Inoculation with endophytic entomopathogenic fungi generates a physiological response and promotes plant growth in poblano pepper plants
DOI:
https://doi.org/10.21640/ns.v12i25.2586Keywords:
endophyte fungi, entomopathogen fungi, seed inoculation, plant growth promotion, net assimilation rate, strains, physiological processes, San Luis Potosi, poblano chili, seeds, efficiency, stomatal conductance, plantsAbstract
Introduction: Some entomopathogenic fungi act as endophytes and promote plant growth. Such benefits can be explained by improvements in physiological processes. In this research, the effect of commercial strains of entomopathogenic endophytic fungi and isolates from agricultural soils of San Luis Potosi on growth, photosynthesis, gas exchange and production in poblano chili plants was evaluated, considering the effect of the inoculation method used.
Methodology: Poblano chili plants (Capsicum annuum L.) was used as a model which was sown under controlled conditions and in a greenhouse. Seven HEE strains were evaluated: three native isolates from agricultural soils of San Luis Potosi that by their characteristics belong to the genus Metarhizium (RV01 strain), Paecilomyces (RV05 strain) and Penicillium (SL14 strain); two strains isolated from insects, Beauveria bassiana [(Bals.-Criv.) Vuill. 1992] (BB42 strain) and Metarhizium anisopliae [(Metschn.) Sorokin 1883) (MA25 strain) and two commercial strains of B. bassiana (BB09 strain) and M. anisopliae (MA25 strain). A conidial solution was prepared, and two methods were tested: 1) seed inoculation; and 2) substrate spraying and a second application when the first true leaf emerged. Controls were included in each treatment (water and the surfactant were inoculated). Photosynthetic parameters (maximum and effective efficiency of PSII, photochemical and non-photochemical dissipation, electron transfer rate), gas exchange parameters (netassimilation rate, stomatal conductance, and transpiration) and colonization percentage of steam, leaf and root were evaluated during the experiment. At the end of the experiment total dried biomass, dry weight of the aerial part of the plant and the root, and root length was measured.
Results: At 33 days after inoculation it was observed how inoculation with RV01, MA25, BB09 and SL14 increased CO2 assimilation and stomatal conductance, with respect to controls, when inoculated by seed or by spraying. Inoculation directly over the seed significantly improved CO2 assimilation, photochemical quenching, and effective efficiency of PSII comparing to plants inoculated by foliar spraying. The isolate RV05 stood out due to the results observed in the greenhouse, with a higher total biomass production. The plants inoculated by seed showed an increase in the production of total biomass, and in the dry weight of the aerial part and roots with respect to the plants inoculated by aspersion. Greater growth in plants was associated with endophytic colonization.
Conclusion: HEE isolated from agricultural soils of San Luis Potosi can compete with commercial strains in promoting growth in poblano chili plants in greenhouse. Direct seed inoculation of endophytic entomopathogenic fungi generated better results, although with variations depending on the strain.
Downloads
References
Akello, J. & Sikora, R. (2012). Systemic acropedal influence of endophyte seed treatment on Acyrthosiphon pisum and Aphis fabae offspring development and reproductive fitness. Biological Control, 61(3), 215–221. DOI: https://doi.org/10.1016/j.biocontrol.2012.02.007
Akutse, K.S., Maniania, N.K., Fiaboe, K.K.M., Van den Berg, J. & Ekesi, S. (2013). Endophytic colonization of Vicia faba and Phaseolus vulgaris (Fabaceae) by fungal pathogens and their effects on the life-history parameters of Liriomyza huidobrensis (Diptera: Agromyzidae). Fungal Ecology, 1–9.
Bamisile, B.S., Dash C.K., Akutse, K.S., Keppanan, R., Afolabi, O.G., Hussain, M., Qasim, M. & Wang, L. (2018). Prospects of endophytic fungal entomopathogens as biocontrol and plant growth promoting agents: An insight on how artificial inoculation methods affect endophytic colonization of host plants. Microbiological Research, 217, 34–50.
Behie, S.W., Moreira, C.C., Sementchoukova, I., Barelli, L., Zelisko, P.M. & Bidochka, M.J. (2017). Carbon translocation from a plant to an insect-pathogenic endophytic fungus. Nature communications, 8(1), 1-5. DOI: 10.1038/ncomms14245
Buchanan, B.B., Gruissem, W. & Jones, R.L. (2015). Biochemistry & Molecular Biology of Plants. Second ed. NJ, USA: John Wiley & Sons, Hoboken.
Castillo-López, D., Zhu-Salzman, K., Ek-Ramos, M.J. & Sword, G.A. (2014). The entomopathogenic fungal endophytes Purpureocillium lilacinum (formerly Paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions. Planta, 9(8), e103891.
Centritto, M., Lauteri, M., Monteverdi, M.C. & Serraj, R. (2009). Leaf gas exchange, carbon isotope discrimination, and grain yield in contrasting rice genotypes subjected to water deficits during the reproductive stage. Journal of Experimental Botany, 60, 2325–2339
Cho, S. M., Kang, B.R., Han, S. H., Anderson, A. J., Park, J. Y., Lee, Y. H., Baik Ho Cho, K.Y. Yang, Ryu C.M., & Young C.K. & Kim, Y.C. (2008). 2R, 3R-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Molecular Plant-Microbe Interactions, 21(8), 1067-1075.
Dogan, A., Erler, F., Erkan, M., Ates, A.O., Sabanci, H.S. & Polat, E. (2016). Microbial-based production system: A novel approach for plant growth and pest and disease management in greenhouse-grown peppers (Capsicum annuum L.). Journal of Agricultural Science and Technology, 18(2), 371–386.
Dubey, A., Malla, M.A., Khan, F., Chowdhary, K., Yadav, S., Kumar, A., Sharm, S. Khare, P.K., & Khan, M.L. (2019). Soil microbiome: a key player for conservation of soil health under changing climate under changing climate. Biodiversity and Conservation, 28(8-9), 2405-2429.
FAOSTAT (2017) www.faostat.fao.org (Revisado el 19 de abril del 2019).
Garcia, J.E., Posadas, J.B., Perticari, A. & Lecuona, R.E. (2011). Metarhizium anisopliae (Metschnikoff) Sorokin promotes growth and has endophytic activity in tomato plants. Adv. Biol. Res, 5, 22–27.
García-Cristobal, J., García-Villaraco, A., Ramos, B., Gutiérrez-Mañero, J. & Lucas, J. A. (2015). Priming of pathogenesis related-proteins and enzymes related to oxidative stress by plant growth promoting rhizobacteria on rice plants upon abiotic and biotic stress challenge. Journal of plant physiology, 188, 72-79. DOI: 10.1016/j.jplph.2015.09.011
Geisen, S., Kostenko, O., Cnossen, M.C., ten Hooven, F.C., Vreš, B., & van der Putten, W.H. (2017). Seed and Root Endophytic Fungi in a Range Expanding and a Related Plant Species. Frontiers in microbiology, 8, 1–11.
Ghaffari, M.R., Mirzaei, M., Ghabooli, M., Khatabi, B., Wu, Y., Zabet-Moghaddam, M., Mohammadi-Nejad, G., Haynes, P.A., Hajirezaei, M.R., Sepehri, M. & Hosseini-Salekdeh, G. (2018). Root endophytic fungus Piriformospora indica improves drought stress adaptation in barley by metabolic and proteomic reprogramming. Environmental and Experimental Botany, 157, 197-210.
Gómez-Vidal, S., López-Llorca, L.V., Jansson, H.B. & Salinas, J. (2006). Endophytic colonization of date palm (Phoenix dactylifera L.) leaves by entomopathogenic fungi. Micron, 37(7), 624-632.
Greenfield, M., Gómez-Jiménez, M.I., Ortiz, V., Vega, F.E., Kramer M. & Parsa S. (2016). Beauveria bassiana and Metarhizium anisopliae endophytically colonize Cassava roots following soil drench inoculation. Biological Control, 95, 40–48. DOI: https://doi.org/10.1016/j.biocontrol.2016.01.002
Gurulingappa, P., Sword, G. A., Murdoch, G. & Mcgee, P.A. (2010). Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biological Control, 55(1), 34–41.
Hiruma, K., Gerlach, N., Bucher, M., Sacristan, S., Nakano, R.T., Hacquard, B.K., Kracher, B. Neumann, U., Ramírez, D., Bucher, M., O´Connell, R.J., & Schulze-Lefert, P. (2016). Root Endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell, 165, 464–474.
Hyde, K.D. & Soytong, K. (2008). The fungal endophyte dilemma. Fungal Diversity, 33, 163–173.
Jaber, L.R. & Enkerli, J. (2016). Fungal entomopathogens as endophytes: ¿can they promote plant growth? Biocontrol Science and Technology, 9, 544.
Jaber, L.R. & Ownley, B.H. (2018). ¿Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biological Control, 116, 36–45.
Joukhadar, I. & Walker, S. (2020). Effect of Stand Reduction at Different Growth Stages on Yield of Paprika-Type Chile Pepper. Horticulturae, 6, 16.
Kalaji, H.M., Schansker, G., Ladle, R.J., Goltsev, V., Bosa, K., Allakhverdiev, S.I., Brestic, M., Bussotti, F., Calatayud, A., Dąbrowski, P., Elsheery, N.I., Ferroni, L., Guidi, L., Hogewoning, S.W., Jajoo, A., Misra, A.N., Nebauer, S.G., Pancaldi, S., Penella, C., Poli, D., Pollastrini, M., Romanowska, D., Zdzislawa, B., Rutkowska, B., Serôdio J, Suresh K., Szulc W, Tambussi, E., Yanniccari, M. & Zivcak, M. (2014). Frequently asked questions about in vivo chlorophyll fluorescence: Practical issues. Photosynthesis Research, 122(2), 121–158.
Khan, A.L, Shinwari, Z.K., Kim, Y.H., Waqas, M., Hamayun, M., Kamran, M. & Lee, I.J. (2012). Role of endophyte Chaetomium globosum lk4 in growth of Capsicum annuum by production of gibberellins and indole acetic acid. Pakistan Journal of Botany, 44(5), 1601–1607.
Khan, A.R., Ullah, I., Waqas, M., Shahzad, R., Hong, S.J., Park, G.S., Park, G. S., Jung B. K., Lee I.J. & Shin, J.H. (2015). Plant growth-promoting potential of endophytic fungi isolated from Solanum nigrum leaves. World Journal of Microbiology and Biotechnology, 31(9), 1461–1466.
Kramer, D.M. & Evans, J.R. (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiology, 155,70–78.
Krell, V., Unger, S., Jakobs-Schoenwandt, D. & Patel, A.V. (2018). Endophytic Metarhizium brunneum mitigates nutrient deficits in potato and improves plant productivity and vitality. Fungal Ecology, 34, 43–49.
Lesk, C., Rowhani, P. & Ramankutty, N. (2016). Influence of extreme weather disasters on global crop production. Nature, 529(7584), 84–87. DOI: https://doi.org/10.1038/nature16467
Li, W., Zhang, S. & Shan, L. (2007). Responsibility of non-stomatal limitations for the reduction of photosynthesis-response of photosynthesis and antioxidant enzyme characteristics in alfalfa (Medicago sativa L.) seedlings to water stress and rehydration. Frontiers of Agriculture in China, 1(3), 255–264.
Liberman, L.M. & Benfey, P. N. (2016). A Friend in Need (of Nutrients) Is a ⋯. Cell, 165(2), 269–271. DOI: https://doi.org/10.1016/j.cell.2016.03.036
Mantzoukas, S., Chondrogiannis,C. & Grammatikopoulos, G. (2015). Effects of three endophytic entomopathogens on sweet sorghum and on the larvae of the stalk borer Sesamia nonagrioides. Entomologia Experimentalis et Applicata, 154(1), 78–87.
Mckinnon, A.C., Saari, S., Nicolai, M.E.M., Raad, M. & Glare, T.R. (2016). Beauveria bassiana as an endophyte: a critical review on associated methodology and biocontrol potential. BioControl, 62(1), 1–17.
Orellana, C. & León, E. (2011). Evaluación de la Producción del Cultivo Hidropónico de 3 Variedades de Pimiento (Capsicum annuum L.) Bajo Invernadero en la Solución Nutritiva La Molina. Cuenca, Ecuador. 119 p.
Ortiz-Espinoza, E., Villegas-Rodríguez, F., Delgado-Sánchez, P., Hernández-Arteaga, L.E. Del S., Marín, J.S., Ramírez-Tobías, H.M. & Villarreal-Guerrero, F. (2019). Inoculation with entomopathogenic fungi reduces seed contamination, improves seed germination and growth of chilli seedlings. African Journal of Agricultural Research, 14(32), 1463-1471.
Ownley, B.H., Griffin, M.R., Klingeman, W.E., Gwinn, K.D., Moulton, J.K. & Pereira, R.M. (2008). Beauveria bassiana : Endophytic colonization and plant disease control. Journal of Invertebrate Pathology, 98(3), 267-270. DOI: 10.1016/j.jip.2008.01.010
Parsa, S., Ortiz, V. & Vega, F.E. (2013). Establishing Fungal Entomopathogens as Endophytes: Towards Endophytic Biological Control Establishing Fungal Entomopathogens as Endophytes: Towards Endophytic. Journal of Visualized Experiment, (76), e50360.
Paul, N.C., Deng, J.X., Lee, J.H. & Yu, S.H. (2013). New records of endophytic Paecilomyces inflatus and Bionectria ochroleuca from Chili Pepper Plants in Korea. Mycobiology, 41(1), 18-24.
Quesada-Moraga, E., Muñoz-Ledesma, F.J. & Santiago-Álvarez, C. (2009). Systemic Protection of Papaver somniferum L. against Iraella luteipes (Hymenoptera: Cynipidae) by an Endophytic Strain of Beauveria bassiana (Ascomycota: Hypocreales). Environmental Entomology, 38(3), 723–730.
Raya-Díaz, S., Sánchez-Rodríguez, A.R., Segura-Fernández, J.M., del Campillo, M.d.C. & Quesada-Moraga, E. (2017). Entomopathogenic fungi-based mechanisms for improved Fe nutrition in sorghum plants grown on calcareous substrates. PLoS One, 12 e0185903.
Rios-Velasco, C., Pérez-Corral, D. A., Salas-Marina, M. Á., Berlanga-Reyes, D.I., Ornelas-Paz, J. J., Acosta Muñiz, C. H., Cambero-Campos J. & Jacobo-Cuellar, J.L. (2014). Pathogenicity of the Hypocreales fungi Beauveria bassiana and Metarhizium anisopliae against insect pests of tomato. Southwestern Entomologist, 39(4), 739-750.
Rothen, C., Miranda, V., Aranda-Rickert, A., Fracchia, S. & Rodríguez, M.A. (2017). Characterization of dark septate endophyte fungi associated with cultivated soybean at two growth stages. Applied Soil Ecology, 120, 62–69.
Rozpądek, P., Wężowicz, K., Nosek, M., Ważny, R., Tokarz, K., Lembicz, M., Miszalski, Z. & Turnau, K. (2015). The fungal endophyte Epichloë typhina improves photosynthesis efficiency of its host orchard grass (Dactylis glomerata). Planta, 242(4), 1025–1035. DOI: https://doi.org/10.1007/s00425-015-2337-x
Samaniego-Gámez, B.Y., Garruña, R., Tun-Suárez, J.M., Kantun-Can, J., Reyes-Ramírez, A., y Cervantes-Díaz, L. (2016). Bacillus spp. inoculation improves photosystem II efficiency and enhances photosynthesis in pepper plants. Chilean Journal of Agricultural Research, 76(4), 409–416.
Sasan, R.K. & Bidochka, M.J., (2012). The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. Am. J. Bot. 99, 101–107.
Sauder, D. C. & DeMars, C.E. (2019). An updated recommendation for multiple comparisons. Advances in Methods and Practices in Psychological Science, 2(1), 26-44.
Sepúlveda, M., Vargas, M., Gerding, M., Ceballos, R. & Oyarzúa, P. (2016). Molecular, morphological and pathogenic characterization of six strains of Metarhizium spp.(Deuteromycotina: Hyphomycetes) for the control of Aegorhinus superciliosus (Coleoptera: Curculionidae). Chilean Journal of Agricultural Research, 76(1), 77-83. DOI: http://dx.doi.org/10.4067/S0718-58392016000100011
Soliman, S.S.M., Trobacher, C.P., Tsao, R., Greenwood, J.S. & Raizada, M.N. (2013). A fungal endophyte induces transcription of genes encoding a redundant fungicide pathway in its host plant. BMC Plant Biology, 13(1), 93.
Tall, S. & Meyling, N.V. (2018). Probiotics for plants? growth promotion by the entomopathogenic fungus Beauveria bassiana depends on nutrient availability. Microbial Ecology, 76(4), 1002–1008. DOI: 10.1007/s00248-018-1180-6
Vidal, S. & Jaber, L.R. (2015). Entomopathogenic fungi as endophytes: Plant-endophyte-herbivore interactions and prospects for use in biological control. Current Science, 109(1), 46–54.
Villegas-Rodríguez, F., Marín-Sánchez, J. & Torres-Castillo J.A. (2014). Management of Bactericera cockerelli (Sulc) (Hemiptera: Triozidae) in Greenhouses with Entomopathogenic Fungi (Hypocreales). Southwestern Entomologist, 39(3), 613.
Villegas-Rodríguez, F., Casas-Flores, J. S., Tamayo-Mejía, F., Aguilar-Medel, S., Díaz-Gómez, O. & Monreal-Vargas, C.T. (2017). Activity of two entomopathogenic fungi, molecularly identified, on Bactericera cockerelli. Revista Colombiana de Entomología, 43(1), 27–33.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2020 Nova Scientia
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Conditions for the freedom of publication: the journal, due to its scientific nature, must not have political or institutional undertones to groups that are foreign to the original objective of the same, or its mission, so that there is no censorship derived from the rigorous ruling process.
Due to this, the contents of the articles will be the responsibility of the authors, and once published, the considerations made to the same will be sent to the authors so that they resolve any possible controversies regarding their work.
The complete or partial reproduction of the work is authorized as long as the source is cited.
