Montmorillonite nanoclay triggers immunity responses in wheat against Puccinia striiformis f. sp. tritici, and suppresses uredospore germination
Published 2024-09-16
Keywords
- Nanoclay,
- host resistance,
- defense,
- Triticum aestivum,
- yellow rust
How to Cite
Copyright (c) 2024 Younes M. RASHAD, Mohamed HAFEZ, Mohamed BOUROUAH, Ahmed M. ABD-ELGAWAD, Hany H.A. EL-SHARKAWY
This work is licensed under a Creative Commons Attribution 4.0 International License.
Funding data
-
Deanship of Scientific Research, King Saud University
Grant numbers RSPD2024R676
Abstract
Puccinia striiformis f. sp. tritici causes the important disease, yellow rust of wheat (Triticum aestivum). Montmorillonite nanoclay (MNC) is naturally occurring and biodegradable. This study assessed in vitro anti-germination effects of MNC on P. striiformis uredospores. Application of MNC at 150 mg L-1 completely inhibited uredospore germination, and MNC at 100 mg L-1 reduced yellow rust severity in wheat plants by 89%. Expression of defense-related genes was increased after MNC treatment at 100 mg L-1, by 5.23-fold for jasmonate and ethylene-responsive factor 3 (JERF3), 4.89-fold for chitinase class II (CHI II), and 2.37-fold for pathogenesis-related protein 1 (PR1). Applying MNC at 100 mg L-1 also activated the antioxidant enzymes POD to 62.1 unit min-1 g-1 fresh wt, PPO to 21.6 units min-1 g-1 fresh wt, and CAT to 36.6 units min-1 g-1 fresh wt. MNC also enhanced phenolic content in wheat leaves (to 1489.53 mg 100 g-1 f. wt), and reduced lipid oxidation levels (to 5.6 μmol MDA g-1 fresh wt). MNC at 100 mg L-1 also mitigated damaging effects of P. striiformis infections on host leaf cell ultrastructure, increased leaf photosynthetic pigments, and increased wheat plant growth. These results show that MNC has potential as a natural control agent for yellow rust of wheat, although field testing of MNC is necessary before this material can be recommended for wheat production.
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- Al-Askar A.A., Abdulkhair W.M., Rashad Y.M., Hafez E.E., Ghoneem K.M., Baka Z.A., 2014. Streptomyces griseorubens E44G: A Potent Antagonist Isolated from Soil in Saudi Arabia. Journal of Pure and Applied Microbiology 8: 221–230.
- Bujdáková H., Bujdáková V., Májeková-Koščová H., Gaálová B., Bizovská V., … Bujdák J., 2018. Antimicrobial activity of organoclays based on quaternary alkylammonium and alkylphosphonium surfactants and montmorillonite. Applied Clay Science 158: 21–28. https://doi.org/10.1016/j.clay.2018.03.010. DOI: https://doi.org/10.1016/j.clay.2018.03.010
- Chance B., Maehly A.C.B.T.-M. in E., 1955. Assay of catalases and peroxidases: In: Methods in Enzymology, Academic Press, 764–775. DOI: https://doi.org/10.1016/S0076-6879(55)02300-8
- Chen W., Wellings C., Chen X., Kang Z., Liu T., 2014. Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici. Molecular Plant Pathology 15: 433–446. https://doi.org/10.1111/mpp.12116. DOI: https://doi.org/10.1111/mpp.12116
- Chen Y.E., Cui J.M., Su Y.Q., Yuan S., Yuan M., Zhang H.Y., 2015. Influence of stripe rust infection on the photosynthetic characteristics and antioxidant system of susceptible and resistant wheat cultivars at the adult plant stage. Frontiers in Plant Science 6: 779. https://doi.org/10.3389/fpls.2015.00779. DOI: https://doi.org/10.3389/fpls.2015.00779
- CoStat, 2005. Cohort Software. 798 Lighthouse Ave., PMB 320 Monterey, USA.
- El-Sharkawy H.H.A., Rashad Y.M., Elazab N.T., 2023a. Biocontrol potential of the endophytic Epicoccum nigrum HE20 against stripe rust of wheat. Pesticide Biochemistry and Physiology 194: 105517. https://doi.org/10.1016/j.pestbp.2023.105517. DOI: https://doi.org/10.1016/j.pestbp.2023.105517
- El-Sharkawy H.H.A., Rashad Y.M., Elazab N.T., 2023b. Induction of multiple defense responses in wheat plants against stripe rust using mycorrhizal fungi and Streptomyces viridosporus HH1. BioControl 68(5): 525–535. https://doi.org/10.1007/s10526-023-10207-4. DOI: https://doi.org/10.1007/s10526-023-10207-4
- Esteban R., Barrutia O., Artetxe U., Fernández-Marín B., Hernández A., García-Plazaola J.I., 2015. Internal and external factors affecting photosynthetic pigment composition in plants: A meta-analytical approach. New Phytologist 206: 268–280. https://doi.org/10.1111/nph.13186. DOI: https://doi.org/10.1111/nph.13186
- Farrakh S., Wang M., Chen X., 2018. Pathogenesis-related protein genes involved in race-specific all-stage resistance and non-race specific high-temperature adult-plant resistance to Puccinia striiformis f. sp. tritici in wheat. Journal of Integrative Agriculture 17: 2478–2491. https://doi.org/10.1016/S2095-3119(17)61853-7. DOI: https://doi.org/10.1016/S2095-3119(17)61853-7
- Galeazzi M.A.M., Sgarbieri V.C., Constantinides S.M., 1981. Isolation, purification and physicochemical characterization of polyphenol oxidase (PPO) from a dwarf variety of banana (Musa cavendishii, L). Journal of Food Science 46: 150–155. https://doi.org/10.1111/j.1365-2621.1981.tb14551.x. DOI: https://doi.org/10.1111/j.1365-2621.1981.tb14551.x
- Guilger-Casagrande M., Migliorini B.B., Germano-Costa T., Bilesky-José N., Harada L.K., … Lima R., 2024. Beauveria bassiana biogenic nanoparticles for the control of Noctuidae pests. Pest Management Science 80: 1325–1337. https://doi.org/10.1002/ps.7863. DOI: https://doi.org/10.1002/ps.7863
- Gultyaeva E., Shaydayuk E., Kosman E., 2022. Virulence Diversity of Puccinia striiformis f. sp. Tritici in Common Wheat in Russian Regions in 2019–2021. Agriculture (Switzerland). DOI: https://doi.org/10.3390/agriculture12111957
- Hafez M., Ahmed A.A., Mohamed A.E., Rashad MM., 2022. Influence of environmental-friendly bio-organic ameliorants on abiotic stress to sustainable agriculture in arid regions: A long term greenhouse study in northwestern Egypt. Journal of King Saud University - Science 34(6): 102212. DOI: https://doi.org/10.1016/j.jksus.2022.102212
- Harborne J.B., 1984. Phytochemical Methods: A guide to Modern Techniques of Plant Analysis. London: Chapman and Hall. DOI: https://doi.org/10.1007/978-94-009-5570-7_1
- Hayat M.A., 2000. Principles and Techniques of Electron Microscopy. Biological Applications, 4th edition. Cambridge University Press, Cambridge, United Kingdom.
- HongBo S., ZongSuo L., MingAn S., 2005. Changes of anti-oxidative enzymes and MDA content under soil water deficits among 10 wheat (Triticum aestivum L.) genotypes at maturation stage. Colloids and Surfaces. B, Biointerfaces, Netherlands 45: 7–13. https://doi.org/10.1016/j.colsurfb.2005.06.016. DOI: https://doi.org/10.1016/j.colsurfb.2005.06.016
- Hossain S.I., Kukushkina E.A., Izzi M., Sportelli M.C., Picca R.A., … Cioffi N., 2023. A Review on Montmorillonite-Based Nanoantimicrobials: State of the Art. Nanomaterials 13(5): 848 DOI: https://doi.org/10.3390/nano13050848
- Iconaru S.L., Groza A., Stan G.E., Predoi D., Gaiaschi S., … Chapon P., 2019. Preparations of Silver/Montmorillonite Biocomposite Multilayers and Their Antifungal Activity. Coatings 9: 817. DOI: https://doi.org/10.3390/coatings9120817
- Ishfaq M., Wang Y., Yan M., Wang Z., Wu L., … Li X., 2022. Physiological Essence of Magnesium in Plants and Its Widespread Deficiency in the Farming System of China. Frontiers in Plant Science 13: 802274. DOI: https://doi.org/10.3389/fpls.2022.802274
- Johnston C.O., Browder L.E., 1966. Seventh revision of the international register of physiologic races of Puccinia recondita f. sp. tritici. Plant Disease Reporter 50: 756–760.
- Kiani T., Mehboob F., Hyder M.Z., Zainy Z., Xu L., … Farrakh S., 2021. Control of stripe rust of wheat using indigenous endophytic bacteria at seedling and adult plant stage. Scientific Reports 11: 14473. https://doi.org/10.1038/s41598-021-93939-6. DOI: https://doi.org/10.1038/s41598-021-93939-6
- Kolaei E.A., Cenatus C., Tweddell R.J., Avis T.J., 2013. Antifungal activity of aluminium-containing salts against the development of carrot cavity spot and potato dry rot. Annals of Applied Biology 163: 311–317. https://doi.org/10.1111/aab.12056. DOI: https://doi.org/10.1111/aab.12056
- Li S., Wang Z., Tang B., Zheng L., Chen H., … Liu D., 2020. A Pathogenesis-Related Protein-Like Gene Is Involved in the Panax notoginseng Defense Response to the Root Rot Pathogen. Frontiers in Plant Science 11: 610176. DOI: https://doi.org/10.3389/fpls.2020.610176
- Liu J., Zong Y., Qin G., Li B., Tian S., 2010. Plasma membrane damage contributes to antifungal activity of silicon against penicillium digitatum. Current Microbiology 61: 274–279. https://doi.org/10.1007/s00284-010-9607-4. DOI: https://doi.org/10.1007/s00284-010-9607-4
- Livak K.J., Schmittgen T.D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402–408. https://doi.org/10.1006/meth.2001.1262. DOI: https://doi.org/10.1006/meth.2001.1262
- Malik C. P. and Singh M. B., 1980. Estimation of total phenols. In: Plant Enzymology and Histo-Enzymology. Kalyani Publishers, New Delhi.
- Maxwell D.P., Bateman D.F., 1967. Changes in the activities of some oxidases in extracts of Rhizoctonia-infected bean hypocotyls in relation to lesion maturation. Phytopathology 57: 132–136.
- Merino D., Tomadoni B., Salcedo M.F., Mansilla A.Y., Casalongué C.A., Alvarez V.A., 2021. Nanoclay as Carriers of Bioactive Molecules Applied to Agriculture. In: Handbook of Nanomaterials and Nanocomposites for Energy and Environmental Applications: Volumes 1-4 (O.V. Kharissova, L.M. Torres-Martínez and B.I. Kharisov, ed.), Cham, Springer International Publishing, 433–454. DOI: https://doi.org/10.1007/978-3-030-36268-3_62
- Nazir M.S., Mohamad Kassim M.H., Mohapatra L., Gilani M.A., Raza M.R., Majeed K., 2016. Characteristic Properties of Nanoclays and Characterization of Nanoparticulates and Nanocomposites. In: Engineering Materials (M. Jawaid, A. el K. Qaiss and R. Bouhfid, ed.), Singapore, Springer Singapore, 35–55. DOI: https://doi.org/10.1007/978-981-10-1953-1_2
- Oliveira-Pinto P.R., Mariz-Ponte N., Gil R.L., Cunha E., Amorim C.G., … Santos C., 2022. Montmorillonite Nanoclay and Formulation with Satureja montana Essential Oil as a Tool to Alleviate Xanthomonas euvesicatoria Load on Solanum lycopersicum. Applied Nano 126–142. DOI: https://doi.org/10.3390/applnano3030009
- Peterson R.F., Campbell A.B., Hannah A.E., 1948. A diagrammatic scale for estimating rust intensity on leaves and stems of cereals. Canadian Journal of Research 26c: 496–500. https://doi.org/10.1139/cjr48c-033. DOI: https://doi.org/10.1139/cjr48c-033
- Poria V., Rana A., Kumari A., Grewal J., Pranaw K., Singh S., 2021. Current perspectives on chitinolytic enzymes and their agro-industrial applications. Biology 10(12):1319. https://doi.org/10.3390/biology10121319. DOI: https://doi.org/10.3390/biology10121319
- Rashad Y.M., Aseel D.G., Hafez E.E., 2018. Antifungal potential and defense gene induction in maize against Rhizoctonia root rot by seed extract of Ammi visnaga (L.) Lam. Phytopathologia Mediterranea 57: 73–88. https://doi.org/10.14601/Phytopathol_Mediterr-21366.
- Rashad Y., Aseel D., Hammad S., 2020a. Phenolic Compounds Against Fungal and Viral Plant Diseases. In: Plant Phenolics in Sustainable Agriculture (R. Lone, R. Shuab and A.N. Kamili, ed.), Singapore, Springer Singapore, 201–219. DOI: https://doi.org/10.1007/978-981-15-4890-1_9
- Rashad Y.M., Abbas M.A., Soliman H.M., Abdel-Fattah G.G., Abdel-Fattah G.M., 2020b. Synergy between endophytic Bacillus amyloliquefaciens GGA and arbuscular mycorrhizal fungi induces plant defense responses against white rot of garlic and improves host plant growth. Phytopathologia Mediterranea 59: 169–186. https://doi.org/10.14601/Phyto-11019. DOI: https://doi.org/10.36253/phyto-11019
- Rashad Y.M., El-Sharkawy H.H.A., Belal B.E.A., Abdel Razik E.S., Galilah D.A., 2021a. Silica Nanoparticles as a Probable Anti-Oomycete Compound Against Downy Mildew, and Yield and Quality Enhancer in Grapevines: Field Evaluation, Molecular, Physiological, Ultrastructural, and Toxicity Investigations. Frontiers in Plant Science 12: 763365. DOI: https://doi.org/10.3389/fpls.2021.763365
- Rashad Y.M., Fekry W.M.E., Sleem M.M., Elazab N.T., 2021b. Effects of Mycorrhizal Colonization on Transcriptional Expression of the Responsive Factor JERF3 and Stress-Responsive Genes in Banana Plantlets in Response to Combined Biotic and Abiotic Stresses. Frontiers in Plant Science 12: 742628. DOI: https://doi.org/10.3389/fpls.2021.742628
- Rashad, Y.M., El-Sharkawy, H.A., Abdalla, S.A., Ibrahim, O. M. and Elazab N.T., 2024. Unraveling the regulation effect of the endophyte Epicoccum nigrum HE20 on the polyphenol biosynthetic pathways genes in wheat against stripe rust. BMC Plant Biology 24:
- Soltan Y.A., Morsy A.S., Hashem N.M., Elazab M.A.I., Sultan M.A., … Sallam S.M.A., 2022. Potential of montmorillonite modified by an organosulfur surfactant for reducing aflatoxin B1 toxicity and ruminal methanogenesis in vitro. BMC Veterinary Research 18: 387. https://doi.org/10.1186/s12917-022-03476-1. DOI: https://doi.org/10.1186/s12917-022-03476-1
- Sundaresha S., Sharma S., Bairwa A., Tomar M., Kumar R., … Chakrabarti S.K., 2022. Spraying of dsRNA molecules derived from Phytophthora infestans, along with nanoclay carriers as a proof of concept for developing novel protection strategy for potato late blight. Pest Management Science 78: 3183–3192. https://doi.org/10.1002/ps.6949. DOI: https://doi.org/10.1002/ps.6949
- Vidossich P., Alfonso-Prieto M., Rovira C., 2012. Catalases versus peroxidases: DFT investigation of H2O 2 oxidation in models systems and implications for heme protein engineering. Journal of Inorganic Biochemistry 117: 292–297. https://doi.org/10.1016/j.jinorgbio.2012.07.002. DOI: https://doi.org/10.1016/j.jinorgbio.2012.07.002
- Wang X., Che M.Z., Khalil H.B., McCallum B.D., Bakkeren G., … Saville B.J., 2020. The role of reactive oxygen species in the virulence of wheat leaf rust fungus Puccinia triticina. Environmental Microbiology 22: 2956–2967. https://doi.org/10.1111/1462-2920.15063. DOI: https://doi.org/10.1111/1462-2920.15063
- Worrall E.A., Hamid A., Mody K.T., Mitter N., Pappu H.R., 2018. Nanotechnology for plant disease management. Agronomy 8(12): 285. DOI: https://doi.org/10.3390/agronomy8120285
- Yousef H.A., Fahmy H.M., Arafa F.N., Abd Allah M.Y., Tawfik Y.M., … Bassily M.E., 2023. Nanotechnology in pest management: advantages, applications, and challenges. International Journal of Tropical Insect Science 43: 1387–1399. https://doi.org/10.1007/s42690-023-01053-z. DOI: https://doi.org/10.1007/s42690-023-01053-z
- Zhang H., Liu W., Wan L., Li F., Dai L., … Huang R., 2010. Functional analyses of ethylene response factor JERF3 with the aim of improving tolerance to drought and osmotic stress in transgenic rice. Transgenic Research 19: 809–818. https://doi.org/10.1007/s11248-009-9357-x. DOI: https://doi.org/10.1007/s11248-009-9357-x
- Zhang S., 2023. Recent Advances of Polyphenol Oxidases in Plants. Molecules 28(5): 2158. DOI: https://doi.org/10.3390/molecules28052158
- Zhao J., Zhang H., Yao J., Paul S., 2011. Identifcation of Berberis spp. as alternate hosts of Puccinia striiformis f. sp. tritici in China. Borlaug Global Rust Initiative workshop, Mycosystema 30: 167.