Hostname: page-component-76fb5796d-9pm4c Total loading time: 0 Render date: 2024-04-26T18:23:11.936Z Has data issue: false hasContentIssue false
  • English
  • Français

The use of secondary metabolites extracted from Trichoderma for plant growth promotion in the Andean highlands

Published online by Cambridge University Press:  31 August 2016

Noel Ortuño ,
José Antonio Castillo ,
Claudia Miranda ,
Mayra Claros  and
Ximena Soto
Noel Ortuño
Affiliation:
Fundación PROINPA, Av. Meneces Km 4, El Paso, Cochabamba, Bolivia.
José Antonio Castillo*
Affiliation:
Fundación PROINPA, Av. Meneces Km 4, El Paso, Cochabamba, Bolivia.
Claudia Miranda
Affiliation:
Fundación PROINPA, Av. Meneces Km 4, El Paso, Cochabamba, Bolivia.
Mayra Claros
Affiliation:
Fundación PROINPA, Av. Meneces Km 4, El Paso, Cochabamba, Bolivia.
Ximena Soto
Affiliation:
Fundación PROINPA, Av. Meneces Km 4, El Paso, Cochabamba, Bolivia.
*
*Corresponding author: j.castillo@proinpa.org
Get access Rights & Permissions [Opens in a new window]

Abstract

Agriculture in the Altiplano and Andean Mountains is experiencing threats to sustainability mainly due to intensive cultivation of quinoa driven by international markets. This recent export-oriented production system is causing the degradation of soils and reducing productivity, therefore, agro-technological innovations are necessary to sustain cropping systems while maintaining organic quality (mostly quinoa). In this work, we searched for native Trichoderma species associated with plants from the Andean highlands to obtain an environmentally friendly and organic alternative to chemical fertilizers. We obtained different Trichoderma isolates from quinoa, potato and maize roots and soil, which were identified as Trichoderma harzianum, as well as other species. Twelve of the isolates were cultured in pairs to stimulate the production and secretion of compounds of diverse chemical nature that we called collectively ‘secondary metabolites’ (SMs). Crude extracts of SMs were used to inoculate selected crops to determine their plant growth promoting potential compared with two commercially available controls, chemical fertilizer and a bio-fertilizer. Results showed that SMs significantly promoted lettuce and radish growth and increased quinoa grain yield. Indole acetic acid was detected in all SM extracts that promoted plant growth, suggesting that this plant regulator might be responsible for the plant growth promoting activity. In conclusion, the Trichoderma-derived SMs approach appears to be a promising, simple and accessible technology for small-scale farmers in order to insure the sustainability, affordability and accessibility of food production in the Andes.

Keywords

TrichodermaAndes Mountainsplant growth promotionsecondary metabolitesorganic fertilizer
Type
Research Papers
Information
Renewable Agriculture and Food Systems , Volume 32 , Issue 4 , August 2017 , pp. 366 - 375
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Current address: École Supérieure d´Agriculture d´Angers, 55 Rue Rabelais, 49007 Angers, France.

References

Aguilera, J., Motavalli, P.P., Gonzales, M.A., and Valdivia, C. 2012. Initial and residual effects of organic and inorganic amendments on soil properties in a potato-based cropping system in the Bolivian Andean Highlands. American Journal of Experimental Agriculture 2:641–666.Google Scholar
Ahamed, A. and Vermette, P. 2008. Enhanced enzyme production from mixed cultures of Trichoderma reesei RUT-C30 and Aspergillus niger LMA grown as fed batch in a stirred tank bioreactor. Biochemical Engineering Journal 42:41–46.CrossRefGoogle Scholar
Bari, M.A., Begum, M.F., Sarker, K.K., Rahman, M.A., Kabir, A.H., and Alam, M.F. 2007. Mode of action of Trichoderma spp. on organic solid waste for bioconversion. Plant Environment Development 1:61–66.Google Scholar
Berg, G. and Smalla, K. 2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology 68:1–13.CrossRefGoogle ScholarPubMed
Berti, M., Wilckens, R., Hevia, F., Serri, H., Vidal, I., and Mendez, C. 2000. Fertilización nitrogenada en quinoa (Chenopodium quinoa Willd.). Ciencia Investigación Agraria 27:81–90.CrossRefGoogle Scholar
Blajos, J., Ojeda, N., Gandarillas, E., and Gandarillas, A. 2014. Economy of quinoa: Perspectives and challenges. Revista de Agricultura (Bolivia) 54:3–10.Google Scholar
Contreras-Cornejo, H.A., Macías-Rodríguez, L., Cortés-Penagos, C., and López-Bucio, J. 2009. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis . Plant Physiology 149:1579–1592.CrossRefGoogle ScholarPubMed
Druzhinina, I.S., Kopchinskiy, A.G., Komoń, M., Bissett, J., Szakacs, G., and Kubicek, C.P. 2005. An oligonucleotide barcode for species identification in Trichoderma and Hypocrea . Fungal Genetics and Biology 42:813–828.CrossRefGoogle ScholarPubMed
Fonte, S.J., Vanek, S.J., Oyarzun, P., Parsa, S., Quintero, D.C., Rao, I.M., and Lavelle, P. 2012. Pathways to agroecological intensification of soil fertility management by smallholder farmers in the Andean highlands. In Sparks, D.L. (ed.). Advances in Agronomy, vol. 116. Academic Press, Burlington. p. 125–184.Google Scholar
Furche, C., Salcedo, S., Krivonosb, E., Rabczukc, P., Jara, B., Fernández, D., and Correa, F. 2015. International quinoa trade. Chapter: 4.1. In Bazile, D., Bertero, D., and Nieto, C. (eds). Estado del arte de la quinua en el mundo. FAO & CIRAD. State of the Art Report of Quinoa in the World in 2013. FAO & CIRAD, Rome. p. 316–329.Google Scholar
Gandarillas, A., Rojas, W., Bonifacio, A., and Ojeda, N. 2015. La quinua en Bolivia: Perspectiva de la Fundación PROINPA. Chapter 5.1.a. In Bazile, D., Bertero, D., and Nieto, C. (eds). Estado del arte de la quinua en el mundo. FAO & CIRAD. State of the Art Report of Quinoa in the World in 2013. FAO & CIRAD, Rome. p. 410–431.Google Scholar
Garcia, M., Raes, D., Jacobsen, S.E., and Michel, T. 2007. Agroclimatic constraints for rainfed agriculture in the Bolivian Altiplano. Journal of Arid Environments 71:109–121.CrossRefGoogle Scholar
García, M., Miranda, R., and Fajardo, H. 2014. Manual de manejo de la fertilidad de suelo bajo riego deficitario para el cultivo de la quinua en el altiplano boliviano. Available at Web site http://www.cazalac.org/mwar_lac/fileadmin/documents/CaribbeanDroughtAtlas/quinua.pdf (verified 5 January 2016).Google Scholar
Ghildiyal, A. and Pandey, A. 2008. Isolation of cold tolerant antifungal strains of Trichoderma sp. from glacial sites of Indian Himalayan region. Research Journal of Microbiology 3:559–564.Google Scholar
Gordon, S.A. and Weber, R.P. 1951. Colorimetric estimation of indole acetic acid. Plant Physiology 26:192–195.CrossRefGoogle Scholar
Gravel, V., Antoun, H., and Tweddell, R.J. 2007. Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: Possible role of indole acetic acid (IAA). Soil Biology and Biochemistry 39:1968–1977.CrossRefGoogle Scholar
Hall, T.A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95–98.Google Scholar
Hammer, Ø., Harper, D.A.T., and Ryan, P.D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4:9.Google Scholar
Harman, G.E. 2006. Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190–194.CrossRefGoogle ScholarPubMed
Hermosa, R., Viterbo, A., Chet, I., and Monte, E. 2012. Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25.CrossRefGoogle ScholarPubMed
Hermosa, R., Rubio, M.B., Cardoza, R.E., Nicolás, C., Monte, E., and Gutiérrez, S. 2013. The contribution of Trichoderma to balancing the costs of plant growth and defense. International Microbiology 16:69–80.Google ScholarPubMed
Howell, C.R. 2003. Mechanisms employed by Trichoderma species in the biological control of plant diseases: The history and evolution of current concepts. Plant Disease 87:4–10.CrossRefGoogle ScholarPubMed
Hoyos-Carvajal, L. and Bissett, J. 2011. Biodiversity of Trichoderma in neotropics. In Grillo, O. (ed.). The Dynamical Processes of Biodiversity—Case Studies of Evolution and Spatial Distribution. InTech, Croatia. p. 303–320.Google Scholar
Hoyos-Carvajal, L., Orduz, S., and Bissett, J. 2009. Genetic and metabolic biodiversity of Trichoderma from Colombia and adjacent neotropic regions. Fungal Genetics and Biology 46:615–631.CrossRefGoogle ScholarPubMed
Kubicek, C.P., Bissett, J., Druzhinina, I., Kullnig-Gradinger, C., and Szakacs, G. 2003. Genetic and metabolic diversity of Trichoderma: A case study on South-East Asian isolates. Fungal Genetics and Biology 38:310–319.CrossRefGoogle ScholarPubMed
Kullnig, C., Szakacs, G., and Kubicek, C.P. 2000. Molecular identification of Trichoderma species from Russia, Siberia and the Himalaya. Mycological Research 104:1117–1125.CrossRefGoogle Scholar
Kullnig-Gradinger, C.M., Szakacs, G., and Kubicek, C.P. 2002. Phylogeny and evolution of the fungal genus Trichoderma—a multigene approach. Mycological Research 106:757–767.CrossRefGoogle Scholar
López-Bucio, J., Pelagio-Flores, R., and Herrera-Estrella, A. 2015. Trichoderma as biostimulant: Exploiting the multilevel properties of a plant beneficial fungus. Scientia Horticulturae 196:109–123.CrossRefGoogle Scholar
Martínez-Medina, A., Alguacil, M.M., Pascual, J.A., and Van Wees, S.C.M. 2014. Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. Journal of Chemical Ecology 40:804–815.CrossRefGoogle ScholarPubMed
Melo, S.C.O., Pungartnik, C., Cascardo, J.C.M., and Brendel, M. 2006. Rapid and efficient protocol for DNA extraction and molecular identification of the basidiomycete Crinipellis perniciosa . Genetics and Molecular Research 5:851–855.Google ScholarPubMed
Mendes, R., Garbeva, P., and Raaijmakers, J.M. 2013. The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiology Reviews 37:634–663.CrossRefGoogle ScholarPubMed
Mukherjee, P.K., Horwitz, B.A., and Kenerley, C.M. 2012. Secondary metabolism in Trichoderma—a genomic perspective. Microbiology 158:35–45.CrossRefGoogle ScholarPubMed
Mulligan, M., Rubiano, J., Hyman, G., White, D., Garcia, J., Saravia, M., Leon, J.G., Selvaraj, J.J., Gutierrez, T., and Saenz-Cruz, L.L. 2010. The Andes basins: Biophysical and developmental diversity in a climate of change. Water International 35:472–492.CrossRefGoogle Scholar
Nagy, V., Seidl, V., Szakacs, G., Komon-Zelazowska, M., Kubicek, C.P., and Druzhinina, I.S. 2007. Application of DNA bar codes for screening of industrially important fungi: The haplotype of Trichoderma harzianum sensu stricto indicates superior chitinase formation. Applied and Environmental Microbiology 73:7048–7058.CrossRefGoogle ScholarPubMed
Ortuño, N., Castillo, J.A., Claros, M., Navia, O., Angulo, M., Barja, D., Gutiérrez, C., and Angulo, V. 2013. Enhancing the sustainability of quinoa production and soil resilience by using bioproducts made with native microorganisms. Agronomy 3:732–746.CrossRefGoogle Scholar
Pugliese, M., Liu, B.P., Gullino, M.L., and Garibaldi, A. 2008. Selection of antagonists from compost to control soil-borne pathogens. Journal of Plant Diseases and Protection 115:220–228.CrossRefGoogle Scholar
Reaves, J.L. and Crawford, R.H. 1994. In vitro Colony Interactions among Species of Trichoderma with Inference Toward Biological Control . Research Paper PNW-RP-474. U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station, Portland, OR, 8 p.CrossRefGoogle Scholar
Saba, H., Vibhash, D., Manisha, M., Prashant, K.S., Farhan, H., and Tauseef, A. 2012. Trichoderma—a promising plant growth stimulator and biocontrol agent. Mycosphere 3:524–531.CrossRefGoogle Scholar
Salas-Marina, M.A., Silva-Flores, M.A., Uresti-Rivera, E.E., Castro-Longoria, E., Herrera-Estrella, A., and Casas-Flores, S. 2011. Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. European Journal of Plant Pathology 131:15–26.CrossRefGoogle Scholar
Schulte-auf'm Erley, G., Kaul, H.P., Kruse, M., and Aufhammer, W. 2005. Yield and nitrogen utilization efficiency of the pseudocereals amaranth, quinoa and buckwheat under differing nitrogen fertilization. European Journal of Agronomy 22:95–100.CrossRefGoogle Scholar
Seiboth, B., Ivanova, C., and Seidl-seiboth, V. 2011. Trichoderma reesei: A fungal enzyme producer for cellulosic biofuels. In Dos Santos, M.A. (ed.). Biofuel Production-Recent Developments and Prospects. InTech, Croatia. p. 309–341.Google Scholar
Sivasithamparam, K. and Ghisalberti, E.L. 1998. Secondary metabolism in Trichoderma and Gliocladium . In Kubicek, C.P. and Harman, G.E. (eds). Trichoderma and Gliocladium. Taylor and Francis Ltd., London, UK. p. 139–191.Google Scholar
Sofo, A., Scopa, A., Manfra, M., De Nisco, M., Tenore, G., Troisi, G., Di Fiori, R., and Novellino, E. 2011. Trichoderma harzianum strain T-22 induces changes in phytohormone levels in cherry rootstocks (Prunus cerasus × P. canescens). Plant Growth Regulation 65:421–425.CrossRefGoogle Scholar
Vinale, F., Manganiello, G., Nigro, M., Mazzei, P., Piccolo, A., Pascale, A., Ruocco, M., Marra, R., Lombardi, N., Lanzuise, S., Varlese, R., Cavallo, P., Lorito, M., and Woo, S.L. 2014. A novel fungal metabolite with beneficial properties for agricultural applications. Molecules 19:9760–9772.CrossRefGoogle ScholarPubMed
Windham, M.T., Elad, Y., and Baker, R. 1986. A mechanism of increased plant growth induced by Trichoderma spp. Phytopathology 76:518–521.CrossRefGoogle Scholar
Zhang, F., Yuan, J., Yang, X., Cui, Y., Chen, L., Ran, W., and Shen, Q. 2013. Putative Trichoderma harzianum mutant promotes cucumber growth by enhanced production of indole acetic acid and plant colonization. Plant Soil 368:433–444.CrossRefGoogle Scholar
Supplementary material: File

Ortuño supplementary material

Tables S1-S2

Download Ortuño supplementary material(File)
File 21.3 KB