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Cell wall degrading enzymes and their impact on Fusarium proliferatum pathogenicity

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Abstract

Fusarium proliferatum is one of the most pathogenic Fusarium species on date palm worldwide. We evaluated the colonization ability of 42 F. proliferatum strains collected from date palm trees with disease symptoms on detached leaflets of cvs Sheeshee and Sukkary. Cell wall degrading enzyme (CWDE) production by these strains was assessed with multiple relative enzyme activity (RA) indices. The ability of F. proliferatum strains to colonize leaflet cuttings varied, and there were significant differences (P < 0.05) in susceptibility between the Sheeshee and Sukkary cvs. All F. proliferatum strains tested could hydrolyze carboxymethylcellulose (CMC), citrus pectin and starch, with different capabilities. RA indices calculated from direct assessment of halo zones were consistent with fungal strain colonization ability, but ratio-based RA indices were not. Based on RA4 index of cellulases, F. proliferatum strains were divided into three groups. The first group (33% of strains) showed very strong reaction in hydrolysing CMC, the second group (62% of strains) showed strong reaction in hydrolysing CMC, and the third group (5%) showed moderate reaction in hydrolysing CMC. Most strains had moderate pectin-hydrolysis activities. Starch-hydrolysis activities ranged from weak to strong. Overall, there was a positive correlation between cellulase production and a strain’s colonization ability. Thus, CWDEs produced by F. proliferatum play a role in the colonization of date palm leaflets and hence may be important pathogenicity factors.

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References

  • Abdalla, M., Al-Rokibah, A., Moretti, A., & Mule, G. (2000). Pathogenicity of toxigenic Fusarium proliferatum from date palm in Saudi Arabia. Plant Disease, 84(3), 321–324.

    Article  CAS  PubMed  Google Scholar 

  • Abouamama, S., Noureddine, K., Anis, B., Ryme, T., Mostafa, C., & Mebrouk, K. (2018). Correlation between hydrolytic enzymes activity, geographical origin and pathogenicity of some isolates of Fusarium oxysporum f. sp. albedinis. Archives of Pharmacy & Pharmacology Research, 1(2), 1–5.

    Article  Google Scholar 

  • Bellincampi, D., Cervone, F., & Lionetti, V. (2014). Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. Frontiers in Plant Science, 5, 228.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradner, J. R., Gillings, M., & Nevalainen, K. M. H. (1999). Qualitative assessment of hydrolytic activities in antarctic microfungi grown at different temperatures on solid media. World Journal of Microbiology and Biotechnology, 15(1), 131–132. https://doi.org/10.1023/a:1008855406319.

    Article  Google Scholar 

  • Brito, N., Espino, J. J., & González, C. (2006). The Endo-β-1,4-Xylanase Xyn11A is required for virulence in Botrytis cinerea. Molecular Plant-Microbe Interactions, 19(1), 25–32.

    Article  CAS  PubMed  Google Scholar 

  • Castellá, G., Bragulat, M. R., & Cabañes, F. J. (1998). Extracellular enzymatic activity of Fusarium section Liseola isolates. Mycopathologia, 144(1), 57–62.

    Article  Google Scholar 

  • Castro, G. R., Baigorí, M. D., & Siñeriz, F. (1995). A plate technique for screening of inulin degrading microorganisms. Journal of Microbiological Methods, 22(1), 51–56.

    Article  Google Scholar 

  • Cha, S. D., Jeon, Y. J., Ahn, G. R., Han, J. I., Han, K. H., & Kim, S. H. (2007). Characterization of Fusarium oxysporum isolated from Paprika in Korea. Mycobiology, 35(2), 91–96.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang, H. X., Yendrek, C. R., Caetano-Anolles, G., & Hartman, G. L. (2016). Genomic characterization of plant cell wall degrading enzymes and in silico analysis of xylanses and polygalacturonases of Fusarium virguliforme. BMC Microbiology, 16(1), 147.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cooper, R. M., Longman, D., Campbell, A., Henry, M., & Lees, P. E. (1988). Enzymic adaptation of cereal pathogens to the monocotyledonous primary wall. Physiological and Molecular Plant Pathology, 32(1), 33–47.

    Article  Google Scholar 

  • Dar, R. A., Saba, I., Shahnawaz, M., Sangale, M. K., Ade, A. B., Rather, S. A., & Qazi, P. H. (2013). Isolation, purification and characterization of carboxymethyl cellulase (CMCase) from endophytic Fusarium oxysporum producing podophyllotoxin. Advances in Enzyme Research, 1(4), 91–96.

    Article  CAS  Google Scholar 

  • El Modafar, C. & El Boustani, E. (2000). Relationship between cell wall susceptibility to cellulases and pectinases of Fusarium oxysporum and susceptibility of date palm cultivars. Biologia Plantarum, 43(4), 571–576.

  • Fang, W., Pava-ripoll, M., Wang, S., & Leger, R. S. (2009). Protein kinase A regulates production of virulence determinants by the entomopathogenic fungus, Metarhizium anisopliae. Fungal Genetics and Biology, 46(3), 277–285.

    Article  CAS  PubMed  Google Scholar 

  • Farrag, E. S., & Abo-Elyousr, K. A. (2011). Occurrence of some fungal diseases on date palm trees in upper Egypt and its control. Plant Pathology Journal, 10(4), 154–160.

    Article  Google Scholar 

  • Fawzi, E. (2003). Production and purification of β-glucosidase and protease by Fusarium proliferatum NRRL 26517 grown on Ficus nitida wastes. Annals of Microbiology, 53(4), 463–476.

    CAS  Google Scholar 

  • Giger, M., Baumgartner, H. R., & Zbinden, G. (1974). Toxicological effects of Evans blue and Congo red on blood platelets. Agents and Actions, 4(3), 173–180.

    Article  CAS  PubMed  Google Scholar 

  • Gulati, R., Saxena, R. K., & Gupta, R. (1997). A rapid plate assay for screening l-asparaginase producing microorganisms. Letters in Applied Microbiology, 24(1), 23–26.

    Article  CAS  PubMed  Google Scholar 

  • Haba, E., Bresco, O., Ferrer, C., Marqués, A., Busquets, M., & Manresa, A. (2000). Isolation of lipase-secreting bacteria by deploying used frying oil as selective substrate. Enzyme and Microbial Technology, 26(1), 40–44. https://doi.org/10.1016/S0141-0229(99)00125-8.

    Article  CAS  Google Scholar 

  • Hameed, M. A. (2012). Inflorescence rot disease of date palm caused by Fusarium proliferatum in southern Iraq. African Journal of Biotechnology, 11, 8616–8621.

    Article  CAS  Google Scholar 

  • Hankin, L. & Anagnostakis, S. L. (1977). Solid media containing carboxymethylcellulose to detect Cx cellulase activity of microorganisms. Microbiology, 98(1), 109–115.

  • Harris, P. J. (2000). Compositions of monocotyledon cell walls: Implications for biosystematics. In K. L. Wilson & D. Morrison (Eds.), Monocots: Systematics and evolution (pp. 114–126). Melbourne: CSIRO Publishing.

    Google Scholar 

  • Hasan, S. (2015). Screening of soil fungi for production of lytic enzymes. Annals of Applied Bio-Sciences, 2(4), A81–A87.

    Google Scholar 

  • Hasan, S., Ahmad, A., Purwar, A., Khan, N., Kundan, R., & Gupta, G. (2013). Production of extracellular enzymes in the entomopathogenic fungus Verticillium lecanii. Bioinformation, 9(5), 238–242.

    Article  PubMed  PubMed Central  Google Scholar 

  • Herculano, P. N., Lima, D. M. M., Fernandes, M. J. S., Neves, R. P., Souza-Motta, C. M., & Porto, A. L. F. (2011). Isolation of cellulolytic fungi from waste of castor (Ricinus communis L.). Current Microbiology, 62(5), 1416–1422.

    Article  CAS  PubMed  Google Scholar 

  • Hernández-Fernaud, J. R., Marina, A., González, K., Vázquez, J., & Falcón, M. A. (2006). Production, partial characterization and mass spectrometric studies of the extracellular laccase activity from Fusarium proliferatum. Applied Microbiology and Biotechnology, 70(2), 212–221.

    Article  CAS  Google Scholar 

  • Jansen, C., Von Wettstein, D., Schäfer, W., Kogel, K.-H., Felk, A., & Maier, F. J. (2005). Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proceedings of the National Academy of Sciences of the United States of America, 102(46), 16892–16897.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jo, W. S., Bae, S. H., Choi, S. Y., Park, S. D., Yoo, Y. B., & Park, S. C. (2010). Development of detection methods for cellulolytic activity of Auricularia auricula-judae. Mycobiology, 38(1), 74–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khaledi, N., Taheri, P., & Rastegar, M. F. (2017). Identification, virulence factors characterization, pathogenicity and aggressiveness analysis of Fusarium spp., causing wheat head blight in Iran. European Journal of Plant Pathology, 147(4), 897–918.

    Article  CAS  Google Scholar 

  • Kikot, G. E., Hours, R. A., & Alconada, T. M. (2009). Contribution of cell wall degrading enzymes to pathogenesis of Fusarium graminearum: A review. Journal of Basic Microbiology, 49(3), 231–241.

    Article  CAS  PubMed  Google Scholar 

  • King, B. C., Waxman, K. D., Nenni, N. V., Walker, L. P., Bergstrom, G. C., & Gibson, D. M. (2011). Arsenal of plant cell wall degrading enzymes reflects host preference among plant pathogenic fungi. Biotechnology for Biofuels, 4(1), 4.

    Article  CAS  PubMed  PubMed Central  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(1), 427–451.

    Article  PubMed  CAS  Google Scholar 

  • Kwon, S. I., & Anderson, A. J. (2001). Laccase isozymes: Production by an opportunistic pathogen, a Fusarium proliferatum isolate from wheat. Physiological and Molecular Plant Pathology, 59(5), 235–242.

    Article  CAS  Google Scholar 

  • Kwon, H. W., Yoon, J. H., Kim, S. H., Hong, S. B., Cheon, Y., & Ko, S. J. (2007). Detection of extracellular enzymes activities in various Fusarium spp. Mycobiology, 35(3), 162–165.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, T., Jian, Q., Wang, Y., Chen, F., Yang, C., Gong, L., Duan, X., Yang, B., & Jiang, Y. (2016). Inhibitory mechanism of butylated hydroxyanisole against infection of Fusarium proliferatum based on comparative proteomic analysis. Journal of Proteomics, 148, 1–11. https://doi.org/10.1016/j.jprot.2016.04.051.

    Article  CAS  PubMed  Google Scholar 

  • Lim, G., Tan, T. K., & Rahim, N. A. (1987). Variations in amylase and protease activities among Rhizopus isolates. MIRCEN Journal of Applied Microbiology and Biotechnology, 3(3), 319–322.

    Article  CAS  Google Scholar 

  • Maia, T. F., & Fraga, M. E. (2017). Bioprospecting Aspergillus section Nigri in Atlantic Forest soil and plant litter. Arquivos do Instituto Biológico, 84, 1–7.

    Article  Google Scholar 

  • Mansoori, B. (2012). Fusarium proliferatum induces gum in xylem vessels as the cause of date bunch fading in Iran. Journal of Agricultural Science and Technology, 14(5), 1133–1140.

    Google Scholar 

  • Marín, S., Sanchis, V., Ramos, A. J., & Magan, N. (1998). Effect of water activity on hydrolytic enzyme production by Fusarium moniliforme and Fusarium proliferatum during colonisation of maize. International Journal of Food Microbiology, 42(3), 185–194.

    Article  PubMed  Google Scholar 

  • Motallebi, M., Zamani, M. R., Jazayeri, O., & Harighi, M. J. (2002). Use of RAPD, enzyme activity staining, and colony size to differentiate phytopathogenic Fuzarium oxysporum isolates from Iran. Brazilian Journal of Microbiology, 33, 299–303.

    Article  Google Scholar 

  • Paccanaro, M. C., Sella, L., Castiglioni, C., Giacomello, F., Martínez-Rocha, A. L., D’Ovidio, R., Schäfer, W., & Favaron, F. (2017). Synergistic effect of different plant cell wall-degrading enzymes is important for virulence of Fusarium graminearum. Molecular Plant-Microbe Interactions, 30(11), 886–895.

    Article  CAS  PubMed  Google Scholar 

  • Peterson, R. A., Bradner, J. R., Roberts, T. H., & Nevalainen, K. M. H. (2009). Fungi from koala (Phascolarctos cinereus) faeces exhibit a broad range of enzyme activities against recalcitrant substrates. Letters in Applied Microbiology, 48(2), 218–225.

  • Pointing, S. B. (1999). Qualitative methods for the determination of lignocellulolytic enzyme production by tropical fungi. Fungal Diversity, 2, 17–31.

    Google Scholar 

  • Potshangbam, M., Devi, S. I., Sahoo, D., & Strobel, G. A. (2017). Functional characterization of endophytic fungal community associated with Oryza sativa L. and Zea mays L. Frontiers in Microbiology, 8(325).

  • Saha, B. C. (2002). Production, purification and properties of xylanase from a newly isolated Fusarium proliferatum. Process Biochemistry, 37(11), 1279–1284.

    Article  CAS  Google Scholar 

  • Saha, B. C. (2003). Purification and properties of an extracellular β-xylosidase from a newly isolated Fusarium proliferatum. Bioresource Technology, 90(1), 33–38.

    Article  CAS  PubMed  Google Scholar 

  • Saleh, A. A., Sharafaddin, A. H., El_Komy, M. H., Ibrahim, Y. E., Hamad, Y. K., & Molan, Y. Y. (2017). Fusarium species associated with date palm in Saudi Arabia. European Journal of Plant Pathology, 148(2), 367–377.

    Article  Google Scholar 

  • Sazci, A., Erenler, K., & Radford, A. (1986). Detection of cellulolytic fungi by using Congo red as an indicator: A comparative study with the dinitrosalicyclic acid reagent method. Journal of Applied Bacteriology, 61(6), 559–562.

    Article  CAS  Google Scholar 

  • Schmitz, K., Protzko, R., Zhang, L., & Benz, J. P. (2019). Spotlight on fungal pectin utilization-from phytopathogenicity to molecular recognition and industrial applications. Applied Microbiology and Biotechnology, 103(6), 2507–2524.

    Article  CAS  PubMed  Google Scholar 

  • Shvetsova, S. V., Zhurishkina, E. V., Bobrov, K. S., Ronzhina, N. L., Lapina, I. M., Ivanen, D. R., Gagkaeva, T. Y., & Kulminskaya, A. A. (2015). The novel strain Fusarium proliferatum LE1 (RCAM02409) produces α-L-fucosidase and arylsulfatase during the growth on fucoidan. Journal of Basic Microbiology, 55(4), 471–479.

    Article  CAS  PubMed  Google Scholar 

  • Yang, L., Xie, L., Xue, B., Goodwin, P. H., Quan, X., Zheng, C., et al. (2015). Comparative transcriptome profiling of the early infection of wheat roots by Gaeumannomyces graminis var. tritici. PLoS ONE, 10(4), e0120691.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoon, J. H., Park, J. E., Suh, D. Y., Hong, S. B., Ko, S. J., & Kim, S. H. (2007). Comparison of dyes for easy detection of extracellular cellulases in fungi. Mycobiology, 35(1), 21–24.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zamani, M., Motallebi, M., & Harighi, M. (2001). Pectic enzyme patterns of Fusarium oxysporum virulent isolates from chickpea in Iran. Journal of Science Islamic Republic of Iran, 12(1), 17–22.

    Google Scholar 

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Acknowledgements

The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through the research group no. RG-1440-001.

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Authors and Affiliations

  1. Department of Plant Protection, College of Food and Agriculture Sciences, King Saud University, Box 2460, Riyadh, 11451, Kingdom of Saudi Arabia

    Anwar H. Sharafaddin, Younis K. Hamad, Mahmoud H. El_Komy, Yasser E. Ibrahim, Arya Widyawan, Younes Y. Molan & Amgad A. Saleh

  2. Plant Pathology Department, Faculty of Agriculture, Alexandria University, Alexandria, Egypt

    Younis K. Hamad

  3. Plant Pathology Institute, Agriculture Research Center, Giza, Egypt

    Mahmoud H. El_Komy & Yasser E. Ibrahim

  4. Agricultural Genetic Engineering Research Institute, Agriculture Research Center, Giza, Egypt

    Amgad A. Saleh

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  1. Anwar H. Sharafaddin
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  3. Mahmoud H. El_Komy
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Correspondence to Amgad A. Saleh.

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Sharafaddin, A.H., Hamad, Y.K., El_Komy, M.H. et al. Cell wall degrading enzymes and their impact on Fusarium proliferatum pathogenicity. Eur J Plant Pathol 155, 871–880 (2019). https://doi.org/10.1007/s10658-019-01818-8

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