Journal of Innovative Agriculture, Volume 8, Issue 3 : 1-10. Doi : 10.37446/jinagri/rsa/8.3.2021.1-10
Research Article

OPEN ACCESS | Published on : 30-Sep-2021

Effects of various metal ions on the growth of some phytopathogenic and biological control fungi

  • Babak Pakdaman Sardrood
  • Department of Plant Protection, Faculty of Agriculture, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Khuzestan, Iran.

Abstract

Metal ions are among important environmental factors that influence various aspects of fungal biology and the knowledge on these effects can be applied in integrated plant disease management and mycotechnology. Therefore, in this study the fungal growth on potato dextrose agar, Czapek'sdox agar (CDA, containing FeSO4), and its derivatives made via the replacement of FeSO4 with either of CaSO4, K2SO4, MnSO4, Na2SO4, and ZnSO4 was studied under incubation conditions of 25°C and darkness. The mycelial growth of three biological control (Trichoderma hamatum, T. harzianum, and T. longibrachiatum) and three plant pathogenic (Ceratocystis radicicola, Fusarium oxysporum, and Macrophomina phaseolina) were measured 48h and 72h after inoculation. T. longibrachiatum exhibited the highest mycelial growth and PDA supported the fastest and the highest mycelial growth of most tested fungi. Interestingly, ZnSO4 led to the highest growth of all Trichoderma species, while most of the pathogenic fungi grow well on the media with K2SO4 or Na2SO4.

Keywords

Ceratocystis, Fusarium, Macrophomina, nutrient, Trichoderma

References

  • Avery, S. V. (2001). Metal toxicity in yeasts and the role of oxidative stress. Advances in Applied Microbiology, 49, 111-142. https://doi.org/10.1016/s0065-2164(01)49011-3

    Babu, B. K., Mesapogu, S., Sharma, A., Somasani, S. R., & Arora, D. K. (2011). Quantitative real-time PCR assay for rapid detection of plant and human pathogenic Macrophomina phaseolina from field and environmental samples. Mycologia, 103, 466-473. https://doi.org/10.3852/10-181

    Bates, S., MacCallum, D. M., Bertram, G., Munro, C. A., Hughes, H. B., Buuman, E. T., Brown, A. J. P., Odds, F. C., & Gow, N. A. R. (2005). Candida albicans Pmr1p, a secretory pathway P-type Ca2+/Mn2+-ATPase, is required for glycosylation and virulence. Journal of Biological Chemistry, 280, 23408-23415. https://doi.org/10.1074/jbc.M502162200

    Čertik, M., Breierová, E., & Juršíková, P. (2005). Effect of cadmium on lipid composition of Aureobasidium pullulans grown with added extracellular polysaccharides. International Biodeterioration& Biodegradation, 55, 195-202. https://doi.org/10.1016/j.ibiod.2004.11.005

    Citiulo, F., Jacobsen, I. D., Miramón, P., Schild, L., Brunke, S., Zipfel, P., Brock, M., Hube, B., & Wilson, D. (2012). Candida albicans scavenges host zinc via Pra1 during endothelial invasion. PLoS Pathogens, 8, e1002777. https://doi.org/10.1371/journal.ppat.1002777

    Comensoli, L., Bindschedler, S., Junier, P., & Joseph, E. (2017). Chapter two- Iron and Fungal Physiology: A Review of Biotechnological Opportunities. Advances in Applied Microbiology, 98, 32-60. https://dx.doi.org/10.1016/bs.aambs.2016.11.001

    Conklin, D. S., Culbertson, M. R., & Kung, C. (1994). Interactions between gene products involved in divalent cation transport in Saccharomyces cerevisiae. Molecularand General Genetics, 244, 303-311. https://doi.org/10.1007/BF00285458

    Corbin, B. D., Seeley, E. H., Raab, A., Feldmann, J., Miller, M. R., Torres, V. J., Anderson, K. L., Dattilo, B. M., Dunman, P. M., Gerads, R., Capriolo, R. M., Nacken, W., Chazin, W. J., & Skaar, E. P. (2008) Metal chelation and inhibition of bacterial growth in tissue abscesses. Science, 319, 962-965. https://doi.org/10.1126/science.1152449 

    Cordero, R. J. B., & Casadevall, A. (2017). Functions of fungal melanin beyond virulence. Fungal Biology Reviews, 31, 99-112. Https://doi.org/10.1016/j.fbr.2016.12.003

    Cuero, R., Quellet, T., Yu, J., & Mogongwa, N. (2003). Metal ion enhancement of fungal growth, gene expression and aflatoxin synthesis in Aspergillus flavus: RT-PCR characterization. Journal of Applied Microbiology, 94, 953-961. Https://doi.org/10.1046/j.1365-2672.2003.01870.x 

    Culotta, V. C, Joh, H. D., Lin, S. J., Slekar, K. H., & Strain, J. (1995). A physiological role for Saccharomyces cerevisiae copper/zinc superoxide dismutase in copper buffering. Journal of Biological Chemistry, 270, 29991-29997. https://doi.org/10.1074/jbc.270.50.29991

    Dürr, G., Strayle, J., Plemper, R., Elbs, S., Klee, S. K., Catty, P., Wolf, D. H., & Rudolph, H. K. (1998). The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2+ and Mn2+ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Molecular Biology of the Cell, 9, 1149-1162. https://doi.org/10.1091/mbc.9.5.1149

    Eisendle, M., Schrettl, M., Kragl, C., Müller, D., Illmer, P., & Haas, H. (2006). The intracellular siderophore ferricrocin is involved in iron storage, oxidative-stress resistance, germination, and sexual development in Aspergillus nidulans. Eukaryotic Cell, 5, 1596-1603. https://doi.org/10.1128/EC.00057-06

    Fogarty, R. V., & Tobin, J. M. (1996). Fungal melanins and their interactions with metals. Enzyme and Microbial Technology, 19, 311-317. Https://doi.org/10.1016/0141-0229(96)00002-6

    Gerwien, F., Skrahina, V., Kaspar, L., Hube, B., & Brunke, S. (2018). Metals in fungal virulence. FEMS Microbiology Reviews fux050, 42, 1-21. https://doi.org/femsre/fux050  

    Gitan, R. S., Luo, H., Rodgers, J., Broderius, M., & Eide, D. (1998). Zinc-induced inactivation of the yeast ZRT1 zinc transporter occurs through endocytosis and vacuolar degradation. Journal of Biological Chemistry, 273, 28617-28624. https://doi.org/10.1074/jbc.273.44.28617

    Gitan, R. S., Shababi, M., Kramer, M., & Eide, D. J. (2003). A cytosolic domain of the yeast Zrt1 zinc transporter is required for its post-translational inactivation in response to zinc and cadmium. Journal of Biological Chemistry, 278, 39558-39564. https://doi.org/10.1074/jbc.M302760200

    González-Chávez, M. C., Carrillo-Gonzalez, R., Wright, S. F., & Nichols, K. A. (2004). The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environmental Pollution, 130, 317-323. https://doi.org/10.1016/j.envpol.2004.01.004

    González-Guerrero, M., Benabdellah, K., Ferrol, N., & Azcón-Aguilar, C. (2009). Mechanisms underlying heavy metal tolerance in arbuscular mycorrhizas, pp 107‒122. In: Azcón-Aguilar, C., Barea, J. M., Gianinazzi, S., & Gianinazzi-Pearson, V. (eds.) Mycorrhizas- Functional Processes and Ecological Impacts. Springer.

    Greenshields, D. L., Liu, G., Feng, J., Selvaraj, G., & Wei, Y. (2007). The siderophore biosynthetic gene SID1, but not the ferroxidase gene FET3, is required for full Fusarium graminearum virulence. Molecular Plant Pathology, 8, 411-421. https://doi.org/10.1111/j.1364-3703.2007.00401.x

    Gu, M., & Imlay, J. A. (2013). Superoxide poisons mononuclear iron enzymes by causing mismetallation. Molecular Microbiology, 89, 123-134. https://doi.org/10.1111/mmi.12263

    He, L., Liu, Y., Mustapha, A., & Lin, M. (2011). Antifungal activity of zinc oxide nanoparticles against Botrytis cinerea and Penicillium expansum. Microbiological Research, 166, 207-215. https:/doi.org/j.micres.2010.03.003

    Hissen, A. H., Wan, A. N., Warwas, M. L., Pinto, L. J., & Moore, M. M. (2005). The Aspergillus fumigatus siderophore biosynthetic gene sidA, encoding L-ornithine N5-oxygenase, is required for virulence. Infection and Immunity, 73, 5493-5503. https://doi.org/10.1128/IAI.73.9.5493-5503.2005

    Hjeljord, L., & Tronsmo, A. (1998). Trichoderma and Gliocladium in biological control: an overview. In: G. E. Harman, C. P. Kubicek (eds.) Trichoderma and Gliocladium (pp. 131-151). Taylor and Francis.

    Robinson, J. R., Isikhuemhen, O. S., & Anike, F. N. (2021). Fungal-metal interactions: a review of toxicity and homeostasis. Journal of Fungi, 7, 225. https://doi.org/10.3390/jof7030225

    Jarosz-Wilkołazka, A., & Gadd, G. M. (2003). Oxalate production by wood-rotting fungi growing in toxic metal-amended medium. Chemosphere, 52, 541-547. https://doi.org/10.1016/S0045-6535(03)00235-2

    Jensen, L. T., Ajua-Alemanji, M., & Culotta, V. C. (2003). The Saccharomyces cerevisiae high affinity phosphate transporter encoded by PHO84 also functions in manganese homeostasis. Journal of Biological Chemistry, 278, 42036-42040. https://doi.org/10.1074/jbc.M307413200

    Lanfranco, L., Balsamo, R., Martino, E., Perotto, S., & Bonfante, P. (2002). Zinc ions alter morphology and chitin deposition in an ericoid fungus. European Journal of Histochemistry, 46, 341-350. https://doi.org/10.4081/1746

    Li, L., Chen, McVey, O. S., Ward, D., & Kaplan, J. (2001). CCC1 is a transporter that mediates vacuolar iron storage in yeast. Journal of Biological Chemistry, 276, 29515-29519. https://doi.org/10.1074/JBC.M103944200

    Li, L., & Kaplan, J. (1998). Defects in the yeast high affinity iron transport system result in increased metal sensitivity because of the increased expression of transporters with a broad transition metal specificity. Journal of Biological Chemistry, 273, 22181-22187. https://doi.org/10.1074/jbc.273.35.22181

    Liang, Q., & Zhou, B. (2007). Copper and manganese induce yeast apoptosis via different pathways. Molecular Biology of the Cell, 18: 4741-4749. https://doi.org/10.1091/mbc.e07-05-0431

    Lombard, L., Sandoval-Denis, M., Lamprecht, S. C., & Crous, P. W. (2019). Epitypification of Fusarium oxysporum- clearing the taxonomic chaos. Persoonia, 43, 1-47. https://doi.org/10.3767/persoonia.2019.43.01

    Lyons, T. J., & Eide, D. J. (2014). Transport and storage of metal ions in biology. In: W. Maret,A. Wedd (eds.) Binding, Transport and Storage of Metal Ions in Biological Cells, Metallobiology, Vol. 2. (Pp. 57-78). Royal Society of Chemistry.

    Marquez, N., Giachero, M. L., Declerck, S., & Ducasse, D. A. (2021). Macrophomina phaseolina: general characteristics of pathogenicity and methods of control. Frontiers in Plant Science, 12, 634397. https://doi.org/10.3389/fpls.2021.634397

    Matzanke, B. F. (1994). Iron storage in fungi. In: G. Winkelman,D. R.Winge (eds) Metal Ions in Fungi (pp. 179-213). Marcel Decker Inc.

    Marschner, H. (1995).Mineral Nutrition of Higher Plants, 2nd Edition, Academic Press.

    McDevitt, C. A., Ogunniyi, A. D., Valkov, E., Lawrence, M. C., Kobe, B., McEwan, A. G., & Paton, J. C. (2011). A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathogens, 7, e1002357. https://doi.org/10.1371/journal.ppat.1002357

    Mirzaee, M. R., Mohammadi, M., & Nasrabad, A. A. (2009). Relative susceptibility of citrus genotypes to fruit rot caused by Ceratocystis radicicola in Iran. Tropical Plant Pathology, 34, 329-332.

    Murakami, M., & Hiano, T. (2008). Intracellular zinc homeostasis and zinc signaling. Cancer Science, 99, 1515-1522. https://doi.org/10.1111/j.cmet.2010.08.001

    Mwangi, E. S. K., Gatebe, E. G., & Ndung'u, M. W. (2014). Effect of selected metal ions on the mycelial growth of Sclerotinia sclerotiorum isolated from soybean field in Rongai, Kenya. International Journal of Chemistry and Materials Research, Conscientia Beam, 2, 116-125.

    Nagy, Z., Montigny, C., Leverrier, P., Yeh, S., Goffeau, A., Garrigos, M., & Falson, P. (2006). Role of the yeast ABC transporter Yor1p in cadmium detoxification. Biochimie, 88, 1665-1671. https://doi.org/10.1074/JBC.M103944200

    Netz, D. J., Stith, C. M., Stumpfig, M., Kopf, G., Vogel, D., Genau, H. M., Stodola, J. L., Lill, R., Burgess, P. M. J., & Pierik, A. J. (2012). Eukaryotic DNA polymerase require an iron-sulfur cluster for the formation of active complexes. Nature Chemical Biology, 8, 125-132. https://doi.org/10.1038/nchembio.721

    Nevitt, T. (2011). War-Fe-re: iron at the core of fungal virulence and host immunity. BioMetals, 24, 547-558. https://doi.org/10.1007/s10534-011-9431-8

    Oide, S., Moeder, W., Krasnoff, S., Gibson, D., Haas, H., Yoshioka, K., & Turgeon, B. G. (2006). NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell, 18: 2836-2853. https://doi.org/10.1105/tpc.106.045633

    Ortiz, D. F., Ruscitti, T., McCue, K. F., & Ow, D. W. (1995). Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. Journal of Biological Chemistry, 270, 4721-4728. https://doi.org/10.1074/jbc.270.9.4721

    Perrone, G. G., Grant, C. M., & Dawes, I. W. (2005). Genetic and environmental factors influencing GSH homeostasis in Saccharomyces cerevisiae. Molecular Biology of the Cell, 16, 218-230. https://doi.org/10.1091/mbc.E04-07-0560

    Pócsi, I. (2011). Toxic metal/ metalloid tolerance in fungi‒ a biotechnology-oriented approach, pp 31-58. In: Bánfalvi, G. (ed.). Cellular Effects of Heavy Metals. Springer Science + Business Media BV; https://dx.doi.org/10.1007/978-94-007-0428-2­_2

    Pócsi, I., Prade, R. A., & Penninckx, M. J. (2004). GSH, altruistic metabolite in fungi. Advances in Microbial Physiology, 49, 1-76. https://doi.org/10.1016/S0065-2911(04)49001-8

    Reddi, A. R., Jensen, L. T., Culotta, V. C. (2009). Manganese homeostasis in Saccharomyces cerevisiae. Chem Review, 109, 4722-4732. https://doi.org/10.1021/cr900031u

    Reddi, A. R., Jensen, L. T., Naranuntarat, A., Rosenfeld, L., Leung, E., Shah, R., & Culotta, V. C. (2009). The overlapping roles of manganese and Cu/Zn SOD in oxidative stress protection. Free Radical Biology & Medicine, 46, 154-162. https://doi.org/10.1016/j.freeradbiomed.2008.09.032

    Schrettl, M., Bignell, E., Kragl, C., Joechl, C., Rogers, T., Arst, H. N., Hayanes, Jr. K., & Haas, H. (2004). Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. Journal of Experimental Medicine, 200, 1213-1219. https://doi.org/10.1084/jem.20041242

    Schrettl, M., Bignell, E., Kragl, C., Sabiha, Y., Loss, O., Eisendle, M., Wallner, A., Arst, H. N. Jr, Haynes, K., & Haas, H. (2007). Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathogens, 3, 1195-1207. https://doi.org/10.1371/journal.ppat.0030128

    Schrettl, M., & Haas, H. (2011). Iron homeostasis-Achilles' heel of Aspergillus fumigatus? Current Opinion in Microbiology, 14, 400-405. https://doi.org/10.1016/j.mib.2011.06.002

    Schrettl, M., Kim, H. S., Eisendle, M., Kragl, C., Nierman, W. C., Heinekamp, T., Werner, E. R., Jacobsen, I., Illmer, P., Yi, H., Brakhage, A. A., & Haas, H. (2008). SreA-mediated iron regulation in Aspergillusfumigatus. Molecular Microbiology, 70, 27-43.https://doi.org/10.1111/j.1365-2958.2008.06376.x

    Song, W. Y., Sohn, E. J., Martinoia, E., Lee, Y. J., Yang, Y. Y., Jasinski, M., Forestier, C., Hwang, I., & Lee, Y. (2003). Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nature Biotechnology, 21, 914-919. https://doi.org/10.1038/nbt850

    Sridharan, A. P., Thangappan, S., Karthikeyen, G., Nakkeeran, S., & Sivakumar, U. (2021). Metabolites of Trichoderma longibrachiatum EF5 inhibit soil borne pathogen, Macrophomina phaseolina by triggering amino acid sugar metabolism. Microbial Pathogenesis, 150, 104714.  https://doi.org/10.1016/j.micpath.2020.104714

    Tamás, M. J., Labarre, J., Toledano, M. B., & Wysocki, R. (2005). Mechanisms of toxic metal tolerance in yeast. In: M. J. Tamás,E. Martinoia (eds.) Molecular biology of metal homeostasis and detoxification: from microbes to man (pp. 395-454). Springer.

    Tkaczuk, C. (2005). The effect of selected heavy metal ions on the growth and conidial germination of the aphid pathogenic fungus Pandora neoaphidis (Remaudire et Hennebert) Humber. Polish Journal of Environmental Studies, 14, 897-902.

    Tristão, G. B., do Prado Assunção, L., dos Santos, L. P. O., Borges, C. L., Silva-Bailão, M. G., de Almeida Soares, C. M., Cavallaro, G., & Bailão, A. M. (2015). Predicting copper-, iron-, and zinc-binding proteins in pathogenic species of the Paracoccidioides genus. Frontiers in Microbiology, 5, 761. https://doi.org/10.3389/fmicb.2014.00761

    Vallino, M., Martino, E., Boella, F., Murat, C., Chiapello, M., & Perotto, S. (2009). Cu, Zn superoxide dismutase and zinc stress in metal-tolerant ericoid mycorrhizal fungus Oidiodendronmaius Zn. FEMS Microbiology Letters, 293, 48-57. https://doi.org/10.1111/j.1574-6968.2009.01503.x

    Vesentini, D., Dickinson, D. J., & Murphy, R. J. (2006). Fungicides affect the production of fungal extracellular mucilaginous material (ECMM) and the peripheral growth unit (PGU) in two wood-rotting basidiomycetes. Mycological Research, 110, 1207-1213. https://doi.org/10.1016/j.mycres.2006.07.009

    Walker, G. M., & White, N. A. (2018). Introduction to fungal physiology. In K. Kavanagh, (ed.) Fungi: Biology and Applications, Third Edition (1-35), John Wiley & Sons Inc.

    Weinberg, E. D. (1970). Biosynthesis of secondary metabolites: roles of trace metals. Advances in Microbial Physiology, 4, 1-44. https://doi.org/10.1016/S0065-2911(08)60438-5

    Wilson, D., Citiulo, F., & Hube, B. (2012). Zinc exploitation by pathogenic fungi. PLoS Pathogens, 8, e1003034. https://doi.org/10.1371/journal.ppat.1003034

    Wysocki, R., & Tamás, M. J. (2010). How Saccharomyces cerevisiae copes with toxic metals and metalloids. FEMS Microbiology Reviews, 34, 925-951. https://doi.org/10.1111/j.1574-6976.2010.00217.x

    Xu, H., Guo, M. Y., Gao, Y. H., Bai, X. H., & Zhou, X. W. (2017). Expression and characteristics of manganese peroxidase from Ganoderma lucidum in Pichia pastoris and its application in the degradation of four dyes and phenol. BMC Biotechnology, 17, 19. https://doi.org/10.118/s12896-017-0338-5

    Zhao, H., & Eide, D. (1996a). The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation. Proceedings of the National Academy of Sciences of the United States of America, 93, 2454-2458. https://doi.org/10.1073/pnas.93.6.2454

    Zhao, H., & Eide, D. (1996b). The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. Journal of Biological Chemistry, 271, 23203-23210. https://doi.org/10.1074/jbc.271.38.23203.

Statistics

  • No.of Views (420)
  • PDF Downloads (202)
;