Skip to main content
Log in

Isolation and identification of Bacillus and abilities of 3 functional strains to control powdery mildew and promote seedling growth of Malus sieversii

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

To effectively control the powdery mildew (Podosphaera leucotricha) of Malus sieversii (Msi) and promote the growth of Msi seedlings, 170 Bacillus strains (NECC10001-NECC10170) were isolated from 10 Msi tree rhizosphere soils from Xinjiang wild fruit forest, China; 55 Bacillus isolates with typical representative characteristics were identified, including 10 Bacillus species. Owing to their rapid growth and good biocontrol effects, B. velezensis NECC10057 (Bve057), B. amyloliquefaciens NECC10112 (Bam112), and B. subtilis NECC10145 (Bsu145) were selected for further study. Bve057, Bam112, and Bsu145 significantly increased the number of lateral roots and biomass of Msi seedlings. Plant height, fresh weight, and dry weight of Msi treated with Bve057, Bam112, and Bsu145 fermentation broths for 30 d was at least 25%, 11%, and 50% higher, respectively, than that of the control. Treatment with fermentation broths of the three Bacillus strains increased the number of lateral roots, which enhanced water and nutrient absorption and promoted Msi seedling growth. After treatment with Bve057, Bam112, and Bsu145 fermentation broth for 6 d, catalase activity of Msi seedlings reached a peak (> 812.83 µmol/min/g), which was 295% higher than that in the control. Furthermore, the hydrogen peroxide and malondialdehyde content of treated Msi leaves was significantly lower than that of the control. Notably, leaves treated with Bacillus showed open stomata, which improves the photosynthetic rate and protects leaf tissue integrity. Thus, the three Bacillus isolates endow Msi with the ability to resist P. leucotricha by increasing the antioxidant capacity and photosynthetic rate. Thus, Bve057, Bam112, and Bsu145 isolated from Msi tree rhizosphere soils from Xinjiang wild fruit forest promoted Msi growth and enhanced its resistance against powdery mildew.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Data Availability

The data that support the findings of this study are available on request from the corresponding author, [Liu], upon reasonable request.

References

  • Abdelaal, K. (2019). Efficacy of certain bioagents on patho-physiological characters of wheat plants under wheat leaf rust stress. Physiological and Molecular Plant Pathology, 106, 102–108.

    Article  Google Scholar 

  • Chen, L., Liu, Y., Wu, G., Zhang, N., Shen, Q. R., & Zhang, R. F. (2017). Beneficial Rhizobacterium Bacillus amyloliquefaciens SQR9 induces plant salt tolerance through spermidine production. Molecular Plant-Microbe Interactions, 30(5), 423–432.

    Article  CAS  PubMed  Google Scholar 

  • Choi, G., Kim, J., Jang, K., & Lee, D. (2007). Antifungal activities of Bacillus thuringiensis isolates on barley and cucumber powdery mildews. Journal of Microbiology & Biotechnology, 17(12), 2071–2075.

    Google Scholar 

  • Choudhary, D.K., & Johri, B.N. (2009). Interactions of Bacillus spp. and plants--with special reference to induced systemic resistance (ISR). Microbiological Research, 164(5):493–513.

  • Chowdappa, P., Kumar, S. M., Lakshmi, M. J., & Upreti, K. K. (2013). Growth stimulation and induction of systemic resistance in tomato against early and late blight by Bacillus subtilis OTPB1 or Trichoderma harzianum OTPB3. Biology Control, 65(1), 109–117.

    Article  Google Scholar 

  • Devyatkin, V., Mishurov, A., & Kolodina, E. (2021). Probiotic effect of Bacillus subtilis B-2998D, B-3057D, and Bacillus licheniformis B-2999D complex on sheep and lambs. Journal of Advanced Veterinary and Animal Research, 8(1), 146–157.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fan, Z. Y., Miao, C. P., Qiao, X. G., Zheng, Y. K., Chen, H. H., Chen, Y. W., Xu, L. H., Zhao, L. X., & Guan, H. L. (2015). Diversity, distribution, and antagonistic activities of rhizobacteria of Panax notoginseng. Journal of Ginseng Research, 40(2), 97–104.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gajbhiye, A., Rai, A. R., Meshram, S. U., & Dongre, A. B. (2010). Isolation, evaluation and characterization of Bacillus subtilis from cotton rhizospheric soil with biocontrol activity against Fusarium oxysporum. World Journal of Microbiology & Biotechnology, 26(7), 1187–1194.

    Article  CAS  Google Scholar 

  • Guo, R. T., Ji, S. D., Wang, Z. Y., Zhang, H. F., Wang, Y. C., & Liu, Z. H. (2021). Trichoderma asperellum xylanases promote growth and induce resistance in poplar. Microbiological Research, 248(9), 126767.

    Article  CAS  PubMed  Google Scholar 

  • Hafez, Y. M., El-Nagar, A. S., Elzaawely, A. A., Said, K., & Maswada, H. F. (2018). Biological control of Podosphaera xanthii the causal agent of squash powdery mildew disease by upregulation of defense-related enzymes. Egyptian Journal of Biological Pest Control, 28(1), 57.

    Article  Google Scholar 

  • Hong, S. H., & Lee, E. Y. (2014). Vegetation restoration and prevention of coastal sand dunes erosion using ion exchange resins and the plant growth-promoting rhizobacteria Bacillus sp. SH1RP8 isolated from indigenous plants. International Biodeterioration & Biodegradation, 95, 262–269.

    Article  CAS  Google Scholar 

  • Hu, X. J., Roberts, D. P., Xie, L. H., Qin, L., Li, Y. S., Liao, X. S., Han, P. P., Yu, C. B., & Liao, X. (2019). Seed treatment containing Bacillus subtilis BY-2 in combination with other Bacillus isolates for control of Sclerotinia sclerotiorum on oilseed rape. Biological Control, 133, 50–57.

    Article  Google Scholar 

  • Huang, C. J., Liu, Y. H., Yang, K. H., & Chen, C. Y. (2012). Physiological response of Bacillus cereus c1l-induced systemic resistance in lily against botrytis leaf blight. European Journal of Plant Pathology, 134(1), 1–12.

    Article  CAS  Google Scholar 

  • Jiang, Y., Liu, X., Yongjiang, X. U., Shi, B., & Wang, B. (2020). Microbiota characteristics in Sebastes schlegelii in testine inearly life stages. Journal of Oceanology and Limnology, 38(001), 275–287.

    Article  CAS  Google Scholar 

  • Karagoz, K., Ates, F., Kotan, R., Karagöz, H., & Çakmakçı, R. (2012). Characterization of plant growth-promoting traits of bacteria isolated from the rhizosphere of grapevine grown in alkaline and acidic soils. European Journal of Soil Biology, 50, 144–150.

    Article  Google Scholar 

  • Kim, Y.S., Song, J.G., Lee, I.K., Yeo, W.H., & Yun, B.S. (2013). Bacillus sp. BS061 suppresses powdery mildew and gray mold. Mycobiology 41(2), 108–111.

  • Kumar, A. S., Lakshmanan, V., Caplan, J. L., Powell, D., Czymmek, K. J., Levia, D. F., & Bais, H. P. (2012). Rhizobacteria Bacillus subtilis restricts foliar pathogen entry through stomata. Plant Journal for Cell & Molecular Biology, 72(4), 694–706.

    Article  CAS  Google Scholar 

  • Lin, P. Y., & Cui, N. R. (2000). Wild fruit forest resources in Tianshan Mountains-Comprehensive research on wild fruit forests in Ili. M. China Forestry Publishing House.

    Google Scholar 

  • Liu, X. S., Lin, P. J., & Zhong, J. P. (1993). Analysis of habitat for wild fruit forests in Ili and discussion on its occurrence. Arid Zone Res, 3, 28–30.

    Google Scholar 

  • Liu, G. Q., Kong, Y. Y., Fan, Y. J., Geng, C., Peng, D. H., & Sun, M. (2017). Whole-genome sequencing of Bacillus velezensis LS69, a strain with a broad inhibitory spectrum against pathogenic bacteria. Journal of Biotechnology, 249, 20–24.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H., Wang, Z., Xu, W., Zeng, J., & Gao, Z. (2020b). Bacillus pumilus lzp02 promotes rice root growth by improving carbohydrate metabolism and phenylpropanoid biosynthesis. Molecular Plant-Microbe Interactions, 33(10), 1222–1231.

    Article  CAS  PubMed  Google Scholar 

  • Liu, A. H., Zhang, X. P., Wen, J. B., Yue, C. Y., Alimu, J., Zhang, S. P., & Kereman, J. W. (2014). Preliminary research on the composite damage of agrilus mali matsumura and valsa mali miyabe et yamada in wild apple trees in tianshan mountain. Xinjiang Agricultural Sciences., 51(12), 5.

    Google Scholar 

  • Liu, A. H., Shang, J., Zhang, J. W., Kong, T. T., & Wen, J. B. (2018). Canker and fine-root loss of malus sieversii (ldb.) roem. caused by phytophthora plurivora in Xinjiang province in China. Journal of Forest Pathology, 48(6), 1-12.

  • Liu B., Ji S.D., Zhang H. F., Wang Y. C., & Liu Z. H. (2020a) Isolation of Trichoderma in the rhizosphere soil of Syringa oblata from Harbin and their biocontrol and growth promotion function[J]. Microbiological Research, 235:126445.

  • Merrifield, D.L., Bradley, G., Baker, R.T.M., & Davies, S.J. (2010). Probiotic applications for rainbow trout (Oncorhynchus mykiss Walbaum) II. Effects on growth performance, feed utilization, intestinal microbiota and related health criteria postantibiotic treatment. Aquaculture Nutrition, 16(5), 496–503.

  • Narasimhan, A., & Shivakumar, S. (2015). Evaluation of Bacillus subtilis (JN032305) biofungicide to control chilli anthracnose in pot controlled conditions. Biocontrol Science and Technology, 25(5), 543–559.

    Article  Google Scholar 

  • Niu, C. W., Wang, J. R., Zhu, X. Q., Chen, X. Y., & Guo, L. Y. (2016). Brown rot pathogens on stone and pome fruit trees in xinjiang wild forest. Mycosystema, 35, 1514–1525.

    Google Scholar 

  • Proca, I.G., Diguta, C.F., Cornea, C.P., Jurcoane, S., & Matei, F. (2020). Halotolerant Bacillus amyloliquefaciens 24.5 useful as a biological agent to control phytopathogenic fungi. Romanian Biotechnological Letters, 25(4), 1744–1753.

  • Seerat, A. Y., Ookawa, T., Kojima, K., Ohkama-Ohtsu, N., Maeda, M., Djedidi, S., Habibi, S., Sekimoto, H., Abe, A., & Yokoyama, T. (2019). Evaluation of the effects of spores and their heat-treated residues from different Bacillus strains on the initial growth of rice plants. Soil Science and Plant Nutrition, 65(2), 122–136.

    Article  CAS  Google Scholar 

  • Shipley, B., & Meziane, D. (2002). The balanced-growth hypothesis and the allometry of leaf and root biomass allocation. Functional Ecology, 16(3), 326–331.

    Article  Google Scholar 

  • Spotts, R. A. (1984). Infection of Anjou Pear Fruit by Podosphaera leucotricha. Plant Disease, 68(1), 857–859.

    Article  Google Scholar 

  • Tan, T. M., Zhu, J. X., Shen, A. R., Li, J. L., Yu, Y. T., Zhang, M. J., Zhao, M. R., Li, Z. M., Chen, J., Gao, C. S., Cheng, Y., Guo, L. T., Yan, L., Sun, X. P., Zeng, L. B., & Yan, Z. (2018). Isolation and identification of a Bacillus subtilis HZ-72 exhibiting biocontrol activity against flax seedling blight. European Journal of Plant Pathology, 153(3), 825–836.

    Article  Google Scholar 

  • Tanaka, K., Fukuda, M., Amaki, Y., Sakaguchi, T., Inai, K., Ishihara, A., & Nakajima, H. (2017). Importance of prumycin produced by Bacillus amyloliquefaciens SD-32 in biocontrol against cucumber powdery mildew disease. Pest Management Science, 73(12), 2419–2428.

    Article  CAS  PubMed  Google Scholar 

  • Tolba, O., Earle, J., Millar, B., Rooney, P., & Moore, J. (2007). Speciation of Bacillus spp. in honey produced in Northern Ireland by employment of 16S rDNA PCR and automated DNA sequencing techniques. World Journal of Microbiology & Biotechnology, 23(12), 1805–1808.

  • Wu, H. J., Gu, Q., Xie, Y. L., Lou, Z. Y., Xue, P. Q., Fang, L., Yu, C. J., Jia, D. D., Huang, G. C., Zhu, B. C., Schneider, A., Blom, J., Lasch, P., Borriss, R., & Gao, X. W. (2019). Cold-adapted Bacilli isolated from the Qinghai-Tibetan Plateau are able to promote plant growth in extreme environments. Environmental Microbiology, 21(9), 3505–3526.

    Article  CAS  PubMed  Google Scholar 

  • Xu, X. X., Huai, W. X., Hamiti, Zhang, X. C., & Zhao, W. X. (2019). Phytophthora Species from Xinjiang Wild Apple Forests in China. Journal of Forests, 10(10), 927.

  • Xue, X., Bian, C., Guo, X. Y., Di, R., & Dong, J. (2020). The MAPK substrate MASS proteins regulate stomatal development in Arabidopsis. Plos Genetics, 16(4), 1–23.

    Article  Google Scholar 

  • Yan, G., & Xu, Z. (2001). Study on the wild fruit tree diseases of Tianshan mountains and their distribution in Xinjiang. Arid Zone Research, 18, 47–49.

    Google Scholar 

  • Yan, G., Hong, L., Song, W., & Chen, R. (2008). Genetic polymorphism of malus sieversii populations in xinjiang, china. Genetic Resources & Crop Evolution, 55(1), 171–181.

    Article  CAS  Google Scholar 

  • Yoder, K. S. (2000). Effect of powdery mildew on apple yield and economic benefits of its management in virginia. Plant Disease, 84(11), 1171–1176.

    Article  PubMed  Google Scholar 

  • Zhang, H. X., Zhang, M. L., & Wang, L. N. (2015). Genetic structure and historical demography of malus sieversii in the yili valley and the western mountains of the junggar basin, xinjiang, china. Journal of Arid Land, 7(2), 264–271.

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the LiaoNing Revitalization Talents Program (XLYC2002044), the National Natural Science Foundation of China (NSFC:31870627) and Startup Funds of Talent Introduction of Shenyang Agricultural University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhihua Liu.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 15 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

Liu, B., Xu, Y., Ji, S. et al. Isolation and identification of Bacillus and abilities of 3 functional strains to control powdery mildew and promote seedling growth of Malus sieversii. Eur J Plant Pathol 167, 11–24 (2023). https://doi.org/10.1007/s10658-023-02680-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-023-02680-5

Keywords

Navigation