Abstract
The occurrence of diseases in rice, mainly rice blast (Magnaporthe oryzae), is the main cause of yield reduction, and it has been controlled with the abusive use of fungicides in the conventional production system. To produce rice in an agroecological system, some measures, such as biological control, facilitates the transition from one system to another. The biological agent C24G classified as Cladosporium cladosporioides has been isolated from the phylloplane of rice plants and is a potential antagonist to rice pathogens. The aim of this study was to verify the efficiency of C. cladosporioides C24G under field conditions, in an agroecological system. During two growing seasons, C. cladosporioides was tested in a randomized block design in 4 replicates. The treatments consisted of: microbiolized rice seeds with C. cladosporioides, plant sprayed (2 applications), microbiolized rice seeds with C. cladosporioides + plant sprayed (2 ap.), plant sprayed (8 ap.) and microbiolized rice seeds with C. cladosporioides + plant sprayed (8 ap.) and control (no microbiolization and no spray). We evaluated leaf and panicle blast severity, physiological parameters associated with gas exchange, and grain yield. Leaf and panicle blast suppression was up to 85.58% and 79.63% in growing season 2016/2017, respectively, and 83.06% and 74.98% in growing season 2017/2018. At growing season 2016/2017, we observed an increase of the following parameters: photosynthetic rate (A) of 70.99% and 53.52% and transpiration (E) of 22.98% and 59.73% at vegetative and reproductive stage respectively, stomatal conductance (gs) of 126.66% at reproductive stage, water use efficiency (WUE) was up to 55.29% at vegetative stage, biomass 34.56% and yield 51.30%. At the growing season 2017/2018, we observed an increase at the photosynthetic rate (A) of 29.71%, at reproductive stage, biomass, 89.40%, and yield, 34.19%. We conclude that the treatments, microbiolized rice seeds or plant sprayed, allows the insertion of C. cladosporioides into the agroecological system, facilitating the agroecological transition with considerable grain yield, and leading to a final product without residues.
Similar content being viewed by others
References
Alves, G. H., Paraginski, R. T., Lamas, N. S., Hoffmann, J. F., Vanier, N. L., & Oliveira, M. (2017). Effects of organic and conventional cropping systems on technological properties and phenolic compounds of freshly harvested and stored rice. Journal of Food Science. https://doi.org/10.1111/1750-3841.13802.
Andrade, S. A. L., Domingues, A. P., & Mazzafera, P. (2015). Photosynthesis is induced in rice plants that associate with arbuscular mycorrhizal fungi and are grown under arsenate and arsenite stress. Chemosphere. https://doi.org/10.1016/j.chemosphere.2015.04.023.
Barratt, B. I. P., Howarth, F. G., Withers, T. M., Kean, J., & Ridley, G. S. (2018). Progress in risk assessment for classical biological control. Biological Control. https://doi.org/10.1007/s10526-017-9831-y.
Bonanomi, G., Lorito, M., Vinale, F., & Woo, S. L. (2018). Organic amendments, beneficial microbes, and soil microbiota: Toward a unified framework for disease suppression. Annual Review of Phytopathology. https://doi.org/10.1146/annurev-phyto-080615-100046.
Chacón, M. R., Rodríguez-Galán, O., Benítez, T., Sousa, S., Rey, M., Llobell, A., et al. (2007). Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum. International Microbiology. https://doi.org/10.2436/20.1501.01.4.
Chaibub, A. A., Carvalho, J. C. B., Silva, C. S., Collevatti, R. G., Gonçalves, F. J., Côrtes, M. V. C. B., et al. (2016). Defence responses in rice plants in prior and simultaneous applications of Cladosporium sp. during leaf blast suppression. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-016-7379-5.
Chaibub, A. A., Sousa, T. P., Araújo, L. G., & Filippi, M. C. C. (2019a). Molecular and morphological characterization of rice phylloplane fungi and determination of the antagonistic activity against rice pathogens. Microbiological Research. https://doi.org/10.1016/j.micres.2019.126353.
Chaibub, A. A., Sousa, T. P., Araújo, L. G., & Filippi, M. C. C. (2019b). Cladosporium cladosporioides C24G modulates gene expression and enzymatic activity during leaf blast suppression in rice plants. Journal of Plant Growth Regulation. https://doi.org/10.1007/s00344-019-10052-9.
Crusciol, C. A. C., Arf, O., Soratto, R. P., & Mateus, G. P. (2008). Grain quality of upland rice cultivars in response to cropping systems in the Brazilian tropical savanna. Scientia Agricola. https://doi.org/10.1590/S0103-90162008000500004.
Doni, F., Isahak, A., Zain, C. R. C. M., & Yusoff, W. M. W. (2014). Physiological and growth response of rice plants (Oryza sativa L.) to Trichoderma spp. inoculants. AMB Express. https://doi.org/10.1186/s13568-014-0045-8.
FAO. (2009). FAO’s director-general on how to feed the world in 2050. Insights from an Expert Meeting at FAO,1, 1–35.
FAO. (2016). Food and Agriculture Organization of the United Nations. Rome: FAOSTAT Statistics Database for Agriculture.
Gliessman, S. R. (2011). Agroecology and food system change. Journal of Sustainable Agriculture. https://doi.org/10.1080/10440046.2011.562029.
Gonçalves, G. K., Neto, L. X. M., Mendes, F. B., Caleffi, H. V., Pozzebon, N. J., & Aguer, J. L. T. (2017). Characterization of the production system of agroecological rice in the gaúcha campanha. Revista Científica Rural-Urcamp,19(1), 20–37.
Hamayun, M., Khan, S. A., Ahmad, N., Tang, D., Kang, S., Na, C., et al. (2009). Cladosporium sphaerospermum as a new plant growth-promoting endophyte from the roots of Glycine max (L.) Merr. World Journal of Microbiology and Biotechnology. https://doi.org/10.1007/s11274-009-9982-9.
Hamayun, M., Khan, S. A., Khan, A. L., Rehman, G., Kim, Y. H., Iqbal, I., et al. (2010). Gibberellin production and plant growth promotion from pure cultures of Cladosporium sp. MH-6 isolated from cucumber (Cucumis sativus L.). Mycologia. https://doi.org/10.3852/09-261.
Hayashi, K., Suzuki, F., & Hayano-Saito, Y. (2017). Multiplex PCR assay for simultaneous detection of MBI-D and QoI resistance in rice blast fungus. Journal of General Plant Pathology. https://doi.org/10.1007/s10327-017-0725-8.
Huang, L., Yang, J., Cui, X., Yang, H., Wang, S., & Zhuang, H. (2016). Synergy and transition of recovery efficiency of nitrogen fertilizer in various rice genotypes under organic farming. Sustainability. https://doi.org/10.3390/su8090854.
International Rice Research Institute (IRRI). (2013). Standard Evaluation System (SES) for Rice 5th ed., Manila.
Köhl, J., Scheer, C., Holb, I. J., Masny, S., & Molhock, W. (2015). Toward an integrated use of biological control by Cladosporium cladosporioides H39 in apple scab (Venturia inaequalis) management. Plant Disease. https://doi.org/10.1094/PDIS-08-14-0836-RE.
Larkin, R. P., & Griffin, T. S. (2007). Control of soilborne potato diseases using Brassica green manures. Crop Protection. https://doi.org/10.1016/j.cropro.2006.10.004.
Lucas, J. A., Solano, B. R., Montes, F., Ojeda, J., Megias, M., & Gutierrez Mañero, F. J. (2009). Use of two PGPR strains in the integrated management of blast disease in rice (Oryza sativa) in Southern Spain. Field Crops Research. https://doi.org/10.1016/j.fcr.2009.09.013.
McKemy, J. M., Gudauskas, R. T., & Morgan-Jones, G. (1993). Leaf blight of Lespedeza spp. caused by Cladosporium vignae. Plant Disease. https://doi.org/10.1094/PD-77-1263C.
Molina, G. M. (2012). Agroecology and politics. How to get sustainability? About the necessity for a political agroecology. Agroecology and Sustainable Food Systems. https://doi.org/10.1080/10440046.2012.705810.
Nalley, L., Tsiboe, F., Durand-Morat, A., Shew, A., & Thoma, G. (2016). Economic and environmental impact of rice blast pathogen (Magnaporthe oryzae) alleviation in the United States. PLoS One. https://doi.org/10.1371/journal.pone.0167295.
Nam, M. H., Park, M. S., Kim, H. S., Kim, T. I., & Kim, H. G. (2015). Cladosporium cladosporioides and C. tenuissimum cause blossom blight in strawberry in Korea. Mycobiology. https://doi.org/10.5941/MYCO.2015.43.3.354.
Nascente, A. S., Filippi, M. C. C., Lanna, A. C., Sousa, T. P., Souza, A. C. A., Lobo, V. L. S., et al. (2017a). Effects of beneficial microorganisms on lowland rice development. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-017-0212-y.
Nascente, A. S., Filippi, M. C. C., Lanna, A. C., Souza, A. C. A., Lobo, V. L. S., & Silva, G. B. (2017b). Biomass, gas exchange, and nutrient contents in upland rice plants affected by application forms of microorganism growth promoters. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-016-8013-2.
Nasini, G., Arnone, A., Assante, G., Bava, A., Moricca, S., & Ragazzi, A. (2004). Secondary mould metabolites of Cladosporium tenuissimum, a hyperparasite of rust fungi. Phytochemistry. https://doi.org/10.1016/j.phytochem.2004.03.013.
Naveed, M., Mitter, B., Reichenauer, T. G., Wieczorek, K., & Sessitsch, A. (2014). Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environmental and Experimental Botany, 97, 30–39.
Paul, D., & Park, K. S. (2013). Identification of volatiles produced by Cladosporium cladosporioides CL-1, a fungal biocontrol agent that promotes plant growth. Sensors. https://doi.org/10.3390/s131013969.
Pieniak, S., Aertsens, J., & Verbeke, W. (2010). Subjective and objective knowledge as determinants of organic vegetables consumption. Food Quality and Preference. https://doi.org/10.1016/j.foodqual.2010.03.004.
Poupin, M. J., Timmermann, T., Vega, A., Zunigan, A., & Gonzalez, B. (2013). Effects of the plant growth-promoting bacterium Burkholderia phytofirmans PsJN throughout the life cycle of Arabidopsis thaliana. PLoS One. https://doi.org/10.1371/journal.pone.0069435.
Prabhu, A. S., Filippi, M. C. C., & Zimmermann, F. J. P. (2003). Cultivar response to fungicide application in relation to rice blast control, productivity and sustainability. Pesquisa Agropecuária Brasileira. https://doi.org/10.1590/S0100-204X2003000100002.
Rais, A., Shakeel, M., Malik, K., Hafeez, F. Y., Yasmin, H., Mumtaz, S., & Hassan, M. N. (2018). Antagonistic Bacillus spp. reduce blast incidence on rice and increase grain yield under field conditions. Microbiological Research, 208, 54–62.
Research and Markets. (2016). Global pesticides market segmented by type, application area and geography. Trends and forecasts (2015–2020). Sustainability, regulation and competition. http://www.researchandmarkets.com/research/4hd338/global_pesticides. Accessed 23 June 2018.
Schrama, M., de Haan, J. J., Kroonen, M., Verstegen, H., & Van der Putten, W. H. (2018). Crop yield gap and stability in organic and conventional farming systems. Agriculture, Ecosystems & Environment. https://doi.org/10.1016/j.agee.2017.12.023.
Shaner, G., & Finney, R. F. (1977). The effects of nitrogen fertilization on the expression slow-mildewing in Knox wheat. Phytopathology. https://doi.org/10.1094/Phyto-67-1051.
Singh, S., & Kapoor, K. K. (1998). Effects of inoculation of phosphate-solubilizing microorganisms and an arbuscular mycorrhizal fungus on mungbean grown under natural soil conditions. Mycorrhiza. https://doi.org/10.1007/s005720050188.
Sousa, T. P., Souza, A. C. A., Filippi, M. C. C., Lanna, A. C., Cortês, M. V., Pinheiro, H. A., et al. (2018). Bioagents and silicon promoting fast early upland rice growth. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-017-0753-0.
Steindorff, A. S., Ramada, M. H., Coelho, A. S., Miller, R. N., Pappas Júnior, G. J., Ulhoa, C. J., et al. (2014). Identification of mycoparasitism-related genes against the phytopathogen Sclerotinia sclerotiorum through transcriptome and expression profile analysis in Trichoderma harzianum. BMC Genomics. https://doi.org/10.1186/1471-2164-15-204.
Torres, D. E., Rojas-Martínez, R. I., Zavaleta-Mejía, E., Guevara-Fefer, P., Márquez-Guzmán, G. J., & Pérez-Martínez, C. (2017). Cladosporium cladosporioides and Cladosporium pseudocladosporioides as potential new fungal antagonists of Puccinia horiana Henn., the causal agent of chrysanthemum white rust. PLoS One. https://doi.org/10.1371/journal.pone.0170782.
van Lenteren, J. C., Bolckmans, K., Köhl, J., Ravensberg, W. J., & Urbaneja, A. (2018). Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl, 63(1), 39–59.
Wang, B., Ebbole, D. J., & Wang, Z. (2017). The arms race between Magnaporthe oryzae and rice: Diversity and interaction of Avr and R genes. Journal of Integrative Agriculture. https://doi.org/10.1016/S2095-3119(17)61746-5.
Woo, S. L., Ruocco, M., Vinale, F., Nigro, M., Marra, R., Lombardi, N., et al. (2014). Trichoderma-based products and their widespread use in agriculture. The Open Mycology Journal. https://doi.org/10.2174/1874437001408010071.
Xu, T., Li, Y., Zeng, X., Yang, X., Yang, Y., Yuan, S., et al. (2017). Isolation and evaluation of endophytic Streptomyces endus OsiSh-2 with potential application for biocontrol of rice blast disease. Journal of the Science of Food and Agriculture. https://doi.org/10.1002/jsfa.7841.
Zanon, J. S., Menezes, L. J. M., Wizniewsky, C. R. F., & Beling, H. M. (2015). The organic rice production in settlement novo horizonte II, located in the municipality of Santa Margarida do Sul/RS. Ciência e Natura. https://doi.org/10.5902/2179460X17491.
Zhan, G., Tian, Y., Wang, F., Chen, X., Guo, J., Jiao, M., et al. (2014). A novel fungal hyperparasite of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. PLoS One. https://doi.org/10.1371/journal.pone.0111484.
Acknowledgements
We thank EMBRAPA Rice and Beans and University of Brasília for supported this work and Coordination of Superior Level Staff Improvement-CAPES and the Brazilian National Council for Scientific and Technological Development-CNPq for financial support to the first author.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
No content conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chaibub, A.A., de Sousa, T.P., de Oliveira, M.I.S. et al. Efficacy of Cladosporium cladosporioides C24G as a Multifunctional Agent in Upland Rice in Agroecological Systems. Int. J. Plant Prod. 14, 463–474 (2020). https://doi.org/10.1007/s42106-020-00097-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42106-020-00097-2