Abstract
Global rice production is seriously affected by many abiotic and biotic factors. Among the aggressive rice pathogens, Xanthomonas oryzae pv. oryzae (X. o. pv. oryzae), Bipolaris oryzae (B. oryzae) and Sphaerulina oryzina (S. oryzina) cause bacterial leaf blight, brown leaf spot and narrow brown leaf spot diseases, respectively. The objective of this study was to evaluate the efficacy of biogenic zinc oxide nanoparticles (ZnO NPs) as antimicrobial agent to control rice pathogens. This is the first report of antifungal activity evaluation of ZnO NPs against B. oryzae and S. oryzina. A pre-characterized bacterial strain Escherichia sp. SINT7 was bio-prospected for synthesis of green ZnO NPs. The NPs were confirmed by a characteristic peak measured at 360.96 nm through UV–Vis spectroscopy. Further, the NPs were characterized to elucidate the surface capping molecules, crystallite structure and morphology by various spectroscopic and imaging techniques, which confirmed the spherical shape of NPs with size ranging from 13.07 to 22.25 nm. In vitro studies against X. o. pv. oryzae pathogen depicted the substantial antibacterial activity (up to 25.7 mm inhibition zone at 20 μg/ml NPs concentration). Similarly, ZnO NPs reduced the mycelial growth of B. oryzae and S. oryzina up to 72.68 and 95.78%, respectively at 50 μg/ml concentration on potato dextrose agar plates, while the mycelial biomass reduction was found to be 64.66 and 68. 49% for B. oryzae and S. oryzina, respectively on potato dextrose broth media as compared to control without the addition of NPs. The green ZnO NPs also significantly reduced the fungal spore germination and a disintegration of fungal hyphae for both fungal strains was observed under the microscope as a result of NPs treatment. Hence, it was concluded that biologically synthesized ZnO NPs are potential antimicrobials and could be compared in greenhouse pathogenicity assays with commercial pesticides to control rice pathogens.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data of this research can be obtained upon request to the corresponding author.
References
Abbas A, Mushtaq A, Cheema AI, Mahmood F, Khan MA, Naqqash T, Shahid M (2020) Heterologous expression of azoreductase-encoding gene azrS of Bacillus sp. MR-1/2 for enhanced azo dye decolorization and wastewater treatment. Arch Microbiol 202:2135–2145. https://doi.org/10.1007/s00203-020-01940-w
Abbas A, Ahmad T, Hussain S, Noman M, Shahzad T, Iftikhar A, Li B (2022) Immobilized biogenic zinc oxide nanoparticles as photocatalysts for degradation of methylene blue dye and treatment of textile effluents. Int J Environ Sci Tech 19:11333–11346. https://doi.org/10.1007/s13762-021-03872-4
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18(2):265–267
Abdallah Y, Liu M, Ogunyemi SO, Ahmed T, Fouad H, Abdelazez A, Li B (2020) Bioinspired green synthesis of chitosan and zinc oxide nanoparticles with strong antibacterial activity against rice pathogen Xanthomonas oryzae pv. oryzae. Molecules 25(20):4795. https://doi.org/10.3390/molecules25204795
Ahmed T, Noman M, Luo J, Muhammad S, Shahid M, Ali MA, Li B (2020) Bioengineered chitosan-magnesium nanocomposite: a novel agricultural antimicrobial agent against Acidovorax oryzae and Rhizoctonia solani for sustainable rice production. Int J Biol Macromol 168:834–845. https://doi.org/10.1016/j.ijbiomac.2020.11.148
Ahmed T, Wu Z, Jiang H, Luo J, Noman M, Shahid M, Li B (2021) Bioinspired Green Synthesis of Zinc Oxide Nanoparticles from a Native Bacillus cereus Strain RNT6: characterization and Antibacterial Activity against Rice Panicle Blight Pathogens Burkholderia glumae and B. gladioli. Nanomaterials 11(4):884. https://doi.org/10.3390/nano11040884
Ajaz S, Ahmed T, Shahid M, Noman M, Shah AA, Mehmood MA, Li B (2021) Bioinspired green synthesis of silver nanoparticles by using a native Bacillus sp. strain AW1–2: characterization and antifungal activity against Colletotrichum falcatum Went. Enzyme Microbial Technol 144:109745. https://doi.org/10.1016/j.enzmictec.2021.109745
Ali M, Ahmed T, Wu W, Hossain A, Hafeez R, Islam Masum M, Li B (2020) Advancements in plant and microbe-based synthesis of metallic nanoparticles and their antimicrobial activity against plant pathogens. Nanomaterials 10(6):1146. https://doi.org/10.3390/nano10061146
Arakha M, Saleem M, Mallick BC, Jha S (2015) The effects of interfacial potential on antimicrobial propensity of ZnO nanoparticle. Sci Rep 5(1):1–10. https://doi.org/10.1038/srep09578
Arciniegas-Grijalba P, Patiño-Portela M, Mosquera-Sánchez L, Guerrero-Vargas J, Rodríguez-Páez J (2017) ZnO nanoparticles (ZnO-NPs) and their antifungal activity against coffee fungus Erythricium salmonicolor. Appl Nanosci 7(5):225–241. https://doi.org/10.1007/s13204-017-0561-3
Da Silva BL, Abuçafy MP, Manaia EB, Junior JAO, Chiari-Andréo BG, Pietro RCR, Chiavacci LA (2019) Relationship between structure and antimicrobial activity of zinc oxide nanoparticles: an overview. Int J Nanomed 14:9395. https://doi.org/10.2147/IJN.S216204
Dananjaya S, Kumar RS, Yang M, Nikapitiya C, Lee J, De Zoysa M (2018) Synthesis, characterization of ZnO-chitosan nanocomposites and evaluation of its antifungal activity against pathogenic Candida albicans. Int J Biol Macromol 108:1281–1288. https://doi.org/10.1016/j.ijbiomac.2017.11.046
Das VL, Thomas R, Varghese RT, Soniya E, Mathew J, Radhakrishnan E (2014) Extracellular synthesis of silver nanoparticles by the Bacillus strain CS 11 isolated from industrialized area. 3 Biotech 4(2):121–126. https://doi.org/10.1007/s13205-013-0130-8
Ealias AM, Saravanakumar M (2017) A review on the classification, characterisation, synthesis of nanoparticles and their application. IOP Conf Ser Mater Sci Eng 263:032019. https://doi.org/10.1088/1757-899X/263/3/032019
Elamawi RM, Bassiouni S, Elkhoby W, Zayed B (2016) Effect of zinc oxide nanoparticles on brown spot disease and rice productivity under saline soil. J Plant Prot Pathol 7(3):171–181
Gautam N, Salaria N, Thakur K, Kukreja S, Yadav N, Yadav R, Goutam U (2020) Green silver nanoparticles for phytopathogen control. Proc Natl Acad Sci, India Sect B Biol Sci 90(2):439–446. https://doi.org/10.1007/s40011-019-01115-8
Government of Pakistan (2020-21) Economic survey of Pakistan. pp 22-23
Griffiths P R., De Haseth J A (2007) Fourier transform infrared spectrometry. John Wiley and Sons 171.https://doi.org/10.1007/978-1-4899-0336-5_13
Gupta M, Tomar RS, Kaushik S, Mishra RK, Sharma D (2018) Effective antimicrobial activity of green ZnO nano particles of Catharanthus roseus. Front Microbiol 9:2030. https://doi.org/10.3389/fmicb.2018.02030
Ibrahim E, Zhang M, Zhang Y, Hossain A, Qiu W, Chen Y, Li B (2020) Green-synthesization of silver nanoparticles using endophytic bacteria isolated from garlic and its antifungal activity against wheat Fusarium head blight pathogen Fusarium graminearum. Nanomaterials 10(2):219. https://doi.org/10.3390/nano10020219
Jayaseelan C, Rahuman AA, Kirthi AV, Marimuthu S, Santhoshkumar T, Bagavan A, Rao KB (2012) Novel microbial route to synthesize ZnO nanoparticles using Aeromonas hydrophila and their activity against pathogenic bacteria and fungi. Spectrochim Acta A 90:78–84. https://doi.org/10.1016/j.saa.2012.01.006
JehangirI A, Hussain A, WaniS H, Mahdi S S, Bhat M A, Ganai M A, Soufan W (2022) Response of Rice (Oryza sativa L.) Cultivars to Variable Rate of Nitrogen under Wet Direct Seeding in Temperate Ecology. Sustainability 14(2): 638. https://doi.org/10.3390/su14020638
Joseph B, Jini D, Sujatha S (2010) Biological and physiological perspectives of specificity in abiotic salt stress response from various rice plants. Asian J Agric Sci 2(3):99–105
Kah M, Kookana RS, Gogos A, Bucheli TD (2018) A critical evaluation of nanopesticides and nanofertilizers against their conventional analogues. Nat Nanotechnol 13(8):677–684. https://doi.org/10.1038/s41565-018-0131-1
Kundu D, Hazra C, Chatterjee A, Chaudhari A, Mishra S (2014) Extracellular biosynthesis of zinc oxide nanoparticles using Rhodococcus pyridinivorans NT2: multifunctional textile finishing, biosafety evaluation and in vitro drug delivery in colon carcinoma. J Photoch Photobiol B 140:194–204. https://doi.org/10.1016/j.jphotobiol.2014.08.001
Lee B-M, Park Y-J, Park D-S, Kang H-W, Kim J-G, Song E-S, Koo B-S (2005) The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res 33(2):577–586. https://doi.org/10.1093/nar/gki206
Liu W, Liu J, Triplett L, Leach JE, Wang G-L (2014) Novel insights into rice innate immunity against bacterial and fungal pathogens. Ann Rev Phytopathol 52:213–241. https://doi.org/10.1146/annurev-phyto-102313-045926
Manamgoda D, Rossman AY, Castlebury L, Crous PW, Madrid H, Chukeatirote E, Hyde KD (2014) The genus bipolaris. Stud Mycol 79(1):221–288. https://doi.org/10.1016/j.simyco.2014.10.002
Mashrai A, Khanam H, Aljawfi RN (2017) Biological synthesis of ZnO nanoparticles using C. albicans and studying their catalytic performance in the synthesis of steroidal pyrazolines. Arab J Chem 10:S1530–S1536. https://doi.org/10.1016/j.simyco.2014.10.002
Mohamed AA, Fouda A, Abdel-Rahman MA, Hassan SE-D, El-Gamal MS, Salem SS, Shaheen TI (2019) Fungal strain impacts the shape bioactivity and multifunctional properties of green synthesized zinc oxide nanoparticles. Biocatal Agric Biotechnol 19:101103. https://doi.org/10.1016/j.bcab.2019.101103
Mohd YH, Mohamad R, Zaidan UH, Rahman A (2019) Microbial synthesis of zinc oxide nanoparticles and their potential application as an antimicrobial agent and a feed supplement in animal industry: a review. J Anim Sci Biotechno 10(1):1–22. https://doi.org/10.1186/s40104-019-0368-z
Negi A, Gangwar R, Vishwakarma RK, Negi DS (2022) Biogenic zinc oxide nanoparticles as an antibacterial, antifungal and photocatalytic tool mediated via leaves of Girardinia diversifolia. Nanotechnol Environ Eng 7(1):223–233. https://doi.org/10.1007/s41204-022-00216-6
Noman M, Shahid M, Ahmed T, Niazi MBK, Hussain S, Song F, Manzoor I (2020) Use of biogenic copper nanoparticles synthesized from a native Escherichia sp. as photocatalysts for azo dye degradation and treatment of textile effluents. Environ Pollut 257:113514. https://doi.org/10.1016/j.envpol.2019.113514
Ogunyemi SO, Abdallah Y, Zhang M, Fouad H, Hong X, Ibrahim E, Li B (2019) Green synthesis of zinc oxide nanoparticles using different plant extracts and their antibacterial activity against Xanthomonas oryzae pv. oryzae. Artif cells Nanomed Biotechnol 47(1):341–352. https://doi.org/10.1080/21691401.2018.1557671
Ogunyemi SO, Zhang M, Abdallah Y, Ahmed T, Qiu W, Ali M, Li B (2020) The bio-synthesis of three metal oxide nanoparticles (zno, mno2, and mgo) and their antibacterial activity against the bacterial leaf blight pathogen. Front Microbiol 11:3099. https://doi.org/10.3389/fmicb.2020.588326
Ons L, Bylemans D, Thevissen K, Cammue B (2020) Combining biocontrol agents with chemical fungicides for integrated plant fungal disease control. Microorganisms 8(12):1930. https://doi.org/10.3390/microorganisms8121930
Pachaiappan R, Rajendran S, Ramalingam G, Vo D-VN, Priya PM, Soto-Moscoso M (2021) Green synthesis of zinc oxide nanoparticles by Justicia adhatoda leaves and their antimicrobial activity. Chen Eng Technol 44(3):551–558. https://doi.org/10.1002/ceat.202000470
Pillai AM, Sivasankarapillai VS, Rahdar A, Joseph J, Sadeghfar F, Rajesh K, Kyzas GZ (2020) Green synthesis and characterization of zinc oxide nanoparticles with antibacterial and antifungal activity. J Mol Struct 1211:128107. https://doi.org/10.1016/j.molstruc.2020.128107
Ramesh M, Anbuvannan M, Viruthagiri G (2015) Green synthesis of ZnO nanoparticles using Solanum nigrum leaf extract and their antibacterial activity. Spectrochim Acta A 136:864–870. https://doi.org/10.1016/j.saa.2014.09.105
Rasmussen JW, Martinez E, Louka P, Wingett DG (2010) Zinc oxide nanoparticles for selective destruction of tumor cells and potential for drug delivery applications. Expert Opin Drug Del 7(9):1063–1077. https://doi.org/10.1517/17425247.2010.502560
Regmi H, Nongmaithem BD, Ngangbam AK (2016) Biotic constraints in rice productivity with special reference to rice root nematode: hirschmanniella spp. a review. J Agric Ecol 5(3):127–133
Selvarajan E, Mohanasrinivasan V (2013) Biosynthesis and characterization of ZnO nanoparticles using Lactobacillus plantarum VITES07. Mater Lett 112:180–182. https://doi.org/10.1016/j.matlet.2013.09.020
Sharma RK, Ghose R (2015) Synthesis of zinc oxide nanoparticles by homogeneous precipitation method and its application in antifungal activity against Candida albicans. Ceram Int 41(1):967–975. https://doi.org/10.1016/j.ceramint.2014.09.016
Sharma D, Rajput J, Kaith B, Kaur M, Sharma S (2010) Synthesis of ZnO nanoparticles and study of their antibacterial and antifungal properties. Thin Solid Films 519(3):1224–1229. https://doi.org/10.1016/j.tsf.2010.08.073
Sharma D, Kanchi S, Bisetty K (2019) Biogenic synthesis of nanoparticles: a review. Arab J Chem 12(8):3576–3600. https://doi.org/10.1016/j.arabjc.2015.11.002
Shobha B, Lakshmeesha TR, Ansari MA, Almatroudi A, Alzohairy MA, Basavaraju S, Chowdappa S (2020) Mycosynthesis of ZnO nanoparticles using Trichoderma spp. isolated from rhizosphere soils and its synergistic antibacterial effect against Xanthomonas oryzae pv. oryzae. J Fungi 6(3):181. https://doi.org/10.3390/jof6030181
Shoeb M, Singh BR, Khan JA, Khan W, Singh BN, Singh HB, Naqvi AH (2013) ROS-dependent anticandidal activity of zinc oxide nanoparticles synthesized by using egg albumen as a biotemplate. Adv Nat Sci Nanosci 4(3):035015. https://doi.org/10.1088/2043-6262/4/3/035015
Steel R G D, and Torrie J H (1960) Principles and procedures of statistics. In: Principles and procedures of statistics
Uppala S, Zhou X (2018) Field efficacy of fungicides for management of sheath blight and narrow brown leaf spot of rice. Crop Prot 104:72–77. https://doi.org/10.1016/j.cropro.2017.10.017
Venkataraju JL, Sharath R, Chandraprabha M, Neelufar E, Hazra A, Patra M (2014) Synthesis, characterization and evaluation of antimicrobial activity of zinc oxide nanoparticles. J Biochem Tech 3(5):151–154
Yasmin S, Hafeez FY, Mirza MS, Rasul M, Arshad HM, Zubair M, Iqbal M (2017) Biocontrol of bacterial leaf blight of rice and profiling of secondary metabolites produced by rhizospheric Pseudomonas aeruginosa BRp3. Front Microbiol 8:1895. https://doi.org/10.3389/fmicb.2017.01895
Yassin MT, Mostafa AA-F, Al-Askar AA, Al-Otibi FO (2022) Facile green synthesis of zinc oxide nanoparticles with potential synergistic activity with common antifungal agents against multidrug-resistant candidal strains. Crystals 12(6):774. https://doi.org/10.3390/cryst12060774
Yoshimi A, Miyazawa K, Abe K (2017) Function and biosynthesis of cell wall α-1, 3-glucan in fungi. J Fungi 3(4):63. https://doi.org/10.3390/jof3040063
Yusof HM, Mohamad R, Zaidan UH, Samsudin AA (2020) Biosynthesis of zinc oxide nanoparticles by cell-biomass and supernatant of Lactobacillus plantarum TA4 and its antibacterial and biocompatibility properties. Sci Rep 10(1):1–13. https://doi.org/10.1038/s41598-020-76402-w
Zhu W, Hu C, Ren Y, Lu Y, Song Y, Ji Y, He J (2021) Green synthesis of zinc oxide nanoparticles using cinnamomum camphora (L.) Presl leaf extracts and its antifungal activity. J Environ Chem Eng 9(6):106659. https://doi.org/10.1016/j.jece.2021.106659
Acknowledgements
We acknowledge the contributions of Mr. Awais Maqsood for his help in data analysis and proof-reading of this manuscript
Funding
We are highly thankful to the partial financial support from the annual departmental research grant allocated to the Department of Bioinformatics by Biotechnology, Government College University, Faisalabad, Pakistan. The authors also acknowledge the PhosAgro/UNESCO/IUPAC/GCUF research grant # 82 for financial support.
Author information
Authors and Affiliations
Contributions
Conceptualization: M Shahid. Methodology: M Shahid, AI Cheema and A Abbas. Formal analysis and investigation: AI Cheema, A Abbas, T Ahmed, M Noman. Writing—original draft preparation: AI Cheema, T Ahmed, M Zubair, A Abbas and M Noman. Writing—review and editing: M Shahid, A Abbas, and M Zubair. Funding acquisition: M Shahid. Supervision: M Shahid.
Corresponding author
Ethics declarations
Conflict of interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
In current study, green zinc oxide nanoparticles were used as antimicrobial agents against three major rice pathogens, Xanthomonas oryzae pv. oryzae (Xoo), Bipolaris oryzae and Sphaerulina oryzina causing bacterial leaf blight, brown leaf spot and narrow brown leaf spot diseases, respectively. Although, ZnONPs have been tested earlier for some of the rice pathogens including Xoo; however, this is the first report of ZnONPs evaluation as antifungal agents against Bipolaris oryzae and Sphaerulina oryzina.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Cheema, A.I., Ahmed, T., Abbas, A. et al. Antimicrobial activity of the biologically synthesized zinc oxide nanoparticles against important rice pathogens. Physiol Mol Biol Plants 28, 1955–1967 (2022). https://doi.org/10.1007/s12298-022-01251-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-022-01251-y