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

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.

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References

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

    Google Scholar 

  2. 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.

    CAS  Article  Google Scholar 

  3. 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.

    CAS  Article  PubMed  Google Scholar 

  4. 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.

    CAS  Article  Google Scholar 

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

    Google Scholar 

  6. 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.

    CAS  Article  Google Scholar 

  7. 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.

  8. 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.

    CAS  Article  Google Scholar 

  9. 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 

  10. 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 

  11. 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 

  12. 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 

  13. 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 

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

    CAS  Article  Google Scholar 

  15. 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 

  16. 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.

    CAS  Article  Google Scholar 

  17. 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 

  18. 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 

  19. 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.

    CAS  Article  Google Scholar 

  20. 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.

    CAS  Article  PubMed  Google Scholar 

  21. 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 

  22. 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.

    CAS  Article  PubMed  Google Scholar 

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

    Google Scholar 

  24. 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.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 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.

    CAS  Article  Google Scholar 

  26. 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.

  27. 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.

    CAS  Article  Google Scholar 

  28. 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 

  29. 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  Google Scholar 

  30. 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.

    CAS  Article  PubMed  Google Scholar 

  31. 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.

    CAS  Article  Google Scholar 

  32. 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.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 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 

  34. 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 

  35. 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 

  36. 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.

    CAS  Article  Google Scholar 

  37. 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  Google Scholar 

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

    CAS  Article  Google Scholar 

  39. 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 

  40. 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 

  41. 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.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. 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 

  43. 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 

  44. 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 

  45. 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.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. 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 

  47. 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 

  48. 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 

  49. 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  Google Scholar 

  50. 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.

  51. 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.

    CAS  Article  Google Scholar 

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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).

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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.

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Correspondence to Zhengxiong Zhao.

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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 (2021). https://doi.org/10.1007/s10658-021-02237-4

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Keywords

  • Flue-cured tobacco
  • Bacterial wilt
  • Rhizospheric microorganism
  • Disease incidence
  • Carbon sources