

571 572

Summary: research needs and future study

573

In summary, the literature suggests that the mode of application and concentration of NPs for

574

bringing about growth promotion, stimulation of physiological processes and induction of

575

toxicity vary according to the plant species and growth stage. Therefore, there is a need to

576

perform plant specific tests to ascertain if a particular NP is beneficial or harmful to plant growth

577

and productivity. It is clear that the uptake and translocation of intact NPs, as well as that of ions

578

dissolved from NPs successfully occurs after application of NPs through either foliar or soil

579

modes. However, the transformation and aggregation of applied NPs prior to uptake can restrict

580

its effectiveness as a nanofertilizer. Therefore, research has to be focused on producing

581

nanofertilizers with sustained release properties enabling slow release of mineral ions entrapped

582

in NPs of biodegradable/ natural polymer/materials such as chitosan, carboxy methyl cellulose,

583

kaolinite, montmorillonite, hydroxyapatite, exopolysaccharide, polyhydroxyalkanoate and

584

mesoporous silica. Biopolymer-mineral nanoconjugates may have scope as novel nanofertilizers

585

with higher stability, biodegradability and reduced toxicity for agricultural applications. It is

586

clear from the literature that physiochemical properties of NPs mainly size can affect the

587

dissolution and stability of NPs in solution and soil, and control plant uptake. However, there is

588

sparse information available on the role of other properties such as shape and charge of NPs in

589

bringing about beneficial or toxic effects in plant systems. Therefore, future investigations

590

directed towards synthesizing new plant-friendly nanomaterials should include a number of


Page 26 of 50

Page 27 of 50


591

physiochemical parameters of NPs to shed more light on their importance in plant systems. Very

592

little research on the effects of foliar application on NPs is available, and research should be

593

directed on synthesis of NPs of minerals with poor bioavailability through soil for application via

594

foliar routes. Exhaustive gene expression and physiology studies should be considered necessary

595

in order to understand the complex interactions of plant associated microbes with NPs. Most

596

importantly, knowledge of the performance of NPs under field conditions is essential to affirm

597

their efficacy on par with laboratory based hydroponic studies and in comparison to existing bulk

598

mineral fertilizers, for increasing acceptability of nanotechnology in agriculture. In future,

599

nanotechnology can provide superior solutions in agriculture for crop improvement, disease

600

prevention and environmental protection.

601

Acknowledgement

602

The Library facilities at Birla Institute of Technology and Science Pilani KK Birla Goa Campus,

603

Goa, India are greatly acknowledged. GAA thanks the Science and Engineering Research Board

604

(SERB), Department of Science and Technology (DST), Govt. of India for financial support

605

(Grant No. PDF/2016/001893).

606 607

Funding Source

608

GAA is supported by the SERB-DST, Govt. of India through the National Post-Doctoral

609

Fellowship (Grant No. PDF/2016/001893).

610 611

Conflict of interest

612

The authors declare no competing financial interest.



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Fig. 1: Schematic representation of the uptake of NPs in plants after foliar and soil/root application in a dicot. After entry through stomata, NPs travel by the apoplastic and symplastic routes to enter the phloem leading to subsequent transport to different plant parts. On application to soil/root system, NPs cross the epidermal cells and are transported mainly via the apoplast until they reach the endodermis. On internalization by the endodermal cells, NPs are first transported unidirectionally to the shoots via the xylem vessels, and later back to the roots from the shoots via the phloem.


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Table 1 Overview of the effects, mechanism of plant growth promotion, physical properties and concentrations of nanoparticles of essential minerals and non-essential elements applied via foliar route. Nanoparticles of essential macronutrients Active

Effects

Particle size and

element Ca

Reference

concentration Increase in Ca uptake and control of insect pests in Z.

60 nm; 26%

38

mauritiana. Mg

Enhanced growth and yield, uptake of minerals and enzyme 0.25-0.5 g.L-1

39

activity in T. aestivum and V. unguiculata subsp. unguiculata.

40

< 5.9 nm; 20 ppm

Nanoparticles of essential micronutrients Zn

Enhanced fibre, carbohydrate, fat and ash content in S. oleracea 10 ppm

48

and increased growth, chlorophyll content and yield in A. 50 nm; 1000 ppm

51

hypogaea, P. americanum, V. radiata and C. arietinum.

25nm; 1000 ppm

52

18.5 nm, 10 mg g.mL-1

53

rate of 16 L.ha-1 Increased yield, fruit numbers, mass, lycopene content and size, 22.4 nm, 10 mg.L-1

Fe

flowering and nutrient mobilizing enzymes in L. esculentum.

250 - 750 mg kg.-1

Heightened Zn content in T. aestivum grains.

325 nm; 20 mg Zn.g-1

Enhancement in carbohydrate content and essential oil 12.6 nm; 1-3 mg.L-1

54

50 56

concentration in O. basilicum. Increased photosynthetic rate, stomatal conductance and 0.25 and 0.5 g.L-1

55

transpiration rates in G. max and growth parameters in C. 500-1000 mg.L-1

57



20-100 mg.L-1

maxima and V. unguiculata subsp. unguiculata.

Si

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Enhanced chlorophyll, protein, phenol contents and redox status 20-40 nm; 15 mg.L-1

58

in Z. mays. Enhanced canopy spread, stem diameter, plant height, ground 2-30 nm; 20 mM

59

cover and the number of achenes in capitulum in C. tinctorius. Alleviation in cadmium toxicity in O. sativa.

60 nm; 2.5 mM

60

Nanoparticles of non-essential elements Ti

Increased growth parameters, organic nitrogen, O2, protein and 5 nm; 0.25%

66

chlorophyll content in S. oleracea. Increases in growth, chlorophyll content, light absorption and 25 nm,

67 -1

total soluble leaf protein in V. radiata.

250 - 1000 mg.kg

Ag

Positive response in growth of B. juncea and V. unguiculata.

35-40 nm; 50 -75 ppm

68

Au

Enhanced growth parameters, redox status and yield in Brassica 10-20 nm; 10-25 ppm

69

juncea under field conditions. Other plant growth enhancing nanomaterials Carbon

Reduction in the oxidative stress generated during growth of B. 30-105 nm; 0.01 and -2

vulgaris grown in drought conditions.

0.001 nmol mm per leaf area


11

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Table 2 Overview of the effects, mechanism of plant growth promotion, physical properties and concentrations of nanoparticles of essential minerals and non-essential elements applied via soil route. Nanoparticles of essential macronutrients Active

Effects

Concentration

Reference

element N

Slow

release

urea-hydroxyapetite

nanorods

enhanced 18 nm; urea: hydroxyapetite

90

bioavailability of urea by in rice seedlings and reduced N 6:1 wastage as compared to bulk urea. N, K

Montmorillonite and Gliricidia sepium wood chip entrapped -

91

urea-HA and K increased growth parameters in Festuca arundinacea seedlings. HA-NP reduced stress response and enhanced growth in

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