Identification of indole acetic acid biosynthesis pathways in Trichoderma asperellum and Trichoderma koningiopsis
Keywords:
indole acetic acid, tryptophan, tryptamine, pyruvic Indole, pathway IAA
Abstract
Trichoderm spp. produces secondary metabolites associated with plant growth promotion, especially the production of indole acetic acid (IAA), the main plant hormone. The tryptophan-dependent (TRP-D) and tryptophan-independent (TRP-I) production pathways, depending on the precursor involved in IAA synthesis, are well known. The objective of this study was to investigate the tryptophan-dependent (TRP-D) production pathway under in vitro liquid culture conditions (Potato Dextrose), supplemented with tryptophan (TRP). The presence of auxinic compounds in TRP-D was quantified using high-performance liquid chromatography (HPLC). Additionally, the morphology of corn seeds was analyzed using scanning electron microscopy (SEM). The interaction of Trichoderma spp. with corn seed germination was evaluated under controlled laboratory conditions, conducting the assay in triplicate and performing an analysis of variance (ANOVA). The results showed that the species T. asperellum and T. koningiopsis can degrade TRP and synthesize IAA through the tryptamine (TRM) and indole acetamide (IAM) pathways. However, IAA synthesis was not detected through the indole pyruvic acid (IPyA) and 3-indole acetonitrile (IAN) pathways. In particular, T. asperellum produced significantly higher concentrations of IAA compared to T. koningiopsis. Additionally, it was observed that tryptophan supplementation increased IAA production in both species. Finally, T. koningiopsis showed a strong relationship with the maize root system, invading the root and establishing a beneficial interaction that could contribute to plant growth and development. These findings suggest that T. koningiopsis has significant potential as a biofertilizer in agricultural systems.
Downloads
Download data is not yet available.
References
Abu-Zaitoon, Y., Aladaileh, S., and Tawaha, A. R. A.. (2016). Contribution of the IAM Pathway to IAA Pool in Developing Rice Grains. Brazilian Archives of Biology and Technology, 59, e16150677. https://doi.org/10.1590/1678-4324-2016150677
Bajguz A. & Piotrowska-Niczyporuk A. (2023). Biosynthetic Pathways of Hormones in Plants. Metabolites, 13(8), 884. https://doi.org/10.3390/metabo13080884.
Braithwaite, M., Johnston, P. R., Ball, S. L., Nourozil, F., Hay, A. J., Shoukouhi, P., Chomic, A., Lange, C., Ohkura, M., Nieto-Jacobo, M. F., Cummings, N. J., Bienkowski, D., Mendoza-Mendoza, A., Hill, R. A., McLean, K. L., Stewart, A., Steyaert, J. M. and Bissett, J. (2017). Trichoderma down under: species diversity and occurrence of Trichoderma in New Zealand. Australasian Plant Pathology. 46, 11–30. https://doi.org/10.1007/s13313-016-0457-9
Cai, F., Chen, W., Wei, Z., Pang, G., Li, R., Ran, W.and Shen, Q. (2015). Colonization of Trichoderma harzianum strain SQR-T037 on tomato roots and its relationship to plant growth, nutrient availability and soil microflora. Plant Soil, 388, 337–350. https://doi.org/10.1007/s11104-014-2326-.
Dam, N. M.& Bouwmeester, H. J. (2016). Metabolomics in the Rhizosphere: Tapping into Belowground Chemical Communication. Trends in Plant Science, 21, 256-265. https://doi.org/10.1016/j.tplants.2016.01.008
Feng, Y., Tian, B., Xiong, Lin,G., Cheng L., Zhang T., Lin B.,, Ke Z., and Xin L. (2024). Exploring IAA biosynthesis and plant growth promotion mechanism for tomato root endophytes with incomplete IAA synthesis pathways. Chemical and Biological Technologies in Agriculture, 11, 187. https://doi.org/10.1186/s40538-024-00712-8
Fu, S.F., Wei, J.Y., Chen, H.W., Liu, Y.Y., Lu, H.Y., and Chou, J.Y. 2015. Indole-3-acetic acid: A widespread physiological code in interactions of fungi with other organisms. Plant Signaling & Behavio,10(8), e1048052. doi: 10.1080/15592324.2015.1048052.
Ghasemi, S., Safaie, N., Shahbazi, S., Shams-Bakhsh, M., and Askari, H. 2020. The Role of Cell Wall Degrading Enzymes in Antagonistic Traits of Trichoderma virens Against Rhizoctonia solani. Iraniab Journal of Biotechnology, 18(4), e2333. doi: 10.30498/IJB.2020.2333.
Guzmán-Guzmán, P., Aleman-Duarte, M. I., Delaye, L., Herrera-Estrella, A., and Olmedo-Monfil, V. (2017). Identification of effector-like proteins in Trichoderma spp. and role of a hydrophobin in the plant-fungus interaction and mycoparasitism. BMC Genetics, 18, 16. https://doi.org/10.1186/s12863-017-0481-y.
Etesami, H., & Glick B. 2024. Bacterial indole-3-acetic acid: A key regulator for plant growth, plant-microbe interactions, and agricultural adaptive resilience, Microbiological Research, 281, 127602. https://doi.org/10.1016/j.micres.2024.127602.
Hernández-Mendoza, J. L., Moreno-Medina, V. R., Quiroz-Velásquez, J. D., García-Olivares, J. G., & Mayek-Pérez, N. (2010). Efecto de diferentes concentraciones de ácido antranílico en el crecimiento del maíz. Revista Colombiana de Biotecnología, XII(1),57-63. doi: https://www.redalyc.org/articulo.oa?id=77617786007
Hirayama, T., & Mochida, K. (2022). Plant Hormonomics: A Key Tool for Deep Physiological Phenotyping to Improve Crop Productivity. Plant and Cell Physiology, 63(12), 1826-1839. https://doi.org/10.1093/pcp/pcac067.
Leontovyčová, H., Trdá, L., Dobrev, P.I., Šašek, V., Gay, E., Balesdent, M.H., and Burketová, L. 2020. Auxin biosynthesis in the phytopathogenic fungus Leptosphaeria maculans is associated with enhanced transcription of indole-3-pyruvate decarboxylase LmIPDC2 and tryptophan aminotransferase LmTAM1. Research in Microbiology, 171(5-6), 174-184. https://doi.org/10.1016/j.resmic.2020.05.001.
Lopez-Coria, M., Hernández-Mendoza, J. L., and Sánchez-Nieto, S. (2016). T. asperellum induces maize seedling growth by activating the PM H+ 1 -2 ATPase. Molecular Plant-Microbe Interactions, 29, 797-806. doi.org/10.1069/MPMI-07-16-0138-R.
Lubna, Asaf, S., Hamayun, M., Gul, H., Lee, I. J., and Hussain, A. (2018). Aspergillus niger CSR3 regulates plant endogenous hormones and secondary metabolites by producing gibberellins and indoleacetic acid. Journal of Plant Interactions, 13(1), 100–111. https://doi.org/10.1080/17429145.2018.1436199.
Naveed, M., Amjad, Q. M., Zahir, Z. A., Hussain, M. B., Sessitsch, A., and Mitter, B. L. (2015). Annals of Microbiology, 65:1381-1389. doi: 10.1007/s13213-014-0976-y
Morffy, N. & Strader, L. (2020) Old Town Roads: routes of auxin biosynthesis across kingdoms, Current Opinion in Plant Biology, 55, 21-27, https://doi.org/10.1016/j.pbi.2020.02.002.
Nieto-Jacobo, M. F., Steyaert, J. M., Salazar-Badillo, F. B., Nguyen, D.V., Rostás, M., Braithwaite, M., and Mendoza-Mendoza, A. (2017). Environmental Growth Conditions of Trichoderma spp. Affects Indole Acetic Acid Derivatives, Volatile Organic Compounds, and Plant Growth Promotion Frontiers in Plant Science. 8, 102. https://doi.org/10.3389/fpls.2017.00102.
Peñafiel-Jaramillo, M. F., Torres-Navarrete, E. D., Barrera-Álvarez, A. E., Prieto-Encalada, H. G., Morante, C. J., and Canchignia-Matínez, H. F. (2016). Ciencias agrarias producing indole-3acetic acid using Pesudomonas veronii R4 and in vitro formation of roots in Thompson seedless grapevine leaves. Ciencia y Tecnología, 9, 31-36. https://revistas.uteq.edu.ec/index.php/cyt/article/view/158/172
Pirog, T.P. & Piatetska, D.V. & Klymenko, N.O. and Iutynska, G.O.. (2022). Ways of Auxin Biosynthesis in Microorganisms. Microbiological Journal, 84, 57-72. doi: https://doi.org/10.15407/microbiolj84.02.057.
SAS Institute Inc. (2004). SAS/STAT ® 9.1 User’s Guide. Cary, NC: SAS Institute Inc.
Saleem, A., Qasim, M. W., Ahmad, A., Bibi, A., Haq, I. U., Khan, A. A., and Sajjad, M. (2024). Recent Advances in Photosynthesis, Plant Hormones and Applications in Plant Growth. Haya: The Saudi Journal of Life Sciences, 9(1), 17-22. http://dx.doi.org/10.36348/sjls.2024.v09i01.003
Sztein, A.E., Ilić, N., Cohen, J.D. et al. (2002). Indole-3-acetic acid biosynthesis in isolated axes from germinating bean seeds: The effect of wounding on the biosynthetic pathway. Plant Growth Regulation 36, 201–207. https://doi.org/10.1023/A:1016586401506
Tang, J. Li, Y., Zhang, L., Mu, J., Jiang, Y., Fu, H., Zhang, Y., Cui, H., Yu, X., and Ye, Z. 2023 Biosynthetic Pathways and Functions of Indole-3-Acetic Acid in Microorganisms. Microorganisms, 11(8), 2077. https://doi.org/10.3390/microorganisms11082077
Tariq, A., & Ahmed, A. (2022). Auxins-Interkingdom Signaling Molecules. IntechOpen. doi: 10.5772/intechopen.102599
Uribe-Bueno, M., Hernández-Mendoza, J.L., García, C., Ancona V., Larios-Serrato, V. (2020). Independent Tryptophan pathway in Trichoderma asperellum and T koningiopsis: New insights with bioinformatic and molecular analysis. bioRxiv preprint doi: https://doi.org/10.1101/2020.07.31.230920.
Yao, X., Guo, H., Zhang, K., Zhao, M., Ruan, J., and Chen, J. 2023.Trichoderma and its role in biological control of plant fungal and nematode disease. Frontiers in Microbiology, 3141160551. doi: 10.3389/fmicb.2023.1160551.
Yin, Q., Zhang, J., Wang, S. Jintang Cheng, Han Gao, Cong Guo, Lianbao Ma, Limin Sun, Xiaoyan Han, Shilin Chen, An Liu. (2021). N-glucosyltransferase GbNGT1 from ginkgo complements the auxin metabolic pathway. Hortic Res 8, 229 https://doi.org/10.1038/s41438-021-00658-0
Zuo W.L., Okmen B., Depotter J.R.L., Ebert M.K., Redkar A., Villamil J.M., and Doehlemann G. 2019. Molecular Interactions between smut fungi and their host plants. Annual Review of Phytopathology, 57, 411–430. doi: 10.1146/annurev-phyto-082718-100139.
Bajguz A. & Piotrowska-Niczyporuk A. (2023). Biosynthetic Pathways of Hormones in Plants. Metabolites, 13(8), 884. https://doi.org/10.3390/metabo13080884.
Braithwaite, M., Johnston, P. R., Ball, S. L., Nourozil, F., Hay, A. J., Shoukouhi, P., Chomic, A., Lange, C., Ohkura, M., Nieto-Jacobo, M. F., Cummings, N. J., Bienkowski, D., Mendoza-Mendoza, A., Hill, R. A., McLean, K. L., Stewart, A., Steyaert, J. M. and Bissett, J. (2017). Trichoderma down under: species diversity and occurrence of Trichoderma in New Zealand. Australasian Plant Pathology. 46, 11–30. https://doi.org/10.1007/s13313-016-0457-9
Cai, F., Chen, W., Wei, Z., Pang, G., Li, R., Ran, W.and Shen, Q. (2015). Colonization of Trichoderma harzianum strain SQR-T037 on tomato roots and its relationship to plant growth, nutrient availability and soil microflora. Plant Soil, 388, 337–350. https://doi.org/10.1007/s11104-014-2326-.
Dam, N. M.& Bouwmeester, H. J. (2016). Metabolomics in the Rhizosphere: Tapping into Belowground Chemical Communication. Trends in Plant Science, 21, 256-265. https://doi.org/10.1016/j.tplants.2016.01.008
Feng, Y., Tian, B., Xiong, Lin,G., Cheng L., Zhang T., Lin B.,, Ke Z., and Xin L. (2024). Exploring IAA biosynthesis and plant growth promotion mechanism for tomato root endophytes with incomplete IAA synthesis pathways. Chemical and Biological Technologies in Agriculture, 11, 187. https://doi.org/10.1186/s40538-024-00712-8
Fu, S.F., Wei, J.Y., Chen, H.W., Liu, Y.Y., Lu, H.Y., and Chou, J.Y. 2015. Indole-3-acetic acid: A widespread physiological code in interactions of fungi with other organisms. Plant Signaling & Behavio,10(8), e1048052. doi: 10.1080/15592324.2015.1048052.
Ghasemi, S., Safaie, N., Shahbazi, S., Shams-Bakhsh, M., and Askari, H. 2020. The Role of Cell Wall Degrading Enzymes in Antagonistic Traits of Trichoderma virens Against Rhizoctonia solani. Iraniab Journal of Biotechnology, 18(4), e2333. doi: 10.30498/IJB.2020.2333.
Guzmán-Guzmán, P., Aleman-Duarte, M. I., Delaye, L., Herrera-Estrella, A., and Olmedo-Monfil, V. (2017). Identification of effector-like proteins in Trichoderma spp. and role of a hydrophobin in the plant-fungus interaction and mycoparasitism. BMC Genetics, 18, 16. https://doi.org/10.1186/s12863-017-0481-y.
Etesami, H., & Glick B. 2024. Bacterial indole-3-acetic acid: A key regulator for plant growth, plant-microbe interactions, and agricultural adaptive resilience, Microbiological Research, 281, 127602. https://doi.org/10.1016/j.micres.2024.127602.
Hernández-Mendoza, J. L., Moreno-Medina, V. R., Quiroz-Velásquez, J. D., García-Olivares, J. G., & Mayek-Pérez, N. (2010). Efecto de diferentes concentraciones de ácido antranílico en el crecimiento del maíz. Revista Colombiana de Biotecnología, XII(1),57-63. doi: https://www.redalyc.org/articulo.oa?id=77617786007
Hirayama, T., & Mochida, K. (2022). Plant Hormonomics: A Key Tool for Deep Physiological Phenotyping to Improve Crop Productivity. Plant and Cell Physiology, 63(12), 1826-1839. https://doi.org/10.1093/pcp/pcac067.
Leontovyčová, H., Trdá, L., Dobrev, P.I., Šašek, V., Gay, E., Balesdent, M.H., and Burketová, L. 2020. Auxin biosynthesis in the phytopathogenic fungus Leptosphaeria maculans is associated with enhanced transcription of indole-3-pyruvate decarboxylase LmIPDC2 and tryptophan aminotransferase LmTAM1. Research in Microbiology, 171(5-6), 174-184. https://doi.org/10.1016/j.resmic.2020.05.001.
Lopez-Coria, M., Hernández-Mendoza, J. L., and Sánchez-Nieto, S. (2016). T. asperellum induces maize seedling growth by activating the PM H+ 1 -2 ATPase. Molecular Plant-Microbe Interactions, 29, 797-806. doi.org/10.1069/MPMI-07-16-0138-R.
Lubna, Asaf, S., Hamayun, M., Gul, H., Lee, I. J., and Hussain, A. (2018). Aspergillus niger CSR3 regulates plant endogenous hormones and secondary metabolites by producing gibberellins and indoleacetic acid. Journal of Plant Interactions, 13(1), 100–111. https://doi.org/10.1080/17429145.2018.1436199.
Naveed, M., Amjad, Q. M., Zahir, Z. A., Hussain, M. B., Sessitsch, A., and Mitter, B. L. (2015). Annals of Microbiology, 65:1381-1389. doi: 10.1007/s13213-014-0976-y
Morffy, N. & Strader, L. (2020) Old Town Roads: routes of auxin biosynthesis across kingdoms, Current Opinion in Plant Biology, 55, 21-27, https://doi.org/10.1016/j.pbi.2020.02.002.
Nieto-Jacobo, M. F., Steyaert, J. M., Salazar-Badillo, F. B., Nguyen, D.V., Rostás, M., Braithwaite, M., and Mendoza-Mendoza, A. (2017). Environmental Growth Conditions of Trichoderma spp. Affects Indole Acetic Acid Derivatives, Volatile Organic Compounds, and Plant Growth Promotion Frontiers in Plant Science. 8, 102. https://doi.org/10.3389/fpls.2017.00102.
Peñafiel-Jaramillo, M. F., Torres-Navarrete, E. D., Barrera-Álvarez, A. E., Prieto-Encalada, H. G., Morante, C. J., and Canchignia-Matínez, H. F. (2016). Ciencias agrarias producing indole-3acetic acid using Pesudomonas veronii R4 and in vitro formation of roots in Thompson seedless grapevine leaves. Ciencia y Tecnología, 9, 31-36. https://revistas.uteq.edu.ec/index.php/cyt/article/view/158/172
Pirog, T.P. & Piatetska, D.V. & Klymenko, N.O. and Iutynska, G.O.. (2022). Ways of Auxin Biosynthesis in Microorganisms. Microbiological Journal, 84, 57-72. doi: https://doi.org/10.15407/microbiolj84.02.057.
SAS Institute Inc. (2004). SAS/STAT ® 9.1 User’s Guide. Cary, NC: SAS Institute Inc.
Saleem, A., Qasim, M. W., Ahmad, A., Bibi, A., Haq, I. U., Khan, A. A., and Sajjad, M. (2024). Recent Advances in Photosynthesis, Plant Hormones and Applications in Plant Growth. Haya: The Saudi Journal of Life Sciences, 9(1), 17-22. http://dx.doi.org/10.36348/sjls.2024.v09i01.003
Sztein, A.E., Ilić, N., Cohen, J.D. et al. (2002). Indole-3-acetic acid biosynthesis in isolated axes from germinating bean seeds: The effect of wounding on the biosynthetic pathway. Plant Growth Regulation 36, 201–207. https://doi.org/10.1023/A:1016586401506
Tang, J. Li, Y., Zhang, L., Mu, J., Jiang, Y., Fu, H., Zhang, Y., Cui, H., Yu, X., and Ye, Z. 2023 Biosynthetic Pathways and Functions of Indole-3-Acetic Acid in Microorganisms. Microorganisms, 11(8), 2077. https://doi.org/10.3390/microorganisms11082077
Tariq, A., & Ahmed, A. (2022). Auxins-Interkingdom Signaling Molecules. IntechOpen. doi: 10.5772/intechopen.102599
Uribe-Bueno, M., Hernández-Mendoza, J.L., García, C., Ancona V., Larios-Serrato, V. (2020). Independent Tryptophan pathway in Trichoderma asperellum and T koningiopsis: New insights with bioinformatic and molecular analysis. bioRxiv preprint doi: https://doi.org/10.1101/2020.07.31.230920.
Yao, X., Guo, H., Zhang, K., Zhao, M., Ruan, J., and Chen, J. 2023.Trichoderma and its role in biological control of plant fungal and nematode disease. Frontiers in Microbiology, 3141160551. doi: 10.3389/fmicb.2023.1160551.
Yin, Q., Zhang, J., Wang, S. Jintang Cheng, Han Gao, Cong Guo, Lianbao Ma, Limin Sun, Xiaoyan Han, Shilin Chen, An Liu. (2021). N-glucosyltransferase GbNGT1 from ginkgo complements the auxin metabolic pathway. Hortic Res 8, 229 https://doi.org/10.1038/s41438-021-00658-0
Zuo W.L., Okmen B., Depotter J.R.L., Ebert M.K., Redkar A., Villamil J.M., and Doehlemann G. 2019. Molecular Interactions between smut fungi and their host plants. Annual Review of Phytopathology, 57, 411–430. doi: 10.1146/annurev-phyto-082718-100139.
Published
2025-06-02
How to Cite
Romero, E., Hernández, J., Gonzalez†, J., Hernández, S., Oliva , A., & Quiroz, J. (2025). Identification of indole acetic acid biosynthesis pathways in Trichoderma asperellum and Trichoderma koningiopsis. Revista De La Facultad De Agronomía De La Universidad Del Zulia, 42(2), e244229. Retrieved from https://mail.produccioncientificaluz.org/index.php/agronomia/article/view/43879
Issue
Section
Crop Production
Copyright (c) 2025 Eliezer Romero Juarez, José Luis Hernández Mendoza, Juan Manuel Gonzalez Prieto, Sanjuana Hernández Delgado, Amanda Alejandra Oliva Hernández, Jesús Di Carlo Quiroz Velásquez.
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
