Identificação das vias de biossíntese de ácido indolacético em Trichoderma asperellum e Trichoderma koningiopsis

• Eliezer Romero Centro de Biotecnología Genómica - Instituto Politécnico Nacional, Blvd. del Maestro esq. Elías Piña, Col. Narciso Mendoza, Reynosa, Tamaulipas, México C.P. 88710. https://orcid.org/0000-0003-0115-6384
• José Hernández Centro de Biotecnología Genómica - Instituto Politécnico Nacional, Blvd. del Maestro esq. Elías Piña, Col. Narciso Mendoza, Reynosa, Tamaulipas, México C.P. 88710. https://orcid.org/0000-0003-0115-6384
• Juan Gonzalez†
• Sanjuana Hernández Centro de Biotecnología Genómica - Instituto Politécnico Nacional, Blvd. del Maestro esq. Elías Piña, Col. Narciso Mendoza, Reynosa, Tamaulipas, México C.P. 88710. https://orcid.org/0000-0003-4597-7889
• Amanda Oliva Centro de Biotecnología Genómica - Instituto Politécnico Nacional, Blvd. del Maestro esq. Elías Piña, Col. Narciso Mendoza, Reynosa, Tamaulipas, México C.P. 88710. https://orcid.org/0000-0002-8904-2164
• Jesús Quiroz Centro de Biotecnología Genómica - Instituto Politécnico Nacional, Blvd. del Maestro esq. Elías Piña, Col. Narciso Mendoza, Reynosa, Tamaulipas, México C.P. 88710. https://orcid.org/0000-0002-6021-0427

Palavras-chave: ácido indol acético, triptofano, triptamina, indol pirúvico, via IAA

Resumo

O microorganismo Trichoderma spp. produz metabólitos secundários associados à promoção do crescimento vegetal, especialmente a produção de ácido indolacético (AIA), o principal hormônio vegetal. As vias de produção dependentes de triptofano (TRP-D) e independentes de triptofano (TRP-I), dependendo do precursor envolvido na síntese de AIA, são bem conhecidas. O objetivo deste estudo foi investigar a via de produção dependente de triptofano (TRP-D) em condições de cultura líquida in vitro (Batata Dextrose), suplementada com triptofano (TRP). A presença de compostos auxínicos em TRP-D foi quantificada usando cromatografia líquida de alta eficiência (HPLC). Além disso, a morfologia das sementes de milho foi analisada usando microscopia eletrônica de varredura (SEM). A interação de Trichoderma spp. com a germinação das sementes de milho foi avaliada em condições controladas de laboratório, conduzindo o ensaio em triplicado e realizando uma análise de variância (ANOVA). Os resultados mostraram que as espécies T. asperellum e T. koningiopsis podem degradar TRP e sintetizar AIA através das vias de triptamina (TRM) e indol acetamida (IAM). No entanto, a síntese de AIA não foi detectada através das vias de ácido indol pirúvico (IPyA) e 3-indol acetonitrilo (IAN). Em particular, T. asperellum produziu concentrações significativamente mais altas de AIA em comparação com T. koningiopsis. Além disso, observou-se que a suplementação com triptofano aumentou a produção de AIA em ambas as espécies. Finalmente, T. koningiopsis mostrou uma forte relação com o sistema radicular do milho, invadindo a raiz e estabelecendo uma interação benéfica que poderia contribuir para o crescimento e desenvolvimento da planta. Esses achados sugerem que T. koningiopsis tem um potencial significativo como biofertilizante em sistemas agrícolas.

Referências

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, 3141160551. 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.