Skip to main content
SpringerLink
Log in

Characterization and evaluation of Bacillus altitudinis BS-4 as a novel potential biocontrol agent against Phytophthora sojae in soybean

  • Original Article
  • Published:
Tropical Plant Pathology Aims and scope Submit manuscript

Abstract

Soybean Phytophthora root rot (PRR) caused by Phytophthora sojae is one of the most devastating diseases of soybean worldwide. This study was conducted to develop new effective biocontrol agents for the control of the disease and explore the action mechanism. Eleven antagonistic bacterial strains against P. sojae were isolated from the soybean field soil samples, and among the strains, BS-4 not only had the strongest inhibitory activity against P. sojae, but also had good inhibition to other four species of oomycetes in Phytophthora and eight fungal pathogens. Based on 16S rDNA sequence analysis and the physiological and biochemical properties, the strain BS-4 was identified as Bacillus altitudinis. Strain BS-4 culture filtrate had significant inhibitory effects on the pathogens, and the inhibition rates were stronger than those in the dual culture. BS-4 filtrate kept a high bioactivity to P. sojae at a high temperature, even at 121℃, and in the pH range of 5 to 12. The germination of zoospores and the formation of sexual organs were seriously affected by BS-4 filtrate. Furthermore, detached leaf assays and greenhouse experiments showed that BS-4 suspension and culture filtrate all had good disease control efficacy, and in the field experiment, BS-4 suspension reduced the disease index and increased the biomass of soybean shoots and roots, significantly (P < 0.05), with control effect of 75.29% on PRR. It is suggested that B. altitudinis strain BS-4 is a novel potential biocontrol agent to control PRR, and will have a broad application prospect in PRR biocontrol.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Arfaoui A, Adam LR, Bezzahou A, Daayf F (2018) Isolation and identification of cultivated bacteria associated with soybeans and their biocontrol activity against Phytophthora sojae. BioControl 63:607–617

    Article  CAS  Google Scholar 

  • Ayoubi N, Zafari D, Mirabolfathy M (2012) Combination of Trichoderma species and Bradyrhizobium japonicum in control of Phytophthora sojae and soybean growth. Journal of Crop Protection 1:67–79

    Google Scholar 

  • Baindara P, Mandal SM, Chawla N, Singh PK, Pinnaka AK, Korpole S (2013) Characterization of two antimicrobial peptides produced by a halotolerant Bacillus subtilis strain SK.DU.4 isolated from a rhizosphere soil sample. AMB Express 3:2–11

    Article  PubMed  PubMed Central  Google Scholar 

  • Baniasadi F, ShahidiBonjar GH, Baghizadeh A, Karimi Nik A (2009) Biological control of Sclerotinia sclerotiorum, causal agent of sunflower head and stem rot disease, by use of soil borne actinomycetes isolates. American Journal of Agricultural and Biological Sciences 4:146–151

    Article  Google Scholar 

  • Ben Ayed H, Hmidet N, Béchet M, Chollet M, Chataigné G, Leclère V, Jacques P, Nasri M (2014) Identification and biochemical characteristics of lipopeptides from Bacillus mojavensis A21. Process Biochemistry 49:1699–1707

    Article  CAS  Google Scholar 

  • Borriss R (2013) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. In: Bruijn FJD (ed) Molecular microbial ecology of the rhizosphere. Wiley Blackwell, Hoboken, pp 883–898

  • Cai M, Miao J, Song X, Lin D, Bi Y, Chen L, Liu X, Tyler B (2016) C239S mutation in the β-tubulin of Phytophthora sojae confers resistance to zoxamide. Frontiers in Microbiology 7:1–10

    Article  Google Scholar 

  • Cao S, Jiang B, Yang G, Pan G, Pan Y, Chen F, Gao Z, Dai Y (2023) Isolation and evaluation of Bacillus subtilis RSS-1 as a potential biocontrol agent against Sclerotinia sclerotiorum on oilseed rape. European Journal of Plant Pathology 166:1–17

    Article  Google Scholar 

  • Chen X, Wang Y (2017) Phytophthora sojae. In: Wan F, Jiang M, Zhan A (eds) Biological Invasions and Its Management in China, 2nd edn. Springer Singapore, Singapore, pp 199–223

    Chapter  Google Scholar 

  • Chida T, Sisler H (1987) Restoration of appressorial penetration ability by melanin precursors in Pyricularia oryzae treated with antipenetrants and in melanin-deficient mutants. Journal of Pesticide Science 12:49–55

    Article  CAS  Google Scholar 

  • Costa A, Corallo B, Amarell V, Stewart S, Pan D, Tiscornia S, Fabiano E (2022) Paenibacillus sp. strain UY79, isolated from a root nodule of Arachis villosa, displays a broad spectrum of antifungal activity. Appl Environ Microbiol 8(2):e01645-21

  • Dorrance AE (2018) Management of Phytophthora sojae of soybean: a review and future perspectives. Canadian Journal of Plant Pathology 40:210–219

    Article  CAS  Google Scholar 

  • Dorrance AE, Berry SA, Anderson TR, Meharg C (2008) Isolation, storage, pathotype characterization, and evaluation of resistance for Phytophthora sojae in soybean. Plant Health Progress 9:35

    Article  Google Scholar 

  • Erwin DC, Ribeiro OK (1996) Phytophthora Diseases Worldwide. APS Press, American Phytopathological Society, St. Paul

    Google Scholar 

  • Falardeau J, Wise C, Novitsky L, Avis TJ (2013) Ecological and mechanistic insights into the direct and indirect antimicrobial properties of Bacillus subtilis lipopeptides on plant pathogens. Journal of Chemical Ecology 39:869–878

    Article  CAS  PubMed  Google Scholar 

  • Farace G, Fernandez O, Jacquens L, Coutte F, Krier F, Jacques P, Clément C, Barka EA, Jacquard C, Dorey S (2015) Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Molecular Plant Pathology 16:177–187

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Bautista N, Domínguez-Núñez JA, Moreno MMC, Berrocal-Lobo M (2016) Plant tissue trypan blue staining during phytopathogen infection. Bio-Protocol 6:e2078

    Article  Google Scholar 

  • Forster H, Tyler BM, Coffey MD (1994) Phytophthora sojae races have arisen by clonal evolution and by rare outcrosses. Molecular Plant-Microbe Interactions 7:780–791

    Article  Google Scholar 

  • Gally M, Ramos AM, Dokmetzian D, Lopez SE (2007) Genetic variability of Phytophthora sojae isolates from Argentina. Mycologia 99:877–883

    Article  CAS  PubMed  Google Scholar 

  • Haas JH, Buzzell RI (1976) New races 5 and 6 of Phytophthora megasperma var. sojae and differential reactions of soybean cultivars for races 1 to 6. Phytopathology 66:1361–1362

    Article  Google Scholar 

  • Han Q, Zhao H, Huang L, Buchenauer H, Zuo Y, Kang Z (2011) Light and electron microscopy studies on the infection of a wild-type and metalaxyl-resistant isolate of Phytophthora sojae in soybean hypocotyls. Journal of Phytopathology 159:368–376

    Article  CAS  Google Scholar 

  • Han Q, Feng H, Zhao H, Huang L, Wang X, Wang X, Kang Z (2013) Effect of a benzothiadiazole on inducing resistance of soybean to Phytophthora sojae. Protoplasma 250:471–481

    Article  CAS  PubMed  Google Scholar 

  • Han X, Shen D, Xiong Q, Bao B, Zhang W, Dai T, Zhao Y, Borriss R, Fan B (2021) The plant-beneficial rhizobacterium Bacillus velezensis FZB42 controls the soybean pathogen Phytophthora sojae due to bacilysin production. Applied and Environmental Microbiology 87:e01601-01621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasan N, Khan IU, Farzand A, Heng Z, Moosa A, Saleem MJ, Canming T (2022) Bacillus altitudinis HNH7 and Bacillus velezensis HNH9 promote plant growth through upregulation of growth-promoting genes in upland cotton. Journal of Applied Microbiology 132:3812–3824

    Article  CAS  PubMed  Google Scholar 

  • Hou J (2012) Biological potential of Pseudomonas sp. BS1 in the control of Phytophthora root rot of soybean. African Journal of Microbiology Research 6:3589–3593

    Google Scholar 

  • Hua C, Wang Y, Zheng X, Dou D, Zhang Z, Govers F, Wang Y (2008) A Phytophthora sojae G-protein alpha subunit is involved in chemotaxis to soybean isoflavones. Eukaryotic Cell 7:2133–2140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jamal Q, Lee Y, Jeon H, Park Y, Kim K (2015) Isolation and biocontrol potential of Bacillus amyloliquefaciens Y1 against fungal plant pathogens. Korean Journal of Soil Science and Fertilizer 48:485–491

    Article  CAS  Google Scholar 

  • Ji SH, Paul NC, Deng JX, Kim YS, Yun B-S, Yu SH (2013) Biocontrol activity of Bacillus amyloliquefaciens CNU114001 against fungal plant diseases. Mycobiology 41:234–242

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones DR, Baker RHA (2007) Introductions of non-native plant pathogens into Great Britain, 1970–2004. Plant Pathology 56:891–910

    Article  Google Scholar 

  • Jourdan E, Henry G, Duby F, Dommes J, Barthélemy JP, Thonart P, Ongena M (2009) Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Molecular Plant-Microbe Interactions 22:456–468

    Article  CAS  PubMed  Google Scholar 

  • Kloepper JW, Ryu C-M, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    Article  CAS  PubMed  Google Scholar 

  • Kushwaha P, Srivastava R, Pandiyan K, Singh A, Chakdar H, Kashyap PL, Bhardwaj AK, Murugan K, Karthikeyan N, Bagul SY, Srivastava AK, Saxena AK (2021) Enhancement in plant growth and zinc biofortification of chickpea (Cicer arietinum L.) by Bacillus altitudinis. Journal of Soil Science and Plant Nutrition 21:922–935

    Article  CAS  Google Scholar 

  • Leclere V, Bechet M, Adam A, Guez JS, Wathelet B, Ongena M, Thonart P, Gancel F, Chollet-Imbert M, Jacques P (2005) Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism’s antagonistic and biocontrol activities. Applied and Environmental Microbiology 71:4577–4584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee KJ, Kamala-Kannan S, Han SS, Seong CK, Lee GW (2007) Biological control of Phytophthora blight in red pepper (Capsicum annuum L.) using Bacillus subtilis. World Journal of Microbiology and Biotechnology 24:1139–1145

    Article  Google Scholar 

  • Li X, Mao Z, Wu Y, Ho H, He Y (2015) Comprehensive volatile organic compounds profiling of Bacillus species with biocontrol properties by head space solid phase microextraction with gas chromatography-mass spectrometry. Biocontrol Science and Technology 25:132–143

    Article  Google Scholar 

  • Lin F, Zhao M, Ping J, Johnson A, Zhang B, Abney S, Hughes T, Ma J (2013) Molecular mapping of two genes conferring resistance to Phytophthora sojae in a soybean landrace PI 567139B. Theoretical and Applied Genetics 126:2177–2185

    Article  CAS  PubMed  Google Scholar 

  • Liu CH, Chen X, Liu TT, Lian B, Gu Y, Caer V, Xue YR, Wang BT (2007) Study of the antifungal activity of Acinetobacter baumannii LCH001 in vitro and identification of its antifungal components. Applied Microbiology and Biotechnology 76:459–466

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Li KY, Hu JL, Wang WY, Liu X, Gao ZM (2019) Biocontrol and action mechanism of Bacillus amyloliquefaciens and Bacillus subtilis in soybean Phytophthora blight. International Journal of Molecular Sciences 20:2908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu X, Zhou D, Chen X, Zhang J, Huang H, Wei L (2017) Isolation and characterization of Bacillus altitudinis JSCX-1 as a new potential biocontrol agent against Phytophthora sojae in soybean [Glycine max (L.) Merr.]. Plant and Soil 416:53–66

    Article  CAS  Google Scholar 

  • Morita T, Tanaka I, Ryuda N, Ikari M, Ueno D, Someya T (2019) Antifungal spectrum characterization and identification of strong volatile organic compounds produced by Bacillus pumilus TM-R. Heliyon 5:e01817

    Article  PubMed  PubMed Central  Google Scholar 

  • Munimbazi C, Bullerman L (1998) Isolation and partial characterization of antifungal metabolites of Bacillus pumilus. Journal of Applied Microbiology 84:959–968

    Article  CAS  PubMed  Google Scholar 

  • Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends in Microbiology 16:115–125

    Article  CAS  PubMed  Google Scholar 

  • Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B, Arpigny J-L, Thonart P (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environmental Microbiology 9:1084–1090

    Article  CAS  PubMed  Google Scholar 

  • Schmitthenner AF (1985) Problems and progress in control of Phytophthora root rot of soybean. Plant Disease 69:362–368

    Article  Google Scholar 

  • Sicuia O, Constantinescu F, Cornea CP (2015) Biodiversity of Bacillus subtilis group and beneficial traits of Bacillus species useful in plant protection. Romanian Biotechnological Letters 20:10737–10750

    Google Scholar 

  • Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Molecular Microbiology 56:845–857

    Article  CAS  PubMed  Google Scholar 

  • Su Y, Shen C (1993) The discovery and biological characteristics studies of Phytophthora megasperma f. sp. glycinea on soybean in China. Acta Phytopathologica Sinica 23:341–347

    Google Scholar 

  • Sugano S, Sugimoto T, Takatsuji H, Jiang CJ (2013) Induction of resistance to Phytophthora sojae in soyabean (Glycine max) by salicylic acid and ethylene. Plant Pathology 62:1048–1056

    Article  CAS  Google Scholar 

  • Suzuki MT, Giovannoni SJ (1996) Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Applied and Environmental Microbiology 62:625–630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tyler BM (2007) Phytophthora sojae: root rot pathogen of soybean and model oomycete. Molecular Plant Pathology 8:1–8

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Mavrodi DV, Ke L, Mavrodi OV, Yang M, Thomashow LS, Na Z, Weller DM, Zhang J (2015) Biocontrol and plant growth-promoting activity of rhizobacteria from Chinese fields with contaminated soils. Microbial Biotechnology 8:403–418

    Article  CAS  Google Scholar 

  • Winnepenninckx B, Backeljau T, de Wachter R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9:407

    Article  CAS  PubMed  Google Scholar 

  • Wrather JA, Koenning SR (2006) Estimates of disease effects on soybean yields in the United States 2003 to 2005. Journal of Nematology 38:173–180

    PubMed  PubMed Central  Google Scholar 

  • Xi X, Fan J, Yang X, Liang Y, Zhao X, Wu Y (2022) Evaluation of the anti-oomycete bioactivity of rhizosphere soil-borne isolates and the biocontrol of soybean root rot caused by Phytophthora sojae. Biological Control 166:104818

    Article  CAS  Google Scholar 

  • Xiao K, Kinkel L, Samac D (2002) Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces. Biological Control 23:285–295

    Article  CAS  Google Scholar 

  • Yang G, Gao Z, Cao S, Jiang T, Wang T (2012) Screening and biocontrol effects of antagonistic bacteria against Phytophthora sojae. Journal of Anhui Agricultural University 39:677–678

    CAS  Google Scholar 

  • Yu S-F, Wang C-L, Hu Y-F, Wen Y, Zhanbin S (2022) Biocontrol of three severe diseases in soybean. Agriculture 12:1391

    Article  CAS  Google Scholar 

  • Zhao B, Lin H, He S (2014) Microbiological Experiment, 2nd edn. Science Press, Beijing

    Google Scholar 

  • Zhao L, Xu Y, Lai X (2018) Antagonistic endophytic bacteria associated with nodules of soybean (Glycine max L.) and plant growth-promoting properties. Brazilian Journal of Microbiology 49:269–278

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Prof. Jingzhi Wen of Northeastern Agricultural University for her kind donation of soybean seeds. And we are thankful to Researcher Zhiping Huang of Anhui Academy of Agricultural Sciences for his help in the soil sample collection.

Funding

This work was financially supported by the National Key R&D Program of China (Grant No. 2018YFD0201000).

Author information

Author notes

  1. Shun Cao and Fangxin Chen contributed equally to this work.

Authors and Affiliations

  1. Anhui Province Key Laboratory of Integrated Pest Management on Crops, College of Plant Protection, Anhui Agricultural University, Hefei, 230036, Anhui, China

    Shun Cao, Fangxin Chen, Yuli Dai, Zhenyu Zhao, Bingxin Jiang, Yuemin Pan & Zhimou Gao

Authors
  1. Shun Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fangxin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuli Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhenyu Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bingxin Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuemin Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhimou Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Shun Cao: conceptualization, methodology, investigation, software, formal analysis, resources, data curation, writing—original draft preparation, writing—review and editing. Fangxin Chen: methodology, investigation, software, validation, formal analysis, writing—original draft preparation. Yuli Dai: investigation, formal analysis. Zhenyu Zhao: investigation, validation. Bingxin Jiang: investigation. Yuemin Pan: resourcese, data curation. Zhimou Gao: conceptualization, writing—review and editing, supervision, project administration. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Zhimou Gao.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 38 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cao, S., Chen, F., Dai, Y. et al. Characterization and evaluation of Bacillus altitudinis BS-4 as a novel potential biocontrol agent against Phytophthora sojae in soybean. Trop. plant pathol. 49, 384–399 (2024). https://doi.org/10.1007/s40858-024-00637-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40858-024-00637-5

Keywords

Search

Navigation