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Abstract

Genetic variability in phytopathogens is one of the main problems encountered for effective plant disease control. This fact may be related to the presence of transposable elements (TEs), but little is known about their role in host genomes. Here, we performed the most comprehensive analysis of insertion sequences (ISs) and transposons (Tns) in the genomes of the most important bacterial plant pathogens. A total of 35 692 ISs and 71 transposons were identified in 270 complete genomes. The level of pathogen–host specialization was found to be a significant determinant of the element distribution among the species. Some Tns were identified as carrying virulence factors, such as genes encoding effector proteins of the type III secretion system and resistance genes for the antimicrobial streptomycin. Evidence for IS-mediated ectopic recombination was identified in genomes. Moreover, we found that IS elements tend to be inserted in regions near virulence and fitness genes, such ISs disrupting avirulence genes in genomes. In addition, transcriptome analysis under different stress conditions revealed differences in the expression of genes encoding transposases in the , , and species. Lastly, we also investigated the role of Tns in regulation via small noncoding regulatory RNAs and found these elements may target plant-cell transcriptional activators. Taken together, the results indicate that TEs may have a fundamental role in variability and virulence in plant pathogenic bacteria.

Funding
This study was supported by the:
  • Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Award 001)
    • Principle Award Recipient: AlexiaSuellen Fernandes
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-04-03
2024-04-30
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References

  1. Alexia S. FERNANDESInvestigating the impact of insertion sequences and transposons in the genomes of the most significant phytopathogenic bacteria Figshare 2024 [View Article]
    [Google Scholar]
  2. Kannan VR, Bastas KK, Devi RS. 20 scientific and economic impact of plant pathogenic bacteria. Sustainable approaches to controlling plant pathogenic bacteria. In Sustainable Approaches to Controlling Plant Pathogenic Bacteria 2015 p 369 [View Article]
    [Google Scholar]
  3. Strange RN, Scott PR. Plant disease: a threat to global food security. Annu Rev Phytopathol 2005; 43:83–116 [View Article] [PubMed]
    [Google Scholar]
  4. Khan M, Seto D, Subramaniam R, Desveaux D. Oh, the places they’ll go! A survey of phytopathogen effectors and their host targets. Plant J 2018; 93:651–663 [View Article] [PubMed]
    [Google Scholar]
  5. Martins PMM, Merfa MV, Takita MA, De Souza AA. Persistence in phytopathogenic bacteria: do we know enough?. Front Microbiol 2018; 9:1099 [View Article] [PubMed]
    [Google Scholar]
  6. Pfeilmeier S, Caly DL, Malone JG. Bacterial pathogenesis of plants: future challenges from a microbial perspective: challenges in bacterial molecular plant pathology. Mol Plant Pathol 2016; 17:1298–1313 [View Article] [PubMed]
    [Google Scholar]
  7. Patricia S. Everyman’s guide to bacterial insertion sequences. Mobile DNA Iii 2015; 555:590 [View Article]
    [Google Scholar]
  8. Ross K, Varani AM, Snesrud E, Huang H, Alvarenga DO et al. TnCentral: a prokaryotic transposable element database and web portal for transposon analysis. mBio 2021; 12:e0206021 [View Article] [PubMed]
    [Google Scholar]
  9. Partridge SR, Kwong SM, Firth N, Jensen SO. Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev 2018; 31:e00088-17 [View Article] [PubMed]
    [Google Scholar]
  10. Oliveira ACP. Transposons and pathogenicity in Xanthomonas: acquisition of murein lytic transglycosylases by Tnxax1 enhances Xanthomonas citri subsp. citri 306 virulence and fitness. PeerJ 2018; 6:e6111 [View Article]
    [Google Scholar]
  11. Serrato-Capuchina A, Matute DR. The role of transposable elements in speciation. Genes 2018; 9:254 [View Article]
    [Google Scholar]
  12. Kapitonov VV, Makarova KS, Koonin EV. ISC, a novel group of bacterial and archaeal DNA transposons that encode Cas9 homologs. J Bacteriol 2016; 198:797–807 [View Article] [PubMed]
    [Google Scholar]
  13. Peters JE, Makarova KS, Shmakov S, Koonin EV. Recruitment of CRISPR-Cas systems by Tn7-like transposons. Proc Natl Acad Sci U S A 2017; 114:E7358–E7366 [View Article] [PubMed]
    [Google Scholar]
  14. Mat Razali N, Cheah BH, Nadarajah K. Transposable elements adaptive role in genome plasticity, pathogenicity and evolution in fungal phytopathogens. Int J Mol Sci 2019; 20:3597 [View Article] [PubMed]
    [Google Scholar]
  15. 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 [View Article] [PubMed]
    [Google Scholar]
  16. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 2012; 13:614–629 [View Article] [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; 12:1–9 [View Article] [PubMed]
    [Google Scholar]
  18. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 2006; 34:D32–6 [View Article] [PubMed]
    [Google Scholar]
  19. Chen L, Yang J, Yu J, Yao Z, Sun L et al. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 2005; 33:D325–8 [View Article] [PubMed]
    [Google Scholar]
  20. 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 [View Article] [PubMed]
    [Google Scholar]
  21. Wang Y, Huang H, Sun M, Zhang Q, Guo D. T3DB: an integrated database for bacterial type III secretion system. BMC Bioinformatics 2012; 13:1–6 [View Article] [PubMed]
    [Google Scholar]
  22. Brian P. ALCOCK CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020D517–D525
    [Google Scholar]
  23. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article]
    [Google Scholar]
  24. Gonçalves OS, Campos KF, de Assis JCS, Fernandes AS, Souza TS et al. Transposable elements contribute to the genome plasticity of Ralstonia solanacearum species complex. Microb Genom 2020; 6:e000374 [View Article] [PubMed]
    [Google Scholar]
  25. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22:4673–4680 [View Article] [PubMed]
    [Google Scholar]
  26. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  27. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004; 14:1394–1403 [View Article] [PubMed]
    [Google Scholar]
  28. Martin DP, Lemey P, Lott M, Moulton V, Posada D et al. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 2010; 26:2462–2463 [View Article] [PubMed]
    [Google Scholar]
  29. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  30. Bourque G, Burns KH, Gehring M, Gorbunova V, Seluanov A et al. Ten things you should know about transposable elements. Genome Biol 2018; 19:199 [View Article] [PubMed]
    [Google Scholar]
  31. Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 2013; 29:2933–2935 [View Article] [PubMed]
    [Google Scholar]
  32. Andreas R. G et al. RNAz 2.0: improved noncoding RNA detection. In Biocomputing 2010 pp 69–79 [View Article]
    [Google Scholar]
  33. Kumar K, Chakraborty A, Chakrabarti S. PresRAT: a server for identification of bacterial small-RNA sequences and their targets with probable binding region. RNA Biol 2021; 18:1152–1159 [View Article] [PubMed]
    [Google Scholar]
  34. Lott SC, Schäfer RA, Mann M, Backofen R, Hess WR et al. GLASSgo - automated and reliable detection of sRNA homologs from a single input sequence. Front Genet 2018; 9:124 [View Article] [PubMed]
    [Google Scholar]
  35. Touchon M, Rocha EPC. Causes of insertion sequences abundance in prokaryotic genomes. Mol Biol Evol 2007; 24:969–981 [View Article] [PubMed]
    [Google Scholar]
  36. Hirose K, Ishiga Y, Fujikawa T. Phytotoxin synthesis genes and type III effector genes of Pseudomonas syringae pv. actinidiae biovar 6 are regulated by culture conditions. PeerJ 2020; 8:e9697 [View Article] [PubMed]
    [Google Scholar]
  37. Kim S, Cho Y-J, Song E-S, Lee SH, Kim J-G et al. Time-resolved pathogenic gene expression analysis of the plant pathogen Xanthomonas oryzae pv. oryzae. BMC Genomics 2016; 17:345 [View Article] [PubMed]
    [Google Scholar]
  38. Hendrich CG, Truchon AN, Dalsing BL, Allen C. Nitric oxide regulates the Ralstonia solanacearum type 3 secretion system. bioRxiv 2020; 10: [View Article]
    [Google Scholar]
  39. Mann RA, Smits THM, Bühlmann A, Blom J, Goesmann A et al. Comparative genomics of 12 strains of Erwinia amylovora identifies a pan-genome with a large conserved core. PLoS One 2013; 8:e55644 [View Article] [PubMed]
    [Google Scholar]
  40. Mariano RLR. Transmissão de fitobacterioses por insetos. In Anais Da Academia Pernambucana de Ciência Agronômica vol 4 2007 pp 214–239
    [Google Scholar]
  41. Comandatore F, Cordaux R, Bandi C, Blaxter M, Darby A et al. Supergroup C Wolbachia, mutualist symbionts of filarial nematodes, have a distinct genome structure. Open Biol 2015; 5:150099 [View Article] [PubMed]
    [Google Scholar]
  42. Moran NA, Plague GR. Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 2004; 14:627–633 [View Article] [PubMed]
    [Google Scholar]
  43. Moya A, Peretó J, Gil R, Latorre A. Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 2008; 9:218–229 [View Article] [PubMed]
    [Google Scholar]
  44. Siguier P, Gourbeyre E, Chandler M. Bacterial insertion sequences: their genomic impact and diversity. FEMS Microbiol Rev 2014; 38:865–891 [View Article] [PubMed]
    [Google Scholar]
  45. Tancos KA, Villani S, Kuehne S, Borejsza-Wysocka E, Breth D et al. Prevalence of streptomycin-resistant Erwinia amylovora in New York apple orchards. Plant Dis 2016; 100:802–809 [View Article]
    [Google Scholar]
  46. Quibod IL, Atieza-Grande G, Oreiro EG, Palmos D, Nguyen MH et al. The green revolution shaped the population structure of the rice pathogen Xanthomonas oryzae pv. oryzae. ISME J 2020; 14:492–505 [View Article] [PubMed]
    [Google Scholar]
  47. Timilsina S, Potnis N, Newberry EA, Liyanapathiranage P, Iruegas-Bocardo F et al. Xanthomonas diversity, virulence and plant-pathogen interactions. Nat Rev Microbiol 2020; 18:415–427 [View Article] [PubMed]
    [Google Scholar]
  48. Bourras S, Rouxel T, Meyer M. Agrobacterium tumefaciens gene transfer: how a plant pathogen hacks the nuclei of plant and nonplant organisms. Phytopathology 2015; 105:1288–1301 [View Article] [PubMed]
    [Google Scholar]
  49. Xin X-F, Kvitko B, He SY. Pseudomonas syringae: what it takes to be a pathogen. Nat Rev Microbiol 2018; 16:316–328 [View Article] [PubMed]
    [Google Scholar]
  50. Sundin GW, Bender CL. Expression of the strA-strB streptomycin resistance genes in Pseudomonas syringae and Xanthomonas campestris and characterization of IS6100 in X. campestris. Appl Environ Microbiol 1995; 61:2891–2897 [View Article] [PubMed]
    [Google Scholar]
  51. Nimchuk ZL, Fisher EJ, Desveaux D, Chang JH, Dangl JL. The HopX (AvrPphE) family of Pseudomonas syringae type III effectors require a catalytic triad and a novel N-terminal domain for function. Mol Plant Microbe Interact 2007; 20:346–357 [View Article] [PubMed]
    [Google Scholar]
  52. Xia Y, Zou R, Escouboué M, Zhong L, Zhu C et al. Secondary-structure switch regulates the substrate binding of a YopJ family acetyltransferase. Nat Commun 2021; 12:5969 [View Article] [PubMed]
    [Google Scholar]
  53. Wu L, Chen H, Curtis C, Fu ZQ. Go in for the kill: how plants deploy effector-triggered immunity to combat pathogens. Virulence 2014; 5:710–721 [View Article] [PubMed]
    [Google Scholar]
  54. Malachowa N, DeLeo FR. Mobile genetic elements of Staphylococcus aureus. Cell Mol Life Sci 2010; 67:3057–3071 [View Article] [PubMed]
    [Google Scholar]
  55. Rezzonico F, Stockwell VO, Duffy B. Plant agricultural streptomycin formulations do not carry antibiotic resistance genes. Antimicrob Agents Chemother 2009; 53:3173–3177 [View Article]
    [Google Scholar]
  56. Assis RAB, Varani AM, Sagawa CHD, Patané JSL, Setubal JC et al. A comparative genomic analysis of Xanthomonas arboricola pv. juglandis strains reveal hallmarks of mobile genetic elements in the adaptation and accelerated evolution of virulence. Genomics 2021; 113:2513–2525 [View Article] [PubMed]
    [Google Scholar]
  57. Erill I, Puigvert M, Legrand L, Guarischi-Sousa R, Vandecasteele C et al. Comparative analysis of Ralstonia solanacearum methylomes. Front Plant Sci 2017; 8:504 [View Article] [PubMed]
    [Google Scholar]
  58. Amman F, D’Halluin A, Antoine R, Huot L, Bibova I et al. Primary transcriptome analysis reveals importance of IS elements for the shaping of the transcriptional landscape of Bordetella pertussis. RNA Biol 2018; 15:967–975 [View Article] [PubMed]
    [Google Scholar]
  59. Bobrovskyy M, Vanderpool CK. Regulation of bacterial metabolism by small RNAs using diverse mechanisms. Annu Rev Genet 2013; 47:209–232 [View Article] [PubMed]
    [Google Scholar]
  60. Ellis MJ, Trussler RS, Charles O, Haniford DB. A transposon-derived small RNA regulates gene expression in Salmonella Typhimurium. Nucleic Acids Res 2017; 45:5470–5486 [View Article] [PubMed]
    [Google Scholar]
  61. Kreth J, Brantl S, Merritt J. Regulatory RNAs. In Encyclopedia of Microbiology Elsevier; 2019 pp 62–84
    [Google Scholar]
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