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Differential modes of disease suppression elicited by silver nanoparticles alone and augmented with Calothrix elenkinii against leaf blight in tomato

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Abstract

An investigation employing a detached leaf assay was performed to evaluate the biocontrol efficacy of silver nanoparticles (AgNPs) augmented Calothrix elenkinii against Alternaria alternata infection in tomato. A dose of 50 mg l− 1 AgNPs was selected, which was based on chlorophyll accumulation (as an index of C. elenkinii growth), microscopic observations and biocidal potential of AgNPs against A. alternata. Higher leaf chlorophyll accumulation and lower endoglucanase activity were recorded in in the AgNPs, C. elenkinii and AgNPs augmented C. elenkinii-treated leaves, compared to pathogen challenge alone. Further, microscopic examination showed that these treatments had an alleviating role towards the damaging effects of A. alternata infection on chloroplasts and leaf structure. PCR based amplification using Internal Transcribed Spacers (ITS)-specific primers revealed no band in the treated samples, illustrating the absence of A. alternata, and the biocontrol efficacy of the treatments. Application of AgNPs, C. elenkinii and AgNPs augmented C. elenkinii imparted a protective effect against A. alternata, by inhibiting the growth of the pathogen in tomato leaves and modulating the growth and enzymatic activities of the host. This method proved valuable for gaining insights into the interplay between cyanobacterium, nanoparticle and pathogen-challenged leaves, and illustrated that AgNPs augmented C. elenkinii has the potential to be scaled up as an effective biocontrol option.

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References

  • Akhtar, K. P., Saleem, M. Y., Asghar, M., & Haq, M. A. (2004). New report of Alternaria alternata causing leaf blight of tomato in Pakistan. Plant Pathology, 53, 816.

    Google Scholar 

  • Awan, Z. A., Shoaib, A., & Khan, K. A. (2018). Variations in total phenolics and antioxidant enzymes cause phenotypic variability and differential resistant response in tomato genotypes against early blight disease. Scientia Horticulturae, 239, 216–223.

    CAS  Google Scholar 

  • Ayres, P. G. (1976). Patterns of stomatal behaviour, transpiration and CO2 exchange in pea following infection by powdery mildew (Erysiphe pisi). Journal of Experimental Botany, 27, 354–363.

    Google Scholar 

  • Babu, A. N., Jogaiah, S., Ito, S. I., Nagaraj, A. K., & Tran, L. S. P. (2015). Improvement of growth, fruit weight and early blight disease protection of tomato plants by rhizosphere bacteria is correlated with their beneficial traits and induced biosynthesis of antioxidant peroxidase and polyphenol oxidase. Plant Science, 231, 62–73.

    Google Scholar 

  • Balashanmugam, P., Balakumaran, M. D., Murugan, R., Dhanapal, K., & Kalaichelvan, P. T. (2016). Phytogenic synthesis of silver nanoparticles, optimization and evaluation of in vitro antifungal activity against human and plant pathogens. Microbiological Research, 192, 52–64.

    CAS  PubMed  Google Scholar 

  • Campbell, D., Hurry, V., Clarke, A. K., Gustafsson, P., & Öquist, G. (1998). Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiology and Molecular Biology Reviews, 62, 667–683.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Conner, P. J. (2002). A detached leaf technique for studying race-specific resistance to Cladosporium caryigenum in pecan. Journal of the American Society for Horticultural Science, 127, 781–785.

    Google Scholar 

  • Dakal, T. C., Kumar, A., Majumdar, R. S., & Yadav, V. (2016). Mechanistic basis of antimicrobial actions of silver nanoparticles. Frontiers in Microbiology, 7, 1831.

    PubMed  PubMed Central  Google Scholar 

  • Darmanti, S., Santosa, L. H., & Dewi, K. (2018). Reactive oxygen species accumulations, phenylalanine ammonia-lyase activity and phenolic acid composition of soybean [Glycine max (l.) Merr.] Cv. Grobogan that exposed to multiple stress of purple nutsedge (Cyperus rotundus L.) Interference and drought. Journal of Animal and Plant Sciences,28, 244–251.

    CAS  Google Scholar 

  • Dixit, R., Agrawal, L., Gupta, S., Kumar, M., Yadav, S., Chauhan, P. S., & Nautiyal, C. S. (2016). Southern blight disease of tomato control by 1-aminocyclopropane-1-carboxylate (ACC) deaminase producing Paenibacillus lentimorbus B-30488. Plant Signalling and Behaviour, 11, e1113363.

    Google Scholar 

  • Duong, T. T., Le, T. S., Tran, T. T. H., Nguyen, T. K., Ho, C. T., Dao, T. H., et al. (2016). Inhibition effect of engineered silver nanoparticles to bloom forming cyanobacteria. Advances in Natural Sciences: Nanoscience and Nanotechnology, 7, 035018.

    Google Scholar 

  • El Omari, B., Fleck, I., Aranda, X., & Moret, A. (2001). Effect of fungal infection on leaf gas-exchange and chlorophyll fluorescence in Quercus ilex. Annals of Forest Science, 58, 165–174.

    Google Scholar 

  • Elmer, W. H., Ma, C., & White, J. C. (2018). Nanoparticles for plant disease management. Current Opinion in Environmental Science & Health, 6, 66–70.

    Google Scholar 

  • Finley, P. J., Norton, R., Austin, C., Mitchell, A., Zank, S., & Durham, P. (2015). Unprecedented silver resistance in clinically isolated Enterobacteriaceae: major implications for burn and wound management. Antimicrobial Agents and Chemotherapy, 59, 4734–4741.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fiore, M. F., & Trevors, J. T. (1994). Cell composition and metal tolerance in cyanobacteria. BioMetals, 7, 83–103.

    CAS  Google Scholar 

  • Ganash, M., Ghany, T. A., & Omar, A. M. (2018). Morphological and biomolecules dynamics of phytopathogenic fungi under stress of silver nanoparticles. BioNanoScience, 8, 566–573.

    Google Scholar 

  • Ghosh, S., Kanwar, P., & Jha, G. (2017). Alterations in rice chloroplast integrity, photosynthesis and metabolome associated with pathogenesis of Rhizoctonia solani. Scientific Reports, 7, 41610.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez-Mendoza, D., Troncoso-Rojas, R., Gonzalez-Soto, T., Grimaldo-Juarez, O., Cecena-Duran, C., Duran-Hernandez, D., & Gutierrez-Miceli, F. (2018). Changes in the phenylalanine ammonia lyase activity, total phenolic compounds, and flavonoids in Prosopis glandulosa treated with cadmium and copper. Anais da Academia Brasileira de Ciências, 90, 1465–1472.

    CAS  PubMed  Google Scholar 

  • Govind, S. R., Jogaiah, S., Abdelrahman, M., Shetty, H. S., & Tran, L. S. P. (2016). Exogenous trehalose treatment enhances the activities of defense-related enzymes and triggers resistance against downy mildew disease of pearl millet. Frontiers in Plant Science, 7, 1593.

    PubMed  PubMed Central  Google Scholar 

  • Hansmann, E. (1973). Growth measurement. In J. R. Stein (Ed.), Handbook of phycological methods–culture methods and growth measurements (pp. 359–368). Cambridge: Cambridge University Press.

    Google Scholar 

  • Hiscox, J. T., & Israelstam, G. F. (1979). A method for the extraction of chlorophyll from leaf tissue without maceration. Canadian Journal of Botany, 57, 1332–1334.

    CAS  Google Scholar 

  • Jadhav, H. P., Shaikh, S. S., & Sayyed, R. Z. (2017). Role of hydrolytic enzymes of rhizoflora in biocontrol of fungal phytopathogens: An overview. Rhizotrophs: Plant growth promotion to bioremediation (pp. 183–203). Singapore: Springer.

    Google Scholar 

  • Jayasinghe, C. K., Wijayaratne, S. C. P., & Fernando, T. H. P. S. (2004). Characterization of cell wall degrading enzymes of Thanatephorus cucumeris. Mycopathologia, 157, 73–79.

    CAS  PubMed  Google Scholar 

  • Kgatle, M. G., Truter, M., Ramusi, T. M., Flett, B., & Aveling, T. A. S. (2018). Alternaria alternata, the causal agent of leaf blight of sunflower in South Africa. European Journal of Plant Pathology, 151, 677–688.

    Google Scholar 

  • Khan, N., Mishra, A., & Nautiyal, C. S. (2012). Paenibacillus lentimorbus B-30488r controls early blight disease in tomato by inducing host resistance associated gene expression and inhibiting Alternaria solani. Biological Control, 62, 65–74.

    Google Scholar 

  • Kreitlow, S., Mundt, S., & Lindequist, U. (1999). Cyanobacteria – a potential source of new biologically active substances. Journal of Biotechnology, 70, 61–63.

    CAS  PubMed  Google Scholar 

  • Kubicek, C. P., Starr, T. L., & Glass, N. L. (2014). Plant cell wall–degrading enzymes and their secretion in plant-pathogenic fungi. Annual Review of Phytopathology, 52, 427–451.

    PubMed  Google Scholar 

  • Kulik, M. M. (1995). The potential for using cyanobacteria (blue green algae) and algae in the biological control of plant pathogenic bacteria and fungi. European Journal of Plant Pathology, 101, 585–599.

    Google Scholar 

  • Kumar, V., Sharma, M., Khare, T., & Wani, S. H. (2018). Impact of nanoparticles on oxidative stress and responsive antioxidative defense in plants. In Nanomaterials in Plants, Algae, and Microorganisms (pp. 393–406). Academic Press.

  • Kumari, M., Pandey, S., Bhattacharya, A., Mishra, A., & Nautiyal, C. S. (2017). Protective role of biosynthesized silver nanoparticles against early blight disease in Solanum lycopersicum. Plant Physiology and Biochemistry, 121, 216–225.

    CAS  PubMed  Google Scholar 

  • Lamsal, K., Kim, S. W., Jung, J. H., Kim, Y. S., Kim, K. S., & Lee, Y. S. (2011). Application of silver nanoparticles for the control of Colletotrichum species in vitro and pepper anthracnose disease in field.. Mycobiology, 39, 194–199.

  • Lok, C. N., Ho, C. M., Chen, R., He, Q. Y., Yu, W. Y., & Sun, H. (2006). Proteomic analysis of the mode of antibacterial action of silver nanoparticles. Journal of Proteome Research, 5, 916–924.

    CAS  PubMed  Google Scholar 

  • Mackinney, G. (1941). Absorption of light by chlorophyll solutions. Journal of Biological Chemistry, 140, 315–322.

    CAS  Google Scholar 

  • Magyarosy, A. C., Schürmann, P., & Buchanan, B. B. (1976). Effect of powdery mildew infection on photosynthesis by leaves and chloroplasts of sugar beets. Plant Physiology, 57, 486–489.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mahawar, H., & Prasanna, R. (2018). Prospecting the interactions of nanoparticles with beneficial microorganisms for developing green technologies for agriculture. Environmental Nanotechnology, Monitoring and Management, 10, 477–485.

    Google Scholar 

  • Mahawar, H., Prasanna, R., Singh, S. B., & Nain, L. (2018). Influence of silver, zinc oxide and copper oxide nanoparticles on the cyanobacterium Calothrix elenkinii. BioNanoScience, 8, 802–810.

    Google Scholar 

  • Manjunath, M., Prasanna, R., Nain, L., Dureja, P., Singh, R., Kumar, A., et al. (2010). Biocontrol potential of cyanobacterial metabolites against damping off disease caused by Pythium aphanidermatum in solanaceous vegetables. Archives of Phytopathology and Plant Protection, 43, 666–677.

    Google Scholar 

  • Martin, K. J., & Rygiewicz, P. T. (2005). Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiology, 5, 28–38.

    PubMed  PubMed Central  Google Scholar 

  • Mishra, S., & Singh, H. B. (2015). Biosynthesized silver nanoparticles as a nanoweapon against phytopathogens: exploring their scope and potential in agriculture. Applied Microbiology and Biotechnology, 99, 1097–1107.

    CAS  PubMed  Google Scholar 

  • Moreira, F. G., Reis, S. D., Costa, M. A. F., Souza, C. G. M. D., & Peralta, R. M. (2005). Production of hydrolytic enzymes by the plant pathogenic fungus Myrothecium verrucaria in submerged cultures. Brazilian Journal of Microbiology, 36, 7–11.

    CAS  Google Scholar 

  • Naik, K., & Kowshik, M. (2017). The silver lining: towards the responsible and limited usage of silver. Journal of Applied Microbiology, 123, 1068–1087.

    CAS  PubMed  Google Scholar 

  • Nandeeshkumar, P., Sudisha, J., Kini, K. R., Prakash, H. S., Niranjana, S. R., & Shetty, H. S. (2008). Chitosan induced resistance to downy mildew in sunflower caused by Plasmopara halstedii. Physiological and Molecular Plant Pathology, 72, 188–194.

    CAS  Google Scholar 

  • Natarajan, C., Prasanna, R., Gupta, V., Dureja, P., & Nain, L. (2012). Characterization of the fungicidal activity of Calothrix elenkinii using chemical methods and microscopy. Applied Biochemistry and Microbiology, 48, 51–57.

    CAS  Google Scholar 

  • Panáček, A., Kvítek, L., Smékalová, M., Večeřová, R., Kolář, M., Röderová, M., Dyčka, F., Šebela, M., Prucek, R., Tomanec, O., & Zbořil, R. (2018). Bacterial resistance to silver nanoparticles and how to overcome it. Nature Nanotechnology, 13, 65–71.

    PubMed  Google Scholar 

  • Petrasch, S., Silva, C. J., Mesquida-Pesci, S. D., Gallegos, K., van den Abeele, C., Papin, V., et al. (2019). Infection strategies deployed by Botrytis cinerea, Fusarium acuminatum, and Rhizopus stolonifer as a function of tomato fruit ripening stage. Frontiers in Plant Science, 10, 223.

    PubMed  PubMed Central  Google Scholar 

  • Prasanna, R., Chaudhary, V., Gupta, V., Babu, S., Kumar, A., Shivay, Y. S., & Nain, L. (2013). Cyanobacteria mediated plant growth promotion and bioprotection against Fusarium wilt in tomato. European Journal of Plant Pathology, 13, 337–353.

    Google Scholar 

  • Saha, S. K., Swaminathan, P., Raghavan, C., Uma, L., & Subramanian, G. (2010). Ligninolytic and antioxidative enzymes of a marine cyanobacterium Oscillatoria willei BDU 130511 during Poly R-478 decolourization. Bioresource Technology, 101, 3076–3084.

    CAS  PubMed  Google Scholar 

  • Scorzoni, L., Sangalli-Leite, F., de Lacorte Singulani, J., Costa-Orlandi, C. B., Fusco-Almeida, A. M., & Mendes-Giannini, M. J. S. (2016). Searching new antifungals: the use of in vitro and in vivo methods for evaluation of natural compounds. Journal of Microbiological Methods, 123, 68–78.

    CAS  PubMed  Google Scholar 

  • Singh, P. K., Rai, S., Pandey, S., Agrawal, C., Shrivastava, A. K., Kumar, S., & Rai, L. C. (2012). Cadmium and UV-B induced changes in proteome and some biochemical attributes of Anabaena sp. PCC7120. Phykos, 42, 39–50.

    Google Scholar 

  • Singh, A., Sarma, B. K., Upadhyay, R. S., & Singh, H. B. (2013). Compatible rhizosphere microbes mediated alleviation of biotic stress in chickpea through enhanced antioxidant and phenylpropanoid activities. Microbiological Research, 168, 33–40.

    CAS  PubMed  Google Scholar 

  • Smith, D. P., & Peay, K. G. (2014). Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PloS one, 9, e90234.

    PubMed  PubMed Central  Google Scholar 

  • Soylu, E. M., Soylu, S., & Baysal, Ö (2003). Induction of disease resistance and antioxidant enzymes by acibenzolar-S-methyl against bacterial canker (Clavibacter michiganensis subsp. michiganensis) in tomato. Journal of Plant Pathology, 85, 175–181.

    CAS  Google Scholar 

  • Spoel, S. H., Johnson, J. S., & Dong, X. (2007). Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proceedings of the National Academy of Sciences of U.S.A., 104, 18842–18847.

  • Stanier, R. Y., Kunisawa, R., Mandel, M., & Cohen-Bazire, G. (1971). Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriological Reviews, 35, 171–205.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Toju, H., Tanabe, A. S., Yamamoto, S., & Sato, H. (2012). High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PloS One,7, e40863.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tripathi, D. K., Singh, S., Singh, V. P., Prasad, S. M., Dubey, N. K., & Chauhan, D. K. (2017). Silicon nanoparticles more effectively alleviated UV-B stress than silicon in wheat (Triticum aestivum) seedlings. Plant Physiology and Biochemistry, 110, 70–81.

    CAS  PubMed  Google Scholar 

  • Underwood, W. (2012). The plant cell wall: a dynamic barrier against pathogen invasion. Frontiers in Plant Science, 3, 85.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vera-Reyes, I., Esparza‐Arredondo, I. J. E., Lira‐Saldivar, R. H., Granados‐Echegoyen, C. A., Alvarez‐Roman, R., Vásquez‐López, A., et al. (2019). In vitro antimicrobial effect of metallic nanoparticles on phytopathogenic strains of crop plants.. Journal of Phytopathology, 167, 461–469.

  • Xie, X., He, Z., Chen, N., Tang, Z., Wang, Q., & Cai, Y. (2019). The roles of environmental factors in regulation of oxidative stress in plant. BioMed Research International,2019, 9732325. https://doi.org/10.1155/2019/9732325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav, O. P., Dabbas, M. R., & Gaur, L. B. (2014). Screening of tomato advanced lines, genotypes against Alternaria solani. Plant Archives, 14, 553–555.

    Google Scholar 

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Acknowledgements

The study was supported by the University Grants Commission who provided fellowship and the Post Graduate School, ICAR-IARI, who provided the facilities towards the fulfilment of Ph.D. program. The study was also partly funded by the AMAAS Network Project on Microorganisms, granted by the Indian Council of Agricultural Research (ICAR), New Delhi, to RP. We are thankful to the Division of Microbiology and Division of Plant Pathology, ICAR-IARI, New Delhi, for providing necessary facilities for undertaking this study.

Funding

The study was supported by the University Grants Commission vide Grant number-RGNF-2014-15-SC-RAJ-57089 and ICAR- AMAAS Network Project on Microorganisms (Project Code T12-122).

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Correspondence to Radha Prasanna.

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Mahawar, H., Prasanna, R., Gogoi, R. et al. Differential modes of disease suppression elicited by silver nanoparticles alone and augmented with Calothrix elenkinii against leaf blight in tomato. Eur J Plant Pathol 157, 663–678 (2020). https://doi.org/10.1007/s10658-020-02021-w

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