Elsevier

Plant Physiology and Biochemistry

Volume 110, January 2017, Pages 194-209
Plant Physiology and Biochemistry

Review
Role of nanomaterials in plants under challenging environments

https://doi.org/10.1016/j.plaphy.2016.05.038Get rights and content

Highlights

  • This review presents recent advances in NMs-plants interaction under abiotic stress.

  • NMs possess the capacity to penetrate targeted cellular locations.

  • NMs protect plants against various abiotic stresses and also cause phytotoxicity.

  • Plants’ defense system and stress-related gene expression are elevated by NMs.

  • NMs are hypothesized to play a role in stress-signal transduction.

Abstract

The application of nanostructured materials, designed for sustainable crop production, reduces nutrient losses, suppresses disease and enhances the yields. Nanomaterials (NMs), with a particle size less than 100 nm, influence key life events of the plants that include seed germination, seedling vigor, root initiation, growth and photosynthesis to flowering. Additionally, NMs have been implicated in the protection of plants against oxidative stress as they mimic the role of antioxidative enzymes such as superoxide dismutase (SOD), catalase (CAT) and peroxidase (POX). However, besides their beneficial effects on plants, applications of NMs have been proved to be phytotoxic too as they enhance the generation of reactive oxygen species (ROS). The elevated level of ROS may damage the cellular membranes, proteins and nucleic acids. Therefore, in such a conflicting and ambiguous nature of NMs in plants, it is necessary to decipher the mechanism of cellular, biochemical and molecular protection render by NMs under stressful environmental conditions. This review systematically summarizes the role of NMs in plants under abiotic stresses such as drought, salt, temperature, metal, UV-B radiation and flooding. Furthermore, suitable strategies adopted by plants in presence of NMs under challenging environments are also being presented.

Introduction

Nanomaterials (NMs), once called by Paul Ehrlich as “Magic Bullets” (Kreuter, 2007), are one of the most studied materials of the century that gave birth to a new branch of science known as ‘nanotechnology’. The specific quality of NMs which make these tiny entities unique, is their size which ranges between 1 and 100 nm (1 nm = 10−9 m) (Ball, 2002). Although, NMs can be prepared from the bulk size materials but small size and shape of these particles make their chemical action entirely different from their parent material (Brunner et al., 2006). Smaller size of NMs helps them to penetrate specific cellular locations and their additional surface area facilitates more adsorption and targeted delivery of substances (Kashyap et al., 2015). The NMs exist in volcanic dust, mineral composites (natural NMs) as well as in anthropogenic waste materials like coal combustion, diesel exhaust, welding fumes etc. (incidental NMs) (Monica and Cremonini, 2009). Moreover, engineered NMs manufactured with nanoscale dimensions are generally grouped into four types viz. carbon based NMs, metal based NMs, metal oxides, dendrimers and composites (Yu-Nam and Lead, 2008).

Engineered NMs have revolutionized almost every field of science and of course, plant science could not remain unaffected. These NMs have been shown to affect plants at every stage of their life cycle (Caňas et al., 2008, Lahiani et al., 2013, Siddiqui and Al-Whaibi, 2014, Liu et al., 2016). Fertilizers are integral part of agriculture that assist growth and development of plants. However, recently employed nano-fertilizers have been proved more efficient alternatives to regular fertilizers. Smaller size of nanoparticles (NPs) provides additional surface area which enhances the availability and facilitates more absorption of fertilizers by the plants and thus reduces losses of fertilizers due to leaching, emissions, and long-term incorporation by soil microorganisms (Liu et al., 2006, DeRosa et al., 2010). Moreover, nano-fertilizers are released at slower rates which help in maintaining soil fertility by decreasing the toxic effects associated with over-application of traditional chemical fertilizers (Suman et al., 2010).

Being sessile organisms, plants have no choice to escape or hide from adverse environmental conditions such as drought, salinity, water logging, extreme temperature, UV-radiation, etc. These stresses create oxidative stress by inducing generation of reactive oxygen species (ROS) such as singlet oxygen (1O2), superoxide radical (O2radical dot), hydroperoxy radical (HO2radical dot), hydrogen peroxide (H2O2) and hydroxyl radical (OHradical dot). Excessive accumulation of ROS damages membrane lipids, proteins and nucleic acids (Foyer and Noctor, 2000), triggers cytotoxicity, genotoxicity (Ghosh et al., 2015, Shen et al., 2010a, Shen et al., 2010b, Yadav et al., 2014) and suppresses growth (Begum et al., 2012). To counter oxidative stress, plants are fitted with a system of enzymatic antioxidants viz. superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR) and non-enzymatic antioxidants (glutathione, ascorbate) which continuously scavenge harmful ROS. Whereas, plants counter osmotic stress by enhancing the accumulation of organic osmolytes such as trehalose, polyols (glycerol, inositols, sorbitols etc.), amino acids (proline, glycine betaine and taurine) which maintain normal hydration level of cells. Under hypoxic conditions plants are deprived of proper supply of oxygen which causes energy depletion and settle the plants with low energy status, however, to maintain energy level plants alter their metabolism and switch over from carbohydrate metabolism to fermentation (Banti et al., 2013). To counteract metal stress plants synthesize metal-chelates, organic acids and polyphosphates that cause restriction and sequestration of toxic metals either in apoplasm or symplasm.

In addition to their role in plant growth and development, NPs play significant role in the protection of plants against various abiotic stresses (Table 1). The NPs mimic the activities of antioxidative enzymes and scavenge these ROS (Rico et al., 2013a, Rico et al., 2013b, Wei and Wang, 2013). Small size and large surface area of NPs provide access for toxic metals for binding and thus reduced availability and toxicity of metals (Worms et al., 2012). Under abiotic stresses, photosynthesis is highly susceptible cellular process, however NMs have been shown to protect photosynthetic system and improve photosynthesis by suppressing oxidative and osmotic stress (Haghighi and Pessarakli, 2013, Qi et al., 2013, Siddiqui et al., 2014). However, response of plants to NMs varies differently depending on plant species and NMs applied (Lin and Xing, 2007). Apart from their beneficial effects several NMs show toxicity symptoms (Slomberg and Schoenfisch, 2012, Begum and Fugetsu, 2012). Presence of NMs in the growth medium induces oxidative stress and causes reduction in germination rate, root and shoot length, and loss of photosynthesis, chlorophyll (Chl), biomass (Barhoumi et al., 2015, Da Costa and Sharma, 2016, Wang et al., 2016), and nutritive value of crop plants (Peralta-Videa et al., 2014). The NMs also alter gene expression involved in biotic and abiotic stress responses, cell biosynthesis, cell organization, electron transport, and energy pathways (Landa et al., 2012, Kaveh et al., 2013, Aken, 2015).

Therefore, role of NMs in growth and development and in the tolerance of plants to abiotic stresses is ambiguous and controversial. In the present article an attempt is made to shed light on the recent updates on the role of NMs under abiotic stress conditions.

Section snippets

Nanomaterials and plant growth

Plants growing under natural environmental conditions are constantly exposed to a combination of biotic and abiotic stresses. As far as abiotic stresses are concerned, drought salinity, water logging, heat, cold, metal, UV radiation etc. are some common stresses which plants face at some or the other stages of their life cycle. Several studies show that NMs play vital role in alleviating abiotic stresses and stress-induced alterations in plants (Table 1).

Seed germination is the first stage of

Nanomaterials and photosynthesis under abiotic stresses

Photosynthesis, the foundation for all the metabolic processes in plants, is considered as one of the most sensitive physiological processes to environmental stresses. Therefore, maintenance of optimal photosynthetic rate is vital for the endurance of plants under stressful conditions. Plants treated with NMs show protection against various abiotic stresses and exhibited improved rate of photosynthesis, stomatal conductance, transpiration rate, water use efficiency, and Chl and proline content

Nanomaterials and plants under abiotic stresses

Overproduction of ROS by various cell organelles is the signature effect of abiotic stress-induced oxidative stress. Apart from damaging effect, ROS are also known to trigger various defense systems through activating cell signaling cascade and inducing or suppressing the expression of many genes (Hancock et al., 2001). Nonetheless, plants are equipped with enzymatic and non-enzymatic system of antioxidants which continuously scavenge harmful ROS (Fig. 2). Regardless of such defense systems,

Phytotoxic effects of nanomaterials

As mentioned in the preceding pages, owing to their small size, shape and larger surface area to mass ratio, NMs enhance plant growth, productivity and provide protection against various abiotic stresses. On contrary, the same properties of NMs make them deliterious as they are known to induce oxidative stress, cytotoxic and genotoxic responses in plants (Tan and Fugetsu, 2007, Lin and Xing, 2007, Lin and Xing, 2008, Lin et al., 2009a, Lin et al., 2009b, Lin et al., 2010, Tan et al., 2009;

Mechanism of action of nanomaterials under abiotic stress

Although, plants are equipped with a network of defense units, but the precise perception and transduction of stress stimulus to the defense system and accurate temporal and spatial activation of these defense units in response to stress stimulus before the onset of stress-induced damage is crucial for the protection of plant’s cellular machinery. While going through the available information on NMs-plant interaction under abiotic stresses, it became evident that generation of ROS is a common

Conclusions

The available information reveals that NMs alleviate abiotic stress-induced damage through activating defense system of plants. Small size of NMs facilitates easy penetration and regulates water channels that assist seed germination and growth of plants; moreover, improved surface area facilitates more adsorption and targeted delivery of substances. On contrary, NMs have also been reported to trigger the generation of ROS and exhibit several toxic effects on plants. The enhanced ROS level by

Contributions

Khan M. N. planned and collected available literature and prepared first draft of the manuscript, Mobin M., Abbas, Z.K. and Siddiqui, Z.H. edited the MS and added their inputs on the section other stresses and AlMutairi, K.A. wrote the section phytotoxic effects of nanomaterials.

Acknowledgements

Financial support (Project no. S-0105-1436) by Deanship of Scientific Research (DSR), University of Tabuk is gratefully acknowledged. Authors are also thankful to the head of the Biology Department and Vice Dean of Higher Studies and Scientific Research, Faculty of Science, University of Tabuk.

References (236)

  • M. Faisal et al.

    Phytotoxic hazards of NiO-nanoparticles in tomato: a study on mechanism of cell death

    J. Hazard. Mater.

    (2013)
  • J. Gao et al.

    Effects of nano-TiO2 on photosynthetic characteristics of Ulmus elongata seedlings

    Environ. Pollut.

    (2013)
  • F. Gottschalk et al.

    Environmental concentrations of engineered nanomaterials: review of modeling and analytical studies

    Environ. Pollut.

    (2013)
  • R.A. Goyer

    Nutrition and metal toxicity

    Am. J. Clin. Nutr.

    (1995)
  • M. Haghighi et al.

    Low and high temperature stress affect the growth characteristics of tomato in hydroponic culture with Se and nano-Se amendment

    Sci. Hortic.

    (2014)
  • M. Haghighi et al.

    Influence of silicon and nano-silicon on salinity tolerance of cherry tomatoes (Solanum lycopersicum L.) at early growth stage

    Sci. Hortic.

    (2013)
  • M. Hasanuzzaman et al.

    Silicon and selenium: two vital trace elements that confer abiotic stress tolerance to plants

  • E. Hideg et al.

    UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates?

    Trends Plant Sci.

    (2013)
  • H. Jang et al.

    Photoluminescence quenching of silicon nanoparticles in phospholipid vesicle bilayers

    J. Photochem. Photobiol. A Chem.

    (2003)
  • P.L. Kashyap et al.

    Chitosan nanoparticle based delivery systems for sustainable agriculture

    Int. J. Biol. Macromol.

    (2015)
  • M.N. Khan et al.

    Interactive role of nitric oxide and calcium chloride in the tolerance of plants to salt stress

    Nitric Oxide

    (2012)
  • L.R. Khot et al.

    Applications of nanomaterials in agricultural production and crop protection: a review

    Crop Prot.

    (2012)
  • M.T.B. Aghdam et al.

    Effects of nanoparticulate anatase titanium dioxide on physiological and biochemical performance of Linum usitatissimum (Linaceae) under well-watered and drought stress conditions

    Braz. J. Bot.

    (2015)
  • B.V. Aken

    Gene expression changes in plants and microorganisms exposed to nanomaterials

    Curr. Opin. Biotechnol.

    (2015)
  • Z.M. Almutairi

    Effect of nano-silicon application on the expression of salt tolerance genes in germinating tomato (Solanum lycopersicum L.) seedlings under salt stress

    Plant Omics J.

    (2016)
  • N.A. Anjum et al.

    Single-bilayer graphene oxide sheet tolerance and glutathione redox system significance assessment in faba bean (Vicia faba L.)

    J. Nanopart Res.

    (2013)
  • W. Armstrong et al.

    Root growth and metabolism under oxygen deficiency

  • S. Arora et al.

    Gold-nanoparticle induced enhancement in growth and seed yield of Brassica juncea

    Plant Growth Regul.

    (2012)
  • P. Ashkavand et al.

    Effect of SiO2 nanoparticles on drought resistance in hawthorn seedlings

    Leśne Prace Badawcze

    (2015)
  • R. Azimi et al.

    Interaction of SiO2 nanoparticles with seed prechilling on germination and early seedling growth of tall wheatgrass (Agropyron elongatum L.)

    Pol. J. Chem. Tech.

    (2014)
  • P. Ball

    Natural strategies for the molecular engineer

    Nanotechnol

    (2002)
  • V. Banti et al.

    Low oxygen response mechanisms in green organisms

    Int. J. Mol. Sci.

    (2013)
  • L. Barhoumi et al.

    Effects of superparamagnetic iron oxide nanoparticles on photosynthesis and growth of the aquatic plant Lemna gibba

    Arch. Environ. Contam. Toxicol.

    (2015)
  • T.I. Brunner et al.

    In vitro cytotoxicity of oxide nanoparticles: comparison to asbestos, silica, and effect of particle solubility

    Environ. Sci. Technol.

    (2006)
  • C.E. Burklew et al.

    Effects of aluminum oxide nanoparticles on the growth, development, and microRNA expression of tobacco (Nicotiana tabacum)

    PLoS ONE

    (2012)
  • J.E. Caňas et al.

    Effects of functionalized and nonfunctionalized single walled carbon nanotubes on root elongation of select crop species

    Environ. Toxicol. Chem.

    (2008)
  • M. Capuana

    Heavy metals and woody plants biotechnologies for phytoremediation

    J. Biogeo. Sci. For.

    (2011)
  • A.W. Carpenter et al.

    Dual action antimicrobials: nitric oxide release from quaternary ammonium-functionalized silica nanoparticles

    Biomacromolecules

    (2012)
  • S. Chandra et al.

    Chitosan nanoparticles: a positive modulator of innate immune responses in plants

    Sci. Rep

    (2015)
  • H. Chen et al.

    Cadmium telluride quantum dots (CdTe-QDs) and enhanced ultraviolet-B (UV-B) radiation trigger antioxidant enzyme metabolism and programmed cell death in wheat seedlings

    PLoS ONE

    (2014)
  • H.-Z.Z.-J. Chen et al.

    Influence of enhanced UV-B radiation on F-actin in wheat division cells

    Plant Diver. Resour.

    (2011)
  • X. Chen et al.

    Photosynthetic toxicity and oxidative damage induced by nano-Fe3O4 on Chlorella vulgaris in aquatic environment

    Open J. Ecol.

    (2012)
  • W.Y. Cheung

    Calmodulin plays a pivotal role in cellular regulation

    Science

    (1980)
  • G.U. Chibuike et al.

    Heavy metal polluted soils: effect on plants and bioremediation methods

    Appl. Environ. Soil Sci.

    (2014)
  • G. Chichiriccò et al.

    Penetration and toxicity of nanomaterials in higher plants

    Nanomaterials

    (2015)
  • F.J. Corpas et al.

    Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development

    Planta

    (2006)
  • F.J. Corpas et al.

    Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants

    Plant Physiol.

    (2004)
  • M.V.J. Da Costa et al.

    Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa

    Photosynthetica

    (2016)
  • J. Dat et al.

    Dual action of the active oxygen species during plant stress responses

    Cell. Mol. Life Sci.

    (2000)
  • N.A. Delk et al.

    CML24, regulated in expression by diverse stimuli, encodes a potential Ca2+ sensor that functions in response to abscisic acid, daylength, and ion stress

    Plant Physiol.

    (2005)
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    This article is part of a special issue entitled “Nanomaterials in Plant”, published in the journal Plant Physiology and Biochemistry 110, 2017.

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