Mixture of Bacillus Amyloliquefaciens and Bacillus Pumilus Modulates Community Structures of Rice Rhizosphere Soil to Suppress Rice Seedling Blight
Received date: 2024-06-15
Accepted date: 2024-09-18
Online published: 2024-09-26
Rice seedling blight, caused by various fungi, including Fusarium oxysporum, poses a severe threat to rice production. As awareness grows regarding the environmental and safety hazards associated with the application of fungicides for managing rice seedling blight, there has been a shift in focus towards biological control agents. In this study, we isolated biocontrol bacteria from paddy fields that significantly inhibited the growth of F. oxysporum in vitro and identified the strains as Bacillus amyloliquefaciens T40 and Bacillus pumilus T208. Additionally, our findings indicated that the combined application of these Bacillus strains in soil was more effective in reducing the incidence of rice seedling blight than their individual use. Analysis of 16S and internal transcribed spacer rRNA gene sequencing data revealed that the mixture of the T40 and T208 strains exhibited the lowest average clustering coefficients, which were negatively correlated with the biomass of F. oxysporum-inoculated rice seedlings. Furthermore, this mixture led to higher stochastic assembly (average |βNTI| < 2) and reduced selection pressures on rice rhizosphere bacteria compared with individual strain applications. The mixture of the T40 and T208 strains also significantly increased the expression of defense-related genes. In conclusion, the mixture of the T40 and T208 strains effectively modulates microbial community structures, enhances microbial network stability, and boosts the resistance against rice seedling blight. Our study supports the development and utilization of biological resources for crop protection.
Jiang Nan, Qiu Jiehua, Tian Dagang, Shi Huanbin, Liu Zhiquan, Wen Hui, Xie Shuwei, Chen Huizhe, Wu Meng, Kou Yanjun . Mixture of Bacillus Amyloliquefaciens and Bacillus Pumilus Modulates Community Structures of Rice Rhizosphere Soil to Suppress Rice Seedling Blight[J]. Rice Science, 2025 , 32(1) : 118 -130 . DOI: 10.1016/j.rsci.2024.09.001
| [1] | Alizadeh H, Behboudi K, Ahmadzadeh M, et al. 2013. Induced systemic resistance in cucumber and Arabidopsis thaliana by the combination of Trichoderma harzianum Tr6 and Pseudomonas sp. Ps14. Biol Contr, 65(1): 14-23. |
| [2] | Backman P A, Wilson M, Murphy J F. 1997. Bacteria for biological control of plant diseases. In: Rechcigl J E. Environmentally Safe Approaches to Crop Disease Control. Boca Raton, USA: CRC Press: 95-109. |
| [3] | Berendsen R L, Pieterse C M J, Bakker P A H M. 2012. The rhizosphere microbiome and plant health. Trends Plant Sci, 17(8): 478-486. |
| [4] | Bolyen E, Rideout J R, Dillon M R, et al. 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol, 37(8): 852-857. |
| [5] | Bubici G, Kaushal M, Prigigallo M I, et al. 2019. Biological control agents against Fusarium wilt of banana. Front Microbiol, 10: 616. |
| [6] | Callahan B J, McMurdie P J, Rosen M J, et al. 2016. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods, 13(7): 581-583. |
| [7] | Cao Y, Ding W, Liu C. 2021. Unraveling the metabolite signature of endophytic Bacillus velezensis strain showing defense response towards Fusarium oxysporum. Agronomy, 11(4): 683. |
| [8] | Cheng T, Yao X Z, Wu C Y, et al. 2020. Endophytic Bacillus megaterium triggers salicylic acid-dependent resistance and improves the rhizosphere bacterial community to mitigate rice spikelet rot disease. Appl Soil Ecol, 156: 103710. |
| [9] | Daraz U, Li Y, Sun Q, et al. 2021. Inoculation of Bacillus spp. modulate the soil bacterial communities and available nutrients in the rhizosphere of vetiver plant irrigated with acid mine drainage. Chemosphere, 263: 128345. |
| [10] | Delgado-Baquerizo M, Maestre F T, Reich P B, et al. 2016. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun, 7: 10541. |
| [11] | Devi A, Mohan S, Rajalakshmi J. 2014. Growth promotion activity and biological control for the management of leaf blight incited by Alternaria helianthi. Arch Phytopathol, 47(18): 2280-2287. |
| [12] | Dobrzyński J, Jakubowska Z, Kulkova I, et al. 2023. Biocontrol of fungal phytopathogens by Bacillus pumilus. Front Microbiol, 14: 1194606. |
| [13] | Elmqvist T, Folke C, Nyström M, et al. 2003. Response diversity, ecosystem change, and resilience. Front Ecol Environ, 1(9): 488-494. |
| [14] | Elnahal A S M, El-Saadony M T, Saad A M, et al. 2022. The use of microbial inoculants for biological control, plant growth promotion, and sustainable agriculture: A review. Eur J Plant Pathol, 162(4): 759-792. |
| [15] | Etesami H, Jeong B R, Glick B R. 2023. Biocontrol of plant diseases by Bacillus spp. Physiol Mol Plant Pathol, 126: 102048. |
| [16] | Fan J B, Bai P F, Ning Y S, et al. 2018. The monocot-specific receptor-like kinase SDS2 controls cell death and immunity in rice. Cell Host Microbe, 23(4): 498-510.e5. |
| [17] | Faust K, Raes J. 2016. CoNet app: Inference of biological association networks using Cytoscape. F1000Research, 5: 1519. |
| [18] | Gadhave K R, Devlin P F, Ebertz A, et al. 2018. Soil inoculation with Bacillus spp. modifies root endophytic bacterial diversity, evenness, and community composition in a context-specific manner. Microb Ecol, 76(3): 741-750. |
| [19] | Gao G F, Peng D, Zhang Y H, et al. 2021. Dramatic change of bacterial assembly process and co-occurrence pattern in Spartina alterniflora salt marsh along an inundation frequency gradient. Sci Total Environ, 755(Pt 1): 142546. |
| [20] | Gurav R, Tang J C, Jadhav J. 2017. Novel chitinase producer Bacillus pumilus RST25 isolated from the shellfish processing industry revealed antifungal potential against phyto-pathogens. Int Biodeterior Biodegrad, 125: 228-234. |
| [21] | International Rice Genome Sequencing Project. 2005. The map- based sequence of the rice genome. Nature, 436: 793-800. |
| [22] | Jetiyanon K, Kloepper J W. 2002. Mixtures of plant growth- promoting rhizobacteria for induction of systemic resistance against multiple plant diseases. Biol Contr, 24(3): 285-291. |
| [23] | Jiang W Y, Liu J X, He Y, et al. 2024. Biological control ability and antifungal activities of Bacillus velezensis Bv S3 against Fusarium oxysporum that causes rice seedling blight. Agronomy, 14(1): 167. |
| [24] | Karjalainen R, Jensen D F. 2006. Special issue: Biological control of plant pathogens. BioControl, 51: 279-400. |
| [25] | Katan J. 2015. Soil solarization: The idea, the research and its development. Phytoparasitica, 43(1): 1-4. |
| [26] | Li Z F, Bai X L, Jiao S, et al. 2021. A simplified synthetic community rescues Astragalus mongholicus from root rot disease by activating plant-induced systemic resistance. Microbiome, 9(1): 217. |
| [27] | Liaw A, Wiener M. 2002. Classification and regression by randomForest. R News, 2(3): 18-22. |
| [28] | Liu J X, Cai Y N, Jiang W Y, et al. 2020. Population structure and genetic diversity of fungi causing rice seedling blight in Northeast China based on microsatellite markers. Plant Dis, 104(3): 868-874. |
| [29] | Liu J X, Zhang R S, Xu C Z, et al. 2022. Characterisation of Pythium aristosporum oomycete: A novel pathogen causing rice seedling blight in China. J Fungi, 8(9): 890. |
| [30] | Liu K, Newman M, McInroy J A, et al. 2017. Selection and assessment of plant growth-promoting rhizobacteria for biological control of multiple plant diseases. Phytopathology, 107(8): 928-936. |
| [31] | Liu K, McInroy J A, Hu C H, et al. 2018. Mixtures of plant- growth-promoting rhizobacteria enhance biological control of multiple plant diseases and plant-growth promotion in the presence of pathogens. Plant Dis, 102(1): 67-72. |
| [32] | Lu R K. 2000. Analytical Method for Soil and Agricultural Chemistry. Beijing: China Agricultural Science and Technology Press. (in Chinese) |
| [33] | Ma B, Wang H Z, Dsouza M, et al. 2016. Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. ISME J, 10(8): 1891-1901. |
| [34] | Ma B, Wang J H, Liu C Z, et al. 2019. Preventive effects of fluoro-substituted benzothiadiazole derivatives and chitosan oligosaccharide against the rice seedling blight induced by Fusarium oxysporum. Plants, 8(12): 538. |
| [35] | Ma L J, Geiser D M, Proctor R H, et al. 2013. Fusarium pathogenomics. Annu Rev Microbiol, 67: 399-416. |
| [36] | 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(7): 1037. |
| [37] | Muñoz-Leoz B, Garbisu C, Charcosset J Y, et al. 2013. Non-target effects of three formulated pesticides on microbially-mediated processes in a clay-loam soil. Sci Total Environ, 449: 345-354. |
| [38] | Park C H, Chen S B, Shirsekar G, et al. 2012. The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice. Plant Cell, 24(11): 4748-4762. |
| [39] | Pinkerton J N, Ivors K L, Reeser P W, et al. 2002. The use of soil solarization for the management of soilborne plant pathogens in strawberry and red raspberry production. Plant Dis, 86(6): 645-651. |
| [40] | Prismantoro D, Akbari S I, Permadi N, et al. 2024. The multifaceted roles of Trichoderma in managing rice diseases for enhanced productivity and sustainability. J Agric Food Res, 18: 101324. |
| [41] | Raupach G S, Kloepper J W. 1998. Mixtures of plant growth- promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology, 88(11): 1158-1164. |
| [42] | Seenivasan N, David P M M, Vivekanandan P, et al. 2012. Biological control of rice root-knot nematode, Meloidogyne graminicola through mixture of Pseudomonas fluorescens strains. Biocontrol Sci Technol, 22(6): 611-632. |
| [43] | Shahzad R, Khan A L, Bilal S, et al. 2017. Plant growth-promoting endophytic bacteria versus pathogenic infections: An example of Bacillus amyloliquefaciens RWL-1 and Fusarium oxysporum f.sp. lycopersici in tomato. PeerJ, 5: e3107. |
| [44] | Sharma N, Reinke R, Sacks E J. 2021. Comparison of methods to evaluate rice (Oryza sativa) germplasm for tolerance to low temperature at the seedling stage. Agronomy, 11(2): 385. |
| [45] | Smith L J, Smith M K, Tree D, et al. 2008. Development of a small-plant bioassay to assess banana grown from tissue culture for consistent infection by Fusarium oxysporum f. sp. cubense. Austral Plant Pathol, 37(2): 171-179. |
| [46] | Stegen J C, Lin X J, Konopka A E, et al. 2012. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J, 6(9): 1653-1664. |
| [47] | Sun H W, Xiang X, Li Q, et al. 2021. Comparative genome analysis of Bacillus thuringiensis strain HD521 and HS18-1. Sci Rep, 11(1): 16590. |
| [48] | Sun X L, Xu Z H, Xie J Y, et al. 2022. Bacillus velezensis stimulates resident rhizosphere Pseudomonas stutzeri for plant health through metabolic interactions. ISME J, 16(3): 774-787. |
| [49] | Sun Z B, Yu S F, Hu Y F, Wen Y C. 2022. Biological control of the cucumber downy mildew pathogen Pseudoperonospora cubensis. Horticulturae, 8(5): 410. |
| [50] | Veneklaas E J, Stevens J, Cawthray G R, et al. 2003. Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil, 248: 187-197. |
| [51] | Wang C N, Wu R L, Li Y Y, et al. 2020. Effects of pesticide residues on bacterial community diversity and structure in typical greenhouse soils with increasing cultivation years in Northern China. Sci Total Environ, 710: 136321. |
| [52] | Wang H T, Wu C F, Zhang H Q, Xiao M L, Ge T D, Zhou Z C, Liu Y J, Peng S G, Peng P Q, Chen J P. 2022. Characterization of the belowground microbial community and co-occurrence networks of tobacco plants infected with bacterial wilt disease. World J Microbiol Biotechnol, 38(9): 155. |
| [53] | Wang J W, He Y H, Li T, et al. 2022. Complex biochemical synergistic interactions between two rhizobacteria grown in consortium, Bacillus subtilis SL-44 and Enterobacter hormaechei Wu-15. Rhizosphere, 24: 100587. |
| [54] | Wang J W, Deng Z H, Gao X Z, et al. 2024. Combined control of plant diseases by Bacillus subtilis SL44 and Enterobacter hormaechei Wu15. Sci Total Environ, 934: 173297. |
| [55] | Wang X B, Liang G B. 2014. Control efficacy of an endophytic Bacillus amyloliquefaciens strain BZ6-1 against peanut bacterial Wilt, Ralstonia solanacearum. Biomed Res Int, 2014: 465435. |
| [56] | Wei Z, Gu Y A, Friman V P, et al. 2019. Initial soil microbiome composition and functioning predetermine future plant health. Sci Adv, 5(9): eaaw0759. |
| [57] | Wen T, Xie P H, Penton C R, et al. 2022. Specific metabolites drive the deterministic assembly of diseased rhizosphere microbiome through weakening microbial degradation of autotoxin. Microbiome, 10(1): 177. |
| [58] | Xu X M, Wang Y Q, Lei T, et al. 2022. Synergistic effects of Bacillus amyloliquefaciens SDTB009 and difenoconazole on Fusarium wilt of tomato. Plant Dis, 106(8): 2165-2171. |
| [59] | Xun W B, Li W, Xiong W, et al. 2019. Diversity-triggered deterministic bacterial assembly constrains community functions. Nat Commun, 10(1): 3833. |
| [60] | Xun W B, Liu Y P, Li W, et al. 2021. Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome, 9(1): 35. |
| [61] | Yuan S F, Wang L L, Wu K, Shi J X, Wang M S, Yang X M, Shen Q R, Shen B. 2014. Evaluation of Bacillus-fortified organic fertilizer for controlling tobacco bacterial wilt in greenhouse and field experiments. Appl Soil Ecol, 75: 86-94. |
| [62] | Zhao Y B, Guan D W, Liu X, et al. 2022. Profound change in soil microbial assembly process and co-occurrence pattern in co-inoculation of Bradyrhizobium japonicum 5038 and Bacillus aryabhattai MB35-5 on soybean. Front Microbiol, 13: 846359. |
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