Biochar and Trichoderma spp. in management of plant diseases caused by soilborne fungal pathogens: a review and perspective
DOI:
https://doi.org/10.33448/rsd-v10i15.22465Keywords:
Black carbon; Biocontrol; Soil Health; Management practices; Plant growth-promoting.Abstract
A better understanding of the use of biochar with Trichoderma spp. (TRI), considered the most studied tool for biological control, would increase our ability to set priorities. However, no studies exist using the two inputs on plant disease management. Here, we hypothesized that biochar and TRI would be used for the management of soilborne plant pathogens, mainly due to changes in soil properties and its interactions. To test this hypothesis, this review assesses papers that used biochar and TRI against plant diseases and we summarize the handling mechanisms for each input. Biochar acts by mechanisms: induction to plant resistance, sorption of allelopathic and fungitoxic compounds, increase of beneficial microorganisms, changes the soil properties that promote health and nutrient availability. Trichoderma as biocontrol agents by different mechanisms: mycoparasitism, enzyme and secondary metabolic production, plant promoter agent, natural decomposition agent, and biological agent of bioremediation. Overall, our findings expand our knowledge about the reuse of wastes transformed in biochar combined with Trichoderma has potential perspective to formulate products as alternative management tool of plant disease caused by soilborne fungal pathogen and add important information that can be suitable for development of strategy for use in the global health concept.
References
Ajeng, A. A., Abdullah, R., Ling, T. C., Ismail, S., Lau, B. F., Ong, H. C., & Chang, J. S. (2020). Bioformulation of biochar as a potential inoculant carrier for sustainable agriculture. Environmental Technology & Innovation, 101168. https://doi org/10 1016/j eti 2020 101168
Al-ani, L. K. T., & Albaayit, S. F. A. (2018). Antagonistic of some Trichoderma against Fusarium oxysporum sp f cubense tropical race 4 (FocTR4).
The Eurasia Proceedings of Science, Engineering & Mathematics, 2, 35–38.
Alfiky, A. (2019). Effects of ultraviolet irradiation on the in vitro antagonistic potential of Trichoderma spp against soil-borne fungal pathogens. Heliyon 5(7), e02111. https://doi org/e02111 10 1016/j heliyon 2019 e02111
Bettiol, W., Pinto, Z. V., da Silva, J. C., Forner, C., de Faria, M. R., Pacifico, M. G., Costa, L. S. A. S. (2019). Produtos comerciais à base de Trichoderma Trichod 1:45.
Bhandari, D. (2017). Bio-control ability of Trichoderma species against spot blotch disease (wheat) causing pathogen Bipolaris sorokiniana under in vitro condition. Journal of Bioscience and Agriculture Research, 14(02): 1194–1201. https://doi org/10 18801/jbar 140217 147
Bora, B., & Ali, M. S. (2019). Evaluation of Microbial Antagonists against Sarocladium oryzae Causing Sheath Rot Disease of Rice (Oryzae sativa L). International Journal of Current Microbiology and Applied Sciences, 8(7), 1755–1760. https://doi org/10 20546/ijcmas 2019 807 208
Chagas. L. F. B., Junior, A. F. C., Soares, L. P., & Fidelis, R. R. (2017). Trichoderma na promoção do crescimento vegetal. Journal of Neotropical Agriculture, 4(3): 97–102. https://doi org/10 32404/rean v4i3 1529
Chaudhary, S., Sagar, S., Lal, M., Tomar, A., Kumar, V., & Kumar, M. (2020). Biocontrol and growth enhancement potential of Trichoderma spp against Rhizoctonia solani causing sheath blight disease in rice. Journal of Environmental Biology, 41(5), 1034–1045. https://doi org/10 22438/jeb/41/5/MRN-1303
Checa, C. O. E., Toro, C. M., & Descanse, V. J. (2017). Antagonism of Trichoderma spp. strains against pea (Pisum sativum L.) Fusarium wilt caused by Fusarium oxysporum f. sp. pisi. Acta Agronómica, 66(3), 442–448.
Cherkupally, R., Amballa, H., & Reddy, B. N. (2017). In vitro antagonistic activity of Trichoderma species against Fusarium oxysporum f sp melongenae. International Journal of Applied Agricultural Research, 12(1), 87–95.
Coelho. L., Reis, M., Guerrero, C., & Dionísio, L. (2020). Use of organic composts to suppress bentgrass diseases in Agrostis stolonifera. Biological control, 141, 104154. https://doi org/10 1016/j biocontrol 2019 104154
Da Silva, J. A. T., de Medeiros, E. V., da Silva, J. M., Tenório, D. D. A., Moreira, K. A., Nascimento, T. C. E. D. S., & Souza‐Motta, C. (2016). Trichoderma aureoviride URM 5158 and Trichoderma hamatum URM 6656 are biocontrol agents that act against cassava root rot through different mechanisms. Journal of Phytopathology, 164(11–12), 1003–1011. https://doi org/10 1111/jph 12521
Dendouga, W., Boureghda, H., & Belhamra, M. (2016). Biocontrol of wheat Fusarium crown and root rot by Trichoderma spp and evaluation of their cell wall degrading enzymes activities. Acta Phytopathologica et Entomologica Hungarica, 51(1), 1–12. https://doi org/10 1556/038 51 2016
Elamathi, E., Malathi, P., Viswanathan, R., & Sundar, A. R. (2018). Expression analysis on mycoparasitism related genes during antagonism of Trichoderma with Colletotrichum falcatum causing red rot in sugarcane. Journal of Plant Biochemistry and Biotechnology, 27(3), 351–361. https://doi org/10 1007/s13562-018-0444-z
El-Gremi, S. M., Draz, I. S., & Youssef, W. A. E. (2017). Biological control of pathogens associated with kernel black point disease of wheat. Crop Protection, 91, 13–19. http://dx doi org/10 1016/j cropro 2016 08 034 0261-2194
Elhadidy, A. E. (2019). Performance of some new bioformulations against tomato fusarium wilt. Egyptian Journal of Desert Research, 69(1), 1–19. http://dx doi org/10 21608/ejdr 2019 10162 1022
Elshahawy, I. E., & El-Mohamedy, R. S. (2019). Biological control of Pythium damping-off and root-rot diseases of tomato using Trichoderma isolates employed alone or in combination. Journal of Plant Pathology, 101(3), 597–608. https://doi org/10 1007/s42161-019-00248-z
Foster, E. J., Hansen, N., Wallenstein, M., & Cotrufo, M. F. (2016). Biochar and manure amendments impact soil nutrients and microbial enzymatic activities in a semi-arid irrigated maize cropping system. Agriculture, Ecosystems & Environment, 233: 404–414. https://doi org/10 1016/j agee 2016 09 029
Galletti, S., Paris, R., & Cianchetta, S. (2020) Selected isolates of Trichoderma gamsii induce different pathways of systemic resistance in maize upon Fusarium verticillioides challenge. Microbiological Research, 233, 126406. https://doi org/10 1016/j micres 2019 126406
Ghorbanpour, M., Omidvari, M., Abbaszadeh-Dahaji, P., Omidvar, R., & Kariman, K. (2018). Mechanisms underlying the protective effects of beneficial fungi against plant diseases. Biological Control, 117, 147–157. https://doi org/10 1016/j biocontrol 2017 11 006
Haddad, P. E., Leite, L. G., Lucon, C. M. M., & Harakava, R. (2017). Selection of Trichoderma spp strains for the control of Sclerotinia sclerotiorum in soybean. Pesquisa Agropecuária Brasileira, 52(12), 1140–1148.
He, A. L., Jia, Liu., Wang, X. H., Zhang, Q. G., Wei, S., & Jie, C. (2019). Soil application of Trichoderma asperellum GDFS1009 granules promotes growth and resistance to Fusarium graminearum in maize. Journal of Integrative Agriculture, 18(3), 599–606.
Hirpara, D. G., Gajera, H. P., Hirpara, H. Z., & Golakiya, B. A. (2016). Molecular diversity and fingerprints of Trichoderma associated with antagonistic potentials against Sclerotium rolfsii Sacc. Journal of Plant Diseases and Protection, 124(1), 31–40. https://doi org/10 1007/s41348-016-0053-9
Hirpara, D. G., Gajera, H. P., Hirpara, H. Z., & Golakiya, B. A. (2017). Antipathy of Trichoderma against Sclerotium rolfsii Sacc: evaluation of cell wall-degrading enzymatic activities and molecular diversity analysis of antagonists. Journal of Molecular Microbiology and Biotechnology, 27(1): 22–28. https://doi org/10 1159/000452997
Hong, S., Jv, H., Lu, M., Wang, B., Zhao, Y., & Ruan, Y. (2020). Significant decline in banana Fusarium wilt disease is associated with soil microbiome reconstruction under chilli pepper-banana rotation. European Journal of Soil Biology, 97, 103154. https://doi org/10 1016/j ejsobi 2020 103154
Jaiswal, A. K., Elad, Y., Cytryn, E., Graber, E. R., & Frenkel, O. (2018). Activating biochar by manipulating the bacterial and fungal microbiome through pre‐conditioning. New Phytologist, 219(1), 363–377. https://doi org/10 1111/nph 15042
Jiang, H., Zhang, L., Zhang, J. Z., Ojaghian, M. R., & Hyde, K. D. (2016). Antagonistic interaction between Trichoderma asperellum and Phytophthora capsici in vitro. Journal of Zheijang University Science B, 17(4), 271–281. http://dx doi org/10 1631/jzus B1500243
Kazerooni, E. A., Al-Shibli, H., Nasehi, A., & Al-Sadi, A. M. (2020). Endophytic Enterobacter cloacae exhibits antagonistic activity against Pythium damping-off of cucumber. Ciência Rural, 50(8), e20191035. https://doi org/10 1590/0103-8478cr20191035
Khaled, N., & Taheri, P. (2016). Biocontrol mechanisms of Trichoderma harzianum against soybean charcoal rot caused by Macrophomina phaseolina. Journal of Plant Protection Research, 56(1), 21–31. https://doi org/10 1515/jppr-2016-0004
Khalili, E., Javed, M. A., Huyop, F., Rayatpanah, S., Jamshidi, S., & Wahab, R. A. (2016). Evaluation of Trichoderma isolates as potential biological control agent against soybean charcoal rot disease caused by Macrophomina phaseolina. Biotechnology & Biotechnological Equipment, 30(3), 479–488. https://doi org/10 1080/13102818 2016 1147334
Kumar, G., Maharshi, A., Patel, J., Mukherjee, A., Singh, H. B., & Sarma, B. K. (2017). Trichoderma: a potential fungal antagonist to control plant diseases. SATSA Mukhapatra Annual Technical Issue, 21, 206–218.
Kuzmanovska, B., Rusevski, R., Jankulovska, M., & Oreshkovikj, K. B. (2018). Antagonistic activity of Trichoderma asperellum and Trichoderma harzianum against genetically diverse Botrytis cinerea isolates. Chilean Journal of Agricultural Research, 78(3), 391–399. http://dx doi org/10 4067/S0718-58392018000300391
Larkin, R. P., & Brewer, M. T. (2020). Effects of crop rotation and biocontrol amendments on Rhizoctonia disease of potato and soil microbial communities. Agriculture 10(4), 128. https://doi org/10 3390/agriculture10040128
Larran, S., Santamarina, S. M. P., Roselló, C. J., Simón, M. R., & Perelló, A. (2020). In vitro antagonistic activity of Trichoderma harzianum against Fusarium sudanense causing seedling blight and seed rot on wheat. ACS omega, 5(36), 23276–23283. https://doi org/10 1021/acsomega 0c03090
Lee, S., Yap, M., Behringer, G., Hung, R., & Bennett, J. W. (2016). Volatile organic compounds emitted by Trichoderma species mediate plant growth. Fungal Biology and Biotechnology, 3(1), 1–14. https://doi org/10 1186/s40694-016-0025-7
Lehmann, J., Rillig, M. C., Thies, J., Masiello, C. A., Hockaday, W. C., & Crowley, D. (2011). Biochar effects on soil biota–a review. Soil Biology & Biochemistry, 43(9), 1812–1836. https://doi org/10 1016/j soilbio 2011 04 022
Li, Y., Sun, R., Yu, J., Saravanakumar, K., & Chen, J. (2016). Antagonistic and biocontrol potential of Trichoderma asperellum ZJSX5003 against the maize stalk rot pathogen Fusarium graminearum. Indian Journal of Microbiology Research, 56(3), 318–327. https://doi org/10 1007/s12088-016-0581-9
Lima, J. R., de Moraes, S. W., de Medeiros, E. V., Duda, G. P., Corrêa, M. M., Martins Filho, A. P., & Hammecker, C. (2018). Effect of biochar on physicochemical properties of a sandy soil and maize growth in a greenhouse experiment. Geoderma, 319, 14–23. https://doi org/10 1016/j geoderma 2017 12 033
Liu, J., Ding, Y., Ji, Y., Gao, G., & Wang, Y. (2020). Effect of maize straw biochar on bacterial communities in agricultural soil. Bulletin of Environmental Contamination and Toxicology, 104: 333–338. http://dx doi org/10 1007/s00128-020-02793-1
Lu, Z. X., Tu, G. P., Zhang, T., Li, Y. Q., Wang, X., H., Zhang, Q. G., & Jie, C. (2020). Screening of antagonistic Trichoderma strains and their application for controlling stalk rot in maize. Journal of Integrative Agriculture, 19(1), 145–152. https://doi org/10 1016/S2095-3119(19)62734-6
Moosa, A., Sahi, S. T., Haq, I. U., Farzand, A., Khan, S. A., & Javaid, K. (2017). Antagonistic potential of Trichoderma isolates and manures against Fusarium wilt of tomato. International Journal of Vegetable Science, 23(3), 207–218. https://doi org/10 1080/19315260 2016 1232329
Muter, O., Grantina-Ievina, L., Makarenkova, G., Vecstaudza, D., Strikauska, S., Selga, T., & Steiner, C. (2017). Effect of biochar and Trichoderma application on fungal diversity and growth of Zea mays in a sandy loam soil. Environmental and Experimental Biology, 15(4), 289–296. https://doi org/10 22364/eeb 15 30
Medeiros, E. V., Moraes, M. C., Costa, D. P., Silva, J. S., Oliveira, J. B., José, R. S., & Hammecker, C. (2020a). Biochar and Trichoderma aureoviride applied to the sandy soil: effect on soil quality and watermelon growth. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 48(2), 735–751. https://doi org/10 15835/nbha48211851
Medeiros, E. V., Moraes, M. C. H. S., Costa, D. P., Duda, G. P., Oliveira, J. B., Silva, J. A., Lima, J. R. S., & Hammecker, C. (2020b). Effect of biochar and inoculation with Trichoderma aureoviride on melon growth and sandy Entisol quality. Australian Journal of Crop Science. 14(06), 971–977. https://doi org/10 21475/ajcs 20 14 06 p2302
Medeiros, E. V., Lima, N. T., de Sousa Lima, J. R., Pinto, K. M., S., da Costa, D. P., Junior, C. L. F., & Hammecker, C. (2021). Biochar as a strategy to manage plant diseases caused by pathogens inhabiting the soil: a critical review. Phytoparasitica 1, 1–14. https://doi org/10 1007/s12600-021-00887-y
Montiel-Rozas, D. M., M., Hurtado-Navarro, M., Díez-Rojo, M. Á., Pascual, J. A., & Ros, M. (2019). Sustainable alternatives to 1, 3-dichloropropene for controlling root-knot nematodes and fungal pathogens in melon crops in Mediterranean soils: Efficacy and effects on soil quality. Environmental Pollution, 247, 1046–1054.
Nawaz, K., Shahid, A. A., Bengyella, L., Subhani, M. N., Ali, M., Anwar, W., & Ali, S. W. (2018). Diversity of Trichoderma species in chili rhizosphere that promote vigor and antagonism against virulent Phytophthora capsici. Scientia Horticulturae, 239, 242–252. https://doi org/10 1016/j scienta 2018 05 048
Nawrocka, J., & Małolepsza, U. (2013). Diversity in plant systemic resistance induced by Trichoderma. Biological control, 67(2), 149–156. https://doi org/10 1016/j biocontrol 2013 07 005
Nwankiti, A. O., & Gwa, V. I. (2018). Evaluation of antagonistic effect of Trichoderma harzianum against Fusarium oxysporum causal agent of white yam (Dioscorearotundata poir) tuber rot. Trends in Technical & Scientific Research, 1(1), 555554. https://doi org/10 19080/TTSR 2018 01 555554
Pimentel, M. F., Arnão, E., Warner, A. J., Subedi, A., Rocha, L. F., Srour, A., & Fakhoury, A. M. (2020). Trichoderma isolates inhibit Fusarium virguliforme growth, reduce root rot, and induce defense-related genes on soybean seedlings. Plant Disease, 104(7), 1949–1959. https://doi org/10 1094/PDIS-08-19-1676-RE
Sallam, N. M., Eraky, A. M., & Sallam, A. (2019). Effect of Trichoderma spp on Fusarium wilt disease of tomato. Molecular Biology Reports, 46(4), 4463–4470. https://doi org/10 1007/s11033-019-04901-9
Sani, M. N. H., Hasan, M., Uddain, J., & Subramaniam, S. (2020). Impact of application of Trichoderma and biochar on growth, productivity and nutritional quality of tomato under reduced NPK fertilization. Annals of Agricultural Sciences, 65(1), 107–115. https://doi org/10 1016/j aoas 2020 06 003
Saravanakumar, K., Li, Y., Yu, C., Wang, Q. Q., Wang, M., Sun, J., & Chen, J. (2017). Effect of Trichoderma harzianum on maize rhizosphere microbiome and biocontrol of Fusarium Stalk rot. Scientific Reports, 7(1), 1–13. https://doi org/10 1038/s41598-017-01680-w
Silva, J. A. T., de Medeiros, E. V., da Silva, J. M., Tenório, D. D. A., Moreira, K. A., da Silva Nascimento, T. C. E., & Souza-Motta, C. (2017). Antagonistic activity of Trichoderma spp against Scytalidium lignicola CMM 1098 and antioxidant enzymatic activity in cassava. Phytoparasitica, 45(2), 219–225. https://doi org/10 1007/s12600-017-0578-x
Silva, C. C. G. D., Medeiros, E. V. D., Fracetto, G. G. M., Fracetto, F. J. C., Martins Filho, A. P., Lima, J. R. D. S., & Hammecker, C. (2021). Coffee waste as an eco-friendly and low-cost alternative for biochar production impacts on sandy soil chemical attributes and microbial gene abundance. Bragantia. 80. https://doi org/10 1590/1678-4499 20200459
Stocco, M. C., Mónaco, C. I., Abramoff, C., Lampugnani, G., Salerno, G., Kripelz, N., & Consolo, V. F. (2016). Selection and characterization of Argentine isolates of Trichoderma harzianum for effective biocontrol of Septoria leaf blotch of wheat. World Journal of Microbiology & Biotechnology, 32(3), 49. https://doi org/10 1007/s11274-015-1989-9
Sumida, C. H., Daniel, J. F., Araujod, A. P. C., Peitl, D. C., Abreu, L. M., Dekker, R. F., & Canteri, M. G. (2018). Trichoderma asperelloides antagonism to nine Sclerotinia sclerotiorum strains and biological control of white mold disease in soybean plants. Biocontrol Science and Technology, 28(2), 142–156. https://doi org/10 1080/09583157 2018 1430743
Vinodkumar, S., Indumathi, T., & Nakkeeran, S. (2017). Trichoderma asperellum (NVTA2) as a potential antagonist for the management of stem rot in carnation under protected cultivation. Biological control, 113, 58–64. https://doi org/10 1016/j biocontrol 2017 07 001
Wang, K. D., Borrego, E. J., Kenerley, C. M., & Kolomiets, M. V. (2020) Oxylipins other than jasmonic acid are xylem-resident signals regulating systemic resistance induced by Trichoderma virens in maize. The Plant Cell, 32(1), 166–185. https://doi org/10 1105/tpc 19 00487
Zhang, F., Ge, H., Zhang, F., Guo, N., Wang, Y., Chen, L., & Li, C. (2016). Biocontrol potential of Trichoderma harzianum isolate T-aloe against Sclerotinia sclerotiorum in soybean. Plant Physiology and Biochemistry, 100, 64–74. http://dx doi org/10 1016/j plaphy 2015 12 017
Zin, N. A., & Badaluddin, N. A. (2020). Biological functions of Trichoderma spp for agriculture applications. Annals of Agricultural Sciences, 65(2), 168–178. http://dx doi org/10 1016/j aoas
Zúñiga-Mendoza, E., & Ceja-Torres, L. F. (2017). In vitro antagonism of Trichoderma harzianum on Sclerotium cepivorum Berk and S rolfsii Sacc, causal agents of onion rot Phyton. Inter. Journal of Experimental Botany, 86, 7–13. http://dx doi org/10 32604/phyton 2017 86 007
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Erika Valente de Medeiros; Lucas Figueira da Silva ; Jenifer Sthephanie Araújo da Silva; Diogo Paes da Costa ; Carlos Alberto Fragoso de Souza; Lúcia Raquel Ramos Berger ; José Romualdo de Souza Lima ; Claude Hammecker
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
