Skip to main content
Log in

Genomic sequencing globally identifies functional genes and potential virulence-related effectors of Xanthomonas axonopodis pv. malvacearum

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

Abstract

Highly virulent strains (HVS) of Xanthomonas axonopodis pathovar (pv.) malvacearum (Xam) infect all commercial cultivars of cotton, including the long-established “immune” cultivar 101-102B. Here, we present high-quality draft sequences of a highly virulent Xam strain (GSPB2388) from Sudan, and a strain of race 18 (GSPB1386) from Nicaragua, using Illumina/Solexa paired-end sequencing. The short sequence reads were assembled into 61 scaffolds for GSPB2388 (N50 of 164 kb) and 127 scaffolds for GSPB1386 (N50 of 100 kb), with draft maps of roughly 5 Mb, which contain 4,665 and 4,520 protein-coding genes, respectively. Through gene annotation and comparisons with plant pathogen proteins, 181 and 178 potential virulence-related genes, including genes encoding a major group of type III effectors, were identified from GSPB2388 and GSPB1386, respectively. The differential effectors and sequence diversity between the HVS and race 18 may enable the identification of key factors that contribute to the high virulence of HVS. Additionally, the average nucleotide identity (ANI) between Xam and Xanthomonas axonopodis pv. citri is 98.4 %, suggesting that these strains belong to the same species.

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

References

  • Bart, R., Cohn, M., Kassen, A., McCallum, E. J., Shybut, M., Petriello, A., et al. (2012). High-throughput genomic sequencing of cassava bacterial blight strains identifies conserved effectors to target for durable resistance. Proceedings of the National Academy of Sciences of the United States of America, 109(28), E1972–E1979.

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarty, P. K., Duan, Y. P., & Gabriel, D. W. (1997). Cloning and characterization of a member of the Xanthomonas avr/pth gene family that evades all commercially utilized cotton R genes in the United States. Phytopathology, 87(11), 1160–1167.

    Article  PubMed  CAS  Google Scholar 

  • Chitsaz, H., Yee-Greenbaum, J. L., Tesler, G., Lombardo, M. J., Dupont, C. L., Badger, J. H., et al. (2011). Efficient de novo assembly of single-cell bacterial genomes from short-read data sets. Nature Biotechnology, 29(10), 915–921. doi:10.1038/nbt.1966.

    Article  PubMed  CAS  Google Scholar 

  • da Silva, A. C., Ferro, J. A., Reinach, F. C., Farah, C. S., Furlan, L. R., Quaggio, R. B., et al. (2002). Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature, 417(6887), 459–463.

    Article  PubMed  Google Scholar 

  • De Feyter, R., Yang, Y., & Gabriel, D. W. (1993). Gene-for-genes interactions between cotton R genes and Xanthomonas campestris pv. malvacearum avr genes. Molecular Plant-Microbe Interactions, 6(2), 225–237.

    Article  PubMed  Google Scholar 

  • Delannoy, E., Lyon, B. R., Marmey, P., Jalloul, A., Daniel, J. F., Montillet, J. L., et al. (2005). Resistance of cotton towards Xanthomonas campestris pv. malvacearum. Annual Review of Phytopathology, 43, 63–82.

    Article  PubMed  CAS  Google Scholar 

  • Dye, D. W., & Lelliott, R. A. (1974). Genus II. Xanthomonas. In R. E. Buchanan & N. E. Gibbons (Eds.), Bergey’s manual of determinative bacteriology (8th ed., pp. 243–249). Baltimore: Williams & Wilkins.

    Google Scholar 

  • Farrer, R. A., Kemen, E., Jones, J. D., & Studholme, D. J. (2009). De novo assembly of the pseudomonas syringae pv. syringae B728a genome using illumina/solexa short sequence reads. FEMS Microbiology Letters, 291(1), 103–111.

    Article  PubMed  CAS  Google Scholar 

  • Follin, J. C. (1983). Races of Xanthomonas campestris pv. malvacearum (Smith) dye in Western and Central Africa. Coton et Fibres Tropicales, 38, 277–280.

    Google Scholar 

  • Follin, J. C., Girardot, B., Mangano, N., & Benitez, R. (1988). New results on inheritance of immunity to bacterial blight, Xanthomonas campestris pv. malvacearum (Smith) Dye race 18 and 20 in cotton plant (Gossypium hirsutum L.). Coton et Fibres Tropicales, 43, 167–174.

    Google Scholar 

  • Goris, J., Konstantinidis, K. T., Klappenbach, J. A., Coenye, T., Vandamme, P., & Tiedje, J. M. (2007). DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. International Journal of Systematic and Evolutionary Microbiology, 57(Pt 1), 81–91. doi:10.1099/ijs.0.64483-0.

    Article  PubMed  CAS  Google Scholar 

  • Hernandez, D., Francois, P., Farinelli, L., Osteras, M., & Schrenzel, J. (2008). De novo bacterial genome sequencing: millions of very short reads assembled on a desktop computer. Genome Research, 18(5), 802–809. doi:10.1101/gr.072033.107gr.072033.107.

    Article  PubMed  CAS  Google Scholar 

  • Huang, X., Zhai, J., Luo, Y., & Rudolph, K. (2008). Identification of a highly virulent strain of Xanthomonas axonopodis pv. malvacearum. European Journal of Plant Pathology, 122(4), 461–469.

    Article  CAS  Google Scholar 

  • Hunter, R. E., Brinkerhoff, L. A., & Bird, L. S. (1968). The development of a set of upland cotton lines for differentiating races of Xanthomonas campestris pv. malvacearum. Phytopathology, 58, 830–832.

    Google Scholar 

  • Kay, S., & Bonas, U. (2009). How Xanthomonas type III effectors manipulate the host plant. Current Opinion in Microbiology, 12(1), 37–43.

    Article  PubMed  CAS  Google Scholar 

  • Lee, B. M., Park, Y. J., Park, D. S., Kang, H. W., Kim, J. G., Song, E. S., et al. (2005). The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Research, 33(2), 577–586. doi:10.1093/nar/gki206.

    Article  PubMed  CAS  Google Scholar 

  • Marmey, P., Jalloul, A., Alhamdia, M., Assigbetse, K., Cacas, J. L., Voloudakis, A. E., et al. (2007). The 9-lipoxygenase GhLOX1 gene is associated with the hypersensitive reaction of cotton Gossypium hirsutum to Xanthomonas campestris pv malvacearum. Plant Physiology and Biochemistry, 45(8), 596–606.

    Article  PubMed  CAS  Google Scholar 

  • Moreira, L. M., Almeida, N. F., Jr., Potnis, N., Digiampietri, L. A., Adi, S. S., Bortolossi, J. C., et al. (2010). Novel insights into the genomic basis of citrus canker based on the genome sequences of two strains of Xanthomonas fuscans subsp. aurantifolii. BMC Genomics, 11, 238. doi:10.1186/1471-2164-11-2381471-2164-11-238.

    Article  PubMed  Google Scholar 

  • Pareja-Tobes, P., Manrique, M., Pareja-Tobes, E., Pareja, E., & Tobes, R. (2012). BG7: a new approach for bacterial genome annotation designed for next generation sequencing data. PLoS One, 7(11), e49239. doi:10.1371/journal.pone.0049239PONE-D-12-08914.

    Article  PubMed  CAS  Google Scholar 

  • Qian, W., Jia, Y., Ren, S. X., He, Y. Q., Feng, J. X., Lu, L. F., et al. (2005). Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. Genome Research, 15(6), 757–767. doi:10.1101/gr.3378705.

    Article  PubMed  CAS  Google Scholar 

  • Rademaker, J. L., Louws, F. J., Schultz, M. H., Rossbach, U., Vauterin, L., Swings, J., et al. (2005). A comprehensive species to strain taxonomic framework for xanthomonas. Phytopathology, 95(9), 1098–1111.

    Article  PubMed  CAS  Google Scholar 

  • Reinhardt, J. A., Baltrus, D. A., Nishimura, M. T., Jeck, W. R., Jones, C. D., & Dangl, J. L. (2009). De novo assembly using low-coverage short read sequence data from the rice pathogen Pseudomonas syringae pv. oryzae. Genome Research, 19(2), 294–305.

    Article  PubMed  CAS  Google Scholar 

  • Sayegh-A lhamdia, M., Marmey, P., Jalloul, A., Champion, A., Petitot, A. S., Clerivet, A., et al. (2008). Association of lipoxygenase response with resistance of various cotton genotypes to the bacterial blight disease. Journal of Phytopathology, 156(9), 542–549.

    Article  CAS  Google Scholar 

  • Schaad, N. W., Postnikova, E., Lacy, G., Sechler, A., Agarkova, I., Stromberg, P. E., et al. (2006). Emended classification of xanthomonad pathogens on citrus. Systematic and Applied Microbiology, 29(8), 690–695.

    Article  PubMed  Google Scholar 

  • Vauterin, L., & Swings, J. (1997). Are classification and phytopathological diversity compatible in Xanthomonas? Journal of Industrial Microbiology and Biotechnology, 19(2), 77–82.

    Article  CAS  Google Scholar 

  • Wall, D., & Kaiser, D. (1999). Type IV pili and cell motility. Molecular Microbiology, 32(1), 1–10.

    Article  PubMed  CAS  Google Scholar 

  • Xia, Z., Xu, H., Zhai, J., Li, D., Luo, H., He, C., et al. (2011). RNA-Seq analysis and de novo transcriptome assembly of Hevea brasiliensis. Plant Molecular Biology, 77(3), 299–308.

    Article  PubMed  CAS  Google Scholar 

  • Zhai, J., Luo, Y., Zheng, D., & Huang, X. (2010). Evaluation of genetic diversity of highly-virulent strains of Xanthomonas campestris pv. malvacearum by REP-PCR fingerprinting. Journal of Phytopathology, 158, 764–768.

    Article  Google Scholar 

Download references

Acknowledgments

We thank the staff of Beijing Genomics Institute of Shenzhen of China for their technical assistance with data analysis. This work was supported by a grant from the Project of Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of Agriculture, Hainan University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xi Huang.

Additional information

Jinling Zhai and Zhihui Xia contributed equally to this work.

Supplementary electronic material

Below is the link to the electronic supplementary material.

Figure S1

(DOC 26 kb)

Figure S2

(DOC 929 kb)

Figure S3

(DOC 1133 kb)

Figure S4

(DOC 453 kb)

Figure S5

(DOC 110 kb)

Table S1

(DOC 296 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhai, J., Xia, Z., Liu, W. et al. Genomic sequencing globally identifies functional genes and potential virulence-related effectors of Xanthomonas axonopodis pv. malvacearum . Eur J Plant Pathol 136, 657–663 (2013). https://doi.org/10.1007/s10658-013-0213-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-013-0213-8

Keywords

Navigation