Hypomyces chrysospermus ACL-01 isolated from Boletus edulis and its effect against fungal cereal pathogens

  • A. Cartagena-Luna
  • A.R. Gayosso-Mexia
  • M.A. Anducho-Reyes
  • E.O. López-Villegas
  • Y. Mercado-Flores
Keywords: Hypomyces chrysospermus, Boletus edulis, Tilletia sp., Sporisorium reilianum

Abstract

In this study, a Hypomyces chrysospermus ACL-01 fungus was isolated from the fruiting body of edible basidiomycete Boletus edulis, collected in Acaxochitlán in the State of Hidalgo, Mexico popularly known as tlacoayel. The effect of the isolated fungus against different fungal cereal pathogens was evaluated. The dual confrontation test and scanning electron microscopy analysis revealed that this ascomycete grows on the basidiomycetes Sporisorium reilianum and Tilletia sp., causing loss of cell viability. However, for the ascomycetes Bipolaris sorokiniana and Pyrenophora teres f. teres no effect was observed. On other hand Stenocarpella maydis and Fusarium sp. inhibited the development of H. chrysospermus ACL-01. The isolated strain produced extracellular enzymatic activities of the acid and basic proteases, chitinase and laccase. Cellulase and lipase activities were not found.

References

Andro, T., Chambost ,J.P., Kotoujansky, A., Catteneo, J., Bertheau, Y., Barras, F., van Gijsegem, F., and Colleno, A. (1984). Mutants of Erwinia chrysanthemi defective in secretion of pectinase and cellulase. J Bacteriol 160, 1199–1203.
Almeida, F.B.R., Cerqueira, F.M., Silva, R.N., Ulhoa, C.J., and Lima, A.L. (2007). Mycoparasitism studies of Trichoderma harzianum strains against Rhizoctonia solani: evaluation of coiling and hydrolytic enzyme production. Biotechnol Lett 29, 1189–1193. https://doi.org/10.1007/s10529-007-9372-z
Álvarez-Cervantes, J.,, Hernández-Domínguez, E.M., Tellez-Tellez, M., Mandujano-González, V., Mercado-Flores, Y., and Díaz-Godinez, G. (2016). Stenocarpella maydis and Sporisorium reilianum: Two pathogenic fungi of maize, In: Fungal Pathogenicity, (S. Sultan ed.), Pp. 45–60. INTECH, Croatia. https://doi.org/10.5772/62662
Atanasova, L., Le Crom, S., Gruber, S.., Coulpier, F., Seidl-Seiboth, V., Kubicek, C.P., and Druzhinina, I.S. (2013). Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genomics 14, 121. https://doi.org/10.1186/1471-2164-14-121
Bell, D.K., Wells, H.D., and Markham, C.R. (1982). In vitro antagonism of Trichoderma species against six fungal plant pathogens. Phytopathology 72, 379–382
Benítez, T., Rincón, A.M., Limón, M.C., and Codón, A,C. (2014). Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7, 249–260.
Bensch, M.J., and van Staden, J. (2006). Ultraestructural histopathology of infection and colonization of maize by Stenocarpella maydis (=Diplodia maydis). J Phytopathol 136, 312–318. https://doi.org/10.1111/j.1439-0434.1992.tb01313.x
Beug, M.W., Bessette, A.E., and Bessette, A.R. (2014). Ascomycete Fungi of North America. A mushroom reference guide. Texas University. USA. Pp 45-48.
Both, E.E. (2006). Personal encounters with the parasitic bolete. Field Mycology 7, 104–110. https://doi.org/10.1016/S1468-1641(10)60485-9
Catalano, V., Vergara, M., Hauzenberger, J.R., Seiboth, B., Sarrocco, S., Vannacci, G., Kubicek, C.P., and Seidl-Seiboth, V. (2011). Use of a non-homologous end-joining-deficient strain (delta-ku70) of the biocontrol fungus Trichoderma virens to investigate the function of the laccase gene lcc1 in sclerotia degradation. Curr Genet 57, 13–23. https://doi.org/10.1007/s00294-010-0322-2
Chairattanamanokorn, P., Imai, T., Kondo, R., Ukita, M., and Prasertsan, P. (2006). Screening thermotolerant white-rot fungi for decolorization of wastewaters. Appl Biochem Biotechnol 128, 195–204.
Chet, I., Inbar, J., and Hadar, I. (1997). Fungal antagonists and mycoparasites. In: The Mycota IV: Environmental and microbial relationships, (D.T. Wicklow, and B. Söderström, eds.), Pp. 165–184. Springer-Verlag, Berlin Germany.
Dornberger, K., Ihn, W., Ritzau, M., Gräfe, U., Schlegel, B., and Fleck, W.F. (1995). Chrysospermins, new peptaibol antibiotics from Apiocrea chrysosperma Ap 101. J Antibiot 48, 977–989.
Douhan, G.W., and Rizzo, D.M. (2003). Host-parasite relationships among bolete infecting Hypomyces species. Mycol Res 107, 1342–1349. https://doi.org/10.1017/S0953756203008542
Duffy, B., Schouten, A., and Raaijmakers, J.M. (2003). Pathogen self-defence: mechanisms to counteract microbial antagonism. Ann Rev Phytopathol 41, 501–538. https://doi.org/10.1146/annurev.phyto.41.052002.095606
Ellwood, S.R., Liu, Z., Syme, R.A., Lai, Z., Hane, J.K., Keiper, F., Moffat, C.S., Oliver, R.P., and Friesen, T.L. (2010). A first genome assembly of the barley fungal pathogen Pyrenophora teres f. teres. Genome Biol 11, R109. https://doi.org/10.1186/gb-2010-11-11-r109
Galarza, L., Akagi, Y., Takao, K., Kim, C.S., Maekawa, N., Itai, A., Peralta, E., Santos, E., and Kodoma, M. (2015). Characterization of Trichoderma species isolated in Ecuador and their antagonistic activities against phytopathogenic fungi from Ecuador and Japan. J Gen Plant Pathol 81, 201–210. https://doi.org/10.1007/s10327-015-0587-x
Garg, S., Pandey, D., Taj, G., Goel, A., and Kumar., A. (2014). TRIPATH: a biological genetic and genomic database of three economically important fungal pathogen of wheat – rust: smut: bunt. Bioinformation 10, 466–468. https://doi.org/10.6026/97320630010466
Ghareeb, H., Becker, A., Iven, T., Feussner, I., and Schirawski, J. (2011). Sporisorium reilianum infection changes inflorescence and branching architectures of maize. Plant Physiol 156, 2037–2052. https://doi.org/10.1104/pp.111.179499
Howell, C.R. (2003). Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87, 4–10. http://dx.doi.org/10.1094/PDIS.2003.87.1.4
Kouker, G., and Jaeger, K.E. (1987). Specific and sensitive plate assay for bacterial lipases. Kouker G, Jaeger KE. Specific and sensitive plate assay for bacterial lipases. Appl Environ Microbiol 53, 211–213.
Kumar, U., Joshi, A.K., Kumar, S., Chand, R., and Röder, M.S. (2009). Mapping of resistance to spot blotch disease caused by Bipolaris sorokiniana in spring wheat. Theor Appl Genet 118, 783–792. https://doi.org/10.1007/s00122-008-0938-5
Makovitzki, A., Viterbo, A., Brotman, Y., Chet, I., and Shai, Y. (2007). Inhibition of fungal and bacterial plant pathogens in vitro and in planta with ultrashort cationic lipopeptides. Appl Environ Microbiol 73, 6629–6636. https://doi.org/10.1128/AEM.01334-07
Mitova, M.I., Stuart, B.G., Cao, G..H, Blunt, J.W., Cole, A.L., and Munro, M.H. (2006). Chrysosporide, a cyclic pentapeptide from a New Zealand sample of the fungus Sepedonium chrysospermum. J Nat Prod 69, 1481–1484. https://doi.org/10.1021/np060137o
Nagao, K., Yoshida, N., Iwai, K., Sakai, T., Tanaka, M., and Miyahara, T. (2006) Production of sepedonin by Sepedonium chrysospermum NT-1 in submerged culture. Environ Sci 13, 251–256.
Nelson, G., and Young, T.W. (1986). Yeast extracellular proteolyticenzymes for chill-proofing beer. J Inst Brew 92, 599-603.
Parry, D.W., Jenkinson, P., and McLeod, L. (1995). Fusarium ear blight (scab) in small grain cereals—A review. Plant Pathol 44, 207–238. https://doi.org/10.1111/j.1365-3059.1995.tb02773.x
Qiu, J., and Shi, J. (2014). Genetic relationships, carbendazim sensitivity and mycotoxin production of the Fusarium graminearum populations from maize, wheat and rice in Eastern China. Toxins 6, 2291–2309. https://doi.org/10.3390/toxins6082291
Roberts, W.K., and Selitrennikoff, C.P. (1988). Plant and bacterial chitinases differ in antifungal activity. J Gen Microbiol 134, 169–176.
Sahr, T., Ammer, H., Besl, H., and Fischer, M. (1999). Infrageneric classification of the boleticolous genus Sepedonium: species delimitation and phylogenetic relationships. Mycologia 91, 935–943. https://doi.org/10.2307/3761625
Savary, S., Teng, P.S., Willocquet, L., Nutter, and F.W.Jr. (2006). Quantification and modeling of crop losses: a review of purposes. Ann Rev Phytopathol 44, 89–112. https://doi.org/10.1146/annurev.phyto.44.070505.143342
Schuster, A., and Schmoll, M. (2010). Biology and biotechnology of Trichoderma. Appl Microbiol Biotechnol 87, 787–799. https://doi.org/10.1007/s00253-010-2632-1
Sobhy, I.S., Erb, M., Lou, Y., and Turlings, T.C.J. (2014). The prospect of applying chemical elicitors and plant strengtheners to enhance the biological control of crop pests. Philos Trans R Soc Lond B Biol Sci 369, 20120283. https://doi.org/10.1098/rstb.2012.0283
Stebbins, M.E., and Robbins, W.J. (1949). Mineral oil and preservation of fungous cultures. Mycologia 41, 632–636. https://doi.org/10.1080/00275514.1949.12017806
Swofford, D.L. (1998). PAUP*. Phylogenetic Analysis Using Parsimony, (*and Other Methods), 4.0b4a. Smithsonian Institute. Washington D. C.
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24, 4876–4882.
Vey, A., Hoagland, R.E., and But, T.M. (2001). Toxic metabolites of fungal biocontrol agents. In: Fungi as biocontrol agents: Progress, problems and potential, (T.M., Butt, C., Jackson, and N. Magan, eds.), Pp. 311–346. CAB International, Bristol U.K.
Wagner, D.B., Furnier, G.R., Saghai-Maroof, M.A., Williams, S.M., Dancik, B.P., and Allard, R.W. (1987). Chloroplast DNA polymorphisms in Lodgepole and Jack pines and their hybrids. Proc Nat Acad Sci USA 84, 2097–2100.
Wang, G., Cao, X., Ma, X., Guo, M., Liu, C., Yan, L., and Bian, Y. (2016). Diversity and effect of Trichoderma spp. associated with green mold disease on Lentinula edodes in China. MicrobiologyOpen 5, 709–718. https://doi.org/10.1002/mbo3.364
Whipps, J.M. (2001). Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52, 487–511. https://doi.org/10.1093/jexbot/52.suppl_1.487
White, T.J., Bruns, T., Lee, S., Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: a guide to methods and applications, (M.A., Innis, D.H., Gelfand, J.J., Sninsky, and T.J., White, eds.), Pp. 315–322. Academic Press, New York, USA.
Yurkov, A., Kruger, D., Begerow, D., Arnold, N., and Tarkka, M.T. (2012). Basidiomycetous yeasts from boletales fruiting bodies and their interactions with the mycoparasite Sepedonium chrysospermum and the host fungus Paxillus. Microb Ecol 63, 295–303. https://doi.org/10.1007/s00248-011-9923-7
Published
2020-01-21
How to Cite
Cartagena-Luna, A., Gayosso-Mexia, A., Anducho-Reyes, M., López-Villegas, E., & Mercado-Flores, Y. (2020). Hypomyces chrysospermus ACL-01 isolated from Boletus edulis and its effect against fungal cereal pathogens. Revista Mexicana De Ingeniería Química, 19(3), 1277-1290. https://doi.org/10.24275/rmiq/Bio795

Most read articles by the same author(s)