Abstract
Application of nanoparticles (NPs) in the management of plant diseases may reduce the use of pesticides and enhance food security. In this study, the effects of TiO2 NPs in 100 and 200 mg L−1 concentrations were examined against Meloidogyne incognita (Mi), Pectobacterium betavasculorum (Pb) and Rhizoctonia solani (Rs) under in vitro conditions and in a pot experiment. TiO2 NPs inhibited the growth of Pb and Rs and significantly reduced the hatching and caused mortality of Mi 2nd stage juveniles. As revealed from the scanning electron microscopy (SEM), TiO2 NPs react directly to the cuticle/cell wall of test pathogens. In pot experiments, TiO2 NPs were used as a foliar spray and seed priming. Foliar spray of TiO2 NPs was found to be more efficient than seed priming in enhancing the growth, activities of defense enzymes, photosynthetic performance, and disease resistance in beetroot. Foliar spray of TiO2 NPs at 200 mg L−1 resulted in the maximum increase in plant growth, activities of defense enzymes and photosynthetic performance of beetroot. Foliar spray of TiO2 NPs at 200 mg L−1 caused the maximum reduction in disease indices, nematode multiplication, and root galling. As revealed from the inductively coupled plasma mass spectrometry (ICP-MS) analysis, TiO2 NPs accumulated across the tissues of both infected and un-infected plants irrespective of the method of application. Overall, the findings show that TiO2 NPs as foliar spray have the potential to be applied for the management of soft rot, root rot and root-knot disease complex of beetroot.
Zusammenfassung
Die Anwendung von Nanopartikeln (NPs) bei der Bekämpfung von Pflanzenkrankheiten kann den Einsatz von Pestiziden reduzieren und die Ernährungssicherheit erhöhen. In dieser Studie wurden die Wirkungen von TiO2-NPs in Konzentrationen von 100 und 200 mg L−1 gegen Meloidogyne incognita (Mi), Pectobacterium betavasculorum (Pb) und Rhizoctonia solani (Rs) unter in vitro-Bedingungen und in einem Topfexperiment untersucht. TiO2-NPs hemmten das Wachstum von Pb und Rs und reduzierten signifikant das Schlüpfen und führten zur Mortalität von Mi-Juvenilen im zweiten Stadium. Wie aus der Rasterelektronenmikroskopie (REM) hervorging, reagieren TiO2-NPs direkt mit der Cuticula/Zellwand der Testpathogene. In Topfexperimenten wurden TiO2-NPs als Blattspray und zur Saatgutvorbehandlung eingesetzt. Die Blattspritzung mit TiO2-NPs erwies sich als effizienter als die Saatgutbehandlung, um das Wachstum, die Aktivitäten von Verteidigungsenzymen, die photosynthetische Leistung und die Krankheitsresistenz von Roter Bete zu steigern. Die Blattapplikation von TiO2-NPs in einer Konzentration von 200 mg L−1 führte zu einer maximalen Steigerung des Pflanzenwachstums, der Aktivitäten von Abwehrenzymen und der photosynthetischen Leistung der Roten Bete. Weiterhin hatte die Blattapplikation von TiO2-NPs bei 200 mg L−1 die maximale Reduzierung der Krankheitsindizes, der Nematodenvermehrung und der Wurzelgallenbildung zur Folge. Wie die Analyse der induktiv gekoppelten Plasma-Massenspektrometrie (ICP-MS) zeigte, reicherten sich TiO2-NPs im Gewebe sowohl infizierter als auch nicht infizierter Pflanzen an, unabhängig von der Applikationsmethode. Insgesamt zeigen die Ergebnisse, dass TiO2-NPs als Blattspray das Potenzial haben, für das Management des Krankheitskomplexes aus Weichfäule, Wurzelfäule und Wurzelknotenkrankheit bei der Roten Bete eingesetzt zu werden.
Similar content being viewed by others
References
Abdel Latef AAH, Srivastava AK, El-sadek MSA, Kordrostami M, Tran LSP (2018) Titanium dioxide nanoparticles improve growth and enhance tolerance of broad bean plants under saline soil conditions. Land Degrad Dev 29(4):1065–1073
Ahanger MA, Agarwal RM, Tomar NS, Shrivastava M (2015) Potassium induces positive changes in nitrogen metabolism and antioxidant system of oat (Avena sativa L cultivar Kent). J Plant Interact 10(1):211–223
Ardakani AS (2013) Toxicity of silver, titanium and silicon nanoparticles on the root-knot nematode, Meloidogyne incognita, and growth parameters of tomato. Nematology 15(6):671–677
Boxi SS, Mukherjee K, Paria S (2016) Ag doped hollow TiO2 nanoparticles as an effective green fungicide against Fusarium solani and Venturia inaequalis phytopathogens. Nanotechnology 27(8):85103
Chezem WR, Memon A, Li FS, Weng JK, Clay NK (2017) SG2-type R2R3-MYB transcription factor MYB15 controls defense-induced lignification and basal immunity in Arabidopsis. Plant Cell 29(8):1907–1926
Choi HG, Moon BY, Bekhzod K, Park KS, Kwon JK, Lee JH, Chao MW, Kang NJ (2015) Effects of foliar fertilization containing titanium dioxide on growth, yield and quality of strawberries during cultivation. Hortic Environ Biotechnol 56(5):575–581
Clifford T, Howatson G, West DJ, Stevenson EJ (2015) The potential benefits of red beetroot supplementation in health and disease. Nutrients 7(4):2801–2822
Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Dordrecht, pp 253–270 https://doi.org/10.1007/978-1-4020-8182-8_12
Cui H, Zhang P, Gu W, Jiang J (2009) Application of anatase TiO2 sol derived from peroxotitannic acid in crop diseases control and growth regulation. NSTI-Nanotech 2:286–289
De Filpo G, Palermo AM, Rachiele F, Nicoletta FP (2013) Preventing fungal growth in wood by titanium dioxide nanoparticles. Int Biodeterior Biodegrad 85:217–222
Derbalah A, Shenashen M, Hamza A, Mohamed A, El Safty S (2018) Antifungal activity of fabricated mesoporous silica nanoparticles against early blight of tomato. Egypt J Basic Appl Sci 5(2):145–150
Desai V, Meenal K (2009) Antimicrobial activity of titanium dioxide nanoparticles synthesized by sol-gel technique. Res J Microbiol 4(3):97–103
Dias MC, Santos C, Pinto G, Silva AM, Silva S (2019) Titanium dioxide nanoparticles impaired both photochemical and non-photochemical phases of photosynthesis in wheat. Protoplasma 256(1):69–78
Dong S, Qu M, Rui Q, Wang D (2018) Combinational effect of titanium dioxide nanoparticles and nanopolystyrene particles at environmentally relevant concentrations on nematode Caenorhabditis elegans. Ecotoxicol Environ Saf 161:444–450
Eisenback J (1986) A comparison of techniques useful for preparing nematodes for scanning electron microscopy. J Nematol 18(4):479
Fenoglio I, Greco G, Livraghi S, Fubini B (2009) Non-UV-induced radical reactions at the surface of TiO2 nanoparticles that may trigger toxic responses. Chemistry 15(18):4614–4621
Fraceto LF, Grillo R, de Medeiros GA, Scognamiglio V, Rea G, Bartolucci C (2016) Nanotechnology in agriculture: which innovation potential does it have? Front Environ Sci 4:20. https://doi.org/10.3389/fenvs.2016.00020
Frazier TP, Burklew CE, Zhang B (2014) Titanium dioxide nanoparticles affect the growth and microRNA expression of tobacco (Nicotiana tabacum). Funct Integr Genomics 14(1):75–83
Garcion C, Lamotte O, Cacas JL, Metraux JP (2014) Mechanisms of defence to pathogens: biochemistry and physiology. In: Walters DR, Newton AC, Lyon GD (eds) Induced resistance for plant defense: A sustainable approach to crop protection, 2nd edn. John Wiley & Sons, Chichester, pp 106–136
Gelover S, Gómez LA, Reyes K, Leal MT (2006) A practical demonstration of water disinfection using TiO2 films and sunlight. Water Res 40(17):3274–3280
Ghormade V, Deshpande MV, Paknikar KM (2011) Perspectives for nano-biotechnology enabled protection and nutrition of plants. Biotechnol Adv 29(6):792–803
Goujon T, Sibout R, Eudes A, MacKay J, Jouanin L (2003) Genes involved in the biosynthesis of lignin precursors in Arabidopsis thaliana. Plant Physiol Biochem 41(8):677–687
Haghi M, Hekmatafshar M, Janipour MB, Gholizadeh S, Faraz M, Sayyadifar F, Ghaedi M (2012) Antibacterial effect of TiO2 nanoparticles on pathogenic strain of E. coli. Int J Adv Biotechnol Res 3(3):621–624
Harveson RM, Hanson LE, Hein GL (2009) Compendium of beet diseases and pests, 2nd edn. American Phytopathological Society (APS Press), St. Paul, p 140
Hussain S, Iqbal N, Brestic M, Raza MA, Pang T, Langham DR, Safdar ME, Ahmed S, Wen B, Gao Y, Liu W, Yang W (2019) Changes in morphology, chlorophyll fluorescence performance and Rubisco activity of soybean in response to foliar application of ionic titanium under normal light and shade environment. Sci Total Environ 658:626–637
Keller AA, McFerran S, Lazareva A, Suh S (2013) Global life cycle releases of engineered nanomaterials. J Nanopart Res 15(6):1692
Khan MR, Siddiqui ZA (2019) Potential of Pseudomonas putida, Bacillus subtilis, and their mixture on the management of Meloidogyne incognita, Pectobacterium betavasculorum, and Rhizoctonia solani disease complex of beetroot (Beta vulgaris L.). Egypt J Biol Pest Control 29:73. https://doi.org/10.1186/s41938-019-0174-0
Khan MR, Siddiqui ZA (2020) Use of silicon dioxide nanoparticles for the management of Meloidogyne incognita, Pectobacterium betavasculorum and Rhizoctonia solani disease complex of beetroot (Beta vulgaris L.). Sci Hortic 265:109211
Kim HS, Thammarat P, Lommel SA, Hogan CS, Charkowski AO (2011) Pectobacterium carotovorum elicits plant cell death with DspE/F but the P. carotovorum DspE does not suppress callose or induce expression of plant genes early in plant–microbe interactions. Mol Plant Microbe Interact 24(7):773–786
Linglan M, Chao L, Chunxiang Q, Sitao Y, Jie L, Fengqing G, Fashui H (2008) Rubisco activase mRNA expression in spinach: modulation by nanoanatase treatment. Biol Trace Elem Res 122(2):168–178
Liu Z, Zhang M, Han X, Xu H, Zhang B, Yu Q, Li M (2016) TiO2 nanoparticles cause cell damage independent of apoptosis and autophagy by impairing the ROS-scavenging system in Pichia pastoris. Chem Biol Interact 252:9–18
Luttrell T, Halpegamage S, Tao J, Kramer A, Sutter E, Batzill M (2014) Why is anatase a better photocatalyst than rutile? Model studies on epitaxial TiO2 films. Sci Rep 4:4043. https://doi.org/10.1038/srep04043
Lyu S, Wei X, Chen J, Wang C, Wang X, Pan D (2017) Titanium as a beneficial element for crop production. Front Plant Sci 8:597
Mashela P (2017) Interrelations between commercial beetroot (Beta vulgaris) cultivars and Meloidogyne species. Acta Agric Scand Sect B Soil Plant Sci 67(2):164–168
Paret ML, Palmateer AJ, Knox GW (2013a) Evaluation of a light-activated nanoparticle formulation of titanium dioxide with zinc for management of bacterial leaf spot on rosa ‘Noare. HortScience 48(2):189–192
Paret ML, Vallad GE, Averett DR, Jones JB, Olson SM (2013b) Photocatalysis: effect of light-activated nanoscale formulations of TiO2 on Xanthomonas perforans and control of bacterial spot of tomato. Phytopathology 103(3):228–236
Pethybridge SJ, Kikkert JR, Hanson LE, Nelson SC (2018) Challenges and prospects for building resilient disease management strategies and tactics for the New York table beet industry. Agronomy 8(7):112
Prasad R, Bhattacharyya A, Nguyen QD (2017) Nanotechnology in sustainable agriculture: recent developments, challenges, and perspectives. Front Microbiol 8:1014
Rai M, Ingle AP, Paralikar P, Anasane N, Gade R, Ingle P (2018) Effective management of soft rot of ginger caused by Pythium spp. and Fusarium spp.: emerging role of nanotechnology. Appl Microbiol Biotechnol 102(16):6827–6839
Raliya R, Biswas P, Tarafdar J (2015a) TiO2 nanoparticle biosynthesis and its physiological effect on mung bean (Vigna radiata L.). Biotechnol Rep 5:22–26
Raliya R, Nair R, Chavalmane S, Wang WN, Biswas P (2015b) Mechanistic evaluation of translocation and physiological impact of titanium dioxide and zinc oxide nanoparticles on the tomato (Solanum lycopersicum L.) plant. Metallomics 7(12):1584–1594
Reyes-Coronado D, Rodríguez-Gattorno G, Espinosa-Pesqueira M, Cab C, de Coss RD, Oskam G (2008) Phase-pure TiO2 nanoparticles: anatase, brookite and rutile. Nanotechnology 19(14):145605
Rezaei ZS, Javed A, Ghani MJ, Soufian S, Barzegari FF, Bayandori MA, Mirjallili SH (2010) Comparative study of antimicrobial activities of TiO2 and CdO nanoparticles against the pathogenic strain of Escherichia coli. Iran J Pathol 5(2):83–89
Rizwan M, Ali S, Ali B, Adrees M, Arshad M, Hussain A, Rehman NZ, Waris AA (2019) Zinc and iron oxide nanoparticles improved the plant growth and reduced the oxidative stress and cadmium concentration in wheat. Chemosphere 214:269–277
Sabir S, Arshad M, Chaudhari SK (2014) Zinc oxide nanoparticles for revolutionizing agriculture: synthesis and applications. Sci World J. https://doi.org/10.1155/2014/925494
Servin A, Elmer W, Mukherjee A, De la Torre-Roche R, Hamdi H, White JC, Bindraban P, Dimkpa C (2015) A review of the use of engineered nanomaterials to suppress plant disease and enhance crop yield. J Nanopart Res 17:92. https://doi.org/10.1007/s11051-015-2907-7
Shah MSAS, Nag M, Kalagara T, Singh S, Manorama SV (2008) Silver on PEG-PU-TiO2 polymer nanocomposite films: an excellent system for antibacterial applications. Chem Mater 20(7):2455–2460
Siddiqui ZA, Khan MR, Abd Allah EF, Parveen A (2019) Titanium dioxide and zinc oxide nanoparticles affect some bacterial diseases, and growth and physiological changes of beetroot. Int J Veg Sci 25(5):409–430
Sneath PH, Sokal RR (1973) Numerical taxonomy. The principles and practice of numerical classification. W. H. Freeman and Company, San Francisco, p 573
Song G, Gao Y, Wu H, Hou W, Zhang C, Ma H (2012) Physiological effect of anatase TiO2 nanoparticles on Lemna minor. Environ Toxicol Chem 31(9):2147–2152
Southey JF (1986) Laboratory methods for work with plant and soil nematodes. Ministry of Agriculture, Fisheries and Food, Her Majesties Stationary Office, London, p 202
Srivastava V, Gusain D, Sharma YC (2015) Critical review on the toxicity of some widely used engineered nanoparticles. Ind Eng Chem Res 54(24):6209–6233
Tumburu L, Andersen CP, Rygiewicz PT, Reichman JR (2015) Phenotypic and genomic responses to titanium dioxide and cerium oxide nanoparticles in Arabidopsis germinants. Environ Toxicol Chem 34(1):70–83
Vulić JJ, Ćebović TN, Čanadanović-Brunet JM, Ćetković GS, Čanadanović VM, Djilas SM, Šaponjac VTT (2014) In vivo and in vitro antioxidant effects of beetroot pomace extracts. J Funct Foods 6:168–175
Wang WN, Tarafdar JC, Biswas P (2013) Nanoparticle synthesis and delivery by an aerosol route for watermelon plant foliar uptake. J Nanopart Res 15:1417. https://doi.org/10.1007/s11051-013-1417-8
Williams DN, Ehrman SH, Holoman TRP (2006) Evaluation of the microbial growth response to inorganic nanoparticles. J Nanobiotechnol 4:3. https://doi.org/10.1186/1477-3155-4-3
Wootton-Beard PC, Ryan L (2011) A beetroot juice shot is a significant and convenient source of bioaccessible antioxidants. J Funct Foods 3(4):329–334
Wruss J, Waldenberger G, Huemer S, Uygun P, Lanzerstorfer P, Müller U, Höglinger O, Weghuber J (2015) Compositional characteristics of commercial beetroot products and beetroot juice prepared from seven beetroot varieties grown in Upper Austria. J Food Compos Anal 42:46–55
Yamori W, Masumoto C, Fukayama H, Makino A (2012) Rubisco activase is a key regulator of non-steady-state photosynthesis at any leaf temperature and, to a lesser extent, of steady-state photosynthesis at high temperature. Plant J 71(6):871–880
Yao X, Li C, Li S, Zhu Q, Zhang H, Wang H, Yu C, Martin SKS, Xie F (2017) Effect of shade on leaf photosynthetic capacity, light-intercepting, electron transfer and energy distribution of soybeans. Plant Growth Regul 83(3):409–416
Zahra Z, Arshad M, Rafique R, Mahmood A, Habib A, Qazi IA, Khan SA (2015) Metallic nanoparticle (TiO2 and Fe3O4) application modifies rhizosphere phosphorus availability and uptake by Lactuca sativa. J Agric Food Chem 63(31):6876–6882
Ze Y, Liu C, Wang L, Hong M, Hong F (2011) The regulation of TiO2 nanoparticles on the expression of light-harvesting complex II and photosynthesis of chloroplasts of Arabidopsis thaliana. Biol Trace Elem Res 143(2):1131–1141
Acknowledgements
We are grateful to the Central Research Facility, Indian Institute of Technology, Delhi, for Inductively Coupled Plasma-Mass-Spectrometry (ICP-MS) analysis and University Sophisticated Instrumentation Facility, Aligarh Muslim University, Aligarh, for Scanning Electron Microscopic studies.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
M.R. Khan and Z.A. Siddiqui declare that they have no competing interests.
Rights and permissions
About this article
Cite this article
Khan, M.R., Siddiqui, Z.A. Efficacy of Titanium Dioxide Nanoparticles in the Management of Disease Complex of Beetroot (Beta vulgaris L.) Caused by Pectobacterium betavasculorum, Rhizoctonia solani, and Meloidogyne incognita . Gesunde Pflanzen 73, 445–464 (2021). https://doi.org/10.1007/s10343-021-00566-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10343-021-00566-2