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Induction of tomato plant biochemical immune responses by the synthesized zinc oxide nanoparticles against wilt-induced Fusarium oxysporum

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Abstract

The current study used zinc oxide nanoparticles (ZnO-NPs) to protect the tomato plant against Fusarium wilt. Gamma rays were used to synthesize ZnO-NPs, and the designed ZnO-NPs were characterized using high-resolution transmission electron microscopy (HRTEM), scanning electron microscope (SEM), dynamic light scattering (DLS), energy-dispersive X-ray spectroscopy (EDX), and ultraviolet–visible (UV-Vis.) spectroscopy. We found that the 20 kGy dose is the most effective for ZnO-NPs synthesis, with the highest O.D. = 1.65 (diluted 3 times) at 400 nm. The scale of ZnO-NPs ranged from 10.45 to 75.25 nm with an average diameter of 40.20 nm. The results showed that the designed ZnO-NPs showed promising activity as a potent inducer of plant physiological immunity against Fusarium wilt disease. Likewise, ZnO-NPs significantly reduced the wilt disease symptoms incidence by 28.57% and high protection by 67.99% against F. oxysporum. Additionally, infected tomato plants treated with ZnO-NPs show improved shoot length (44.71%), root length (40.0%), number of leaves (60.0 %), chlorophyll a (36.93%), chlorophyll b (16.46%), and carotenoids (21.87%) versus infected plants. Notably, in the treatment of tomato seedlings, the beneficial effects of ZnO-NPs extended to increase not only in osmolyte contents but also total phenol contents in comparison with control plants. In conclusion, the designed ZnO-NPs can control Fusarium wilt disease and improve and develop biochemical compounds responsible for defense against fusarial infection.

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Data availability

The datasets used and analyzed during the current study are available from the corresponding author upon reasonable request.

References

  • Abd Alhakim A, Hashem A, Abdelaziz AM, Attia MS (2022) Impact of plant growth promoting fungi on biochemical defense performance of tomato under Fusarial infection. Egypt J Chem

  • Abdelaziz AM, Attia MS, Salem MS, Refaay DA, Alhoqail WA, Senousy HH (2022a) Cyanobacteria-mediated immune responses in pepper plants against Fusarium wilt. Plants 11:2049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abdelaziz AM, Dacrory S, Hashem AH, Attia MS, Hasanin M, Fouda HM, Kamel S, ElSaied H (2021) Protective role of zinc oxide nanoparticles based hydrogel against wilt disease of pepper plant. Biocatal Agric Biotechnol 35:102083

    Article  CAS  Google Scholar 

  • Abdelaziz AM, El-Wakil DA, Attia MS, Ali OM, AbdElgawad H, Hashem AH (2022b) Inhibition of Aspergillus flavus growth and aflatoxin production in Zea mays L. Using Endophytic Aspergillus fumigatus. J Fungi 8:482

    Article  CAS  Google Scholar 

  • Abdelaziz AM, Salem SS, Khalil A, El-Wakil DA, Fouda HM, Hashem AH (2022c) Potential of biosynthesized zinc oxide nanoparticles to control Fusarium wilt disease in eggplant (Solanum melongena) and promote plant growth. BioMetals:1–16

  • Adisa IO, Pullagurala VLR, Peralta-Videa JR, Dimkpa CO, Elmer WH, Gardea-Torresdey JL, White JC (2019) Recent advances in nano-enabled fertilizers and pesticides: a critical review of mechanisms of action. Environ Sci Nano 6:2002–2030

    Article  CAS  Google Scholar 

  • Ahammed GJ, Mao Q, Yan Y, Wu M, Wang Y, Ren J, Guo P, Liu A, Chen S (2020) Role of melatonin in arbuscular mycorrhizal fungi-induced resistance to Fusarium wilt in cucumber. Phytopathology 110:999–1009

    Article  CAS  PubMed  Google Scholar 

  • Aldinary AM, Abdelaziz AM, Farrag AA, Attia MS (2021) Biocontrol of tomato Fusarium wilt disease by a new Moringa endophytic Aspergillus isolates. Mater Today

  • Al-Doori SAMA (2021) Response of three flax genotypes (Linum usitatissimum L.) to foliar spraying with different concentration of zinc and boron under the dryland conditions of Nineveh governorate. Coll Basic Educ Res J 17:1680–1700

    Article  Google Scholar 

  • Ashour A, El-Batal AI, Maksoud MA, El-Sayyad GS, Labib S, Abdeltwab E, El-Okr M (2018) Antimicrobial activity of metal-substituted cobalt ferrite nanoparticles synthesized by sol–gel technique. Particuology

  • Attia MS, Abdelaziz AM, Al-Askar AA, Arishi AA, Abdelhakim AM, Hashem AH (2022a) Plant growth-promoting fungi as biocontrol tool against fusarium wilt disease of tomato plant. J Fungi 8:775

    Article  CAS  Google Scholar 

  • Attia MS, El-Naggar HA, Abdel-Daim MM, El-Sayyad GS (2021a) The potential impact of Octopus cyanea extracts to improve eggplant resistance against Fusarium-wilt disease: in vivo and in vitro studies. Environ Sci Pollut Res 28:35854–35869

    Article  CAS  Google Scholar 

  • Attia MS, El-Sayyad GS, Abd Elkodous M, Khalil WF, Nofel MM, Abdelaziz AM, Farghali AA, El-Batal AI, El Rouby WM (2021b) Chitosan and EDTA conjugated graphene oxide antinematodes in Eggplant: toward improving plant immune response. Int J Biol Macromol 179:333–344

    Article  CAS  PubMed  Google Scholar 

  • Attia MS, El-Wakil DA, Hashem AH, Abdelaziz AM (2022b) Antagonistic effect of plant growth-promoting fungi against fusarium wilt disease in tomato: in vitro and in vivo study. Appl Biochem Biotechnol:1–19

  • Attia MS, Younis AM, Ahmed AF, Elaziz A (2016) Comprehensive management for wilt disease caused by Fusarium oxysporum in tomato plant. Int J Innov Sci Eng Technol 4:2348–7968

    Google Scholar 

  • Awed AS, El-Sayyad GS, El-ghandour A, Hameed MFO, Abdel Maksoud MIA, El-Batal AI, Obayya SSA (2019) Unveiling antimicrobial activity of metal iodide (CuI, AgI, and PbI2) nanoparticles: towards biomedical surfaces applications. J Clust Sci

  • Badawy AA, Alotaibi MO, Abdelaziz AM, Osman MS, Khalil AM, Saleh AM, Mohammed AE, Hashem AH (2021) Enhancement of seawater stress tolerance in barley by the endophytic fungus Aspergillus ochraceus. Metabolites 11:428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baraka A, Dickson S, Gobara M, El-Sayyad GS, Zorainy M, Awaad MI, Hatem H, Kotb MM, Tawfic A (2017) Synthesis of silver nanoparticles using natural pigments extracted from Alfalfa leaves and its use for antimicrobial activity. Chem Pap 71:2271–2281

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Benhamou N (1996) Elicitor-induced plant defence pathways. Trends Plant Sci 1:233–240

    Article  Google Scholar 

  • Boccia F, Di Donato P, Covino D, Poli A (2019) Food waste and bio-economy: a scenario for the Italian tomato market. J Clean Prod 227:424–433

    Article  Google Scholar 

  • Borah R, Verbruggen SW (2020) Silver-gold bimetallic alloy versus core-shell nanoparticles: implications for plasmonic enhancement and photothermal applications. J Phys Chem C

  • Bröer S, Fairweather SJ (2018) Amino acid transport across the mammalian intestine. Compr Physiol 9:343–373

    Article  PubMed  Google Scholar 

  • Casanova-Sáez R, Mateo-Bonmatí E, Ljung K (2021) Auxin metabolism in plants. Cold Spring Harb Perspect Biol 13:a039867

    Article  PubMed  PubMed Central  Google Scholar 

  • Castro-Longoria E, Vilchis-Nestor AR, Avalos-Borja M (2011) Biosynthesis of silver, gold and bimetallic nanoparticles using the filamentous fungus Neurospora crassa. Colloids Surf B Biointerfaces 83:42–48

    Article  CAS  PubMed  Google Scholar 

  • Chandrasekaran M, Boopathi T, Manivannan P (2021) Comprehensive assessment of ameliorative effects of AMF in alleviating abiotic stress in tomato plants. J Fungi 7:303

    Article  CAS  Google Scholar 

  • Chudobová D, Cihalova K, Kopel P, Ruttkay-Nedecky B, Vaculovicova M, Krozek R, Adam V (2015) Antimicrobial nanomaterials in the food industry. Kvasny Prumysl 61:51–56

    Article  Google Scholar 

  • Clément M, Abdellah I, Martini C, Fossard F, Dragoe D, Remita H, Huc V, Lampre I (2020) Gold (I)–silver (I)-calix [8] arene complexes, precursors of bimetallic alloyed Au–Ag nanoparticles. Nanoscale Adv

  • Cohen-Bazire G, Sistrom W, Vernon L, Seeley G (1966) The chlorophylls. Academic Press, New York

    Google Scholar 

  • Dai G, Andary C, Cosson-Mondolot L, Boubals D (1993) Polyphenols and resistance of grapevines to downy mildew. Int Symp Nat Phenols Plant Resistance 381:763–766

    Google Scholar 

  • Dayarathne MC, Mridha AU, Wang Y (2020) Diagnosis of fungal plant pathogens using conventional and molecular approaches, Diagnostics of Plant Diseases. IntechOpen

    Google Scholar 

  • Elbasuney S, El-Sayyad GS, Attia MS, Abdelaziz AM (2022) Ferric oxide colloid: towards green nano-fertilizer for tomato plant with enhanced vegetative growth and immune response against Fusarium wilt disease. J Inorg Organomet Polym Mater:1–14

  • El-Batal AI, Abd Elkodous M, El-Sayyad GS, Al-Hazmi NE, Gobara M, Baraka A (2020a) Gum Arabic polymer-stabilized and gamma rays-assisted synthesis of bimetallic silver-gold nanoparticles: powerful antimicrobial and antibiofilm activities against pathogenic microbes isolated from diabetic foot patients. Int J Biol Macromol 165:169–186

    Article  CAS  PubMed  Google Scholar 

  • El-Batal AI, Mosallam FM, Ghorab M, Hanora A, Gobara M, Baraka A, Elsayed MA, Pal K, Fathy RM, Abd Elkodous M (2020b) Factorial design-optimized and gamma irradiation-assisted fabrication of selenium nanoparticles by chitosan and Pleurotus ostreatus fermented fenugreek for a vigorous in vitro effect against carcinoma cells. Int J Biol Macromol 156:1584–1599

    Article  CAS  PubMed  Google Scholar 

  • El-Batal AI, Nada HG, El-Behery RR, Gobara M, El-Sayyad GS (2020c) Nystatin-mediated bismuth oxide nano-drug synthesis using gamma rays for increasing the antimicrobial and antibiofilm activities against some pathogenic bacteria and Candida species. RSC Adv 10:9274–9289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Khallal SM (2007) Induction and modulation of resistance in tomato plants against Fusarium wilt disease by bioagent fungi (arbuscular mycorrhiza) and/or hormonal elicitors (jasmonic acid & salicylic acid): 1-changes in growth, some metabolic activities and endogenous hormones related to defence mechanism. Aust J Basic Appl Sci 1:691–705

    CAS  Google Scholar 

  • El-Sheekh MM, Mousa ASH, Farghl AA (2020) Biological control of Fusarium wilt disease of tomato plants using seaweed extracts. Arab J Sci Eng 45:4557–4570

    Article  CAS  Google Scholar 

  • Farrag A, Attia MS, Younis A, Abd Elaziz A (2017) Potential impacts of elicitors to improve tomato plant disease resistance. Al Azhar Bull Sci 9:311–321

    Google Scholar 

  • Fathy RM, Mahfouz AY (2021) Eco-friendly graphene oxide-based magnesium oxide nanocomposite synthesis using fungal fermented by-products and gamma rays for outstanding antimicrobial, antioxidant, and anticancer activities. J Nanostruct Chem 11:301–321

    Article  CAS  Google Scholar 

  • Gopinath K, Kumaraguru S, Bhakyaraj K, Mohan S, Venkatesh KS, Esakkirajan M, Kaleeswarran P, Alharbi NS, Kadaikunnan S, Govindarajan M (2016) Green synthesis of silver, gold and silver/gold bimetallic nanoparticles using the Gloriosa superba leaf extract and their antibacterial and antibiofilm activities. Microb Pathog 101:1–11

    Article  CAS  PubMed  Google Scholar 

  • Hashem AH, Abdelaziz AM, Askar AA, Fouda HM, Khalil AM, Abd-Elsalam KA, Khaleil MM (2021) Bacillus megaterium-mediated synthesis of selenium nanoparticles and their antifungal activity against Rhizoctonia solani in Faba Bean Plants. J Fungi 7:195

    Article  CAS  Google Scholar 

  • Iqbal M, Umar S (2019) Nano-fertilization to enhance nutrient use efficiency and productivity of crop plants, Nanomaterials and plant potential. Springer, pp 473–505

    Google Scholar 

  • Irigoyen J, Einerich D, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiol Plant 84:55–60

    Article  CAS  Google Scholar 

  • Jayamohan NS, Patil SV, Kumudini BS (2018) Reactive oxygen species (ROS) and antioxidative enzyme status in Solanum lycopersicum on priming with fluorescent Pseudomonas spp. against Fusarium oxysporum. Biologia 73:1073–1082

    Article  CAS  Google Scholar 

  • Joshi R (2018) A review of Fusarium oxysporum on its plant interaction and industrial use. J Med Plants Stud 6:112–115

    Article  CAS  Google Scholar 

  • Khalil AM, Ahmed AF, Mahmoud EE, Abdelaziz AM (2015) Influence of organic farming system on microbial biomass and fungal communities of agricultural soil. Afr J Mycol Biotechnol 20:23–40

    Google Scholar 

  • Khalil AMA, Hashem AH, Abdelaziz AM (2019) Occurrence of toxigenic Penicillium polonicum in retail green table olives from the Saudi Arabia market. Biocatal Agric Biotechnol 21:101314

    Article  Google Scholar 

  • Khater E-SG, Bahnasawy AH, Shams AE-HS, Hassaan MS, Hassan YA (2015) Utilization of effluent fish farms in tomato cultivation. Ecol Eng 83:199–207

    Article  Google Scholar 

  • Lattanzio V, Lattanzio VM, Cardinali A (2006) Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. Phytochem Adv Res 661:23–67

    Google Scholar 

  • Lisar S, Motafakkerazad R, Hossain MM, Rahman I (2012) Causes, effects and responses. Water Stress 25:33

    Google Scholar 

  • Lowry O, Rosebrough N, Farr A, Randall R (1951) Of these enzymes than MQ. zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA. Biol Chem 193:265–275

    Article  CAS  Google Scholar 

  • Loza K, Heggen M, Epple M (2020) Synthesis, structure, properties, and applications of bimetallic nanoparticles of noble metals. Adv Funct Mater 30:1909260

    Article  CAS  Google Scholar 

  • Mohsin M, Jawad M, Yameen MA, Waseem A, Shah SH, Shaikh AJ (2020) An insight into the coating behavior of bimetallic silver and gold core-shell nanoparticles. Plasmonics

  • MS A, Sridharan K, Puthur JT, Dhankher OP (2021) Priming with nanoscale materials for boosting abiotic stress tolerance in crop plants. J Agric Food Chem 69:10017–10035

    Article  CAS  Google Scholar 

  • Munis MFH, Alamer KH, Althobaiti AT, Kamal A, Liaquat F, Haroon U, Ahmed J, Chaudhary HJ, Attia H (2022) ZnO nanoparticle-mediated seed priming induces biochemical and antioxidant changes in chickpea to alleviate Fusarium wilt. J Fungi 8:753

    Article  Google Scholar 

  • Oliveira M, Varanda C, Félix M (2016) Induced resistance during the interaction pathogen x plant and the use of resistance inducers. Phytochem Lett 15:152–158

    Article  CAS  Google Scholar 

  • Parveen A, Siddiqui ZA (2022) Zirconium dioxide nanoparticles affect growth, photosynthetic pigments, defense enzymes activities and mitigate severity of bacterial and fungal diseases of tomato. Gesunde Pflanzen:1–14

  • Pastuszak J, Szczerba A, Dziurka M, Hornyák M, Kopeć P, Szklarczyk M, Płażek A (2021) Physiological and biochemical response to Fusarium culmorum infection in three durum wheat genotypes at seedling and full anthesis stage. Int J Mol Sci 22:7433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Persley D, Cooke T, House S (2010) Diseases of vegetable crops in Australia. Csiro Publishing

    Book  Google Scholar 

  • Prakash V, Rai P, Sharma NC, Singh VP, Tripathi DK, Sharma S, Sahi S (2022) Application of zinc oxide nanoparticles as fertilizer boosts growth in rice plant and alleviates chromium stress by regulating genes involved in regulating oxidative stress. Chemosphere:134554

  • Ramy SY, Osama FA (2013) In vitro study of the antifungal efficacy of zinc oxide nanoparticles against Fusarium oxysporum and Penicilium expansum. Afr J Microbiol Res 7:1917–1923

    Article  Google Scholar 

  • Rivera Fernandez RD, Rodriguez Jarama F, Mesías Gallo F, Mendoza Intriago DA (2018) Hydrogel for improving water use efficiency of Capsicum annuum crops in Fluvisol soil. Rev Fac Cienc Agrar 50

  • Roohi A, Nazish B, Maleeha M, Waseem S (2011) A critical review on halophytes: salt tolerant plants. J Med Plant Res 5:7108–7118

    Google Scholar 

  • Ruan Y-L (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67

    Article  CAS  PubMed  Google Scholar 

  • Scott P (2013) Physiology and behaviour of plants. John Wiley & Sons

    Google Scholar 

  • Siddiqui ZA, Parveen A, Ahmad L, Hashem A (2019) Effects of graphene oxide and zinc oxide nanoparticles on growth, chlorophyll, carotenoids, proline contents and diseases of carrot. Sci Hortic 249:374–382

    Article  CAS  Google Scholar 

  • Singh A, Ná S, Afzal S, Singh T, Hussain I (2018) Zinc oxide nanoparticles: a review of their biological synthesis, antimicrobial activity, uptake, translocation and biotransformation in plants. J Mater Sci 53:185–201

    Article  CAS  Google Scholar 

  • Sivaselvam S, Selvakumar R, Viswanathan C, Ponpandian N (2021) Rapid one-pot synthesis of PAM-GO-Ag nanocomposite hydrogel by gamma-ray irradiation for remediation of environment pollutants and pathogen inactivation. Chemosphere 275:130061

    Article  CAS  PubMed  Google Scholar 

  • Sturikova H, Krystofova O, Huska D, Adam V (2018) Zinc, zinc nanoparticles and plants. J Hazard Mater 349:101–110

    Article  CAS  PubMed  Google Scholar 

  • Umair Hassan M, Aamer M, Umer Chattha M, Haiying T, Shahzad B, Barbanti L, Nawaz M, Rasheed A, Afzal A, Liu Y (2020) The critical role of zinc in plants facing the drought stress. Agriculture 10:396

    Article  Google Scholar 

  • Wang X, Ramalingam M, Chen G, Ma P, Cui F-Z (2013) Biomimetics: advancing nanobiomaterials and tissue engineering. John Wiley & Sons

    Google Scholar 

  • Zuverza-Mena N, Martínez-Fernández D, Du W, Hernandez-Viezcas JA, Bonilla-Bird N, López-Moreno ML, Komárek M, Peralta-Videa JR, Gardea-Torresdey JL (2017) Exposure of engineered nanomaterials to plants: insights into the physiological and biochemical responses-a review. Plant Physiol Biochem 110:236–264

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Dr. Mohamed Abouzid from the Department of Physical Pharmacy and Pharmacokinetics, Faculty of Pharmacy, Poznan University of Medical Sciences, Poland, for English proofreading the manuscript. The authors thank National Center for Radiation Research and Technology (NCRRT), Egyptian Atomic Energy Authority (EAEA), Cairo, Egypt, for the possibility of using their equipment and facilities during the gamma irradiation process.

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Authors and Affiliations

  1. Biology Department, Science College, Taibah University, Al Madinah Al Munawwarah, 42317-8599, Saudi Arabia

    Nahla A. Bouqellah

  2. Department of Microbiology and Immunology, Faculty of Pharmacy, Ahram Canadian University, sixth of October City, Giza, Egypt

    Gharieb S. El-Sayyad

  3. Department of Microbiology and Immunology, Faculty of Pharmacy, Galala University, New Galala City, Suez, Egypt

    Gharieb S. El-Sayyad

  4. Drug Microbiology Lab., Drug Radiation Research Department, National Center for Radiation Research and Technology (NCRRT), Egyptian Atomic Energy Authority (EAEA), Cairo, Egypt

    Gharieb S. El-Sayyad

  5. Botany and Microbiology Department, Faculty of Science, Al-Azhar University, Cairo, Egypt

    Mohamed S. Attia

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NAB suggested the research topic, investigated the article, planned the research methodology, wrote the original draft, and participated in data representation and article revising and editing. GSE suggested the research topic, investigated the article, planned the research methodology, wrote the original draft, and participated in data representation and article revising and editing. MSA supervised, suggested the research topic, investigated the article, planned the research methodology, wrote the original draft, and participated in data representation and article revising and editing.

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Bouqellah, N.A., El-Sayyad, G.S. & Attia, M.S. Induction of tomato plant biochemical immune responses by the synthesized zinc oxide nanoparticles against wilt-induced Fusarium oxysporum. Int Microbiol 27, 435–448 (2024). https://doi.org/10.1007/s10123-023-00404-7

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