1887

Abstract

The extensive genetic diversity of , a serious soil-borne phytopathogen, has led to the concept that encompasses a species complex [ species complex (RSSC)]. Insertion sequences (ISs) are suggested to play an important role in the genome evolution of this pathogen. Here, we identified and analysed transposable elements (TEs), ISs and transposons, in 106 RSSC genomes and 15 spp. We mapped 10 259 IS elements in the complete genome of 62 representative RSSC strains and closely related spp. A unique set of 20 IS families was widespread across the strains, IS and IS being the most abundant. Our results showed six novel transposon sequences belonging to the Tn family carrying passenger genes encoding antibiotic resistance and avirulence proteins. In addition, internal rearrangement events associated with ISs were demonstrated in strains. We also mapped IS elements interrupting avirulence genes, which provided evidence that ISs plays an important role in virulence evolution of RSSC. Additionally, the activity of ISs was demonstrated by transcriptome analysis and DNA hybridization in isolates. Altogether, we have provided collective data of TEs in RSSC genomes, opening a new path for understanding their evolutionary impact on the genome evolution and diversity of this important plant pathogen.

Funding
This study was supported by the:
  • Osiel Silva Gonçalves , Coordenação de Aperfeiçoamento de Pessoal de Nível Superior , (Award 001)
  • Mateus Ferreira Santana , Fundação Arthur Bernardes
  • Mateus Ferreira Santana , Conselho Nacional de Desenvolvimento Científico e Tecnológico
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000374
2020-05-07
2020-06-04
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/5/mgen000374.html?itemId=/content/journal/mgen/10.1099/mgen.0.000374&mimeType=html&fmt=ahah

References

  1. Peyraud R, Dubiella U, Barbacci A, Genin S, Raffaele S et al. Advances on plant-pathogen interactions from molecular toward systems biology perspectives. Plant J 2017; 90:720–737 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  2. Schneider DJ, Collmer A. Studying plant-pathogen interactions in the genomics era: beyond molecular Koch's postulates to systems biology. Annu Rev Phytopathol 2010; 48:457–479 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  3. Bobay L-M, Ochman H. The evolution of bacterial genome architecture. Front Genet 2017; 8:72 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  4. Mira A, Klasson L, Andersson SGE. Microbial genome evolution: sources of variability. Curr Opin Microbiol 2002; 5:506–512 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  5. Gil R, Latorre A. Factors behind junk DNA in bacteria. Genes 2012; 3:634–650 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  6. Kleckner N. Transposable elements in prokaryotes. Structure 1981; 15:341–404
    [Google Scholar]
  7. Siguier P, Gourbeyre E, Chandler M. Bacterial insertion sequences: their genomic impact and diversity. FEMS Microbiol Rev 2014; 38:865–891 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  8. Arnold DL, Jackson RW. Bacterial genomes: evolution of pathogenicity. Curr Opin Plant Biol 2011; 14:385–391 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  9. Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S et al. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 2002; 415:497–502 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  10. Castillo JA, Greenberg JT. Evolutionary dynamics of Ralstonia solanacearum. Appl Environ Microbiol 2007; 73:1225–1238 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  11. Li P, Wang D, Yan J, Zhou J, Deng Y et al. Genomic analysis of phylotype I strain EP1 reveals substantial divergence from other strains in the Ralstonia solanacearum species complex. Front Microbiol 2016; 7:1719 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  12. Remenant B, Coupat-Goutaland B, Guidot A, Cellier G, Wicker E et al. Genomes of three tomato pathogens within the Ralstonia solanacearum species complex reveal significant evolutionary divergence. BMC Genomics 2010; 11:379 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  13. Prior P, Ailloud F, Dalsing BL, Remenant B, Sanchez B et al. Genomic and proteomic evidence supporting the division of the plant pathogen Ralstonia solanacearum into three species. BMC Genomics 2016; 17:90 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  14. Safni I, Cleenwerck I, Vos PD, Fegan M, Sly L et al. 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. Int J Syst Evol Microbiol 2014; 64:3087–3103
    [Google Scholar]
  15. McGinnis S, Madden TL. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 2004; 32:W20–W25 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  16. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 2006; 34:D32–D36 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  17. Varani AM, Siguier P, Gourbeyre E, Charneau V, Chandler M. ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes. Genome Biol 2011; 12:R30 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  18. Robinson DG, Lee M-C, Marx CJ. OASIS: an automated program for global investigation of bacterial and archaeal insertion sequences. Nucleic Acids Res 2012; 40:e174 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  19. Siguier P, Gourbeyre E, Varani A, Ton-Hoang B, Chandler M. Everyman's guide to bacterial insertion sequences. Microbiol Spectr 2015; 3:550–590 [CrossRef]
    [Google Scholar]
  20. Tansirichaiya S, Rahman MA, Roberts AP. The Transposon Registry. Mob DNA 2019; 10:40 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  21. Urban M, Cuzick A, Rutherford K, Irvine A, Pedro H et al. PHI-base: a new interface and further additions for the multi-species pathogen–host interactions database. Nucleic Acids Res 2017; 45:D604–D610 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  22. Sabbagh CRR, Carrere S, Lonjon F, Vailleau F, Macho AP et al. Pangenomic type III effector database of the plant pathogenic Ralstonia spp. PeerJ 2019; 7:e7346 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  23. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res 2017; 45:D566–D573 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  24. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  25. Kumar S, Stecher G, Li M, Knyaz C, Tamura K et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  26. Letunic I, Bork P. Interactive tree of life (iTOL) V4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  27. Ailloud F, Lowe TM, Robène I, Cruveiller S, Allen C et al. In planta comparative transcriptomics of host-adapted strains of Ralstonia solanacearum. PeerJ 2016; 4:e1549 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  28. Leinonen R, Sugawara H, Shumway M. International Nucleotide Sequence Database Collaboration The sequence read archive. Nucleic Acids Res 2011; 39:D19–D21 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  29. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  30. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  31. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26:139–140 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  32. Sambrook J, Russel DW. Molecular Cloning: a Laboratory Manual. , 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 2001
  33. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004; 14:1394–1403 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  34. Vandecraen J, Chandler M, Aertsen A, Van Houdt R. The impact of insertion sequences on bacterial genome plasticity and adaptability. Crit Rev Microbiol 2017; 43:709–730 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  35. Stapley J, Santure AW, Dennis SR. Transposable elements as agents of rapid adaptation may explain the genetic paradox of invasive species. Mol Ecol 2015; 24:2241–2252 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  36. Seidl MF, Thomma BPHJ. Transposable elements direct the coevolution between plants and microbes. Trends Genet 2017; 33:842–851 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  37. Adams MD, Bishop B, Wright MS. Quantitative assessment of insertion sequence impact on bacterial genome architecture. Microb Genom 2016; 2:e000062 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  38. Fling ME, Kopf J, Richards C. Nucleotide sequence of the transposon Tn7 gene encoding an aminoglycoside-modifying enzyme, 3"(9)-O-nucleotidyltransferase. Nucleic Acids Res 1985; 13:7095–7106 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  39. Krause KM, Serio AW, Kane TR, Connolly LE. Aminoglycosides: an overview. Cold Spring Harb Perspect Med 2016; 6:a027029 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  40. Leach JE, White FF. Bacterial avirulence genes. Annu Rev Phytopathol 1996; 34:153–179 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  41. Gabriel DW. Why do pathogens carry avirulence genes?. Physiol Mol Plant Pathol 1999; 55:205–214 [CrossRef]
    [Google Scholar]
  42. Flor HH. Current status of the gene-for-gene concept. Annu Rev Phytopathol 1971; 9:275–296 [CrossRef]
    [Google Scholar]
  43. Grennan AK. Plant response to bacterial pathogens: overlap between innate and gene-for-gene defense response. Plant Physiol 2006; 142:809–811 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  44. Deslandes L, Rivas S. Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci 2012; 17:644–655 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  45. Kim JF, Charkowski AO, Alfano JR, Collmer A, Beer SV. Sequences related to transposable elements and bacteriophages flank avirulence genes of Pseudomonas syringae. Mol Plant Microbe Interact 1998; 11:1247–1252 [CrossRef]
    [Google Scholar]
  46. Inami K, Yoshioka-Akiyama C, Morita Y, Yamasaki M, Teraoka T et al. A genetic mechanism for emergence of races in Fusarium oxysporum f. sp. lycopersici: inactivation of avirulence gene AVR1 by transposon insertion. PLoS One 2012; 7:e44101 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  47. Li X, Huang X, Chen G, Zou L, Wei L et al. Complete genome sequence of the sesame pathogen Ralstonia solanacearum strain SEPPX 05. Genes Genomics 2018; 40:657–668 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  48. Jiang G, Wei Z, Xu J, Chen H, Zhang Y et al. Bacterial wilt in China: history, current status, and future perspectives. Front Plant Sci 2017; 8:1549 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  49. Genin S, Denny TP. Pathogenomics of the Ralstonia solanacearum species complex. Annu Rev Phytopathol 2012; 50:67–89 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  50. Jeong EL, Timmis JN. Novel insertion sequence elements associated with genetic heterogeneity and phenotype conversion in Ralstonia solanacearum. J Bacteriol 2000; 182:6541 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  51. Chen D, Liu B, Zhu Y, Zhang H, Chen Z et al. Complete genome sequence of Ralstonia solanacearum FJAT-91, a high-virulence pathogen of tomato wilt. Genome Announc 2017; 5:e00900-17 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  52. Jones P, Garcia BJ, Furches A, Tuskan GA, Jacobson D. Plant host-associated mechanisms for microbial selection. Front Plant Sci 2019; 10:862 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  53. Lee H, Doak TG, Popodi E, Foster PL, Tang H. Insertion sequence-caused large-scale rearrangements in the genome of Escherichia coli. Nucleic Acids Res 2016; 44:7109–7119 [CrossRef][PubMed][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000374
Loading
/content/journal/mgen/10.1099/mgen.0.000374
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error