Abstract
The traditional way of dealing with plant diseases has been the use of chemical products, but these harm the environment and are incompatible with the global effort for sustainable development. The use of Bacillus and related species in the biological control of plant diseases is a trend in green agriculture. Many studies report the positive effect of these bacteria, but a synthesis is still necessary. So, the objective of this work is to perform a meta-analysis of Bacillus biocontrol potential and identify factors that drive its efficacy. Data were compiled from articles published in journals listed in two of the main scientific databases between 2000 and 2021. Among 6159 articles retrieved, 399 research papers met the inclusion criteria for a systematic review. Overall, Bacilli biocontrol agents reduced disease by 60% compared to control groups. Furthermore, experimental tests with higher concentrations show a strong protective effect, unlike low and single concentration essays. Biocontrol efficacy also increased when used as a protective inoculation rather than therapeutic inoculation. Inoculation directly in the fruit has a greater effect than soil drenching. The size of the effect of Bacillus-based commercial products is lower than the newly tested strains. The findings presented in this study confirm the power of Bacillus-based bioinoculants and provide valuable guidance for practitioners, researchers, and policymakers seeking effective and sustainable solutions in plant disease management.
Highlights
Bacillus biological control agents significantly reduced disease by 60% when compared to negative control groups;
The concentration of the inoculum drives the protection effect of Bacillus inoculation;
Protective inoculation has a greater effect than therapeutic inoculation;
Inoculation directly in the fruit has a greater effect than soil drenching;
In comparison with test strains, commercial bioproducts have a lower protective effect.
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Data availability
The data that support the findings of this study is provided within the manuscript or supplementary information files.
References
Abd-Elgawad MMM, Askary TH (2020) Factors affecting success of biological agents used in controlling the plant-parasitic nematodes. Egypt J Biol Pest Control 30:17. https://doi.org/10.1186/s41938-020-00215-2
Allaire JJ, Ellis P, Gandrud C et al (2017) networkD3: D3 JavaScript network graphs from R. R package version 0.4, URL http://CRAN.R-project.org/package= networkD3
Aly AA, El-Mahdy OM, Habeb MM et al (2022) Pathogenicity of Bacillus strains to cotton seedlings and their effects on some biochemical components of the infected seedlings. Plant Pathol J 38(2):90–101. https://doi.org/10.5423%2FPPJ.OA.11.2021.0173
Andrić S, Meyer T, Ongena M (2020) Bacillus responses to plant-associated fungal and bacterial communities. Front Microbiol 11:1350. https://doi.org/10.3389/fmicb.2020.01350
Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319. https://doi.org/10.1104/pp.103.028712
Bardin M, Comby MAL, Roullier G, Nicot P (2013) Diversity in susceptibility of Botrytis cinerea to biocontrol products inducing plant defense mechanisms. IOBC-WPRS Bull 88:45–49
Bardin M, Ajouz S, Comby M et al (2015) Is the efficacy of biological control against plant diseases likely to be more durable than that of chemical pesticides? Front Plant Sci 6:566. https://doi.org/10.3389/fpls.2015.00566
Bebber DP, Field E, Gui H et al (2019) Many unreported crop pests and pathogens are probably already present. Glob Chang Biol 25:2703–2713. https://doi.org/10.1111/gcb.14698
Blake C, Christensen MN, Kovács ÁT (2021) Molecular aspects of plant growth promotion and protection by Bacillus subtilis. Mol plant-microbe Interact 34:15–25. https://doi.org/10.1094/MPMI-08-20-0225-CR
Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to Meta-Analysis. Wiley, USA
Cai X-C, Liu C-H, Wang B-T, Xue Y-R (2017) Genomic and metabolic traits endow Bacillus velezensis CC09 with a potential biocontrol agent in control of wheat powdery mildew disease. Microbiol Res 196:89–94. https://doi.org/10.1016/j.micres.2016.12.007
Chandrasekaran M, Subramanian D, Yoon E et al (2016) Meta-analysis reveals that the Genus Pseudomonas can be a better choice of biological control agent against bacterial wilt disease caused by Ralstonia solanacearum. Plant Pathol J 32:216–227. https://doi.org/10.5423/PPJ.OA.11.2015.0235
Chen XH, Koumoutsi A, Scholz R et al (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007–1014. https://doi.org/10.1038/nbt1325
Cheng Y, Gao X, He H et al (2022) Dual RNA sequencing analysis of Bacillus amyloliquefaciens and sclerotinia sclerotiorum during infection of soybean seedlings by S. Sclerotiorum unveils antagonistic interactions. Front Microbiol 13:924313. https://doi.org/10.3389/fmicb.2022.924313
Collinge DB, Jensen DF, Rabiey M et al (2022) Biological control of plant diseases – what has been achieved and what is the direction? Plant Pathol 71:1024–1047. https://doi.org/10.1111/ppa.13555
Conrath U, Beckers GJM, Flors V et al (2006) Priming: getting ready for battle. Mol Plant-Microbe Interact 19:1062–1071. https://doi.org/10.1094/MPMI-19-1062
Cook RJ (1993) Making greater use of introduced microorganisms for biological control of plant pathogens. Annu Rev Phytopathol 31:53–80. https://doi.org/10.1146/annurev.py.31.090193.000413
Cooper H, Hedges LV, Valentine JC (2009) The handbook of research synthesis and meta-analysis, 2nd edn. Russell Sage Foundation, NY, US
Dawar S, Wahab S, Tariq M, Zaki MJ (2010) Application of Bacillus species in the control of root rot diseases of crop plants. Arch Phytopathol Plant Prot 43:412–418. https://doi.org/10.1080/03235400701850870
de Souza EM, Granada CE, Sperotto RA (2016) Plant pathogens affecting the establishment of plant-symbiont interaction. Front Plant Sci 7:15. https://doi.org/10.3389/fpls.2016.00015
Delgado-Baquerizo M, Guerra CA, Cano-Díaz C et al (2020) The proportion of soil-borne pathogens increases with warming at the global scale. Nat Clim Chang 10:550–554. https://doi.org/10.1038/s41558-020-0759-3
Deng Y, Zhu Y, Wang P et al (2011) Complete genome sequence of Bacillus subtilis BSn5, an endophytic bacterium of Amorphophallus konjac with antimicrobial activity for the plant pathogen Erwinia carotovora subsp. carotovora. J Bacteriol 193:2070–2071. https://doi.org/10.1128/JB.00129-11
R Development Core Team (2015) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.r-project. org/
Dimkić I, Janakiev T, Petrović M et al (2022) Plant-associated Bacillus and Pseudomonas antimicrobial activities in plant disease suppression via biological control mechanisms - a review. Physiol Mol Plant Pathol 117:101754. https://doi.org/10.1016/j.pmpp.2021.101754
Duffy B, Schouten A, Raaijmakers JM (2003) Pathogen self-defense: mechanisms to counteract microbial antagonism. Annu Rev Phytopathol 41:501–538. https://doi.org/10.1146/annurev.phyto.41.052002.095606
Dunlap CA, Kim SJ, Kwon SW, Rooney AP (2016) Bacillus velezensis is not a later heterotypic synonym of Bacillus amyloliquefaciens; Bacillus methylotrophicus, Bacillus amyloliquefaciens subsp. Plantarum and ‘Bacillus oryzicola’ are later heterotypic synonyms of Bacillus velezensis based on phylogenome. Int J Syst Evol Microbiol 66:1212–1217. https://doi.org/10.1099/ijsem.0.000858
Dunlap CA, Bowman MJ, Rooney AP (2019) Iturinic lipopeptide diversity in the Bacillus subtilis species group - important antifungals for plant disease biocontrol applications. Front Microbiol 10:1794. https://doi.org/10.3389/fmicb.2019.01794
Fan B, Blom J, Klenk H-P, Borriss R (2017) Bacillus amyloliquefaciens, Bacillus velezensis, and Bacillus siamensis form an operational Group B. amyloliquefaciens within the B. subtilis species complex. Front Microbiol 8:22. https://doi.org/10.3389/fmicb.2017.00022
Fan B, Wang C, Song X et al (2018) Bacillus velezensis FZB42 in 2018: the Gram-positive model strain for plant growth promotion and biocontrol. Front Microbiol 9:2491. https://doi.org/10.3389/fmicb.2018.02491
Fan H, He P, Xu S et al (2023) Banana disease-suppressive soil drives Bacillus assembled to defense fusarium wilt of banana. Front Microbiol 14:1211301. https://doi.org/10.3389/fmicb.2023.1211301
Fira D, Dimkić I, Berić T et al (2018) Biological control of plant pathogens by Bacillus species. J Biotechnol 285:44–55. https://doi.org/10.1016/j.jbiotec.2018.07.044
Franco-Franklin V, Moreno-Riascos S, Ghneim-Herrera T (2021) Are endophytic bacteria an option for increasing heavy metal tolerance of plants? A meta-analysis of the effect size. Front Environ Sci 8:603668. https://doi.org/10.3389/fenvs.2020.603668
Godebo AT, Wee NMJ, Yost CK et al (2022) A meta-analysis to determine the state of biological control of Aphanomyces root rot. Front Mol Biosci 8:777042. https://doi.org/10.3389/fmolb.2021.777042
Gu Y, Banerjee S, Dini-Andreote F et al (2022) Small changes in rhizosphere microbiome composition predict disease outcomes earlier than pathogen density variations. ISME J 16:2448–2456. https://doi.org/10.1038/s41396-022-01290-z
Gurevitch J, Koricheva J, Nakagawa S, Stewart G (2018) Meta-analysis and the science of research synthesis. Nature 555:175–182. https://doi.org/10.1038/nature25753
Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914. https://doi.org/10.1139/m97-131
Hawkins NJ, Bass C, Dixon A, Neve P (2019) The evolutionary origins of pesticide resistance. Biol Rev Camb Philos Soc 94:135–155. https://doi.org/10.1111/brv.12440
He D-C, He M-H, Amalin DM et al (2021) Biological control of plant diseases: an evolutionary and eco-economic consideration. Pathogens 10:1311. https://doi.org/10.3390/pathogens10101311
He P, Cui W, Peng L (2022) Biocontrol efficacy of Bacillus velezensis HC-8 against powdery mildew of honeysuckle caused by Erysiphe lonicerae var. Lonicerae Biol Control 166:104834. https://doi.org/10.1016/j.biocontrol.2021.104834
Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156. https://doi.org/10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2
Ibáñez A, Garrido-Chamorro S, Barreiro C (2023) Microorganisms and climate change: a not so invisible effect. Microbiol Res 14:918–947. https://doi.org/10.3390/microbiolres14030064 Irtwange S V (2006) Application of biological control agents in pre- and postharvest operations. Biol Control VIII:1–12
Jin S, Wang N, Zhou Z et al (2022) Identification of Bacillus species causing bacterial leaf spot of peach in China. J Phytopathol 170:811–819. https://doi.org/10.1111/jph.13144
Kaminsky LM, Trexler RV, Malik RJ et al (2019) The inherent conflicts in developing soil microbial inoculants. Trends Biotechnol 37:140–151. https://doi.org/10.1016/j.tibtech.2018.11.011
Khan MS, Gao J, Zhang M et al (2020) Isolation and characterization of plant growth-promoting endophytic bacteria bacillus stratosphericus LW-03 from Lilium Wardii. 3 Biotech 10(7):305. https://doi.org/10.1007/s13205-020-02294-2
Kiesewalter HT, Lozano-Andrade CN, Wibowo M et al (2021) Genomic and chemical diversity of Bacillus subtilis secondary metabolites against plant pathogenic fungi. mSystems 6:e00770–e00720. https://doi.org/10.1128/msystems.00770-20
Kröber M, Wibberg D, Grosch R et al (2014) Effect of the strain Bacillus amyloliquefaciens FZB42 on the microbial community in the rhizosphere of lettuce under field conditions analyzed by whole metagenome sequencing. Front Microbiol 27:5:252. https://doi.org/10.3389/fmicb.2014.00252
Krupnik TJ, Andersson JA, Rusinamhodzi L et al (2019) Does size matter? A critical review of meta-analysis in agronomy. Exp Agric 55:200–229. https://doi.org/10.1017/S0014479719000012
Kumar S, Diksha, Sindhu SS, Kumar R (2022) Biofertilizers: an ecofriendly technology for nutrient recycling and environmental sustainability. Curr Res Microb Sci 3:100094. https://doi.org/10.1016/j.crmicr.2021.100094
Lajeunesse MJ (2011) On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecol 92:2049–2055. https://doi.org/10.1890/11-0423.1
Lastochkina O, Seifikalhor M, Aliniaeifard S et al (2019) Bacillus spp.: efficient biotic strategy to control postharvest diseases of fruits and vegetables. Plants 8(4):97. https://doi.org/10.3390/plants8040097
Lau J, Schmid CH, Chalmers TC (1995) Cumulative meta-analysis of clinical trials builds evidence for exemplary medical care. J Clin Epidemiol 48:45–57. https://doi.org/10.1016/0895-4356(94)00106-Z
LeBlanc N (2022) Bacteria in the genus Streptomyces are effective biological control agents for management of fungal plant pathogens: a meta-analysis. Biocontrol 67:111–121. https://doi.org/10.1007/s10526-021-10123-5
Legein M, Smets W, Vandenheuvel D et al (2020) Modes of action of microbial biocontrol in the phyllosphere. Front Microbiol 11:1619. https://doi.org/10.3389/fmicb.2020.01619
Li H, Leifert C (1994) Development of resistance in Botryotinia fuckeliana (de Barry) Whetzel against the biological control agent Bacillus subtilis CL27. J Plant Dis Prot 101:414–418
Lin L, Li C, Ren Z et al (2023) Transcriptome profiling of genes regulated by phosphate-solubilizing bacteria bacillus megaterium P68 in potato (Solanum tuberosum L). Front Microbiol 14:1140752. https://doi.org/10.3389/fmicb.2023.1140752
Liu H, Carvalhais LC, Crawford M et al (2017) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol 8:2552. https://doi.org/10.3389/fmicb.2017.02552
Liu Y, Teng K, Wang T et al (2020) Antimicrobial Bacillus velezensis HC6: production of three kinds of lipopeptides and biocontrol potential in maize. J Appl Microbiol 128:242–254. https://doi.org/10.1111/jam.14459
Luo L, Zhao C, Wang E et al (2022) Bacillus amyloliquefaciens as an excellent agent for biofertilizer and biocontrol in agriculture: an overview for its mechanisms. Microbiol Res 259:127016. https://doi.org/10.1016/j.micres.2022.127016
Madriz-Ordeñana K, Pazarlar S, Jørgensen HJL et al (2022) The Bacillus cereus strain ec9 primes the plant immune system for superior biocontrol of Fusarium oxysporum. Plants (Basel) 11:687. https://doi.org/10.3390/plants11050687
Mahapatra S, Yadav R, Ramakrishna W (2022) Bacillus subtilis impact on plant growth, soil health and environment: Dr. Jekyll Mr Hyde J Appl Microbiol 132:3543–3562. https://doi.org/10.1111/jam.15480
Mandadi KK, Scholthof K-BG (2013) Plant immune responses against viruses: how does a virus cause disease? Plant Cell 25:1489–1505. https://doi.org/10.1105/tpc.113.111658
Manjunatha L, Rajashekara H, Uppala LS et al (2022) Mechanisms of Microbial Plant Protection and Control of Plant Viruses. Plants (Basel) 11:3449. https://doi.org/10.3390/plants11243449
Martínez-Álvarez JC, Castro-Martínez C, Sánchez-Peña P et al (2016) Development of a powder formulation based on Bacillus cereus sensu lato strain B25 spores for biological control of Fusarium verticillioides in maize plants. World J Microbiol Biotechnol 32:75. https://doi.org/10.1007/s11274-015-2000-5
Másmela-Mendoza JE, Moreno-Velandia CA (2022) Bacillus velezensis supernatant mitigates tomato fusarium wilt and affects the functional microbial structure in the rhizosphere in a concentration-dependent manner. Rhizosphere 21:100475. https://doi.org/10.1016/j.rhisph.2022.100475
Massa F, Defez R, Bianco C (2022) Exploitation of plant growth promoting bacteria for sustainable agriculture: hierarchical approach to link laboratory and field experiments. Microorganisms 10:865. https://doi.org/10.3390/microorganisms10050865
Mckenney PT, Driks A, Eichenberger P (2013) The Bacillus subtilis endospore: Assembly and functions of the multilayered coat. Nat Rev Microbiol 11:33–44. https://doi.org/10.1038/nrmicro2921
Miljaković D, Marinković J, Balešević-Tubić S (2020) The significance of Bacillus spp. in disease suppression and growth promotion of field and vegetable crops. Microorganisms 8:1037. https://doi.org/10.3390/microorganisms8071037
Miller SA, Forrest JL (2001) Enhancing your practice through evidence-based decision making: PICO, learning how to ask good questions. J Evid Based Dent Pract 1:136–141. https://doi.org/10.1016/S1532-3382(01)70024-3
Minchev Z, Kostenko O, Soler R, Pozo MJ (2021) Microbial consortia for effective biocontrol of root and foliar diseases in tomato. Front Plant Sci 12:756368. https://doi.org/10.3389/fpls.2021.756368
Misra S, Chauhan PS (2020) ACC deaminase-producing rhizosphere competent Bacillus spp. mitigate salt stress and promote Zea mays growth by modulating ethylene metabolism. 3 Biotech 10:119. https://doi.org/10.1007/s13205-020-2104-y
Morales P, González M, Salvatierra-Martínez R et al (2022) New insights into BacillusPrimed Plant responses to a necrotrophic pathogen derived from the Tomato - Botrytis Pathosystem. Microorganisms 10:1547. https://doi.org/10.3390/microorganisms10081547
Nakagawa S, Santos ESA (2012) Methodological issues and advances in biological meta-analysis. Evol Ecol 26:1253–1274. https://doi.org/10.1007/s10682-012-9555-5
Ngalimat MS, Yahaya RSR, Baharudin MMA-A et al (2021) A review on the biotechnological applications of the operational group Bacillus amyloliquefaciens. Microorganisms 9:614. https://doi.org/10.3390/microorganisms9030614
Ngugi HK, Esker PD, Scherm H (2011) Meta-analysis to determine the effects of plant disease management measures: review and case studies on soybean and apple. Phytopathology 101:31–41. https://doi.org/10.1094/PHYTO-03-10-0068
Ojiambo PS, Scherm H (2006) Biological and application-oriented factors influencing plant disease suppression by biological control: a meta-analytical review. Phytopathology 96:1168–1174. https://doi.org/10.1094/PHYTO-96-1168
Olanrewaju OS, Ayilara MS, Ayangbenro AS, Babalola OO (2021) Genome mining of three plant growth-promoting Bacillus species from maize rhizosphere. Appl Biochem Biotechnol 193:3949–3969. https://doi.org/10.1007/s12010-021-03660-3
Orozco-Mosqueda M, del Flores C, Rojas-Sánchez A B, et al (2021) Plant growth-promoting bacteria as bioinoculants: attributes and challenges for sustainable crop improvement. Agronomy 11:1167. https://doi.org/10.3390/agronomy11061167
Page MJ, McKenzie JE, Bossuyt PM et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71. https://doi.org/10.1136/bmj.n71
Pathak VM, Verma VK, Rawat BS et al (2022) Current status of pesticide effects on environment, human health and it’s eco-friendly management as bioremediation: a comprehensive review. Front Microbiol 13:962619. https://doi.org/10.3389/fmicb.2022.962619
Peiris PUS, Li Y, Brown P, Xu C (2020) Fungal biocontrol against Meloidogyne spp. in agricultural crops: a systematic review and meta-analysis. Biol Control 144:104235. https://doi.org/10.1016/j.biocontrol.2020.104235
Peng G, Mcgregor L, Lahlali R et al (2011) Potential biological control of clubroot on canola and crucifer vegetable crops. Plant Pathol 60:566–574. https://doi.org/10.1111/j.1365-3059.2010.02400.x
Perea-Molina PA, Pedraza-Herrera LA, Beauregard PB, Uribe-Vélez D (2022) A biocontrol Bacillus velezensis strain decreases pathogen Burkholderia glumae population and occupies a similar niche in rice plants. Biol Control 176:105067. https://doi.org/10.1016/j.biocontrol.2022.105067
Portieles R, Xu H, Yue Q et al (2021) Heat-killed endophytic bacterium induces robust plant defense responses against important pathogens. Sci Rep 11:12182. https://doi.org/10.1038/s41598-021-91837-5
Raaijmakers JM, Paulitz TC, Steinberg C et al (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361. https://doi.org/10.1007/s11104-008-9568-6
Rabbee MF, Hwang B-S, Baek K-H (2023) Bacillus velezensis: a beneficial biocontrol agent or facultative phytopathogen for sustainable agriculture. Agronomy 13:840. https://doi.org/10.3390/agronomy13030840
Radhakrishnan R, Hashem A, Abd Allah EF (2017) Bacillus: a biological tool for crop improvement through bio-molecular changes in adverse environments. Front Physiol 8:667. https://doi.org/10.3389/fphys.2017.00667
Rana KL, Kour D, Kaur T et al (2020) Endophytic microbes: biodiversity, plant growth-promoting mechanisms and potential applications for agricultural sustainability. Antonie van Leeuwenhoek, Int J Gen Mol Microbiol 113:1075–1107. https://doi.org/10.1007/s10482-020-01429-y
Rho H, Hsieh M, Kandel SL et al (2018) Do endophytes promote growth of host plants under stress? A meta-analysis on plant stress mitigation by endophytes. Microb Ecol 75:407–418. https://doi.org/10.1007/s00248-017-1054-3
Richard B, Qi A, Fitt BDL (2022) Control of crop diseases through integrated crop management to deliver climate-smart farming systems for low- and high-input crop production. Plant Pathol 71:187–206. https://doi.org/10.1111/ppa.13493
Rosenberg M, Rothstein HR, Gurevitch J (2013) Effect sizes: conventional choices and calculations. In: Koricheva J, Gurevitch, Mengersen K (eds) Handbook of meta-analysis in ecology and evolution. Princeton University Press, Princeton and Oxford, pp 61–71
Rosenthal R (1979) The file drawer problem and tolerance for null results. Psychol Bull 86:638–641. https://doi.org/10.1037/0033-2909.86.3.638
Rosenthal R (1991) Meta-analytic procedures for social research (rev. ed.). Sage Publications, Inc. https://doi.org/10.4135/9781412984997
Saeid A, Prochownik E, Dobrowolska-Iwanek J (2018) Phosphorus solubilization by Bacillus species. Molecules 23:2897. https://doi.org/10.3390/molecules23112897
Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99. https://doi.org/10.1016/j.micres.2015.11.008
Savary S, Willocquet L, Pethybridge SJ et al (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3:430–439. https://doi.org/10.1038/s41559-018-0793-y
Sepúlveda Chavera GF, Macuer MA, Torres PM (2020) Endospore-forming bacteria present in a commercial stabilized poultry manure determines the Fusarium biocontrol and the tomato growth Promotion. Agronomy 10:1636. https://doi.org/10.3390/agronomy10111636
Shahzad R, Waqas M, Khan AL et al (2016) Seed-borne endophytic Bacillus amyloliquefaciens RWL-1 produces gibberellins and regulates endogenous phytohormones of Oryza sativa. Plant Physiol Biochem 106:236–243. https://doi.org/10.1016/j.plaphy.2016.05.006
Sharma RR, Singh D, Singh R (2009) Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: a review. Biol Control 50:205–221. https://doi.org/10.1016/j.biocontrol.2009.05.001
Singh RK, Singh P, Li H-B et al (2020) Diversity of nitrogen-fixing rhizobacteria associated with sugarcane: a comprehensive study of plant-microbe interactions for growth enhancement in Saccharum spp. BMC Plant Biol 20:220. https://doi.org/10.1186/s12870-020-02400-9
Smith CA, Ashby B (2023) Tolerance-conferring defensive symbionts and the evolution of parasite virulence. Evol Lett 7:262–272. https://doi.org/10.1093/evlett/qrad015
Soni R, Keharia H (2021) Phytostimulation and Biocontrol potential of Gram-positive endospore-forming Bacilli. Planta 254:49. https://doi.org/10.1007/s00425-021-03695-0
Sorokan A, Cherepanova E, Burkhanova G et al (2020) Endophytic Bacillus spp. as a prospective biological tool for control of viral diseases and non-vector Leptinotarsa decemlineata say. In Solanum tuberosum L. Front Microbiol 11(569457). https://doi.org/10.3389/fmicb.2020.569457
Stridh LJ, Mostafanezhad H, Andersen CB et al (2022) Reduced efficacy of biocontrol agents and plant resistance inducers against potato early blight from greenhouse to field. J Plant Dis Prot 129:923–938. https://doi.org/10.1007/s41348-022-00633-4
Tudi M, Daniel Ruan H, Wang L et al (2021) Agriculture development, pesticide application and its impact on the environment. Int J Environ Res Public Health 18:1112. https://doi.org/10.3390/ijerph18031112
Tufail MA, Bejarano A, Shakoor A et al (2021) Can bacterial endophytes be used as a promising bio-inoculant for the mitigation of salinity stress in crop plants? — a global meta-analysis of the last decade (2011–2020). Microorganisms 9:1861. https://doi.org/10.3390/microorganisms9091861
Tufail MA, Ayyub M, Irfan M et al (2022) Endophytic bacteria perform better than endophytic fungi in improving plant growth under drought stress: a meta-comparison spanning 12 years (2010–2021). Physiol Plant 174:e13806. https://doi.org/10.1111/ppl.13806
Venkatesh N, Keller NP (2019) Mycotoxins in conversation with bacteria and fungi. Front Microbiol 10:403. https://doi.org/10.3389/fmicb.2019.00403
Veselova SV, Sorokan AV, Burkhanova GF et al (2022) By modulating the hormonal balance and ribonuclease activity of tomato plants Bacillus subtilis induces defense response against potato virus x and potato virus y. Biomol (Basel Switzerland) 12:288. https://doi.org/10.3390/biom12020288
Viechtbauer W (2010) Conducting meta-analyses in R with the metafor. J Stat Softw 36:1–48
Wang L, Li X-B, Suo H-C et al (2017) Soft rot of potatoes caused by Bacillus amyloliquefaciens in Guangdong province, China. Can J Plant Pathol 39:533–539. https://doi.org/10.1080/07060661.2017.1381994
Wang SY, Herrera-Balandrano DD, Wang YX et al (2022) Biocontrol ability of the Bacillus amyloliquefaciens Group, B. amyloliquefaciens, B. velezensis, B. nakamurai, and B. siamensis, for the management of fungal postharvest diseases: A review. J Agric Food Chem 70:6591–6616. https://doi.org/10.1021/acs.jafc.2c01745
Wang F, Szu-Han C, Tsai C-H et al (2023) Developing fermentation liquid of Bacillus amyloliquefaciens pmb04 to control bacterial leaf spot of sweet pepper. Agric 13:1456. https://doi.org/10.3390/agriculture13071456
Watts D, Palombo EA, Jaimes Castillo A, Zaferanloo B (2023) Endophytes in agriculture: potential to improve yields and tolerances of agricultural crops. Microorganisms 11:1276. https://doi.org/10.3390/microorganisms11051276
Wickham H (2016) Ggplot2: elegant graphics for data analysis. Springer-
Xie S, Jiang H, Ding T et al (2018) Bacillus amyloliquefaciens FZB42 represses plant miR846 to induce systemic resistance via a jasmonic acid-dependent signalling pathway. Mol Plant Pathol 19:1612–1623. https://doi.org/10.1111/mpp.12634
Xu W, Ren H, Ou T et al (2019) Genomic and functional characterization of the endophytic Bacillus subtilis 7PJ-16 strain, a potential biocontrol agent of mulberry fruit sclerotiniose. Microb Ecol 77:651–663. https://doi.org/10.1007/s00248-018-1247-4
Yánez-Mendizabal V, Viñas I, Usall J et al (2012) Endospore production allows using spray-drying as a possible formulation system of the biocontrol agent Bacillus subtilis CPA-8. Biotechnol Lett 34:729–735. https://doi.org/10.1007/s10529-011-0834-y
Yue Z, Liu Y, Chen Y et al (2023) Comprehensive genomics and proteomics analysis reveals the multiple response strategies of endophytic Bacillus sp. WR13 to iron limitation. Microorganisms 11:367. https://doi.org/10.3390/microorganisms11020367
Zhang JX, Xue AG, Tambong JT (2009) Evaluation of seed and soil treatments with novel Bacillus subtilis strains for control of soybean root rot caused by Fusarium oxysporum and F. Graminearum. Plant Dis 93:1317–1323. https://doi.org/10.1094/PDIS-93-12-1317
Zhang Z, Li J, Zhang Z et al (2021) Tomato endophytic bacteria composition and mechanism of suppressiveness of wilt disease (Fusarium oxysporum). Front Microbiol 12:731764. https://doi.org/10.3389/fmicb.2021.731764
Zhang N, Wang Z, Shao J et al (2023) Biocontrol mechanisms of Bacillus: improving the efficiency of green agriculture. Microb Biotechnol 16:2250–2263. https://doi.org/10.1111/1751-7915.14348
Zhao G, Zhu X, Zheng G et al (2024) Development of biofertilizers for sustainable agriculture over four decades (1980–2022). Geogr Sustain 5:19–28. https://doi.org/10.1016/j.geosus.2023.09.006
Zhou C, Zhu J, Qian N et al (2021a) Bacillus subtilis SL18r induces tomato resistance against Botrytis Cinerea, involving activation of long non-coding RNA, MSTRG18363, to Decoy miR1918. Front Plant Sci 11:634819. https://doi.org/10.3389/fpls.2020.634819
Zhou H, Zhu HJ, Ren ZH et al (2021b) Efficacy of Bacillus tequilensis strain JN-369 to biocontrol of rice blast and enhance rice growth. Biol Control 160:104652. https://doi.org/10.1016/j.biocontrol.2021.104652
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The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil.
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Conceptualization: C.P. Serrão, J.C.G Ortega, P.C. Rodrigues and C.R.B. de Souza. Material preparation, data collection and analysis: C.P. Serrão and J.C.G. Ortega. Writing—original draft preparation: C.P. Serrão. Writing—review and editing: J.C.G Ortega, P.C. Rodrigues and C.R.B. de Souza. Reading and approval of the final version of the manuscript: C.P. Serrão, J.C.G Ortega, P.C. Rodrigues and C.R.B. de Souza.
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Serrão, C.P., Ortega, J.C.G., Rodrigues, P.C. et al. Bacillus species as tools for biocontrol of plant diseases: A meta-analysis of twenty-two years of research, 2000–2021. World J Microbiol Biotechnol 40, 110 (2024). https://doi.org/10.1007/s11274-024-03935-x
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DOI: https://doi.org/10.1007/s11274-024-03935-x