1887

Abstract

Bacterial wilt caused by the species complex (RSSC) threatens the cultivation of important crops worldwide. We sequenced 30 RSSC phylotype I () strains isolated from pepper () and tomato () across the Republic of Korea. These isolates span the diversity of phylotype I, have extensive effector repertoires and are subject to frequent recombination. Recombination hotspots among South Korean phylotype I isolates include multiple predicted contact-dependent inhibition loci, suggesting that microbial competition plays a significant role in evolution. Rapid diversification of secreted effectors presents challenges for the development of disease-resistant plant varieties. We identified potential targets for disease resistance breeding by testing for allele-specific host recognition of T3Es present among South Korean phyloype I isolates. The integration of pathogen population genomics and molecular plant pathology contributes to the development of location-specific disease control and development of plant cultivars with durable resistance to relevant threats.

Funding
This study was supported by the:
  • Max Planck Society
  • National Research Foundation, Republic of Korea Ministry of Science and ICT (Award NRF-2019R1A2C2084705)
  • Rural Development Administration, Republic of Korea Ministry of Science and ICT (Award 2018R1A5A1023599)
  • Marsden Fast-Start, Royal Society of New Zealand (Award MAU1709)
  • Creative-Pioneering Researchers, Seoul National University
  • Plant Molecular Breeding Center, Next-Generation BioGreen 21 Program (Award PJ01317501)
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2020-11-05
2021-07-29
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References

  1. Genin S, Denny TP. Pathogenomics of the Ralstonia solanacearum species complex. Annu Rev Phytopathol 2012; 50:67–89 [View Article]
    [Google Scholar]
  2. Lowe-Power TM, Khokhani D, Allen C. How Ralstonia solanacearum exploits and thrives in the flowing plant xylem environment. Trends Microbiol 2018; 26:929–942 [View Article]
    [Google Scholar]
  3. Yabuuchi E, Kosako Y, Oyaizu H, Yano I, Hotta H et al. Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol Immunol 1992; 36:1251–1275 [View Article]
    [Google Scholar]
  4. Yabuuchi E, Kosako Y, Yano I, Hotta H, Nishiuchi Y. Transfer of two Burkholderia and an Alcaligenes species to Ralstonia gen. nov. Microbiol Immunol 1995; 39:897–904 [View Article]
    [Google Scholar]
  5. diCenzo GC, Finan TM. The divided bacterial genome: structure, function, and evolution. Microbiol Mol Biol Rev 2017; 81:e00019–17 [View Article]
    [Google Scholar]
  6. 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 [View Article]
    [Google Scholar]
  7. Wicker E, Lefeuvre P, de Cambiaire J-C, Lemaire C, Poussier S et al. Contrasting recombination patterns and demographic histories of the plant pathogen Ralstonia solanacearum inferred from MLSA. Isme J 2012; 6:961–974 [View Article]
    [Google Scholar]
  8. Chewapreecha C, Harris SR, Croucher NJ, Turner C, Marttinen P et al. Dense genomic sampling identifies highways of pneumococcal recombination. Nat Genet 2014; 46:305–309 [View Article]
    [Google Scholar]
  9. Bertolla F, Frostegård Åsa, Brito B, Nesme X, Simonet P. During infection of its host, the plant pathogen Ralstonia solanacearum naturally develops a state of competence and exchanges genetic material. MPMI 1999; 12:467–472 [View Article]
    [Google Scholar]
  10. Coupat B, Chaumeille-Dole F, Fall S, Prior P, Simonet P et al. Natural transformation in the Ralstonia solanacearum species complex: number and size of DNA that can be transferred. FEMS Microbiol Ecol 2008; 66:14–24 [View Article]
    [Google Scholar]
  11. Wyres KL, Wick RR, Judd LM, Froumine R, Tokolyi A et al. Distinct evolutionary dynamics of horizontal gene transfer in drug resistant and virulent clones of Klebsiella pneumoniae . PLoS Genet 2019; 15:e1008114 [View Article]
    [Google Scholar]
  12. Deslandes L, Genin S. Opening the Ralstonia solanacearum type III effector tool box: insights into host cell subversion mechanisms. Curr Opin Plant Biol 2014; 20:110–117 [View Article]
    [Google Scholar]
  13. Peeters N, Carrère S, Anisimova M, Plener L, Cazalé A-C et al. Repertoire, unified nomenclature and evolution of the Type III effector gene set in the Ralstonia solanacearum species complex. BMC Genomics 2013; 14:859 [View Article]
    [Google Scholar]
  14. Dillon MM, Almeida RND, Laflamme B, Martel A, Weir BS et al. Molecular evolution of Pseudomonas syringae Type III secreted effector proteins. Front Plant Sci 2019; 10:418 [View Article]
    [Google Scholar]
  15. Timilsina S, Potnis N, Newberry EA, Liyanapathiranage P, Iruegas-Bocardo F et al. Xanthomonas diversity, virulence and plant–pathogen interactions. Nat Rev Microbiol 20201–13
    [Google Scholar]
  16. Jones JDG, Dangl JL. The plant immune system. Nature 2006; 444:323–329 [View Article]
    [Google Scholar]
  17. Carney BF, Denny TP. A cloned avirulence gene from Pseudomonas solanacearum determines incompatibility on Nicotiana tabacum at the host species level. J Bacteriol 1990; 172:4836–4843 [View Article]
    [Google Scholar]
  18. Poueymiro M, Cunnac S, Barberis P, Deslandes L, Peeters N et al. Two Type III secretion system effectors from Ralstonia solanacearum GMI1000 determine host-range specificity on tobacco. MPMI 2009; 22:538–550 [View Article]
    [Google Scholar]
  19. Nakano M, Mukaihara T. The type III effector RipB from Ralstonia solanacearum RS1000 acts as a major avirulence factor in Nicotiana benthamiana and other Nicotiana species. Mol Plant Pathol 2019; 20:1237–1251 [View Article]
    [Google Scholar]
  20. Clarke CR, Studholme DJ, Hayes B, Runde B, Weisberg A et al. Genome-enabled phylogeographic investigation of the quarantine pathogen Ralstonia solanacearum race 3 biovar 2 and screening for sources of resistance against its core effectors. Phytopathology 2015; 105:597–607 [View Article]
    [Google Scholar]
  21. Jeon H, Kim W, Kim B, Lee S, Jayaraman J et al. Ralstonia solanacearum Type III effectors with predicted nuclear localization signal localize to various cell compartments and modulate immune responses in Nicotiana spp. Plant Pathology J 2020; 36:43–53
    [Google Scholar]
  22. Sang Y, Yu W, Zhuang H, Wei Y, Derevnina L et al. Intra-strain elicitation and suppression of plant immunity by Ralstonia solanacearum type-III effectors in Nicotiana benthamiana . Plant Commun 2020; 100025:
    [Google Scholar]
  23. Solé M, Popa C, Mith O, Sohn KH, Jones JDG et al. The awr gene family encodes a novel class of Ralstonia solanacearum Type III effectors displaying virulence and avirulence activities. MPMI 2012; 25:941–953 [View Article]
    [Google Scholar]
  24. Ailloud F, Lowe T, Cellier G, Roche D, Allen C et al. Comparative genomic analysis of Ralstonia solanacearum reveals candidate genes for host specificity. BMC Genomics 2015; 16:270 [View Article]
    [Google Scholar]
  25. Baym M, Kryazhimskiy S, Lieberman TD, Chung H, Desai MM et al. Inexpensive multiplexed library preparation for megabase-sized genomes. PLoS One 2015; 10:e0128036 [View Article]
    [Google Scholar]
  26. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article]
    [Google Scholar]
  27. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article]
    [Google Scholar]
  28. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article]
    [Google Scholar]
  29. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
    [Google Scholar]
  30. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article]
    [Google Scholar]
  31. 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 [View Article]
    [Google Scholar]
  32. Bi D, Xu Z, Harrison EM, Tai C, Wei Y et al. ICEberg: a web-based resource for integrative and conjugative elements found in bacteria. Nucleic Acids Res 2012; 40:D621–D626 [View Article]
    [Google Scholar]
  33. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–W21 [View Article]
    [Google Scholar]
  34. Li H, Durbin R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 2010; 26:589–595 [View Article]
    [Google Scholar]
  35. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 2011; 27:2987–2993 [View Article]
    [Google Scholar]
  36. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841–842 [View Article]
    [Google Scholar]
  37. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006; 22:2688–2690 [View Article]
    [Google Scholar]
  38. Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput Biol 2015; 11:e1004041–18 [View Article]
    [Google Scholar]
  39. Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 2015; 16:157 [View Article]
    [Google Scholar]
  40. Loytynoja A, Goldman N. Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis. Science 2008; 320:1632–1635 [View Article]
    [Google Scholar]
  41. Cheng L, Connor TR, Sirén J, Aanensen DM, Corander J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol 2013; 30:1224–1228 [View Article]
    [Google Scholar]
  42. Huerta-Cepas J, Serra F, Bork P. ETE 3: reconstruction, analysis, and visualization of phylogenomic data. Mol Biol Evol 2016; 33:1635–1638 [View Article]
    [Google Scholar]
  43. Engler C, Kandzia R, Marillonnet S. A one pot, one step, precision cloning method with high throughput capability. PLoS One 2008; 3:e3647 [View Article]
    [Google Scholar]
  44. Anderson MS, Garcia EC, Cotter PA. The Burkholderia bcpAIOB genes define unique classes of two-partner secretion and contact dependent growth inhibition systems. PLoS Genet 2012; 8:e1002877 [View Article]
    [Google Scholar]
  45. Willett JLE, Gucinski GC, Fatherree JP, Low DA, Hayes CS. Contact-dependent growth inhibition toxins exploit multiple independent cell-entry pathways. Proc Natl Acad Sci U S A 2015; 112:11341–11346 [View Article]
    [Google Scholar]
  46. Garcia EC, Perault AI, Marlatt SA, Cotter PA. Interbacterial signaling via Burkholderia contact-dependent growth inhibition system proteins. Proc Natl Acad Sci U S A 2016; 113:8296–8301 [View Article]
    [Google Scholar]
  47. Willett JLE, Ruhe ZC, Goulding CW, Low DA, Hayes CS et al. Cdi) and CdiB/CdiA two-partner secretion proteins. J Mol Biol 2015; 427:3754–3765
    [Google Scholar]
  48. Murai Y, Mori S, Konno H, Hikichi Y, Kai K. Ralstonins A and B, lipopeptides with chlamydospore-inducing and phytotoxic Activities from the plant pathogen Ralstonia solanacearum . Org Lett 2017; 19:4175–4178 [View Article]
    [Google Scholar]
  49. Spraker JE, Sanchez LM, Lowe TM, Dorrestein PC, Keller NP. Ralstonia solanacearum lipopeptide induces chlamydospore development in fungi and facilitates bacterial entry into fungal tissues. Isme J 2016; 10:2317–2330 [View Article]
    [Google Scholar]
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