Characterization and biocontrol potential of some rhizobacteria against fungal pathogens causing foliar diseases in maize

Rhizobacteria control of fungal pathogens of maize

Authors

  • Akinlolu Olalekan Akanmu Food Security and Safety Focus Area, Faculty of Natural and Agricultural Sciences, North-West University, Private Mail Bag X2046, Mmabatho 2735, South Africa https://orcid.org/0000-0003-2816-9820
  • Olubukola Oluranti Babalola Food Security and Safety Focus Area, Faculty of Natural and Agricultural Sciences, North-West University, South Africa. ✉Corresponding author, E-mail: olubukola.babalola@nwu.ac.za https://orcid.org/0000-0003-4344-1909

DOI:

https://doi.org/10.24193/subbbiol.2024.1.10

Keywords:

Antifungicidal potential, biocontrol, biofungicide, fungi, inhibition, microbial formulations, rhizosphere, zero hunger

Abstract

Maize is one of the most consumed cereal crops worldwide, and it is a strategic crop to the attainment of SDG 2 of Zero hunger. Despite its importance, the cultivation of maize has been significantly impaired by fungal pathogens causing foliar diseases. The occurrence of this disease in maize plantations at the University farm, Molelewane, Mafikeng, prompted this investigation.

Samples of diseased maize rhizosphere soil were aseptically collected. Bacteria species associated with the rhizosphere were isolated and characterized as; Bacillus siamensis, Enterobacter asburiae, Enterobacter chengduensis, Priestia aryabhattai, Burkholderia sp., Priestia megaterium strain AOA6 and Priestia megaterium strain AOA7. The anti-fungicidal potentials of the bacterial species were evaluated against pathogenic fungal species, Nigrospora sphaerica, Alternaria alternata and Fusarium equiseti in-vitro. The percentage mycelia growths were calculated, and the data were subjected to ANOVA using SAS version 9.8.

All the seven bacteria isolates tested positive to ammonia, phosphate siderophore and ACC deaminase tests. The percentage mycelia inhibition showed Nigrospora sphaerica (36.29%), A. alternata (26.19%) and F. equiseti (20.63%) as the order of fungal inhibition by the bacteria species. Furthermore, E. asburiae > P. megatarium strain AOA7 > B. siamensis > P. aryabhattai > E. chengduensis > Bulkholderia sp. were the order of antifungal efficacy of the bacteria species evaluated. In conclusion, the efficacy of the bacteria especially E. asburiae, P. megatarium strain AOA7 and B. siamensis over various fungal pathogens.

The result obtained, therefore, justifies the further investigation, formulation and deployment of the bacteria species as biofungicide in the management of foliar diseases of maize.

References

Agunbiade, V.F., & Babalola, O.O. (2023). Endophytic and rhizobacteria functionalities in alleviating drought stress in maize plants. Plant Prot. Sci., 59(1), 1–18.

Akanmu, A.O., Akol, A.M., Ndolo, D.O., Kutu, F.R., & Babalola, O.O. (2023a). Agroecological techniques: Adoption of safe and sustainable agricultural practices among the smallholder farmers in Africa. Front. Sustain. Food Syst., 7, 310.

Akanmu, A.O., Ajiboye, T.O., Seleke, M., Mhlanga, S.D., Onwudiwe, D.C., & Babalola, O.O. (2023b). The potency of graphitic carbon nitride (gC3N4) and bismuth sulphide nanoparticles (Bi2S3) in the management of foliar fungal pathogens of maize. Appl. Sci., 13(6), 3731.

Akanmu, A.O., Sobowale, A.A., Abiala, M.A., Olawuyi, O.J., & Odebode, A.C. (2020). Efficacy of biochar in the management of Fusarium verticillioides Sacc. causing ear rot in Zea mays L. Biotechnol. Rep., 26, e00474. doi:https://doi.org/10.1016/j.btre.2020.e00474

Ali, M.A., Ren, H., Ahmed, T., Luo, J., An, Q., Qi, X., & Li, B. (2020). Antifungal effects of rhizospheric Bacillus species against bayberry twig blight pathogen Pestalotiopsis versicolor. Agronomy, 10(11), 1811.

Ali, S., Charles, T.C., & Glick, B.R. (2014). Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol. Biochem., 80, 160-167.

Aveling, T.A., De Ridder, K., Olivier, N.A., & Berger, D.K. (2020). Seasonal variation in mycoflora associated with asymptomatic maize grain from small-holder farms in two provinces of South Africa. J. Agric. Rural Dev. Trop. Subtrop. (JARTS), 121(2), 265-275.

Babalola, O.O. (2010). Beneficial bacteria of agricultural importance. Biotechnol. Lett., 32, 1559-1570.

Babalola, O.O., Dlamini, S.P., & Akanmu, A.O. (2022). Shotgun metagenomic survey of the diseased and healthy maize (Zea mays L.) rhizobiomes. Microbiol. Resour. Announc., 11(10), e00498-00422.

Belisário, R., Robertson, A.E., & Vaillancourt, L.J. (2022). Maize anthracnose stalk rot in the genomic era. Plant Dis., 106(9), 2281-2298.

Benaissa, A. (2024). Rhizosphere: Role of bacteria to manage plant diseases and sustainable agriculture—A review. J. Basic Microbiol., 64(3), 2300361.

Holt J.G., Krieg N.R., Sneath P.H.A., Staley J.T., & Williams S.T. (1994) Bergey’s manual of determinative bacteriology, 9th edn. Williams and Wikins co, Baltimore, USA, p 566.

Biedendieck, R., Knuuti, T., Moore, S.J., & Jahn, D. (2021). The “beauty in the beast”—the multiple uses of Priestia megaterium in biotechnology. Appl. Microbiol. Biotechnol., 105, 5719-5737.

Coenye, T., & Vandamme, P. (2003). Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ. Microbiol., 5(9), 719-729.

Degani, O., Gordani, A., Becher, P., Chen, A., & Rabinovitz, O. (2022). Crop rotation and minimal tillage selectively affect maize growth promotion under late wilt disease stress. J. Fungi, 8(6), 586.

Dlamini, S.P., Akanmu, A.O., & Babalola, O.O. (2022). Rhizospheric microorganisms: The gateway to a sustainable plant health. Front. Sustain. Food Syst., 6, 925802.

Dlamini, S.P., Akanmu, A.O., & Babalola, O.O. (2023a). Variations in the functional diversity of rhizosphere microbiome of healthy and Northern corn leaf blight infected maize (Zea mays L.). Span. J. Soil Sci., 13, 10964.

Dlamini, S.P., Akanmu, A.O., Fadiji, A.E., & Babalola, O.O. (2023b). Maize rhizosphere modulates the microbiome diversity and community structure to enhance plant health. Saudi J. Biol. Sci., 30(1), 103499.

Dworkin, M., & Foster, J. (1958). Experiments with some microorganisms which utilize ethane and hydrogen. J. Bacteriol., 75(5), 592-603.

Enebe, M.C., & Babalola, O.O. (2018). The influence of plant growth-promoting rhizobacteria in plant tolerance to abiotic stress: a survival strategy. Appl. Microbiol. Biotechnol., 102, 7821-7835.

Esikova, T.Z., Anokhina, T.O., Abashina, T.N., Suzina, N.E., & Solyanikova, I.P. (2021). Characterization of soil bacteria with potential to degrade benzoate and antagonistic to fungal and bacterial phytopathogens. Microorganisms, 9(4), 755.

Etesami, H., & Maheshwari, D.K. (2018). Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: Action mechanisms and future prospects. Ecotoxicol. Environ. Saf., 156, 225-246.

Fadiji, A.E., Ayangbenro, A.S., Akanmu, A.O., & Babalola, O.O. (2022). Draft genome sequence of Enterobacter mori AYS9, a potential plant growth-promoting rhizobacterium. Microbiol. Resour. Announc., 11(12), e01008-01022.

Fadiji, A.E., Ayangbenro, A.S., & Babalola, O.O. (2023). Genomic assessment of Enterobacter mori AYS9: A potential plant growth-promoting drought-resistant rhizobacteria. Span. J. Soil Sci., 13, 11302.

Fadiji, A.E., Santoyo, G., Yadav, A.N., & Babalola, O.O. (2022). Efforts towards overcoming drought stress in crops: Revisiting the mechanisms employed by plant growth-promoting bacteria. Front. Microbiol., 13.

Farooq, U., & Bano, A. (2013). Screening of indigenous bacteria from rhizosphere of maize (Zea mays L.) for their plant growth promotion ability and antagonism against fungal and bacterial pathogens. J. Anim. Plant Sci, 23(6), 1642-1652.

Fasusi, O.A., Amoo, A.E., & Babalola, O.O. (2021). Characterization of plant growth-promoting rhizobacterial isolates associated with food plants in South Africa. Antonie van Leeuwenhoek, 114(10), 1683-1708.

Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39(4), 783-791.

Gadag, R.N., Bhat, J.S., Mukri, G., Gogoi, R., Suby, S.B., Das, A.K., Yadav, S., Yadava, P., Nithyashree, M.L., Naidu, G.K., Yadav, S.K., & Shilpa, K. (2021). Chapter 3: Resistance to biotic stress: Theory and applications in maize breeding. In C. Kole (Ed.), Genomic designing for biotic stress resistant cereal crops (pp. 129-175). Springer Nature Switzerland AG. DOI: 10.1007/978-3-030-75879-0_3.

Govan, J., Hughes, J.E., & Vandamme, P. (1996). Burkholderia cepacia: medical, taxonomic and ecological issues. J. Med. Microbiol., 45(6), 395-407.

Gupta, S. & Pandey, S. (2023). Plant growth promoting rhizobacteria to mitigate biotic and abiotic stress in plants. In: Singh, N., Chattopadhyay, A., Lichtfouse, E. (eds) Sustainable agriculture reviews, vol. 60. Springer, Cham. https://doi.org/10.1007/978-3-031-24181-9_3.

He, H., Zhai, Q., Tang, Y., Gu, X., Pan, H., & Zhang, H. (2023). Effective biocontrol of soybean root rot by a novel bacterial strain Bacillus siamensis HT1. Physiol. Mol. Plant Pathol., 125, 101984.

Imade, E.E., & Babalola, O.O. (2021). Biotechnological utilization: the role of Zea mays rhizospheric bacteria in ecosystem sustainability. Appl. Microbiol. Biotechnol., 105(11), 4487-4500.

Islam, M.R., Madhaiyan, M., Deka Boruah, H.P., Yim, W., Lee, G., Saravanan, V., ... Sa, T. (2009). Characterization of plant growth-promoting traits of free-living diazotrophic bacteria and their inoculation effects on growth and nitrogen uptake of crop plants. J. Microbiol. Biotechnol., 19(10), 1213-1222.

Jayakumar, A., Nair, I.C., & Radhakrishnan, E. (2021). Environmental adaptations of an extremely plant beneficial Bacillus subtilis Dcl1 identified through the genomic and metabolomic analysis. Microb. Ecol., 81, 687-702.

Jeong, H., Jeong, D.-E., Kim, S.H., Song, G.C., Park, S.-Y., Ryu, C.-M., ... Choi, S.-K. (2012). Draft genome sequence of the plant growth-promoting bacterium Bacillus siamensis KCTC 13613. J. Bacteriol., 194(15), 4148-4149. doi:10.1128/jb.00805-12.

Jha, C.K., Sharma, P., Shukla, A., Parmar, P., Patel, R., Goswami, D., & Saraf, M. (2021). Microbial enzyme, 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase: an elixir for plant under stress. Physiol. Mol. Plant Pathol., 115, 101664.

Jiao, X., Takishita, Y., Zhou, G., & Smith, D.L. (2021). Plant associated rhizobacteria for biocontrol and plant growth enhancement. Front. Plant Sci., 12, 634796.

Kabeer, R., Sylas V.P., Praveen Kumar, C.S., Thomas, A.P., Shanthiprabha, V., Radhakrishnan, E.K., & Baiju, K.R. (2022). Role of heavy metal tolerant rhizosphere bacteria in the phytoremediation of Cu and Pb using Eichhornia crassipes (Mart.) Solms. Int. J. Phytorem., 24(11), 1120-1132.

Korsman, J., Meisel, B., Kloppers, F.J., Crampton, B.G., & Berger, D.K. (2012). Quantitative phenotyping of grey leaf spot disease in maize using real-time PCR. Eur. J. Plant Pathol., 133, 461-471.

Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol., 35(6), 1547.

Lau, E.T., Tani, A., Khew, C.Y., Chua, Y.Q., & San Hwang, S. (2020). Plant growth-promoting bacteria as potential bio-inoculants and biocontrol agents to promote black pepper plant cultivation. Microbiol. Res, 240, 126549.

Liu, J.-M., Liang, Y.-T., Wang, S.-S., Jin, N., Sun, J., Lu, C., ... Wang, F.-Z. (2023). Antimicrobial activity and comparative metabolomic analysis of Priestia megaterium strains derived from potato and dendrobium. Sci. Rep., 13(1), 5272.

Liu, S., Guo, N., Ma, H., Sun, H., Zheng, X., & Shi, J. (2021). First report of root rot caused by Bipolaris zeicola on maize in Hebei Province. Plant Dis., 105(8), 2247.

Lyu, D., Backer, R., Robinson, W.G., & Smith, D.L. (2019). Plant growth-promoting rhizobacteria for cannabis production: yield, cannabinoid profile and disease resistance. Front. Microbiol., 1761.

Marco, S., Loredana, M., Riccardo, V., Raffaella, B., Walter, C., & Luca, N. (2022). Microbe-assisted crop improvement: a sustainable weapon to restore holobiont functionality and resilience. Hort. Res., 9, uhac160.

Ngoune Tandzi, L., & Mutengwa, C.S. (2019). Estimation of maize (Zea mays L.) yield per harvest area: Appropriate methods. Agron., 10(1), 29.

Orole, O.O., Adejumo, T.O., Link, T., & Voegele, R.T. (2023). Molecular identification of endophytes from maize roots and their biocontrol potential against toxigenic fungi of Nigerian maize. Sci. Prog., 106(3), 00368504231186514.

Padrilah, S.N., Samsudin, N.I.P., Shukor, M.Y.A., & Masdor, N.A. (2024). Nanoemulsion strategies in controlling fungal contamination and toxin production on grain corn using essential oils. Green Chem. Lett. Rev., 17(1), 2315138.

Parke, J.L., & Gurian-Sherman, D. (2001). Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu. Rev. Phytopathol., 39(1), 225-258.

Penrose, D.M., & Glick, B.R. (2003). Methods for isolating and characterizing ACC deaminase‐containing plant growth‐promoting rhizobacteria. Physiol. Plant., 118(1), 10-15.

Poole, N., Donovan, J., & Erenstein, O. (2021). Agri-nutrition research: revisiting the contribution of maize and wheat to human nutrition and health. Food Policy, 100, 101976.

Prasanna, B.M., Cairns, J.E., Zaidi, P., Beyene, Y., Makumbi, D., Gowda, M., ... Das, A. (2021). Beat the stress: breeding for climate resilience in maize for the tropical rainfed environments. Theor. Appl. Genet., 134(6), 1729-1752.

Rajan, L., Chakraborty, K., & Chakraborty, R.D. (2021). Pharmacological properties of some mangrove sediment-associated Bacillus isolates. Arch. Microbiol., 203, 67-76.

Saikia, J., Kotoky, R., Debnath, R., Kumar, N., Gogoi, P., Yadav, A., & Saikia, R. (2023). De novo genomic analysis of Enterobacter asburiae EBRJ12, a plant growth-promoting rhizobacteria isolated from the rhizosphere of Phaseolus vulgaris L. J. Appl. Microbiol., 134(2), lxac090.

Saqib, S., Uddin, S., Zaman, W., Ullah, F., Ayaz, A., Asghar, M., ... Chaudhary, H.J. (2020). Characterization and phytostimulatory activity of bacteria isolated from tomato (Lycopersicon esculentum Mill.) rhizosphere. Microb. Pathogenesis, 140, 103966.

Scortichini, M. (2022). Sustainable management of diseases in horticulture: Conventional and new options. Horticulturae, 8(6), 517.

Shahid, M., Zeyad, M.T., Syed, A., Singh, U.B., Mohamed, A., Bahkali, A.H., ... Pichtel, J. (2022). Stress-tolerant endophytic isolate Priestia aryabhattai BPR-9 modulates physio-biochemical mechanisms in wheat (Triticum aestivum L.) for enhanced salt tolerance. Int. J. Environ. Res. Public Health, 19(17), 10883.

Sharma, A., Abrahamian, P., Carvalho, R., Choudhary, M., Paret, M.L., Vallad, G. E., & Jones, J.B. (2022). Future of bacterial disease management in crop production. Annu. Rev. Phytopathol., 60, 259-282.

Tagele, S.B., Kim, S.W., Lee, H.G., & Lee, Y.S. (2019). Potential of novel sequence type of Burkholderia cenocepacia for biological control of root rot of maize (Zea mays L.) caused by Fusarium temperatum. Int. J. Mol. Sci., 20(5), 1005.

Tamura, K., & Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol., 10(3), 512-526.

Tripathi, K., Kumar, N., Singh, M., & Singh, R.K. (2020). Fungal siderophore: Biosynthesis, transport, regulation, and potential applications. In S.K. Sharma, U.B. Singh, P.K. Sahu, H.V. Singh, & P.K. Sharma (Eds.), (Series Ed. N.K. Arora), Microorganisms for sustainability. Springer Nature Singapore Pte Ltd., Vol. 23, pp. 387-408.

Vandamme, P., Holmes, B., Coenye, T., Goris, J., Mahenthiralingam, E., LiPuma, J.J., & Govan, J.R. (2003). Burkholderia cenocepacia sp. nov.—a new twist to an old story. Res. Microbiol., 154(2), 91-96.

Vary, P.S., Biedendieck, R., Fuerch, T., Meinhardt, F., Rohde, M., Deckwer, W.-D., & Jahn, D. (2007). Bacillus megaterium—from simple soil bacterium to industrial protein production host. Appl. Microbiol. Biotechnol., 76, 957-967.

Wahid, F., Fahad, S., Danish, S., Adnan, M., Yue, Z., Saud, S., ... Datta, R. (2020). Sustainable management with mycorrhizae and phosphate solubilizing bacteria for enhanced phosphorus uptake in calcareous soils. Agriculture, 10(8), 334.

Walterson, A.M., & Stavrinides, J. (2015). Pantoea: Insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiol. Rev., 39(6), 968-984.

Wei, X., Xie, B., Wan, C., Song, R., Zhong, W., Xin, S., & Song, K. (2024). Enhancing soil health and plant growth through microbial fertilizers: Mechanisms, benefits, and sustainable agricultural practices. Agronomy, 14(3), 609.

Wu, W., Feng, Y., & Zong, Z. (2019). Characterization of a strain representing a new Enterobacter species, Enterobacter chengduensis sp. nov. Antonie Van Leeuwenhoek, 112, 491-500.

Xie, Z., Li, M., Wang, D., Wang, F., Shen, H., Sun, G., ... Sun, X. (2021). Biocontrol efficacy of Bacillus siamensis LZ88 against brown spot disease of tobacco caused by Alternaria alternata. Biol. Control., 154, 104508.

Xue, Y., Hu, M., Chen, S., Hu, A., Li, S., Han, H., ... Zhou, J. (2021). Enterobacter asburiae and Pantoea ananatis causing rice bacterial blight in China. Plant Dis., 105(8), 2078-2088.

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2024-06-27

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