Skip to main content

Advertisement

SpringerLink
Log in

Study on the relationship between bacterial wilt and rhizospheric microbial diversity of flue-cured tobacco cultivars

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

Abstract

Bacterial wilt caused by Ralstonia solanacearum, is one of the serious soil-borne diseases in flue-cured tobacco production areas in China. However, it was found that the occurrence of bacterial wilt not only varied with different cultivars but also varied with various sites even under the condition of planting the same variety. It suggests that the occurrence of bacterial wilt could be controlled by regulating soil microorganism and the growth environment. Therefore, the relationship between microorganism’s diversity in the rhizosphere and actual incidences were evaluated on the number of symptomatic plants and the functional diversity of soil microorganisms in field trials on two sites. The results showed that the incidence of bacterial wilt in the same cultivar was varied between the two experimental sites. However, the same trend was found in the number of rhizospheric microbes among the three varieties except for fungi. Also, a good relationship was found between the number of pathogens, microbial functional diversity in the rhizosphere, and actual incidences. The utilization intensity of carbohydrates, amino acids, carboxylic acids, polymers, amines, and carbon utilization of rhizospheric soil microbial community was negatively related with the occurrence of bacterial wilt while it was on the opposite for the utilization intensity of phenolic acids. The results revealed that the mechanism for resistance in flue-cured tobacco was directly associated with the number of pathogenic microorganisms in rhizosphere and the diversity of rhizospheric microbes. By improving the diversity of rhizospheric microbes, the incidence of tobacco bacterial wilt disease can be reduced.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bao, S. D. (2000). Soil and agricultural chemistry analysis. Beijing, China: China Agricultural University Press.

    Google Scholar 

  • Benitez, M. S., & Gardener, B. B. M. (2009). Linking sequence to function in soil bacteria: Sequence-directed isolation of novel bacteria contributing to soil-borne plant disease suppression. Applied and Environmental Microbiology, 75(4), 915–924.

    Article  CAS  PubMed  Google Scholar 

  • Berendsen, R. L., Pieterse, C. M. J., & Bakker, P. A. H. M. (2012). The rhizosphere microbiome and plant health. Trends in Plant Science, 17(8), 478–486. https://doi.org/10.1016/j.tplants.2012.04.001.

    Article  CAS  PubMed  Google Scholar 

  • Borrero, C., Ordovas, J., Trillas, M. I., & Aviles, M. (2006). Tomato Fusarium wilt suppressiveness. The relationship between the organic plant growth media and their microbial communities as characterized by biolog®. Soil Biology and Biochemistry, 38(7), 1631–1637. https://doi.org/10.1016/j.soilbio.2005.11.017.

    Article  CAS  Google Scholar 

  • Buddenhagen, I. W. (1962). Designations of races in Pseudomonas solanacearum. Phytopathology, 52, 726.

    Google Scholar 

  • Cha, J. Y., Han, S., Hong, H. J., Cho, H., Kim, D., Kwon, Y., Kwon, S. K., Crusemann, M., Lee, Y. B., Kim, J. F., & Giaever, G. (2016). Microbial and biochemical basis of a Fusarium wilt suppressive soil. The ISME Journal, 10(1), 119–129.

    Article  CAS  PubMed  Google Scholar 

  • Channel, I, P. (2013). General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China. doi: https://doi.org/10.3389/fmicb.2020.00701, 11.

  • Dong, Y., Dong, K., Tang, L., Zheng, Y., Yang, Z. X., Xiao, J. X., Zhao, P., & Hu, G. B. (2013). Relationship between rhizosphere microbial community functional diversity and faba bean fusarium wilt occurrence in wheat and faba bean intercropping system. Acta Ecologica Sinica, 33(23), 7445–7454.

    Article  CAS  Google Scholar 

  • Dou, Y. Q., Li, D. F., Gu, Y. M., Fen, K., Yin, H. H., Lu, X. H., & Zhang, Z. F. (2017). Screening of flue-cured tobacco varieties with highly resistance to bacterial wilt in Wenshan prefecture. Guangdong Agricultural Sciences, 44(6), 90–95 (In Chinese, with English summary).

    Google Scholar 

  • Duan, Y. P., Liang, M., & Qin, X. Y. (2008). Pathogen identification of Ralstonia solanacearum E. F Smith on tobacco and its occurrence in Baoshan. Chinese Tobacco Science, 29(05), 48–51 (in Chinese, with English summary).

    Google Scholar 

  • Elphinstone, J., & G. (2005). The current bacterial wilt situation: A global overview (pp. 9–28). Minnesota USA: Bacterial wilt disease and the Ralstonia solanacearum species complex. APS press.

    Google Scholar 

  • Hao, W. Y., Shen, Q. R., Ran, W., Xu, Y. C., & Ren, L. X. (2011). The effects of exudates sugars and amino acids in watermelon and rice root exudates on the growth of Fusarium oxysporum f.sp. niveum. Journal of Nanjing Agriculture University, 34, 77–82.

    CAS  Google Scholar 

  • He, Y., & Xue, L. (2005). Biological effects of rare earth elements and their action mechanisms. Ying yong sheng tai xue bao. The Journal of Applied Ecology, 16(10), 1983–1989.

    CAS  Google Scholar 

  • Guo, M. (2009). Soil sampling and methods of analysis. Journal of Environmental Quality, 38(1), 375–375.

    Article  CAS  Google Scholar 

  • Irikiin, Y., Nishiyama, M., Otsuka, S., & Senoo, K. (2006). Rhizobacterial community level, sole carbon source utilization pattern affects the delay in the bacterial wilt of tomato grown in rhizobacterial community model system. Applied Soil Ecology, 34(1), 27–32.

    Article  Google Scholar 

  • Janvier, C., Villeneuve, F., Alabouvette, C., Edel-Hermann, V., Mateille, T., & Steinberg, C. (2007). Soil health through soil disease suppression: Which strategy from descriptors to indicators? Soil Biology and Biochemistry, 39(1), 1–23. https://doi.org/10.1016/j.soilbio.2006.07.001.

    Article  CAS  Google Scholar 

  • Kelman, A. (1998). One hundred and one years of research on bacterial wilt. In bacterial wilt disease (pp. 1–5). Berlin, Heidelberg: Springer.

    Google Scholar 

  • Kim, B. S., French, E., Caldwell, D., Harrington, E. J., & Iyer-Pascuzzi, A. S. (2016). Bacterial wilt disease: Host resistance and pathogen virulence mechanisms. Physiological and Molecular Plant Pathology, 95, 37–43. https://doi.org/10.1016/j.pmpp.2016.02.007.

    Article  Google Scholar 

  • Larkin, R. P. (2003). Characterization of soil microbial communities under different potato cropping systems by microbial population dynamics, substrate utilization, and fatty acid profiles. Soil Biology and Biochemistry, 35(11), 1451–1466.

    Article  CAS  Google Scholar 

  • Lebeau, A., Daunay, M. C., Frary, A., Palloix, A., Wang, J. F., Dintinger, J., & Prior, P. (2011). Bacterial wilt resistance in tomato, pepper, and eggplant: Genetic resources respond to diverse strains in the Ralstonia solanacearum species complex. Phytopathology, 101(1), 154–165. https://doi.org/10.1094/phyto-02-10-0048.

    Article  CAS  PubMed  Google Scholar 

  • Li, S., Liu, K., & Liao, Z. (2010). Method for simplification of characteristic carbon sources for biolog analysis of soil microbial community and its application. Scientia Agricultura Sinica, 43(3), 523–528.

    CAS  Google Scholar 

  • Li, Y., Feng, J., Liu, H., Wang, L., Hsiang, T., Li, X., & Huang, J. (2016). Genetic diversity and pathogenicity of Ralstonia solanacearum causing tobacco bacterial wilt in China. Plant Disease, 100(7), 1288–1296. https://doi.org/10.1094/pdis-04-15-0384-re.

    Article  CAS  PubMed  Google Scholar 

  • Liu, X. G. (2010). Soil microbial research principles and methods. Beijing: Higher Education. Press (In Chinese).

    Google Scholar 

  • Liu, L., Sun, C., Liu, S., Chai, R., Huang, W., Liu, X., & Zhang, Y. (2015). Bioorganic fertilizer enhances soil suppressive capacity against bacterial wilt of tomato. PLoS One, 10(4), e0121304. https://doi.org/10.1371/journal.pone.0121304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, Y., Wu, D., Liu, Q., Zhang, S., Tang, Y., Jiang, G., Li, S., & Ding, W. (2017). The sequevar distribution of Ralstonia solanacearum in tobacco growing zones of China is structured by elevation. European Journal of Plant Pathology, 147(3), 541–551.

    Article  CAS  Google Scholar 

  • Lukyanenko, A, N. (1991). Disease resistance in tomato. Monographs on theoretical and applied Genetics, 99–119. doi:https://doi.org/10.1007/978-3-642-84275-7_9.

  • Luo, H. F., Qi, H. Y., & Zhang, H. X. (2004). Assessment of the bacterial diversity in fenvalerate-treated soil. World Journal of Microbiology and Biotechnology, 20(5), 509–515. https://doi.org/10.1023/b:wibi.0000040401.46606.a4.

    Article  CAS  Google Scholar 

  • Ma, L., Zhang, H. Y., Zhou, X. K., Yang, C. G., Zheng, S. C., Duo, J. L., & Mo, M. H. (2018). Biological control tobacco bacterial wilt and black shank and root colonization by bio-organic fertilizer containing bacterium Pseudomonas aeruginosa NXHG29. Applied Soil Ecology, 129, 136–144. https://doi.org/10.1016/j.apsoil.2018.05.011.

    Article  Google Scholar 

  • Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., & Foster, G. D. (2012). Top 10 plant pathogenic bacteria in molecular plant pathology. Molecular Plant Pathology, 13(6), 614–629.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mendes, R., Garbeva, P., & Raaijmakers, J. M. (2013). The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiology Reviews, 37(5), 634–663. https://doi.org/10.1111/1574-6976.12028.

    Article  CAS  PubMed  Google Scholar 

  • Moynihan, J. A., Morrissey, J. P., Coppoolse, E. R., Stiekema, W. J., O'Gara, F., & Boyd, E. F. (2009). Evolutionary history of the phl gene cluster in the plant-associated bacterium Pseudomonas fluorescens. Applied and Environmental Microbiology, 75(7), 2122–2131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penton, C. R., Gupta, V. V. S. R., Tiedje, J. M., Neate, S. M., Ophel-Keller, K., Gillings, M., & Roget, D. K. (2014). Fungal community structure in disease suppressive soils assessed by 28S LSU gene sequencing. PLoS One, 9(4), e93893. https://doi.org/10.1371/journal.pone.0093893.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reed, T. D., Johnson, C. S., Semtner, P. J., & Wilkinson, C. A. (2011). Flue-cured tobacco production guide, 2012. Blacksburg, VA: Virginia Cooperative Extension.

    Google Scholar 

  • Shao, L., Jin, Y., & Yang, Y. H. (2002). Influences of ecological conditions on the yield and quality of different flue-cured cultivars. Tobacco Science & Technology, 10, 40–45.

    Google Scholar 

  • Smith, E. F. (1908). The Granville tobacco wilt, by Erwin F. Smith, US Government Printing Office. U.S. Dept Agric bur plant Ind bull (part II), 141, 17–24.

    Google Scholar 

  • Sofo, A., & Ricciuti, P. (2019). A standardized method for estimating the functional diversity of soil bacterial community by biolog® EcoPlatesTM assay—The case study of a sustainable olive orchard. Applied Sciences, 9(19), 4035.

    Article  CAS  Google Scholar 

  • Tang, Z., Chen, L., Chen, Z., Fu, Y., Sun, X., Wang, B., & Xia, T. (2020). Climatic factors determine the yield and quality of Honghe flue-cured tobacco. Scientific Reports, 10(1), 1–12.

    Article  CAS  Google Scholar 

  • Thies, J. E. (2007). Soil microbial community analysis using terminal restriction fragment length polymorphisms. Soil Science Society of America Journal, 71(2), 579–591.

    Article  CAS  Google Scholar 

  • Van Elsas, J. D., Garbeva, P., & Salles, J. (2002). Effects of agronomical measures on the microbial diversity of soils as related to the suppression of soil borne plant pathogens. Biodegradation, 13(1), 29–40. https://doi.org/10.1023/a:1016393915414.

    Article  PubMed  Google Scholar 

  • Wang, G., Yang, H., Zhao, Z., Li, F., & Yi, J. (2012). Microbe quantity and functional diversity in rhizospheres of different flue-cured tobacco cultivars. Plant Nutrition and Fertilizer Science, 18(2), 451–458.

    Google Scholar 

  • Wang, R., Zhang, H., Sun, L., Qi, G., Chen, S., & Zhao, X. (2017). Microbial community composition is related to soil biological and chemical properties and bacterial wilt outbreak. Scientific Reports, 7(1), 343. https://doi.org/10.1038/s41598-017-00472-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, H., Li, J., Xiao, Y., Gu, Y., Liu, H., Liang, Y., & Yin, H. (2017). An integrated insight into the relationship between soil microbial community and tobacco bacterial wilt disease. Frontiers in Microbiology, 8(2179), 8.

    Google Scholar 

  • Yi, Y. J., Liu, R. S., Yin, H. Q., Luo, K., Liu, E. M., & Liu, X. D. (2007). Isolation, identification and field control efficacy of an endophytic strain against tobacco bacterial wilt (Ralstonia solanacarum). Ying Yong Sheng Tai Xue Bao, 18, 554–558.

    CAS  PubMed  Google Scholar 

  • Yuan, Y., Li, M., Hu, W., Zhang, J., Zhao, L., & Li, H. (2011). Effects of biological organic fertilizer on tomato bacterial wilt and soil microorganisms. Journal of Agro-Environment Science, 30(7), 1344–1350.

    CAS  Google Scholar 

  • Yuliar, N., Yanetri, A., & Toyota, K. (2015). Recent trends in control methods for bacterial wilt diseases caused by Ralstonia solanacearum. Microbes and Environments, 30(1), 1–11. https://doi.org/10.1264/jsme2.me14144.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhan, F. D., Lu, Y. G., & Guan, G. J. (2005). Community structures of microorganisms and their dynamics in the rhizosphere of flue-cured tobacco. Acta Pedologica Sinica, 42(03), 488–494 (in Chinese, with English summary).

    Google Scholar 

  • Zhang, X. D., Cao, H., Xu, D. Q., Jin, Y. F., & Chen, Y. K. (2008). Effects of photosynthetic bacteria and organic fertilizer on soil microorganisms and soil enzyme activities. Soils, 40(3), 443–447.

    CAS  Google Scholar 

  • Zhang, Z., Feng, H., Xiao, X., & Li, H. (2010). Influence of bio-fertilizers on control of banana wilt disease and soil microbial diversity. Journal of Fruit Science, 27(4), 575–579.

    CAS  Google Scholar 

  • Zhang, J., Wei, L., Yang, J., Ahmed, W., Wang, Y., Fu, L., & Ji, G. (2020). Probiotic consortia: Reshaping the rhizospheric microbiome and its role in suppressing root-rot disease of Panax notoginseng. Frontiers in Microbiology, 11, 701.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou, X. J., Wang, J., Yang, Y. W., Zhao, T. C., & Gao, B. D. (2012a). Advances in tobacco bacterial wilt disease. Microbiology/Weishengwuxue Tongbao, 39(10), 1479–1486.

  • Zhou, T., Chen, D., Li, C., Sun, Q., Li, L., Liu, F., et al. (2012b). Isolation and characterization of Pseudomonas brassicacearum J12 as an antagonist against Ralstonia solanacearum and identification of its antimicrobial components. Microbiological research, 167(7), 388–394.

    Article  CAS  PubMed  Google Scholar 

Download references

Availability of data and material

This material is the authors’ own original work, which has not been previously published elsewhere and have no conflict of interest.

Funding

This study was financially supported by Yunnan Agricultural University Scientific Research Foundation (KX900187), Key Research and Development Program of Yunnan Province, China (2018BB019), and the Key Science and Technology Program of Yunnan Tobacco Company, China (2017YN06, 2018530000241017).

Author information

Author notes

  1. Qiuhua Cai, Guisu Zhou and Waqar Ahmed contributed equally to this work.

Authors and Affiliations

  1. College of Tobacco Science, Yunnan Agricultural University, Kunming, 650201, Yunnan, China

    Qiuhua Cai, Guisu Zhou & Meiwei Zhao

  2. Key Laboratory of Agriculture Biodiversity for Plant Disease Management Under the Ministry of Education, Yunnan Agricultural University, Kunming, 650201, Yunnan, China

    Waqar Ahmed

  3. College of Resources and Envirnomental Sciences, Yunnan Agricultural University, Kunming, 650201, Yunnan, China

    Waqar Ahmed & Zhengxiong Zhao

  4. Smeal College, Pennsylvania State University, University Park, PA16802, USA

    Yuying Cao

  5. Kunming Tobacco Company, Kunming, 650000, Yunnan, China

    Zhonghuan Li

Authors
  1. Qiuhua Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guisu Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Waqar Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuying Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Meiwei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhonghuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhengxiong Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ZZ conceived and designed the experiments. QC, GZ, YC and MZ performed the experiments. QC, GZ and WA analyzed the data. ZZ and ZL contributed reagents, materials and analysis tools. QC, GZ and WA wrote the manuscript. All authors contributed to the final draft of the manuscript.

Corresponding author

Correspondence to Zhengxiong Zhao.

Ethics declarations

Ethical statement

The paper reflects the authors’ own research and analysis in a truthful and complete manner. All authors have been personally and actively involved in substantial work leading to the paper, and will take public responsibility for its content.

Consent to participate

All authors have been personally and actively involved in substantive work leading to the manuscript and contributed in the preparation of final draft of the manuscript.

Consent for publication

The manuscript has not been published in whole or in part elsewhere, and is not currently being considered for publication in another journal. All the authors seen the final version of manuscript.

Conflict of interest

The authors declare that they have no conflicts of interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cai, Q., Zhou, G., Ahmed, W. et al. Study on the relationship between bacterial wilt and rhizospheric microbial diversity of flue-cured tobacco cultivars. Eur J Plant Pathol 160, 265–276 (2021). https://doi.org/10.1007/s10658-021-02237-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-021-02237-4

Keywords

Search

Navigation