European Journal of Plant Pathology

, Volume 136, Issue 4, pp 657–663 | Cite as

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

  • Jinling Zhai
  • Zhihui Xia
  • Wei Liu
  • Xingyu Jiang
  • Xi Huang
Article

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.

Keywords

Cotton bacterial blight Effectors Genomic sequencing 

Supplementary material

10658_2013_213_MOESM1_ESM.doc (26 kb)
Figure S1(DOC 26 kb)
10658_2013_213_MOESM2_ESM.doc (930 kb)
Figure S2(DOC 929 kb)
10658_2013_213_MOESM3_ESM.doc (1.1 mb)
Figure S3(DOC 1133 kb)
10658_2013_213_MOESM4_ESM.doc (453 kb)
Figure S4(DOC 453 kb)
10658_2013_213_MOESM5_ESM.doc (110 kb)
Figure S5(DOC 110 kb)
10658_2013_213_MOESM6_ESM.doc (296 kb)
Table S1(DOC 296 kb)

References

  1. 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.PubMedCrossRefGoogle Scholar
  2. 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.PubMedCrossRefGoogle Scholar
  3. 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.PubMedCrossRefGoogle Scholar
  4. 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.PubMedCrossRefGoogle Scholar
  5. 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.PubMedCrossRefGoogle Scholar
  6. 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.PubMedCrossRefGoogle Scholar
  7. 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
  8. 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.PubMedCrossRefGoogle Scholar
  9. 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
  10. 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
  11. 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.PubMedCrossRefGoogle Scholar
  12. 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.PubMedCrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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
  15. Kay, S., & Bonas, U. (2009). How Xanthomonas type III effectors manipulate the host plant. Current Opinion in Microbiology, 12(1), 37–43.PubMedCrossRefGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. 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.PubMedCrossRefGoogle Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. 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.PubMedCrossRefGoogle Scholar
  22. 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.PubMedCrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. Vauterin, L., & Swings, J. (1997). Are classification and phytopathological diversity compatible in Xanthomonas? Journal of Industrial Microbiology and Biotechnology, 19(2), 77–82.CrossRefGoogle Scholar
  26. Wall, D., & Kaiser, D. (1999). Type IV pili and cell motility. Molecular Microbiology, 32(1), 1–10.PubMedCrossRefGoogle Scholar
  27. 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.PubMedCrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar

Copyright information

© KNPV 2013

Authors and Affiliations

  • Jinling Zhai
    • 1
  • Zhihui Xia
    • 1
  • Wei Liu
    • 1
  • Xingyu Jiang
    • 1
  • Xi Huang
    • 1
    • 2
  1. 1.Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of AgricultureHainan UniversityHaikouPeople’s Republic of China
  2. 2.Institute of Bioscience and Technology, College of AgricultureHainan UniversityHaikouPeople’s Republic of China

Personalised recommendations