Skip to main content
Log in

Root exudates from two tobacco cultivars affect colonization of Ralstonia solanacearum and the disease index

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

Abstract

The colonization of rhizosphere by microorganisms is directly associated with bacterial growth, chemotaxis, biofilm formation, and the interaction with host plant root exudates. In this study, the responses of Ralstonia solanacearum to the root exudates from two tobacco cultivars (Hongda, susceptible; K326, resistant) were determined. The results showed that the population of R. solanacearum was much higher in the rhizosphere soil of Hongda than in the rhizosphere soil of K326, resulting in a higher disease index for the Hongda treatments (92.73 %). The attraction of R. solanacearum to Hongda root exudates (HRE) was stronger than the response to K326 root exudates (KRE). Four organic acids, oxalic acid, malic acid, citric acid, and succinic acid, from the root exudates were identified and subsequently evaluated. The amount of oxalic acid from HRE was significantly higher than that from KRE. The results also showed that oxalic acid could both significantly induce the chemotactic response and increase the biofilm biomass of R. solanacearum. Both malic acid and citric acid could significantly increase the chemotaxis ability in vitro and the recruitment of R. solanacearum to tobacco root under gnotobiotic conditions. Overall, these data suggested that the colonization of tobacco rhizosphere by pathogenic bacterial strains was influenced by the organic acids secreted from the roots. The results expand our understanding of the roles of root exudates in plant-microbe interactions and will be useful for screening and applying beneficial bacteria for better control of plant wilt diseases.

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

References

  • Bacilio-Jiménez, M., Aguilar-Flores, S., Ventura-Zapata, E., Pérez-Campos, E., Bouquelet, S., & Zenteno, E. (2003). Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil, 249, 271–277.

    Article  Google Scholar 

  • Bais, H. P. (2004). Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol, 134, 307–319.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Beauregard, P. B., Chai, Y., Vlamakis, H., Losick, R., & Kolter, R. (2013). Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci U S A, 110, E1621–E1630.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brencic, A., & Winans, S. C. (2005). Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev, 69, 155–194.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Broeckling, C. D., Broz, A. K., Bergelson, J., Manter, D. K., & Vivanco, J. M. (2008). Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol, 74, 738–744.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cessna, S. G., Sears, V. E., Dickman, M. B., & Low, P. S. (2000). Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell, 12, 2191–2199.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Elphinstone, J., Hennessy, J., Wilson, J., & Stead, D. (1996). Sensitivity of different methods for the detection of Ralstonia solanacearum in potato tuber extracts. EPPO Bull, 26, 663–678.

    Article  Google Scholar 

  • Germida, J., & Siciliano, S. (2001). Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biol Fertil Soils, 33, 410–415.

    Article  Google Scholar 

  • Grayston, S. J., Wang, S., Campbell, C. D., & Edwards, A. C. (1998). Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem, 30, 369–378.

    Article  CAS  Google Scholar 

  • Gupta Sood, S. (2003). Chemotactic response of plant‐growth‐promoting bacteria towards roots of vesicular‐arbuscular mycorrhizal tomato plants. FEMS Microbiol Ecol, 45, 219–227.

    Article  CAS  PubMed  Google Scholar 

  • Hamon, M. A., & Lazazzera, B. A. (2001). The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol, 42, 1199–1209.

    Article  CAS  PubMed  Google Scholar 

  • Hao, W. Y., Ren, L. X., Ran, W., & Shen, Q. R. (2010). Allelopathic effects of root exudates from watermelon and rice plants on Fusarium oxysporum f. sp. niveum. Plant Soil, 336, 485–497.

    Article  CAS  Google Scholar 

  • Hartmann, A., Schmid, M., van Tuinen, D., & Berg, G. (2009). Plant-driven selection of microbes. Plant Soil, 321, 235–257.

    Article  CAS  Google Scholar 

  • Hendrick, C. A., & Sequeira, L. (1984). Lipopolysaccharide-defective mutants of the wilt pathogen Pseudomonas solanacearum. Appl Environ Microbiol, 48, 94–101.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jones, D. L. (1998). Organic acids in the rhizosphere–a critical review. Plant Soil, 205, 25–44.

    Article  CAS  Google Scholar 

  • Kim, K. S., Min, J. Y., & Dickman, M. B. (2008). Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol Plant-Microbe Interact, 21, 605–612.

    Article  CAS  PubMed  Google Scholar 

  • Kourtev, P. S., Ehrenfeld, J. G., & Häggblom, M. (2002). Exotic plant species alter the microbial community structure and function in the soil. Ecology, 83, 3152–3166.

    Article  Google Scholar 

  • Mark, G. L., Dow, J. M., Kiely, P. D., Higgins, H., Haynes, J., Baysse, C., Abbas, A., Foley, T., Franks, A., & Morrissey, J. (2005). Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proc Natl Acad Sci U S A, 102, 17454–17459.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Morgan, J., Bending, G., & White, P. (2005). Biological costs and benefits to plant–microbe interactions in the rhizosphere. J Exp Bot, 56, 1729–1739.

    Article  CAS  PubMed  Google Scholar 

  • Rudrappa, T., Czymmek, K. J., Paré, P. W., & Bais, H. P. (2008). Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol, 148, 1547–1556.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Scherf, J. M., Milling, A., & Allen, C. (2010). Moderate temperature fluctuations rapidly reduce the viability of Ralstonia solanacearum race 3, biovar 2, in infected geranium, tomato, and potato plants. Appl Environ Microbiol, 76, 7061–7067.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schoonbeek, H. J., Jacquat-Bovet, A. C., Mascher, F., & Métraux, J. P. (2007). Oxalate-degrading bacteria can protect Arabidopsis thaliana and crop plants against Botrytis cinerea. Mol Plant-Microbe Interact, 20, 1535–1544.

    Article  CAS  PubMed  Google Scholar 

  • Smalla, K., Wieland, G., Buchner, A., Zock, A., Parzy, J., Kaiser, S., Roskot, N., Heuer, H., & Berg, G. (2001). Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol, 67, 4742–4751.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tan, S., Yang, C., Mei, X., Shen, S., Raza, W., Shen, Q., & Xu, Y. (2013). The effect of organic acids from tomato root exudates on rhizosphere colonization of Bacillus amyloliquefaciens T-5. Appl Soil Ecol, 64, 15–22.

    Article  Google Scholar 

  • Van de Broek, A., Lambrecht, M., & Vanderleyden, J. (1998). Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology, 144, 2599–2606.

    Article  Google Scholar 

  • Walker, T. S., Bais, H. P., Déziel, E., Schweizer, H. P., Rahme, L. G., Fall, R., & Vivanco, J. M. (2004). Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol, 134, 320–331.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whipps, J. M. (2001). Microbial interactions and biocontrol in the rhizosphere. Plant Physiol, 52, 487–511.

    CAS  Google Scholar 

  • Wu, K., Yuan, S., Wang, L., Shi, J., Zhao, J., Shen, B., & Shen, Q. (2014). Effects of bio-organic fertilizer plus soil amendment on the control of tobacco bacterial wilt and composition of soil bacterial communities. Biol Fertil Soils, 50, 961–971.

    Article  Google Scholar 

  • Yao, J., & Allen, C. (2006). Chemotaxis is required for virulence and competitive fitness of the bacterial wilt pathogen Ralstonia solanacearum. J Bacteriol, 188, 3697–3708.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yao, J., & Allen, C. (2007). The plant pathogen Ralstonia solanacearum needs aerotaxis for normal biofilm formation and interactions with its tomato host. J Bacteriol, 189, 6415–6424.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yao, H., & Wu, F. (2010). Soil microbial community structure in cucumber rhizosphere of different resistance cultivars to fusarium wilt. FEMS Microbiol Ecol, 72, 456–463.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, N., Wang, D., Liu, Y., Li, S., Shen, Q., & Zhang, R. (2014). Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil, 374, 689–700.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was financially supported by the projects of the 111 project (B12009), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), the Chinese Ministry of Agriculture (201103004), the National Natural Science Foundation of China (41361075), and the Applied and Basic Research Foundation of Yunnan province (2013FA015).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Biao Shen.

Additional information

Kai Wu and Saifei Yuan are equal to this work.

Highlights

>Root exudates affect chemotaxis and biofilm formation of Ralstonia. >Four organic acids were identified from both two tobacco cultivars. >Organic acids induced the chemotaxis and biofilm formation of Ralstonia. >Report on the stimulation of biofilm formation of Ralstonia by oxalic acid. >Organic acids affect the Ralstonia colonization at rhizosphere.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOC 33 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, K., Yuan, S., Xun, G. et al. Root exudates from two tobacco cultivars affect colonization of Ralstonia solanacearum and the disease index. Eur J Plant Pathol 141, 667–677 (2015). https://doi.org/10.1007/s10658-014-0569-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-014-0569-4

Keywords

Navigation