SpringerLink
Log in

Phylogenetic analysis and molecular signatures specific to the Ralstonia solanacearum species complex

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

Abstract

Ralstonia solanacearum species complex is a highly destructive bacterial plant pathogen recognized as a group of genotypically-diverse strains with broad geographic distribution and wide host range. Strains are divided into four phylotypes (I, II, III and IV) relating to their geographical origins. Based on the polyphasic approach, phylotypes I and III have been reclassified as R. pseudosolanacearum, phylotype IV as R. syzygii species and phylotype II as R. solanacearum. The large data sets of whole genome sequences for the members of R. solanacearum allow us to discover novel molecular markers to evaluate the phylogenetic relationships within this species. In the phylogenetic tree based on concatenated amino acid sequences of 57 housekee** genes, members of R. solanacearum species complex formed strongly supported clades that clearly distinguished as R. solanacearum, R. pseudosolanacearum and R. syzygii species. In this study, the conserved signature indels (CSIs) which are specifically present in protein sequences and can be used to differentiate various groups of Ralstonia species are reported. Comparative analysis of whole protein sequences from the three species has identified seven CSIs that are specific to R. solanacearum (phylotype II), 6 CSIs specific to R. pseudosolanacearum strains (phylotype I and III) and five CSIs that are specifically shared by members of R. syzygii (phylotype IV). These CSIs are flanked by conserved sequence regions, providing highly specific tools for identification of previously known or novel strains of these species.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

References

  • Adeolu, M., Alnajar, S., Naushad, S., & Gupta, R. S. (2016). Genome-based phylogeny and taxonomy of the 'Enterobacteriales': proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. International Journal of Systematic and Evolutionary Microbiology, 66, 5575–5599.

    Article  CAS  PubMed  Google Scholar 

  • Buddenhagen, I. (1986). Bacterial wilt revisited. In G. J. Persley (Ed.), Bacterial wilt disease in Asia and the South Pacific (pp. 126–143). Canberra: ACIAR.

    Google Scholar 

  • Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.

    Article  CAS  PubMed  Google Scholar 

  • Cellier, G., Remenant, B., Chiroleu, F., Lefeuvre, P., & Prior, P. (2012). Phylogeny and population structure of brown rot- and moko disease-causing strains of Ralstonia solanacearum phylotype II. Applied and Environmental Microbiology, 78, 2367–2375.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Comas, I., Moya, A., & Gonzales-Candelas, F. (2007). Phylogenetic signal and functional categories in Proteobacteria genomes. BMC Evolutionary Biology, 7, S7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cook, D., & Sequeira, L. (1994). Strain differentiation of Pseudomonas solanacearum by molecular genetic methods. In A. C. Hayward & G. L. Hartman (Eds.), Bacterial wilt, the disease and its causative agent, Pseudomonas solanacearum (pp. 77–93). Wallingford: CAB International.

    Google Scholar 

  • Cook, D., Barlow, E., & Sequeira, L. (1989). Genetic diversity of Pseudomonas solanacearum: Detection of restriction fragment length polymorphisms with DNA probes that specify virulence and the hypersensitive response. Molecular Plant-Microbe Interactions, 2, 113–121.

    Article  Google Scholar 

  • Fegan, M., & Prior, P. (2005). How complex is the Ralstonia solanacearum species complex. In C. Allen, P. Prior, & A. C. Hayward (Eds.), Bacterial wilt disease and the Ralstonia solanacearum species complex (pp. 449–462). St. Paul: APS Press.

    Google Scholar 

  • Fegan, M., Taghavi, M., Sly, L. I., & Hayward, A. C. (1998). Phylogeny, diversity and molecular diagnostics of Ralstonia solanacearum. In P. Prior, C. Allen, & J. Elphinstone (Eds.), Bacterial wilt disease: Molecular and ecological aspects (pp. 19–33). Paris: INRA Editions.

    Chapter  Google Scholar 

  • Gil, R., Silva, F. J., Peretó, J., & Moya, A. (2004). Determination of the core of a minimal bacterial gene set. Microbiology and Molecular Biology Reviews, 68, 518–537.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gillings, M., & Fahy, P. (1994). Genomic fingerprinting: Toward a unified view of the Pseudomonas solanacearum species complex. In A. C. Hayward & G. L. Hartmann (Eds.), Bacterial wilt: The disease and its causative agent, Pseudomonas solanacearum (pp. 95–112). Wallingford: CAB International.

    Google Scholar 

  • Gillings, M., Fahy, P., & Davies, C. (1993). Restriction analysis of an amplified polygalacturonase gene fragment differentiates strains of the phytopathogenic bacterium Pseudomonas solanacearum. Letters in Applied Microbiology, 17, 44–48.

    Article  CAS  PubMed  Google Scholar 

  • Greecy, M. R., Albuquerque, L. A., Santos, K. C. S., et al. (2014). Moko disease-causing strains of Ralstonia solanacearum from Brazil extend known diversity in paraphyletic phylotype II. Phytopathology, 104, 1175–1182.

    Article  Google Scholar 

  • Griffiths, E., & Gupta, R. S. (2006). Molecular signatures in protein sequences that are characteristics of the phylum Aquificae. International Journal of Systematic and Evolutionary Microbiology, 56, 99–107.

    Article  CAS  PubMed  Google Scholar 

  • Gupta, R. S. (2014). Identification of conserved indels that are useful for classification and evolutionary studies. In M. Goodfellow, I. Sutcliffe, & J. Chun (Eds.), Methods in microbiology: New approaches to prokaryotic systematics (pp. 153–182). Oxford: Academic Press.

    Chapter  Google Scholar 

  • Gupta, R. S. (2016). Impact of genomics on the understanding of microbial evolution and classification: the importance of Darwin,s views on classification. FEMS Microbiology Reviews, 40, 520–553.

    Article  CAS  PubMed  Google Scholar 

  • Hayward, A. C. (1991). Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annual Review of Phytopathology, 29, 67–87.

    Article  Google Scholar 

  • Hayward, A. C. (1994). The hosts of Pseudomonas solanacearum. In A. C. Hayward & G. L. Hartmann (Eds.), Bacterial wilt: The disease and its causative agent, Pseudomonas solanacearum (pp. 9–24). Wallingford: CAB International.

    Google Scholar 

  • Horita, M., & Tsuchiya, K. (2001). Genetic diversity of Japanese strains of Ralstonia solanacearum. Phytopathology, 91, 399–407.

    Article  CAS  PubMed  Google Scholar 

  • Jeong, Y., Kim, J., Kang, Y., Lee, S., & Hwang, I. (2007). Genetic diversity and distribution of Korean isolates of Ralstonia solanacearum. Plant Disease, 91, 1277–1287.

    Article  CAS  PubMed  Google Scholar 

  • Lefeuvre, P., Cellier, G., Remenant, B., Chiroleu, F., & Prior, P. (2013). Constraints on genome dynamics revealed from gene distribution among the Ralstonia solanacearum species. PLoS One, 8, e63155.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mansfield, J., Genin, S., Magori, S., Citovsky, V., et al. (2012). Top 10 plant pathogenic bacteria in molecular plant pathology. Molecular Plant Pathology, 13, 614–629.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moriuchi, R., Dohra, H., Kanesaki, Y., & Ogawa, N. (2019). Complete genome sequence of 3-chlorobenzoate-degrading bacterium Cupriavidus necator NH9 and reclassification of the strains of the genera Cupriavidus and Ralstonia based on phylogenetic and whole-genome sequence analyses. Frontiers in Microbiology, 10, 133.

    Article  PubMed  PubMed Central  Google Scholar 

  • N’Guessan, C. A., Brisse, S., Le Roux-Nio, A. C., Poussier, S., et al. (2013). Development of variable number of tandem repeats ty** schemes for Ralstonia solanacearum, the agent of bacterial wilt, banana Moko disease and potato brown rot. Journal of Microbiological Methods, 92, 366–374.

    Article  PubMed  Google Scholar 

  • Naushad, H. S., & Gupta, R. S. (2013). Phylogenomics and molecular signatures for species from the plant pathogen-containing order Xanthomonadales. PLoS One, 8, e55612.

    Article  Google Scholar 

  • Naushad, H. S., Lee, B., & Gupta, R. S. (2014). Conserved signature indels and signature proteins as novel tools for understanding microbial phylogeny and systematics: Identification of molecular signatures that are specific for the phytopathogenic genera Dickeya, Pectobacterium and Brenneria. International Journal of Systematic and Evolutionary Microbiology, 64, 366–383.

    Article  CAS  PubMed  Google Scholar 

  • Nouri, S., Bahar, M., & Fegan, M. (2009). Diversity of Ralstonia solanacearum causing potato bacterial wilt in Iran and the first record of phylotype II/biovar 2T strains outside South America. Plant Pathology, 58, 243–249.

    Article  Google Scholar 

  • Poussier, S., Prior, P., Luisetti, J., Hayward, C., & Fegan, M. (2000). Partial sequencing of the hrpB and endoglucanase genes confirms and expands the known diversity within the Ralstonia solanacearum species complex. Systematic and Applied Microbiology, 23, 479–486.

    Article  CAS  PubMed  Google Scholar 

  • Prior, P., Ailloud, F., Dalsing, B. L., Remenant, B., Sanchez, B., & Allen, C. (2016). Genomic and proteomic evidence supporting the division of the plant pathogen Ralstonia solanacearum into three species. BMC Genomics, 17, 90.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ravelomanantsoa, S., Robène, I., Chiroleu, F., Guérin, F., Poussier, S., Pruvost, O., & Prior, P. (2016). A novel multilocus variable number tandem repeat analysis ty** scheme for African phylotype III strains of the Ralstonia solanacearum species complex. PeerJ., 4, e1949.

    Article  PubMed  PubMed Central  Google Scholar 

  • Remenant, B., Coupat-Goutaland, B., Guidot, A., Cellier, G., et al. (2010). Genomes of three tomato pathogens within the Ralstonia solanacearum species complex reveal significant evolutionary divergence. BMC Genomics, 11, 379.

    Article  PubMed  PubMed Central  Google Scholar 

  • Remenant, B., de Cambiaire, J. C., Cellier, G., Jacobs, J. M., et al. (2011). Ralstonia syzygii, the Blood disease bacterium and some Asian R. solanacearum strains form a single genomic species despite divergent lifestyles. PLoS One, 6, e24356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Safni, I., Cleenwerck, I., De Vos, P., Fegan, M., Sly, L., & Kappler, U. (2014). Polyphasic taxonomic revision of the Ralstonia solanacearum species complex: proposal to emend the descriptions of Ralstonia solanacearum and Ralstonia syzygii and reclassify current R. syzygii strains as Ralstonia syzygii subsp. syzygii subsp. nov., R. solanacearum phylotype IV strains as Ralstonia syzygii subsp. indonesiensis subsp. nov., banana blood disease bacterium strains as Ralstonia syzygii subsp. celebesensis subsp. nov. and R. solanacearum phylotype I and III strains as Ralstonia pseudosolanacearum sp. nov. International Journal of Systematic and Evolutionary Microbiology, 64, 3087–3103.

    Article  CAS  PubMed  Google Scholar 

  • Safni, I., Subandiyah, S., & Fegan, M. (2018). Ecology, epidemiology and disease management of Ralstonia syzygii in Indonesia. Frontiers in Microbiology, 9, 419.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sawana, A., Adeolu, M., & Gupta, R. S. (2014). Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Frontiers in Genetics, 5, 429.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whelan, S., & Goldman, N. (2001). A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Molecular Biology and Evolution, 18, 691–699.

    Article  CAS  PubMed  Google Scholar 

  • Wicker, E., Lefeuvre, P., de Cambiaire, J. C., Lemaire, C., et al. (2012). Contrasting recombination patterns and demographic histories of the plant pathogen Ralstonia solanacearum inferred from MLSA. International Society for Microbial Ecology Journal, 6, 961–974.

    CAS  Google Scholar 

  • Zhang, Y., & Qiu, S. (2016). Phylogenomic analysis of the genus Ralstonia based on 686 single-copy genes. Antonie Van Leeuwenhoek, 109, 71–82.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This research study was supported by the University of Kurdistan, Iran.

Author information

Authors and Affiliations

  1. Department of Plant Protection, Faculty of Agriculture, University of Kurdistan, Sanandaj, Iran

    F. Etminani, M. Yousefvand & B. Harighi

Authors
  1. F. Etminani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Yousefvand
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. Harighi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B. Harighi.

Ethics declarations

Conflict of interest

We have no conflict of interest to declare.

Research involving human participants and/or animals

We declare that no human or animal were involved during the research.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Ethical statement for European journal of plant pathology

I testify on behalf of all co-authors that our article submitted to European journal of plant pathology. All authors have been personally and actively involved in substantive work leading to the manuscript, and will hold themselves jointly and individually responsible for its content.

Electronic supplementary material

ESM 1

(PDF 369 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Etminani, F., Yousefvand, M. & Harighi, B. Phylogenetic analysis and molecular signatures specific to the Ralstonia solanacearum species complex. Eur J Plant Pathol 158, 261–279 (2020). https://doi.org/10.1007/s10658-020-02073-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-020-02073-y

Keywords

Search

Navigation