Characterization of broad-spectrum biocontrol efficacy of Bacillus velezensis against Fusarium oxysporum in Triticum aestivum L.
Abstract
Fungi are the most important phytopathogens that cause yield losses. The mycotoxins released by fungi cause spoilage of stored food consumed by humans and feed supplied to animals. Fungi-antagonistic microbes are gaining attention as potential biocontrol agents (BCAs). This study was designed to isolate bacterial isolates from different crops and evaluate their in vitro antifungal assay against three phytopathogens, plant growth promoting (PGP) characteristics, molecular identification, and in vivo efficiency against the most devastating phytopathogenic fungus Fusarium oxysporum Schltdl. In the in vitro experiment, the 3 isolates BA, GL-1, and 5a out of 360 isolates showed more than 60% inhibitory activity against the selected fungi in this study. On the basis of 16S rRNA sequencing and phylogenetic analysis, BA isolate was identified as Bacillus velezensis. All three isolates produced indole acetic acid (IAA), hydrogen cyanide (HCN), and cellulase enzymes, while the BA and GL-1 isolates also produced siderophores and the BA isolate also produced ammonia. BA was selected on basis of not only Biocontrol efficacy but also maximum PGPR activity compared to GL-1 and 5a. In vivo assay, the isolate BA showed a significant decrease in disease severity caused by Fusarium oxysporum by 64.97% after 100 days of inoculation on wheat (FD-08) seedlings in a greenhouse assay and enhanced the shoot root height, fresh and dry mass. The wide-ranging antagonistic action of Bacillus velezensis isolated from the phyllosphere of wheat crops showed promising fungicidal and plant growth-promoting capabilities, suggesting it can be used as a biofungicide.
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References
Ajayi‐Oyetunde O, Bradley C (2018). Rhizoctonia solani: taxonomy, population biology and management of rhizoctonia seedling disease of soybean. Plant Pathology 67(1):3-17. https://doi.org/10.1111/ppa.12733
Amanda N (2015). Survey of Fusarium oxysporum f. sp. vasinfectum in the United States. The Journal of Cotton Science. The Cotton Foundation 19:328-336.
Awais M, Tariq M, Ali A, Ali Q, Khan A, Tabassum B, … Husnain T (2017). Isolation, characterization and inter-relationship of phosphate solubilizing bacteria from the rhizosphere of sugarcane and rice. Biocatalysis and Agricultural Biotechnology 11:312-321. https://doi.org/10.1016/j.bcab.2017.07.018
Azeem S, Agha SI, Jamil N, Tabassum B, Ahmed S, Raheem A, … Khan A (2022). Characterization and survival of broad-spectrum biocontrol agents against phytopathogenic fungi. Revista Argentina de Microbiología. https://doi.org/10.1016/j.ram.2021.10.005
Das A, Bhattacharya S, Murali L (2010). Production of cellulase from a thermophilic Bacillus sp. isolated from cow dung. American-Eurasian Journal of Agriculture and Environmental Sciences 8:685-691.
Dennis C, Webster J (1971). Antagonistic properties of species-groups of Trichoderma: III. Hyphal interaction. Transactions of the British Mycological Society 57(3):363-IN2. https://doi.org/10.1016/s0007-1536(71)80077-3
Dita M, Barquero M, Heck D, Mizubuti ES, Staver CP (2018). Fusarium wilt of banana: current knowledge on epidemiology and research needs toward sustainable disease management. Frontiers in plant science 9:1468. https://doi.org/10.3389/fpls.2018.01468
Eid AM, Fouda A, Abdel-Rahman MA, Salem SS, Elsaied A, Oelmüller R, … Hassan SED (2021). Harnessing bacterial endophytes for promotion of plant growth and biotechnologi applications: an overview. Plants 10(5):935. https://doi.org/10.3390/plants10050935
Fernandes MFR, Ribeiro TG, Rouws JR, de Barros Soares LH, Zilli JÉ (2021). Biotechnological potential of bacteria from genera Bacillus paraburkholderia and Pseudomonas to control seed fungal pathogens. Brazilian Journal of Microbiology 1-10. https://doi.org/10.1007/s42770-021-00448-9
Gajbhiye M, Kesharwani J, Ingle A, Gade A, Rai M (2009). Fungus-mediated synthesis of silver nanoparticles and their activity against pathogenic fungi in combination with fluconazole. Nanomedicine: Nanotechnology, Biology and Medicine 5(4):382-386. https://doi.org/10.1016/j.nano.2009.06.005
Ghodsalavi B, Ahmadzadeh M, Soleimani M, Madloo PB, Taghizad-Farid R (2013). Isolation and characterization of rhizobacteria and their effects on root extracts of Valeriana officinalis. Australian Journal of Crop Science 7(3):338-344.
Gilbert S, Xu J, Acosta K, Poulev A, Lebeis S, Lam E (2018). Bacterial production of indole related compounds reveals their role in association between duckweeds and endophytes. Frontiers in Chemistry 6:265. https://doi.org/10.3389/fchem.2018.00265
Haidar R, Roudet J, Bonnard O, Dufour MC, Corio-Costet MF, Fert M, … Fermaud M (2016). Screening and modes of action of antagonistic bacteria to control the fungal pathogen Phaeomoniella chlamydospora involved in grapevine trunk diseases. Microbiological Research 192:172-184. https://doi.org/10.1016/j.micres.2016.07.003
Jacob S, Sajjalaguddam RR, Kumar KVK, Varshney R, Sudini HK (2016). Assessing the prospects of Streptomyces sp. RP1A-12 in managing groundnut stem rot disease caused by Sclerotium rolfsii Sacc. Journal of General Plant Pathology 82(2):96-104. https://doi.org/10.1007/s10327-016-0644-0
Jasrotia S, Salgotra RK, Sharma M (2021). Efficacy of bioinoculants to control of bacterial and fungal diseases of rice (Oryza sativa L.) in northwestern Himalaya. Brazilian Journal of Microbiology:1-18. https://doi.org/10.1007/s42770-021-00442-1
Ji SH, Gururani MA, Chun SC (2014). Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiological Research 169:183-198. https://doi.org/10.1016/j.micres.2013.06.003
Jiang C-H, Yao X-F, Mi D-D, Li Z-J, Yang B-Y, Zheng Y, … Guo J-H (2019). Comparative transcriptome analysis reveals the biocontrol mechanism of Bacillus velezensis F21 against Fusarium wilt on watermelon. Frontiers in Microbiology 10:652. https://doi.org/10.3389/fmicb.2019.00652
Joseph B, Ranjan Patra R, Lawrence R (2012). Characterization of plant growth promoting rhizobacteria associated with chickpea (Cicer arietinum L.). International Journal of Plant Production 1(2):141-152.
Kgatle M, Truter M, Ramusi T, Flett B, Aveling T (2018). Alternaria alternata, the causal agent of leaf blight of sunflower in South Africa. European Journal of Plant Pathology 151(3):677-688. https://doi.org/10.1007/s10658-017-1402-7
Khan A, Tabassum B, Aaliya K, Tariq M, Nasir I, Hassan S, … Ponya Z (2019). The effectiveness of recombinant chitinase obtained from barley (Hordeum vulgare L.) against potato pathogens. Applied Ecology and Environmental Research 17(2):4147-4157. https://doi.org/10.15666/aeer/1702_41474157
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6):1547-1549.
Leiminger J, Bäßler E, Knappe C, Bahnweg G, Hausladen H (2015). Quantification of disease progression of Alternaria spp. on potato using real-time PCR. European Journal of Plant Pathology 141(2):295-309. https://doi.org/10.1007/s10658-014-0542-2
Lorck H (1948). Production of hydrocyanic acid by bacteria. Physiologia Plantarum 1(2):142-146. https://doi.org/10.1111/j.1399-3054.1948.tb07118.x
Lucero CT, Lorda GS, Anzuay MS, Ludueña LM, Taurian T (2021). Peanut endophytic phosphate solubilizing bacteria increase growth and p content of soybean and maize plants. Current Microbiology 78:1961-1972. https://doi.org/10.1007/s00284-021-02469-x
Madhaiyan M, Poonguzhali S, Kwon S-W, Sa T-M (2010). Bacillus methylotrophicus sp. nov., a methanol-utilizing, plant-growth-promoting bacterium isolated from rice rhizosphere soil. International Journal of Systematic and Evolutionary Microbiology 60(10):2490-2495. https://doi.org/10.1099/ijs.0.015487-0
Mitchell NJ, Bowers E, Hurburgh C, Wu F (2016). Potential economic losses to the US corn industry from aflatoxin contamination. Food Additives & Contaminants: Part A 33(3):540-550. https://doi.org/10.1080/19440049.2016.1138545
Nautiyal CS (1999). An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS microbiology Letters 170(1):265-270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
Passari AK, Mishra VK, Leo VV, Gupta VK, Singh BP (2016). Phytohormone production endowed with antagonistic potential and plant growth promoting abilities of culturable endophytic bacteria isolated from Clerodendrum colebrookianum Walp. Microbiological Research 193:57-73. https://doi.org/10.1016/j.micres.2016.09.006
Pastuszak J, Szczerba A, Dziurka M, Hornyák M, Kopeć P, Szklarczyk M, Płażek A (2021). Physiological and biochemical response to Fusarium culmorum infection in three durum wheat genotypes at seedling and full anthesis stage. International Journal of Molecular Sciences 22(14):7433. https://doi.org/10.3390/ ijms22147433
Pereira BdA, Castro-Silva MA (2010). Rizobactérias formadoras de endósporos associadas à Tibouchina urvilleana de áreas impactadas por rejeitos da mineração do carvão. Revista Brasileira de Ciência do Solo 34(2):563-567. https://doi.org/10.1590/s0100-06832010000200030
Ramzan M, Tabassum B, Nasir IA, Khan A, Tariq M, Awan MF, … Toufiq N (2016). Identification and application of biocontrol agents against cotton leaf curl virus disease in Gossypium hirsutum under greenhouse conditions. Biotechnology and Biotechnological Equipment 30(3):469-478. https://doi.org/10.1080/13102818.2016.1148634
Rana A, Sahgal M, Johri B (2017). Fusarium oxysporum: genomics, diversity and plant–host interaction. Developments in Fungal Biology and Applied Mycology. Springer, pp 159-199 https://doi.org/10.1007/978-981-10-4768-8_10
Saitou N, Nei M (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4(4):406-425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Schwyn B, Neilands J (1987). Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry 160(1):47-56. https://doi.org/10.1016/0003-2697(87)90612-9
Shafi U, Mumtaz R, Shafaq Z, Zaidi SMH, Kaifi MO, Mahmood Z, Zaidi SAR (2022). Wheat rust disease detection techniques: a technical perspective. Journal of Plant Diseases and Protection 1-16. https://doi.org/10.1007/s41348-022-00575-x
Shimodaira H, Hasegawa M (2001). CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17(12):1246-1247. https://doi.org/10.1093/bioinformatics/17.12.1246
Sivasankari B (2016). Indole-3-Acetic acid production by the bacterial strains isolated from vermicomposts in the presence and absence of tryptophan. International Journal of Innovative Research in Science, Engineering and Technology 5(5):92-107.
Syed R, Lodhi A, Jiskani M, Rajput K, Khaskheli M, Khanzada M, … Rajput A (2015). First report of Panama wilt disease of banana caused by Fusarium oxysporum f. sp. cubense in Pakistan. Journal of Plant Pathology 97(1):213.
Tabli N, Rai A, Bensidhoum L, Palmieri G, Gogliettino M, Cocca E, … Nabti E (2018). Plant growth promoting and inducible antifungal activities of irrigation well water-bacteria. Biological Control 117:78-86. https://doi.org/10.1016/j.biocontrol.2017.10.010
Tewoldemedhin Y, Lamprecht S, McLeod A, Mazzola M (2006). Characterization of Rhizoctonia spp. recovered from crop plants used in rotational cropping systems in the Western Cape province of South Africa. Plant Disease 90(11):1399-1406. https://doi.org/10.1094/PD-90-1399
Toppo S, Naik U (2015). Isolation and characterization of bacterial antagonist to plant pathogenic fungi (Fusarium spp.) from agro based area of Bilaspur. International Journal of Research Studies in Biosciences 6-14.
Tsegaye Z, Gizaw B, Tefera G, Feleke A, Chaniyalew S, Alemu T, Assefa F (2019). Isolation and biochemical characterization of plant growth promoting (pgp) bacteria colonizing the rhizosphere of Tef crop during the seedling stage. Biomedical Journal of Scientific and Technical Research 14:013-027.
Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y, … Otani H (2013). Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiology Reviews 37(1):44-66. https://doi.org/10.1111/j.1574-6976.2012.00350.x
Vasebi Y, Safaie N, Alizadeh A (2013). Biological control of soybean charcoal root rot disease using bacterial and fungal antagonists In Vitro and greenhouse condition. Journal of Crop Protection 2(2):139-150. https://doi.org/10.1515/jppr-2016-0004
Velivelli SL, Lojan P, Cranenbrouck S, de Boulois HD, Suarez JP, Declerck S, … Prestwich BD (2015). The induction of Ethylene response factor 3 (ERF3) in potato as a result of co-inoculation with Pseudomonas sp. R41805 and Rhizophagus irregularis MUCL 41833–a possible role in plant defense. Plant Signaling & Behavior 10(2):e988076. https://doi.org/10.4161/15592324.2014.988076
Vipul V, Alpika V, Akhilesh K (2012). Isolation & production of cellulase enzyme from bacteria isolated from agricultural fields in district Hardoi, Uttar Pradesh, India. Advances in Applied Science Research 3(1):171-174.
Wang C, Zhao D, Qi G, Mao Z, Hu X, Du B, … Ding Y (2020a). Effects of Bacillus velezensis FKM10 for promoting the growth of Malus hupehensis Rehd. and inhibiting Fusarium verticillioides. Frontiers in Microbiology 10:2889. https://doi.org/10.3389/fmicb.2019.02889
Wang S, Sun L, Zhang W, Chi F, Hao X, Bian J, Li Y (2020b). Bacillus velezensis BM21, a potential and efficient biocontrol agent in control of corn stalk rot caused by Fusarium graminearum. Egyptian Journal of Biological Pest Control 30(1):9. https://doi.org/10.1186/s41938-020-0209-6
Yang C, Hamel C, Vujanovic V, Gan Y (2011). Fungicide: modes of action and possible impact on nontarget microorganisms. ISRN Ecology 2011:130289. https://doi.org/10.5402/2011/130289
Yigit F, Dikilitas M (2007). Control of fusarium wilt of tomato by combination of fluorescent Pseudomonas, non-pathogen Fusarium and Trichoderma harzianum T-22 in greenhouse conditions. Plant Pathology Journal 6:159-163. https://doi.org/10.3923/ppj.2007.159.163
Yoon M-Y, Cha B, Kim J-C (2013). Recent trends in studies on botanical fungicides in agriculture. The Plant Pathology Journal 29(1):1-9. https://doi.org/10.5423/ppj.rw.05.2012.0072
Zhu L, Ni W, Liu S, Cai B, Xing H, Wang S (2017). Transcriptomics analysis of apple leaves in response to Alternaria alternata apple pathotype infection. Frontiers in Plant Science 8:22. https://doi.org/10.3389/fpls.2017.00022
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