The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Colony Age of Trichoderma azevedoi Alters the Profile of Volatile Organic Compounds and Ability to Suppress Sclerotinia sclerotiorum in Bean Plants

  • Received : 2022.08.07
  • Accepted : 2022.11.14
  • Published : 2023.02.01
Download PDF
⟨ Previous Next ⟩

Abstract

Common bean (Phaseolus vulgaris L.) is one of the most important crops in human food production. The occurrence of diseases, such as white mold, caused by Sclerotinia sclerotiorum can limit the production of this legume. The use of Trichoderma has become an important strategy in the suppression of this disease. The aim of the present study was to evaluate the effect of volatile organic compounds (VOCs) emitted by Trichoderma azevedoi CEN1241 in five different growth periods on the severity of white mold in common bean. The in vitro assays were carried out in double-plate and split-plate, and the in vivo assays, through the exposure of the mycelia of S. sclerotiorum to the VOCs of T. azevedoi CEN1241 and subsequent inoculation in bean plants. Chemical analysis by gas chromatography coupled to mass spectrometry detected 37 VOCs produced by T. azevedoi CEN1241, covering six major chemical classes. The profile of VOCs produced by T. azevedoi CEN1241 varied according to colony age and was shown to be related to the ability of the biocontrol agent to suppress S. sclerotiorum. T. azevedoi CEN1241 VOCs reduced the size of S. sclerotiorum lesions on bean fragments in vitro and reduced disease severity in a greenhouse. This study demonstrated in a more applied way that the mechanism of antibiosis through the production of volatile compounds exerted by Trichoderma can complement other mechanisms, such as parasitism and competition, thus contributing to a better efficiency in the control of white mold in bean plants.

Keywords

Acknowledgement

The authors thank the National Council for Scientific and Technological Development (CNPq) for the technological and industrial development grant (DTI-A), granted to the first author and Federal District Research Support Foundation (FAPDF) for the financial support.

References

  1. Bisset, J. 1984. A revision of the genus Trichoderma. I. Section Longibrachiatum sect. nov. Can. J. Bot. 62:924-931. https://doi.org/10.1139/b84-131
  2. Cardoso, R. M. and Ferreira, E. P. B. 2021. Assessment of consortia inoculation effects on the agronomical performance of the common bean. Commun. Soil Sci. Plant Anal. 52:1971-1980. https://doi.org/10.1080/00103624.2021.1908319
  3. Carvalho, D. D. C., de Mello, S. C. M., Lobo Junior, M. and Geraldine, A. M. 2011. Biocontrol of seed pathogens and growth promotion of common bean seedlings by Trichoderma harzianum. Pesq. Agropec. Bras. 46:822-828. https://doi.org/10.1590/S0100-204X2011000800006
  4. Carvalho, D. D. C., Geraldine, A. M., Lobo Junior, M. and de Mello, S. C. M. 2015. Biological control of white mold by Trichoderma harzianum in common bean under field conditions. Pesq. Agropec. Bras. 50:1220-1224. https://doi.org/10.1590/S0100-204X2015001200012
  5. Castillo, F. D. H., Padilla, A. M. B., Morales, G. G., Siller, M. C., Herrera, R. R., Gonzales, C. N. A. and Reyes, F. C. 2011. In vitro antagonist action of Trichoderma strains against Sclerotinia sclerotiorum and Sclerotium cepivorum. Am. J. Agric. Biol. Sci. 6:410-417. https://doi.org/10.3844/ajabssp.2011.410.417
  6. Cruz-Magalhaes, V., Nieto-Jacobo, M. F., van Zijll de Jong, E., Rostas, M., Padilla-Arizmendi, F., Kandula, D., Kandula, J., Hampton, J., Herrera-Estrella, A., Steyaert, J. M., Stewart, A., Loguercio, L. L. and Mendoza-Mendoza, A. 2019. The NADPH oxidases Nox1 and Nox2 differentially regulate volatile organic compounds, fungistatic activity, plant growth promotion and nutrient assimilation in Trichoderma atroviride. Front. Microbiol. 9:3271.
  7. da Silva, L. R., de Mello, S. C. M., Valadares-Inglis, M. C., do Carmo Costa, M. M., Saraiva, M. A. P., Rego, E. C. S., Zacaroni, A. B., Muniz, P. H. P. C. and Pappas, M. C. R. 2022. Transcriptional responses and reduction in carpogenic germination of Sclerotinia sclerotiorum exposed to volatile organic compounds of Trichoderma azevedoi. Biol. Control 169:104897.
  8. da Silva, L. R., Muniz, P. H. P. C., Peixoto, G. H. S., Luccas, B. E. G. D., da Silva, J. B. T. and de Mello, S. C. M. 2021a. Mycelial inhibition of Sclerotinia sclerotiorum by Trichoderma spp. volatile organic compounds in distinct stages of development. Pak. J. Biol. Sci. 24:527-536. https://doi.org/10.3923/pjbs.2021.527.536
  9. da Silva, L. R., Valadares-Inglis, M. C., Moraes, M. C. B., Magalhaes, D. M., Sifuentes, D. N., Martins, I. and de Mello, S. C. M. 2020. Morphological and protein alterations in Sclerotinia sclerotiorum (Lib.) de Bary after exposure to volatile organic compounds of Trichoderma spp. Biol. Control 147:104279.
  10. da Silva, L. R., Valadares-Inglis, M. C., Peixoto, G. H. S., de Luccas, B. E. G., Muniz, P. H. P. C., Magalhaes, D. M., Moraes, M. C. B. and Mello, S. C. M. 2021b. Volatile organic compounds emitted by Trichoderma azevedoi promote the growth of lettuce plants and delay the symptoms of white mold. Biol. Control 152:104447.
  11. de Figueiredo, G. S., Figueiredo, L. C., Cavalcanti, F. C. N., dos Santos, A. C., da Costa, A. F. and de Oliveira, N. T. 2010. Biological and chemical control of Sclerotinia sclerotiorum using Trichoderma spp. and Ulocladium atrum and pathogenicity to bean plants. Braz. Arch. Biol. Technol. 53:1-9. https://doi.org/10.1590/S1516-89132010000100001
  12. Dennis, C. and Webster, J. 1971. Antagonistic properties of species-groups of Trichoderma, II. Production of volatile antibiotic. Trans. Br. Mycol. Soc. 57:41-48. https://doi.org/10.1016/s0007-1536(71)80078-5
  13. Elsherbiny, E. A., Amin, B. H., Aleem, B., Kingsley, K. L. and Bennett, J. W. 2020. Trichoderma volatile organic compounds as a biofumigation tool against late blight pathogen Phytophthora infestans in postharvest potato tubers. J. Agric. Food Chem. 68:8163-8171. https://doi.org/10.1021/acs.jafc.0c03150
  14. Eslahi, N., Kowsari, M., Zamani, M. R. and Motallebi, M. 2021. Correlation study between biochemical and molecular pathways of Trichoderma harzianum recombinant strains on plant growth and health. J. Plant Growth Regul. 41:1561-1577. https://doi.org/10.1007/s00344-021-10396-1
  15. Estrada-Rivera, M., Rebolledo-Prudencio, O. G., Perez-Robles, D. A., Rocha-Medina, M. D. C., Gonzalez-Lopez, M. D. C. and Casas-Floresa, S. 2019. Trichoderma histone deacetylase HDA-2 modulates multiple responses in Arabidopsis. Plant Physiol. 179:1343-1361. https://doi.org/10.1104/pp.18.01092
  16. Ferreira, D. F. 2011. Sisvar: a computer statistical analysis system. Cienc. Agrotec. 35:1039-1042. https://doi.org/10.1590/S1413-70542011000600001
  17. Ganascini, D., Laureth, J. C. U., Mendes, I. S., Tokura, L. K., Sutil, E. L., de Villa, B., Alovisi, A. M. T., Caon, I. L., Mercante, E. and Coelho, S. R. M. 2019. Analysis of the production chain of bean culture in Brazil. J. Agric. Sci. 11:256-267. https://doi.org/10.5539/jas.v11n7p256
  18. Geraldine, A. M., Lopes, F. A. C., Carvalho, D. D. C., Barbosa, E. T., Rodrigues, A. R., Brandao, R. S., Ulhoa, C. J. and Lobo Junior, M. 2013. Cell wall-degrading enzymes and parasitism of sclerotia are key factors on field biocontrol of white mold by Trichoderma spp. Biol. Control 67:308-316. https://doi.org/10.1016/j.biocontrol.2013.09.013
  19. Gonzalez-Perez, E., Ortega-Amaro, M. A., Salazar-Badillo, F. B., Bautista, E., Douterlungne, D. and Jimenez-Bremont, J. F. 2018. The Arabidopsis-Trichoderma interaction reveals that the fungal growth medium is an important factor in plant growth induction. Sci. Rep. 8:16427.
  20. Guo, Y., Ghirardo, A., Weber, B., Schnutzier, J.-P., Philip Benz, J. and Rosenkranz, M. 2019. Trichoderma species differ in their volatile profiles and in antagonism toward ectomycorrhiza Laccaria bicolor. Front. Microbiol. 10:891.
  21. Hicks, J., Yu, J. H., Keller, N. P. and Adams, T. H. 1997. Aspergillus sporulation and mycotoxin production both require inactivation of the FadA G-alpha protein-dependent signaling pathway. EMBO J. 16:4916-4923. https://doi.org/10.1093/emboj/16.16.4916
  22. IBRAFE. 2021. Boletim so feijao. URL https://www.ibrafe.org/ boletim-so-feijao/ [1 February 2022].
  23. Inglis, P. W., Mello, S. C. M., Martins, I., Silva, J. B. T., Macedo, K., Sifuentes, D. N. and Valadares-Inglis, M. C. 2020. Trichoderma from Brazilian garlic and onion crop soils and description of two new species: Trichoderma azevedoi and Trichoderma peberdyi. PLoS ONE 15:e0228485.
  24. Intana, W., Kheawleng, S. and Sunpapao, A. 2021. Trichoderma asperellum T76-14 released volatile organic compounds against postharvest fruit rot in muskmelons (Cucumis melo) caused by Fusarium incarnatum. J. Fungi 7:46.
  25. Kamaruzzaman, M., Islam, M. S., Mahmud, S., Polash, S. A., Sultana, R., Hasan, M. A., Wang, C. and Jiang, C. 2021. In vitro and in silico approach of fungal growth inhibition by Trichoderma asperellum HbGT6-07 derived volatile organic compounds. Arab. J. Chem. 14:103290.
  26. Karimi, A. K. and Altinok, H. H. 2019. In vitro anifungal activity of Trichoderma harzianum Rifai and PGPR strains as biocontrol agents against gray mold and white mold in eggplant. Fresenius Environ. Bull. 28:6166-6173.
  27. Kubicek, C. P., Herrera-Estrella, A., Seidl-Seiboth, V., Martinez, D. A., Druzhinina, I. S., Thon M., Zeilinger, S., CasasFlores, S., Horwitz, B. A., Mukherjee, P. K., Mukherjee, M., Kredics, L., Alcaraz, L. D., Aerts, A., Antal, Z., Atanasova, L., Cervantes-Badillo, M. G., Challacombe, J., Chertkov, O., McCluskey, K., Coulpier, F., Deshpande, N., von Dohren, H., Ebbole, D. J., Esquivel-Naranjo, E. U., Fekete, E., Flipphi, M., Glaser, F., Gomez-Rodriguez, E. Y., Gruber, S., Han, C., Henrissat, B., Hermosa, R., Hernandez-Onate, M., Karaffa, L., Kosti, I., Le Crom, S., Lindquist, E., Lucas, S., Lubeck, M., Lubeck, P. S., Margeot, A., Metz, B., Misra, M., Nevalainen, H., Omann, M., Packer, N., Perrone, G., Uresti-Rivera, E. E., Salamov, A., Schmoll, M., Seiboth, B., Shapiro, H., Sukno, S., Tamayo-Ramos, J. A., Tisch, D., Wiest, A., Wilkinson, H. H., Zhang, M., Coutinho, P. M., Kenerley, C. M., Monte, E., Baker, S. E. and Grigoriev, I. V. 2011. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol. 12:R40. https://doi.org/10.1186/gb-2011-12-4-r40
  28. Kumar, S., Shukla, V., Dubey, M. K. and Upadhyay, R. S. 2021. Activation of defense response in common bean against stem rot disease triggered by Trichoderma erinaceum and Trichoderma viride. J. Basic Microbiol. 61:910-922. https://doi.org/10.1002/jobm.202000749
  29. Lazazzara, V., Vicelli, B., Bueschl, C., Parich, A., Pertot, I., Schuhmacher, R. and Perazzolli, M. 2021. Trichoderma spp. volatile organic compounds protect grapevine plants by activating defense-related processes against downy mildew. Physiol. Plant. 172:1950-1965. https://doi.org/10.1111/ppl.13406
  30. Lee, S., Hung, R., Yap, M. and Bennett, J. W. 2015. Age matters: the effects of volatile organic compounds emitted by Trichoderma atroviride on plant growth. Arch. Microbiol. 197:723-727. https://doi.org/10.1007/s00203-015-1104-5
  31. Lee, S., Yap, M., Behringer, G., Hung, R. and Bennett, J. W. 2016. Volatile organic compounds emitted by Trichoderma species mediate plant growth. Fungal Biol. Biotechnol. 3:7.
  32. Li, N., Alfiky, A., Wang, W., Islam, M., Nourollahi, K., Liu, X. and Kang, S. 2018. Volatile compound-mediated recognition and inhibition between Trichoderma biocontrol agents and Fusarium oxysporum. Front. Microbiol. 9:2614.
  33. Mahoney, K. J., McCreary, C. M. and Gillard, C. L. 2014. Response of dry bean white mold [Sclerotinia sclerotiorum (Lib.) de Bary, causal organism] to fungicides. Can. J. Plant Sci. 94:905-910. https://doi.org/10.4141/cjps2013-311
  34. Mayo-Prieto, S., Porteous-Alvarez, A. J., Mezquita-Garcia, S., Rodriguez-Gonzalez, A., Carro-Huerga, G., del Ser-Herrero, S., Gutierrez, S. and Casquero, P. A. 2021. Influence of physicochemical characteristics of bean crop soil in Trichoderma spp. development. Agronomy 11:274.
  35. Miklas, P. N., Porter, L. D., Kelly, J. D. and Myers, J. R. 2013. Characterization of white mold disease avoidance in common bean. Eur. J. Plant Pathol. 135:525-543. https://doi.org/10.1007/s10658-012-0153-8
  36. Motlagh, M. R. S. and Abolghasemi, M. 2022. The effect of Trichoderma spp. isolates on some morphological traits of canola inoculated with Sclerotinia sclerotiorum and evaluation of their efficacy in biological control of pathogen. J. Saudi Soc. Agric. Sci. 21:217-231.
  37. Mukherjee, P. K., Horwitz, B. A. and Kenerley, C. M. 2012. Secondary metabolism in Trichoderma: a genomic perspective. Microbiology 158:35-45. https://doi.org/10.1099/mic.0.053629-0
  38. National Institute of Standards and Technology. 2020. Chemdata.Nist.Gov Mass Spectrometry Data Center. URL https://chemdata.nist.gov/dokuwiki/doku.php?id=chemdata:downloads:start [1 February 2022].
  39. Nawrocka, J., Szczech, M. and Malolepsza, U. 2018. Trichoderma atroviride enhances phenolic synthesis and cucumber protection against Rhizoctonia solani. Plant Prot. Sci. 54:17-23. https://doi.org/10.17221/126/2016-PPS
  40. Nieto-Jacobo, M. F., Steyaert, J. M., Salazar-Badillo, F. B., Vi Nguyen, D., Rostas, M., Braithwaite, M., De Souza, J. T., Jimenez-Bremont, J. F., Ohkura, M., Stewart, A. and Mendoza-Mendoza, A. 2017. Environmental growth conditions of Trichoderma spp. affects indole acetic acid derivatives, volatile organic compounds, and plant growth promotion. Front. Plant Sci. 8:102.
  41. O'Brien, P. A. 2017. Biological control of plant diseases. Aust. Plant Pathol. 46:293-304. https://doi.org/10.1007/s13313-017-0481-4
  42. Ojaghian, S., Wang, L., Xie, G.-L. and Zhang, J.-Z. 2019. Effect of volatiles produced by Trichoderma spp. on expression of glutathione transferase genes in Sclerotinia sclerotiorum. Biol. Control 136:103999.
  43. Ordonez-Valencia, C., Ferrera-Cerrato, R., Quintanar-Zuniga, R. E., Flores-Ortiz, C. M., Guzman, G. J. M., Alarcon, A., Larsen, J. and Garcia-Barradas, O. 2015. Morphological development of sclerotia by Sclerotinia sclerotiorum: a view from light and scanning electron microscopy. Ann. Microbiol. 65:765-770. https://doi.org/10.1007/s13213-014-0916-x
  44. R Core Team. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/ [1 February 2022].
  45. Rajani, P., Rajasekaran, C., Vasanthakumari, M. M., Olsson, S. B., Ravikanth, G. and Shaanker, R. U. 2021. Inhibition of plant pathogenic fungi by endophytic Trichoderma spp. through mycoparasitism and volatile organic compounds. Microbiol. Res. 242:126595.
  46. Ruangwong, O.-U., Wonglom, P., Suwannarach, N., Kumla, J., Thaochan, N., Chomnunti, P., Pitija, K. and Sunpapao, A. 2021. Volatile organic compound from Trichoderma asperelloides TSU1: impact on plant pathogenic fungi. J. Fungi 7:187.
  47. Siddiquee, S., Cheong, B. E., Taslima, K., Kausar, H. and Hasan, M. M. 2012. Separation and identification of volatile compounds from liquid cultures of Trichoderma harzianum by GC-MS using three different capillary columns. J. Chromatogr. Sci. 50:358-367. https://doi.org/10.1093/chromsci/bms012
  48. Smolinska, U. and Kowalska, B. 2018. Biological control of the soil-borne fungal pathogen Sclerotinia sclerotiorum: a review. J. Plant Pathol. 100:1-12. https://doi.org/10.1007/s42161-018-0023-0
  49. Spiteller, P. 2015. Chemical ecology of fungi. Nat. Prod. Rep. 32:971-993. https://doi.org/10.1039/C4NP00166D
  50. Srivastava, M., Kumar, V., Shahid, M., Pandey, S. and Singh, A. 2016. Trichoderma: a potential and effective bio fungicide and alternative source against notable phytopathogens: a review. Afr. J. Agric. Res.11:310-316. https://doi.org/10.5897/AJAR2015.9568
  51. Trail, F., Mahanti, N. and Linz, J. 1995. Molecular biology of aflatoxin biosynthesis. Microbiology 141:755-765.  https://doi.org/10.1099/13500872-141-4-755
  52. Wonglom, P., Ito, S.-I. and Sunpapao, A. 2020. Volatile organic compounds emitted from endophytic fungus Trichoderma asperellum T1 mediate antifungal activity, defense response and promote plant growth in lettuce (Lactuca sativa). Fungal Ecol. 43:100867.
  53. You, J., Li, G., Li, C., Zhu, L., Yang, H., Song, R. and Gu, W. 2022. Biological control and plant growth promotion by volatile organic compounds of Trichoderma koningiopsis T-51. J. Fungi 8:131.