Abstract
Effects of zinc oxide nanoparticles (ZnO NPs) and Rhizobium leguminosarum alone and in combination were observed on the disease complex of pea caused by Meloidogyne incognita and Pseudomonas syringae pv. pisi. Plants inoculated with M. incognita and P. syringae pv. pisi, alone or in combination, showed a significant reduction in plant growth, chlorophyll and carotenoid content compared to uninoculated controls. Use of ZnO NPs (0.10 ml−1) as seed priming resulted in a greater increase in plant growth than 0.10 ml−1 foliar spray. Plants inoculated with R. leguminosarum had better plant growth, chlorophyll and carotenoid content than plants without R. leguminosarum. Greater plant growth, chlorophyll and carotenoid content were observed when NPs primed seeds were grown with R. leguminosarum than the use of NPs foliar spray plus R. leguminosarum. Plants inoculated with R. leguminosarum showed higher root nodulation while only few nodules were observed in plants without R. leguminosarum. Both tested pathogens had adverse effect on nodulation, while use of ZnO NPs with R. leguminosarum also reduced nodulation. ZnO NPs and R. leguminosarum reduced blight disease indices, galling and nematode population. Use of ZnO NPs primed seeds with R. leguminosarum resulted in the highest reduction in disease indices, galling and nematode population. The segregation of various treatments in the biplot of principal component analysis demonstrates a suppressive role of ZnO NPs on blight disease complex of pea.
Zusammenfassung
Es wurden die Auswirkungen von Zinkoxid-Nanopartikeln (ZnO NP) und Rhizobium leguminosarum allein und in Kombination auf den durch Meloidogyne incognita und Pseudomonas syringae pv. pisi verursachten Krankheitskomplex der Erbse beobachtet. Pflanzen, die allein oder in Kombination mit M. incognita und P. syringae pv. pisi inokuliert wurden, zeigten eine signifikante Verringerung des Pflanzenwachstums, des Chlorophyll- und Carotinoidgehalts im Vergleich zur nicht inokulierten Kontrollgruppe. Die Verwendung von ZnO NP (0,10 ml−1) als Saatgutvorbereitung führte zu einem stärkeren Anstieg von Pflanzenwachstum, Chlorophyll und Carotinoiden als 0,10 ml−1 Blattspray. Pflanzen, die mit R. leguminosarum inokuliert wurden, hatten ein besseres Pflanzenwachstum, einen höheren Chlorophyll- und Carotinoidgehalt als Pflanzen ohne R. leguminosarum. Es wurden ein besseres Pflanzenwachstum, ein höherer Chlorophyll- und Carotinoidgehalt beobachtet, wenn mit NP behandelte Samen mit R. leguminosarum angebaut wurden, als bei der Verwendung von NP-Blattspray plus R. leguminosarum. Pflanzen, die mit R. leguminosarum inokuliert wurden, zeigten eine höhere Wurzelknöllchenbildung, während bei Pflanzen ohne R. leguminosarum nur wenige Knöllchen beobachtet wurden. Beide getesteten Krankheitserreger wirkten sich negativ auf die Nodulation aus, während die Verwendung von ZnO NP mit R. leguminosarum ebenfalls die Nodulation reduzierte. ZnO NP und R. leguminosarum reduzierten Bakterienbrand, Wurzelgallenbildung und den Nematodenbefall. Die Verwendung von mit ZnO NP behandeltem Saatgut mit R. leguminosarum führte zur stärksten Reduzierung der Krankheitswerte, der Gallenbildung und des Nematodenbefalls. Die Aufteilung der verschiedenen Behandlungen im Biplot der Hauptkomponentenanalyse zeigt eine supprimierende Rolle von ZnO NP auf den Krankheitskomplex Bakterienbrand bei Erbsen.
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References
Ashoub A, Amara M (2010) Biocontrol activity of some bacterial genera against root-knot nematode, Meloidogyne incognita. J Am Sci 6:321–328
Bopaiah BM, Patil RB, Reddy DDR (1976) Effect of Meloidogyne javanica on nodulation and symbiotic nitrogen fixation in mung, Vigna radiata. Ind J Nematol 6:124–130
Bozbuga R, Lilley CJ, Knox JP, Urwin PE (2018) Host-specific signatures of the cell wall changes induced by the plant parasitic nematode, Meloidogyne incognita. Sci Rep 8(1):17302
Brayner R, Ferrari-Iliou R, Brivois N, Djediat S, Benedetti MF, Fiévet F (2006) Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Lett 6:866–870
Cakmak I (2000) Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol 146:185–205
Dimkpa CO, McLean JE, Britt DW, Anderson AJ (2013) Antifungal activity of ZnO nanoparticles and their interactive effect with a biocontrol bacterium on growth antagonism of the plant pathogen Fusarium graminearum. Biometals 26(6):913–924
Elbadry M, Taha R, Eldougdoug KA, Gamal-Eldin H (2006) Induction of systemic resistance in faba bean (Vicia faba L.) to bean yellow mosaic potyvirus (BYMV) via seed bacterization with plant growth promoting rhizobacteria. J Plant Dis Protect 113:247–251
Elmer W, White JC (2018) The future of nanotechnology in plant pathology. Annu Rev Phytopathol 56:111–133
Fang M, Chen JH, Xu XL, Yang PH, Hildebrand HF (2006) Antibacterial activities of inorganic agents on six bacteria associated with oral infections by two susceptibility tests. Int J Antimicrob Agents 27:513–517
Feris K, Otto C, Tinker J, Wingett D, Punnoose A, Thurber A, Kongara M, Sabetian M, Quinn B, Hanna C (2010) Electrostatic interactions affect nanoparticle-mediated toxicity to Gram-negative bacterium Pseudomonas aeruginosa PAO1. Langmuir 26:4429–4436. https://doi.org/10.1021/la903491z
Golding CG, Lamboo LL, Beniac DR, Booth TF (2016) The scanning electron microscope in microbiology and diagnosis of infectious disease. Sci Rep 6:26516. https://doi.org/10.1038/srep26516
Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CLL, Krishnamurthy L (2015) Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech 5:355–377
Gupta S, Kushwah T, Vishwakarma A, Yadav S (2015) Optimization of ZnO-NPs to investigate their safe application by assessing their effect on soil nematode Caenorhabditis elegans. Nanoscale Res Lett 10:303. https://doi.org/10.1186/s11671-015-1010-4
Hou J, Liu H, Wang L, Duan L, Li S, Wang X (2018b) Molecular toxicity of metal oxide nanoparticles in Danio rerio. Environ Sci Technol 52:7996–8004
Hou J, Wu Y, Li X, Wei B, Li S, Wang X (2018a) Toxic effects of different types of zinc oxide nanoparticles on algae, plants, invertebrates, vertebrates and microorganisms. Chemosphere 193:852–860
Kashyap D, Siddiqui ZA (2020) Effect of different inocula of Meloidogyne incognita and Pseudomonas syringae pv. pisi with and without Rhizobium leguminosarum on growth, chlorophyll, carotenoid and proline contents of pea. Ind Phytopath 73:499–506
Khan MR, Siddiqui ZA (2021) Role of zinc oxide nanoparticles in the management of disease complex of beetroot (Beta vulgaris L.) caused by Pectobacterium betavasculorum, Meloidogyne incognita and Rhizoctonia solani. Hortic Environ Biotechnol 62:225–241. https://doi.org/10.1007/s13580-020-00312-z
Lindström K, Mousavi SA (2019) Effectiveness of nitrogen fixation in rhizobia. Microb Biotechnol 13(5):1314–1335
Mackinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322
Maclachlan S, Zalik S (1963) Plastid structure, chlorophyll concentration and free amino acid composition of a chlorophyll mutant of barley. Can J Bot 41:1053–1062
Manzo S, Rocco A, Carotenuto R, Picione LF, Miglietta ML, Rametta G, Di Francia G (2011) Investigation of ZnO nanoparticles’ ecotoxicological effects towards different soil organisms. Environ Sci Pollut Res Int 18:756–763. https://doi.org/10.1007/s11356-010-0421-0
Martin-Sanz A, De La Vega MP, Murillo J, Caminero C (2013) Strains of Pseudomonas syringae pv. syringae from pea are phylogenetically and pathogenically diverse. Phytopathology 103(7):673–681
Mishra S, Keswani C, Abhilash PC, Fraceto LF, Singh HB (2017) Integrated approach of agri-nanotechnology: challenges and future trends. Front Plant Sci 8:471. https://doi.org/10.3389/fpls.2017.00471
Nesha R, Siddiqui ZA (2013) Interactions of Pectobacterium carotovorum pv. carotovorum, Xanthomonas campestris pv. carotae, and Meloidogyne javanica on the disease complex of Carrot. Int J Veg Sci 19(4):403–411
Oelke EA, Oplinger ES, Hanson CV, Davis DW, Putnam DH, Fuller EI, Rosen CJ (1991) Alternative field crops manual, University of Wisconsin Cooperative or Extension Service, Department of Agronomy, Madison, WI. https://hort.purdue.edu/newcrop/afcm/drypea.html
Osdaghi E, Alizadeh A, Shams-bakhsh M, Lak MR, Hatami Maleki H (2011) Induction of resistance in common bean by Rhizobium leguminosarum bv. phaseoli and decrease of common bacterial blight. Phytopathol Medit 50:45–54
Prasad TNVKV, Sudhakar P, Sreenivas Ulu Y, Latha P, Muna Swamy V, Reddy KR, Sreeprasad TS, Sajanlal PR, Pradeep T (2012) Effect of nanoscale zinc oxide particles on the germination, growth and yield of peanut. J Plant Nutr 35:905–927
Reitz M, Rudolph K, Schröder I, Hoffmann-Hergarten S, Hallmann J, Sikora RA (2000) Lipopolysaccharides of Rhizobium etli strain G12 act in potato roots as an inducing agent of systemic resistance to infection by the cyst nematode Globodera pallida. Appl Environ Microbiol 66(8):3515–3518. https://doi.org/10.1128/aem.66.8.3515-3518.2000
Richardson HJ, Hollaway GJ (2011) Bacterial blight caused by Pseudomonas syringae pv. syringae shown to be an important disease of field pea in south eastern Australia. Australas Plant Pathol 40:260–268
Rungruangmaitree R, Jiraungkoorskul W (2017) Pea, Pisum sativum and its anticancer activity. Pharmacogn Rev 11(21):39–42. https://doi.org/10.4103/phrev.phrev_57_16
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
Sharma GL (1989) Estimated losses due to root-knot nematode Meloidogyne incognita and M. javanica in pea crop. Int Nematol Network Newsl 6:28–29
Sharma PD (2001) Microbiology. Rastogi and Company, Meerut, p 359
Sharma S, Sidhu RK, Prasad VR (2014) Technique for en-masse cryo-fixation and processing of second-stage juveniles of Meloidogyne incognita for scanning electron microscopy. Afric J Biotechnol 13(36):3689–3691. https://doi.org/10.5897/AJB2013.13243
Da Silva LC, Oliva MA, Azevedo AA, De Araujo MJ (2006) Response of restinga plant species to pollution from an iron pelletization factory. Water Air Soil Pollut 175:241–256
Sistani NR, Kaul HP, Desalegn G, Wienkoop S (2017) Rhizobium impacts on seed productivity, quality, and protection of Pisum sativum upon disease stress caused by Didymella pinodes: Phenotypic, Proteomic, and Metabolomic Traits. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01961
Sneath PH, Sokal RR (1973) Numerical Taxonomy. The Principles and Practice of Numerical Classification. W. H. Freeman and Company, San Francisco, 573 pp
Sood ML, Kalra S (1977) Histochemical studies on the body wall of nematodes: Haemonchus contortus (rud., 1803) and Xiphinema insigne Loos, 1949. Z Parasitenkd 51:265–273
Soto MJ, Sanjuan J, Olivares J (2006) Rhizobia and plant-pathogenic bacteria: common infection weapons. Microbiology 152:3167–3174. https://doi.org/10.1099/mic.0.29112-0
Sunanda K, Kikuchi Y, Hashimoto K, Fujishima A (1998) Bactericidal and detoxification effects of TiO2 thin film photocatalysts. Environ Sci Technol 32:726–728
Sávoly Z, Hrács K, Pemmer B, Streli C, Záray G, Nagy PI (2016) Uptake and toxicity of nano-ZnO in the plant-feeding nematode, Xiphinema vuittenezi: the role of dissolved zinc and nanoparticle-specific effects. ESPR 23:9669–9678
Upadhyay KD, Dwivedi K (1987) Analysis of crop losses in pea and gram due to Meloidogyne incognita. Int Nematol Network Newsl 4:6–7
Verma AK, Arora P, Agrawal K (2016) Incidence of bacterial blight pathogen Pseudomonas syringae pv. pisi in pea seeds grown in Rajasthan, India. Legum Res 39(6):1034–1037
Volpiano CG, Lisboa BB, Granada CE, São JJFB, de Oliveira AMR, Beneduzi A, Perevalova Y, Passaglia LMP, Vargas LK (2019) Rhizobia for biological control of plant diseases. In: Kumar V, al (eds) Microbiome in plant health and disease. Springer, Singapore, pp 315–336. ISBN 978-9-81138-495-0
Welch RM, Webb MJ, Loneragan JF (1982) Zinc in membrane function and its role in phosphorus toxicity. In: Scaife A (ed) Proc 9th Intern Plant Nutrition Colloquium. CAB International, Warwick Wallingford, pp 710–715
Yamamoto O, Komatsu M, Sawai J, Nakagawa Z (2008) Antibacterial activity of ZnO powder with crystallographic orientation. J Mater Sci Mater Med 19:1407–1412
Zhang H, Chen G (2009) Potent antibacterial activities of Ag / TiO2 nanocomposite powders synthesized by a one-pot sol-gel method. Environ Sci Technol 43:2905–2910
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First author is thankful to Aligarh Muslim University, Aligarh, UP, India and University Grants Commission, New Delhi, India for the award of a University Fellowship to carry out this work.
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D. Kashyap and Z.A. Siddiqui declare that they have no competing interests.
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Kashyap, D., Siddiqui, Z.A. Effect of Zinc Oxide Nanoparticles and Rhizobium leguminosarum on Growth, Photosynthetic Pigments and Blight Disease Complex of Pea. Gesunde Pflanzen 74, 29–40 (2022). https://doi.org/10.1007/s10343-021-00586-y
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DOI: https://doi.org/10.1007/s10343-021-00586-y