Optimizing wheat seed treatment with entomopathogenic fungi for improving plant growth at early development stages

  • Adrián González-Guzmán University of Córdoba, ETSIAM, Dept. Agronomy. Building C4 (Celestino Mutis), Ctra. Madrid, Km 396, Campus Rabanales. 14071 Córdoba
  • Antonio R. Sánchez-Rodríguez University of Córdoba, ETSIAM, Dept. Agronomy. Building C4 (Celestino Mutis), Ctra. Madrid, Km 396, Campus Rabanales. 14071 Córdoba
  • Enrique Quesada-Moraga University of Córdoba, ETSIAM, Dept. Agronomy. Building C4 (Celestino Mutis), Ctra. Madrid, Km 396, Campus Rabanales. 14071 Córdoba
  • Maria C. del Campillo University of Córdoba, ETSIAM, Dept. Agronomy. Building C4 (Celestino Mutis), Ctra. Madrid, Km 396, Campus Rabanales. 14071 Córdoba
  • Meelad Yousef-Yousef University of Córdoba, ETSIAM, Dept. Agronomy. Building C4 (Celestino Mutis), Ctra. Madrid, Km 396, Campus Rabanales. 14071 Córdoba
Keywords: Beauveria bassiana, Metarhizium brunneum, seed inoculation, soil drenching, SPAD, cotyledon

Abstract

Aim of study: Entomopathogenic fungi (EPF) are biocontrol agents, plant growth promoters, and increase tolerance to biotic-abiotic stresses. In this study we investigated the factors associated to the application method, which are crucial for the interaction between the fungus and the host plant at initial crop growth stages.

Area of study: The study was performed in Cordoba (Spain)

Material and methods: Three experiments were performed to investigate: (i) the effect of different concentrations of the surfactant Tween® 80 (0, 0.5, 1, 5, and 10%) on wheat seed coating with conidia of Metarhizium brunneum and seed and conidia viability; (ii) the performance of wheat seedlings at first growth stages after their inoculation with Beauveria bassiana or M. brunneum via seed coating or soil drenching; and (iii) the role of soil sterilization and seed disinfection on leaf concentration of chlorophyll (SPAD) and B. bassiana or M. brunneum colonization.

Main results: Tween® 80 concentration linearly improved seed coating (up to 127%) without altering wheat seeds and fungal conidia germination. Seedling length of inoculated plants was significantly increased with B. bassiana and M. brunneum (67% and 46%, respectively) via seed coating. Seed disinfection was key to achieve an enhancement in wheat SPAD (10-18%) with B. bassiana or M. brunneum concerning Control, that combined with sterilization of soil showed the highest endophyte colonization rates (up to 83.3% with both fungi)

Research highlights: The surfactant concentration, application method, seed disinfection, and soil sterilization are key parameters to improve the potential benefits on the EPF-plant relationship.

Downloads

Download data is not yet available.

References

Adholeya A, Tiwari P, Singh R, 2005. Large scale inoculum production of arbuscular mycorrhizal fungi on root organs and inoculation strategies. In: Soil biology in vitro culture of mycorrhizae; Declerck S et al. (Ed.). Springer-Verlag, Heidelberg, Berlin, pp: 315-338. https://doi.org/10.1007/3-540-27331-X_17

Akello J, Dubois T, Coyne D, Kyamanywa S, 2009. The effects of Beauveria bassiana dose and exposure duration on colonization and growth of tissue cultured banana (Musa sp.) plants. Biol Control 49: 6-10. https://doi.org/10.1016/j.biocontrol.2008.06.002

Balzergue C, Chabaud M, Barker DG, Bécard G, Rochange SF, 2013. High phosphate reduces host ability to develop arbuscular mycorrhizal symbiosis without affecting root calcium spiking responses to the fungus. Front Plant Sci 4: 1-15. https://doi.org/10.3389/fpls.2013.00426

Bamisile BS, Dash CK, Akutse KS, Keppanan R, Afolabi OG, Hussain M, et al., 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. Microbiol Res 217: 34-50. https://doi.org/10.1016/j.micres.2018.08.016

Barelli L, Moreira CC, Bidochka MJ, 2018. Initial stages of endophytic colonization by Metarhizium involves rhizoplane colonization. Microbiology 164: 1531-1540. https://doi.org/10.1099/mic.0.000729

Behie SW, Bidochka MJ, 2013. Potential agricultural benefits through biotechnological manipulation of plant fungal associations. BioEssays 35: 328-331. https://doi.org/10.1002/bies.201200147

Behie SW, Bidochka MJ, 2014. Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: An additional branch of the soil nitrogen cycle. Appl Environ Microbiol 80: 1553-1560. https://doi.org/10.1128/AEM.03338-13

Behie SW, Zelisko PM, Bidochka MJ, 2012. Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336: 1576-1578. https://doi.org/10.1126/science.1222289

Berg G, 2009. Plant-microbe interactions promoting plant growth and health: Perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84: 11-18. https://doi.org/10.1007/s00253-009-2092-7

Blanke V, Renker C, Wagner M, Füllner K, Held M, Kuhn AJ, et al., 2005. Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytol 166: 981-992. https://doi.org/10.1111/j.1469-8137.2005.01374.x

Bruck, DJ, 2010. Fungal entomopathogens in the rhizosphere. BioControl 55: 103-112. https://doi.org/10.1007/s10526-009-9236-7

Burges HD, 1998. Formulation of microbial biopesticides. Beneficial microorganisms, nematodes and seed treatment. Springer Sci, Dordrecht, 412 pp. https://doi.org/10.1007/978-94-011-4926-6

Chang G, Zhang Q, Zhang L, Yajuan L, 2015. Degradation of lignin in ionic liquid with HCl as catalyst. Environ Prog Sust Energ 35: 809-814. https://doi.org/10.1002/ep.12276

Dara SK, 2019. Non-entomopathogenic roles of entomopathogenic fungi in promoting plant health and growth. Insects 10: 277. https://doi.org/10.3390/insects10090277

Dara SK, Dara SSR, Dara, SS, 2017. Impact of entomopathogenic fungi on the growth, development, and health of cabbage growing under water stress. Am J Plant Sci 8: 1224-1233. https://doi.org/10.4236/ajps.2017.86081

de Bruin W, Merwe CVD, Kritzinger Q, Bornman R, Korsten L, 2017. Ultrastructural and developmental evidence of phytotoxicity on cos lettuce (Lactuca sativa) associated with nonylphenol exposure. Chemosphere 169: 428-436. https://doi.org/10.1016/j.chemosphere.2016.11.020

Deaker R, Roughley RJ, Kennedy IR, 2004. Legume seed inoculation technology - A review. Soil Biol Biochem 36: 1275-1288. https://doi.org/10.1016/j.soilbio.2004.04.009

Doige CA, Yu X, Sharom FJ, 1993. The effects of lipids and detergents on ATPase-active. Biochim Biophys Acta 1146: 65-72. https://doi.org/10.1016/0005-2736(93)90339-2

FAO, 2015. The economic lives of smallholder farmers. Food and Agriculture Organization of the United Nations, Rome.

Gálvez A, López-Galindo A, Peña A, 2018. Effect of different surfactants on germination and root elongation of two horticultural crops: implications for seed coating. New Zeal J Crop Hortic Sci 47: 83-98. https://doi.org/10.1080/01140671.2018.1538051

Garrido-Jurado I, Ruano F, Campos M, Quesada-Moraga E, 2011. Effects of soil treatments with entomopathogenic fungi on soil dwelling non-target arthropods at a commercial olive orchard. Biol Control 59: 239-244. https://doi.org/10.1016/j.biocontrol.2011.07.001

Garrido-Jurado I, Resquín-Romero G, Amarilla SP, Ríos-Moreno A, Carrasco L, Quesada-Moraga E, 2016. Transient endophytic colonization of melon plants by entomopathogenic fungi after foliar application for the control of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae). J Pest Sci 90: 319-330. https://doi.org/10.1007/s10340-016-0767-2

Gee GW, Bauder JW, 1986. Particle-size analysis. In: Methods of soil analysis, Part 1. Physical and mineralogical methods, Klute, A. (Ed.). Agron Monogr 9. Am Soc Agron & Soil Sci Soc Am, Madison, WI, USA. pp: 383-412.

González-Guzmán A, Sacristán D, Quesada-Moraga E, Torrent J, del Campillo MC, Sánchez-Rodríguez AR, 2020a. Effects of entomopathogenic fungi on growth and nutrition in wheat grown on two calcareous soils: influence of the fungus application method. Ann Appl Biol 177: 26-40. https://doi.org/10.1111/aab.12596

González-Guzmán A, Sacristán D, Sánchez-Rodríguez AR, Barrón V, Torrent J, del Campillo MC, 2020b. Soil nutrients effects on the performance of durum wheat inoculated with entomopathogenic fungi. Agronomy 10: 20. https://doi.org/10.3390/agronomy10040589

Greenfield M, Gómez-Jiménez MI, Ortiz V, Vega FE, Kramer M, Parsa S, 2016. Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biol Control 95: 40-48. https://doi.org/10.1016/j.biocontrol.2016.01.002

Hallmann J, Mahaffee WF, Kloepper JW, 1997. Bacterial endophytes in agricultural crops. Can J Microbiol 43: 895-914. https://doi.org/10.1139/m97-131

Hermosa R, Belén Rubio M, Cardoza RE, Nicolás C, Monte E, Gutiérrez S, 2013. The contribution of Trichoderma to balancing the costs of plant growth and defense. Int Microbiol 16: 69-80.

Hu G, St Leger RJ, 2002. Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. Appl Environ Microbiol 68: 6383-6387. https://doi.org/10.1128/AEM.68.12.6383-6387.2002

Jaber LR, Enkerli J, 2016. Effect of seed treatment duration on growth and colonization of Vicia faba by endophytic Beauveria bassiana and Metarhizium brunneum. Biol Control 103: 187-195. https://doi.org/10.1016/j.biocontrol.2016.09.008

Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE, 2009. Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41: 1233-1244. https://doi.org/10.1016/j.soilbio.2009.03.005

Kessler P, Matzke H, Keller S, 2003. The effect of application time and soil factors on the occurrence of Beauveria brongniartii applied as a biological control agent in soil. J Invertebr Pathol 84: 15-23. https://doi.org/10.1016/j.jip.2003.08.003

Khan AL, Hamayun M, Khan SA, Kang SM, Shinwari ZK, Kamran M, et al., 2012. Pure culture of Metarhizium anisopliae LHL07 reprograms soybean to higher growth and mitigates salt stress. World J Microbiol Biotechnol 28: 1483-1494. https://doi.org/10.1007/s11274-011-0950-9

Kobae Y, Ohmori Y, Saito C, Yano K, Ohtomo R, Fujiwara T, 2016. Phosphate treatment strongly inhibits new arbuscule development but not the maintenance of arbuscule in mycorrhizal rice roots. Plant Physiol 171: 566-579. https://doi.org/10.1104/pp.16.00127

Krell V, Unger S, Jakobs-Schoenwandt D, Patel A V, 2018a. Endophytic Metarhizium brunneum mitigates nutrient deficits in potato and improves plant productivity and vitality. Fungal Ecol 34: 43-49. https://doi.org/10.1016/j.funeco.2018.04.002

Krell V, Unger S, Jakobs-Schoenwandt D, Patel A V, 2018b. Importance of phosphorus supply through endophytic Metarhizium brunneum for root : shoot allocation and root architecture in potato plants. Plant Soil 430: 87-97. https://doi.org/10.1007/s11104-018-3718-2

Lugtenberg BJJ, Caradus JR, Johnson LJ, 2016. Fungal endophytes for sustainable crop production. FEMS Microbiol Ecol 92: fiw194. https://doi.org/10.1093/femsec/fiw194

Maniania NK, Sithanantham S, Ekesi S, Ampong-Nyarko K, Baumgärtner J, Löhr B, Matoka CM, 2003. A field trial of the entomogenous fungus Metarhizium anisopliae for control of onion thrips, Thrips tabaci. Crop Prot 22: 553-559. https://doi.org/10.1016/S0261-2194(02)00221-1

Morgan, JAW, Bending GD, White PJ, 2005. Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot 56: 1729-1739. https://doi.org/10.1093/jxb/eri205

Murphy J, Riley JP, 1962. A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27: 31-36. https://doi.org/10.1016/S0003-2670(00)88444-5

Olsen SR, Cole CV, Watanabe FS, Dean LA, 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circ No 939: 18.

Panpatte DG, Jhala YK, Vyas RV, Shelat HN (eds), 2017. Microorganisms for green revolution, Vol I: Microbes for sustainable crop production. Springer. ISBN: 978-981-13-4836-5 https://doi.org/10.1007/978-981-10-6241-4

Parsa S, Ortiz V, Vega FE, 2013. Establishing fungal entomopathogens as endophytes: towards endophytic biological control. J Vis Exp 74: 50360 https://doi.org/10.3791/50360

Partida-Martínez LP, Heil M, 2011. The microbe-free plant: fact or artifact. Front Plant Sci 2: 16. https://doi.org/10.3389/fpls.2011.00100

Pieterse MJ, Dieuwertje V der D, Zamioudis C, Leon-Reyes A, Wees SCM Van, 2012. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28: 489-521. https://doi.org/10.1146/annurev-cellbio-092910-154055

Quesada-Moraga E, Muñoz-Ledesma FJ, Santiago-Alvarez C, 2009. Systemic protection of Papaver somniferum L. against Iraella luteipes (Hymenoptera: Cynipidae) by an endophytic strain of Beauveria bassiana (Ascomycota: Hypocreales). Environ Entomol 38: 723-730. https://doi.org/10.1603/022.038.0324

Quesada-Moraga E, Rodríguez-Sánchez AR, Garrido-Jurado I, 2019. Hongos patógenos de insectos como endófitos. In: Micopatología de Artrópodos: Hongos entomopatógenos para ser usados como bioinsumos en el control microbiano de plagas, López-Lastra C & Lecuona RE (Ed.), pp: 151-166. INTA, CABA, Argentina.

Quesada-Moraga E, Yousef-Naef M, Garrido-Jurado I, 2020. Advances in the use of entomopathogenic fungi as biopesticides in suppressing crop insect pests. In: Biopesticides for sustainable agriculture. Birch N & Glare T (Eds.). Burleigh Dodds Science. https://doi.org/10.19103/AS.2020.0073.05

Raya-Díaz S, Quesada-Moraga E, Barrón V, del Campillo MC, Sánchez-Rodríguez AR, 2017a. Redefining the dose of the entomopathogenic fungus Metarhizium brunneum (Ascomycota, Hypocreales) to increase Fe bioavailability and promote plant growth in calcareous and sandy soils. Plant Soil 418: 387-404. https://doi.org/10.1007/s11104-017-3303-0

Raya-Díaz S, Sánchez-Rodríguez AR, Segura-Fernández JM, del Campillo MC, Quesada-Moraga E, 2017b. Entomopathogenic fungi-based mechanisms for improved Fe nutrition in sorghum plants grown on calcareous substrates. PLoS One 12: 1-28. https://doi.org/10.1371/journal.pone.0185903

Resquín-Romero G, Garrido-Jurado I, Delso C, Ríos-Moreno A, Quesada-Moraga E, 2016. Transient endophytic colonizations of plants improve the outcome of foliar applications of mycoinsecticides against chewing insects. J Invertebr Pathol 136: 23-31. https://doi.org/10.1016/j.jip.2016.03.003

Rinallo C, Bennici A, Cenni E, 1988. Effects of two surfactants on Triticum durum desf. plantlets. Environ Exp Bot 28: 367-374. https://doi.org/10.1016/0098-8472(88)90061-5

Rivas-Franco F, Hampton JG, Morán-Diez ME, Rostás M, Wessman P, Jackson TA et al., 2019. Effect of coating maize seed with entomopathogenic fungi on plant growth and resistance against Fusarium graminearum and Costelytra giveni . Biocontrol SciTechnol 29: 877-900. https://doi.org/10.1080/09583157.2019.1611736

Rocha I, Ma Y, Souza-Alonso P, Vosátka M, Freitas H, Oliveira RS, 2019. Seed coating: A tool for delivering beneficial microbes to agricultural crops. Front Plant Sci 10: 1357. https://doi.org/10.3389/fpls.2019.01357

Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, et al., 2008. Stress tolerance in plants via habitat-adapted symbiosis. Int Soc Microb Ecol 2: 404-416. https://doi.org/10.1038/ismej.2007.106

Sánchez-Rodríguez AR, del Campillo MC, Quesada-Moraga E, 2015. Beauveria bassiana: An entomopathogenic fungus alleviates Fe chlorosis symptoms in plants grown on calcareous substrates. Sci Hortic (Amsterdam) 197: 193-202. https://doi.org/10.1016/j.scienta.2015.09.029

Sánchez-Rodríguez AR, Barrón V, del Campillo, MC, 2016. The entomopathogenic fungus Metarhizium brunneum: A tool to alleviate Fe chlorosis. Plant Soil 406: 295-310. https://doi.org/10.1007/s11104-016-2887-0

Sánchez-Rodríguez AR, Raya-Díaz S, Zamarreños AM, García-Mina JM, del Campillo MC, Quesada-Moraga E, 2018. An endophytic Beauveria bassiana strain increases spike production in bread and durum wheat plants and effectively controls cotton leafworm (Spodoptera littoralis) larvae. Biol Control 116: 90-102. https://doi.org/10.1016/j.biocontrol.2017.01.012

Serrasolses I, Romanyà J, Khanna PK, 2008. Effects of heating and autoclaving on sorption and desorption of phosphorus in some forest soils. Biol Fertil Soils 44: 1063-1072. https://doi.org/10.1007/s00374-008-0301-7

St Leger RJ, 2008. Studies on adaptations of Metarhizium anisopliae to life in the soil. Invertebr Pathol 98: 271-276. https://doi.org/10.1016/j.jip.2008.01.007

Tefera T, Vidal S, 2009. Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. BioControl 54: 663-669. https://doi.org/10.1007/s10526-009-9216-y

Vänninen I, Tyni-Juslin J, Hokkanen H, 2000. Persistence of augmented Metarhizium anisopliae and Beauveria bassiana in Finnish agricultural soils. BioControl 45: 201-222. https://doi.org/10.1023/A:1009998919531

Vega FE, 2018. The use of fungal entomopathogens as endophytes in biological control: A review. Mycologia 110: 4-30. https://doi.org/10.1080/00275514.2017.1418578

Vosátka M, Látr A, Gianinazzi S, Albrechtová J, 2012. Development of arbuscular mycorrhizal biotechnology and industry: Current achievements and bottlenecks. Symbiosis 58: 29-37. https://doi.org/10.1007/s13199-012-0208-9

Williams-Linera G, Ewel JJ, 1984. Effect of autoclave sterilization of a tropical andept on seed germination and seedling growth. Plant Soil 82: 263-268. https://doi.org/10.1007/BF02220253

Yousef M, Lozano-Tovar MD, Garrido-Jurado I, Quesada-Moraga E, 2013. Biocontrol of Bactrocera oleae (Diptera: Tephritidae) with Metarhizium brunneum and its extracts. Biol Microb Control 106: 1118-1125. https://doi.org/10.1603/EC12489

Zamioudis C, Pieterse CMJ, 2012. Modulation of host immunity by beneficial microbes. Int Soc Mol Plant-Microbe Interact 25: 139-150. https://doi.org/10.1094/MPMI-06-11-0179

Published
2021-11-30
How to Cite
González-GuzmánA., Sánchez-RodríguezA. R., Quesada-MoragaE., del CampilloM. C., & Yousef-YousefM. (2021). Optimizing wheat seed treatment with entomopathogenic fungi for improving plant growth at early development stages. Spanish Journal of Agricultural Research, 19(4), e1004. https://doi.org/10.5424/sjar/2021194-17120
Section
Plant protection