1887

Microbiology Society logo

Volume 158, Issue 11

Genome drafts of four phytoplasma strains of the ribosomal group 16SrIII Free

Abstract

By applying a coverage-based read selection and filtration through a healthy plant dataset, and a post-assembly contig selection based on homology and linkage, genome sequence drafts were obtained for four phytoplasma strains belonging to the 16SrIII group (X disease clade), namely Vaccinium Witches’ Broom phytoplasma (647 754 nt in 272 contigs), Italian Clover Phyllody phytoplasma strain MA (597 245 nt in 197 contigs), Poinsettia branch-inducing phytoplasma strain JR1 (631 440 nt in 185 contigs) and Milkweed Yellows phytoplasma (583 806 nt in 158 contigs). Despite assignment to different 16SrIII subgroups, the genomes of the four strains were similar, comprising a highly conserved core (92–98 % similar in their nucleotide sequence among each other over alignments about 500 kb in length) and a minor strain-specific component. As far as their protein complement was concerned, they did not differ significantly in their basic metabolism potential from the genomes of other wide-host-range phytoplasmas sequenced previously, but were distinct from strains of other species, as well as among each other, in genes encoding functions conceivably related to interactions with the host, such as membrane trafficking components, proteases, DNA methylases, effectors and several hypothetical proteins of unknown function, some of which are likely secreted through the Sec-dependent secretion system. The four genomes displayed a group of genes encoding hypothetical proteins with high similarity to a central domain of IcmE/DotG, a core component of the type IVB secretion system of Gram-negative spp. Conversely, genes encoding functional GroES/GroEL chaperones were not detected in any of the four drafts. The results also indicated the significant role of horizontal gene transfer among different ‘ Phytoplasma’ species in shaping phytoplasma genomes and promoting their diversity.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.061432-0
2012-11-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/11/2805.html?itemId=/content/journal/micro/10.1099/mic.0.061432-0&mimeType=html&fmt=ahah

References

  1. Ahrens U., Seemuller E. ( 1992). Detection of DNA of plant pathogenic mycoplasmalike organisms by a polymerase chain reaction that amplifies a sequence of the 16S rRNA gene. Phytopathology 82:828–832 [View Article]
     [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. ( 1990). Basic local alignment search tool. J Mol Biol 215:403–410 [PubMed] [CrossRef]
     [Google Scholar]
  3. Bai X., Zhang J., Ewing A., Miller S. A., Jancso Radek A., Shevchenko D. V., Tsukerman K., Walunas T., Lapidus A. & other authors ( 2006). Living with genome instability: the adaptation of phytoplasmas to diverse environments of their insect and plant hosts. J Bacteriol 188:3682–3696 [View Article] [PubMed]
     [Google Scholar]
  4. Bai X., Correa V. R., Toruño T. Y., Ammar D., Kamoun S., Hogenhout S. A. ( 2009). AY-WB phytoplasma secretes a protein that targets plant cell nuclei. Mol Plant Microbe Interact 22:18–30 [View Article] [PubMed]
     [Google Scholar]
  5. Blomquist C. L., Barbara D. J., Davies D. L., Clark M. F., Kirkpatrick B. C. ( 2001). An immunodominant membrane protein gene from the Western X-disease phytoplasma is distinct from those of other phytoplasmas. Microbiology 147:571–580 [PubMed]
     [Google Scholar]
  6. Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., Madden T. L. ( 2009). blast+: architecture and applications. BMC Bioinformatics 10:421 [View Article] [PubMed]
     [Google Scholar]
  7. Carraro L., Osler R., Loi N., Favali M. A. ( 1991). Transmission characteristics of the clover phyllody agent by dodder. J Phytopathol 133:15–22 [CrossRef]
     [Google Scholar]
  8. Cettul E., Firrao G. ( 2011). Development of phytoplasma-induced flower symptoms in Arabidopsis thaliana . Physiol Mol Plant Pathol 76:204–211 [View Article]
     [Google Scholar]
  9. Cimerman A., Arnaud G., Foissac X. ( 2006). Stolbur phytoplasma genome survey achieved using a suppression subtractive hybridization approach with high specificity. Appl Environ Microbiol 72:3274–3283 [View Article] [PubMed]
     [Google Scholar]
  10. Cimerman A., Pacifico D., Salar P., Marzachì C., Foissac X. ( 2009). Striking diversity of vmp1, a variable gene encoding a putative membrane protein of the stolbur phytoplasma. Appl Environ Microbiol 75:2951–2957 [View Article] [PubMed]
     [Google Scholar]
  11. Delcher A. L., Bratke K. A., Powers E. C., Salzberg S. L. ( 2007). Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679 [View Article] [PubMed]
     [Google Scholar]
  12. Firrao G., Smart C. D., Kirkpatrick B. C. ( 1996a). Physical map of the Western X-disease phytoplasma chromosome. J Bacteriol 178:3985–3988 [PubMed]
     [Google Scholar]
  13. Firrao G., Carraro L., Gobbi E., Locci R. ( 1996b). Molecular characterization of a phytoplasma causing phyllody in clover and other herbaceous hosts in Northern Italy. Eur J Plant Pathol 102:817–822 [CrossRef]
     [Google Scholar]
  14. Firrao G., Gibb K., Streten C. ( 2005). Short taxonomic guide to the genus “Candidatus Phytoplasma”. J Plant Pathol 87:249–263
     [Google Scholar]
  15. Galbraith D. W., Harkins K. R., Maddox J. M., Ayres N. M., Sharma D. P., Firoozabady E. ( 1983). Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051 [View Article] [PubMed]
     [Google Scholar]
  16. Garcia-Chapa M., Batlle A., Rekab D., Rosquete M. R., Firrao G. ( 2004). PCR-mediated whole genome amplification of phytoplasmas. J Microbiol Methods 56:231–242 [View Article] [PubMed]
     [Google Scholar]
  17. Gasparich G. E. ( 2010). Spiroplasmas and phytoplasmas: microbes associated with plant hosts. Biologicals 38:193–203 [View Article] [PubMed]
     [Google Scholar]
  18. Glass J. I., Assad-Garcia N., Alperovich N., Yooseph S., Lewis M. R., Maruf M., Hutchison C. A. III, Smith H. O., Venter J. C. ( 2006). Essential genes of a minimal bacterium. Proc Natl Acad Sci U S A 103:425–430 [View Article] [PubMed]
     [Google Scholar]
  19. Griffiths H. M., Gundersen D. E., Sinclair W. A., Lee I.-M., Davis R. E. ( 1994). Mycoplasmalike organisms from milkweed, goldenrod, and spyrea, represent two new 16SrRNA subgroups and three new strain subclusters related to peach X-disease MLOs. Can J Phytopathol 16:255–260 [View Article]
     [Google Scholar]
  20. Gundersen D. E., Lee I.-M., Schaff D. A., Harrison N. A., Chang C. J., Davis R. E., Kingsbury D. T. ( 1996). Genomic diversity and differentiation among phytoplasma strains in 16S rRNA groups I (aster yellows and related phytoplasmas) and III (X-disease and related phytoplasmas). Int J Syst Bacteriol 46:64–75 [View Article] [PubMed]
     [Google Scholar]
  21. Hopfe M., Hoffmann R., Henrich B. ( 2004). P80, the HinT interacting membrane protein, is a secreted antigen of Mycoplasma hominis . BMC Microbiol 4:46 [PubMed] [CrossRef]
     [Google Scholar]
  22. Hoshi A., Oshima K., Kakizawa S., Ishii Y., Ozeki J., Hashimoto M., Komatsu K., Kagiwada S., Yamaji Y., Namba S. ( 2009). A unique virulence factor for proliferation and dwarfism in plants identified from a phytopathogenic bacterium. Proc Natl Acad Sci U S A 106:6416–6421 [View Article] [PubMed]
     [Google Scholar]
  23. Huang W., Umbach D. M., Vincent Jordan N., Abell A. N., Johnson G. L., Li L. ( 2011). Efficiently identifying genome-wide changes with next-generation sequencing data. Nucleic Acids Res 39:e130 [View Article] [PubMed]
     [Google Scholar]
  24. IRPCM Phytoplasma/Spiroplasma Working Team – Phytoplasma taxonomy group ( 2004). ‘Candidatus Phytoplasma’, a taxon for the wall-less, non-helical prokaryotes that colonize plant phloem and insects. Int J Syst Evol Microbiol 54:1243–1255 [View Article] [PubMed]
     [Google Scholar]
  25. Katoh K., Kuma K., Toh H., Miyata T. ( 2005). mafft version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518 [View Article] [PubMed]
     [Google Scholar]
  26. Kawar P. G., Pagariya M. C., Dixit G. B., Prasad D. T. ( 2010). Identification and isolation of SCGS phytoplasma-specific fragments by riboprofiling and development of specific diagnostic tool. J Plant Biochem Biotechnol 19:185–194 [CrossRef]
     [Google Scholar]
  27. Kollar A., Seemüller E. ( 1989). Base composition of the DNA of mycoplasma-like organisms associated with various plant diseases. J Phytopathol 127:177–186 [View Article]
     [Google Scholar]
  28. Kube M., Schneider B., Kuhl H., Dandekar T., Heitmann K., Migdoll A. M., Reinhardt R., Seemüller E. ( 2008). The linear chromosome of the plant-pathogenic mycoplasma ‘Candidatus Phytoplasma mali’. BMC Genomics 9:306 [PubMed] [CrossRef]
     [Google Scholar]
  29. Kube M., Mitrovic J., Duduk B., Rabus R., Seemüller E. ( 2012). Current view on phytoplasma genomes and encoded metabolism. Scientific World Journal 2012:185942 [PubMed] [CrossRef]
     [Google Scholar]
  30. Kurtz S., Phillippy A., Delcher A. L., Smoot M., Shumway M., Antonescu C., Salzberg S. L. ( 2004). Versatile and open software for comparing large genomes. Genome Biol 5:R12 [View Article] [PubMed]
     [Google Scholar]
  31. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A. & other authors ( 2007). clustal w and clustal x version 2.0. Bioinformatics 23:2947–2948 [View Article] [PubMed]
     [Google Scholar]
  32. Lee I.-M., Davis R. E., Gundersen-Rindal D. E. ( 2000). Phytoplasma: phytopathogenic mollicutes. Annu Rev Microbiol 54:221–255 [PubMed] [CrossRef]
     [Google Scholar]
  33. Li H., Durbin R. ( 2009). Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760 [View Article] [PubMed]
     [Google Scholar]
  34. Liefting L. W., Kirkpatrick B. C. ( 2003). Cosmid cloning and sample sequencing of the genome of the uncultivable mollicute, Western X-disease phytoplasma, using DNA purified by pulsed-field gel electrophoresis. FEMS Microbiol Lett 221:203–211 [View Article] [PubMed]
     [Google Scholar]
  35. MacLean A. M., Sugio A., Makarova O. V., Findlay K. C., Grieve V. M., Tóth R., Nicolaisen M., Hogenhout S. A. ( 2011). Phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants. Plant Physiol 157:831–841 [View Article] [PubMed]
     [Google Scholar]
  36. Marcelletti S., Ferrante P., Petriccione M., Firrao G., Scortichini M. ( 2011). Pseudomonas syringae pv. actinidiae draft genomes comparison reveal strain-specific features involved in adaptation and virulence to Actinidia species. PLoS ONE 6:e27297 [View Article] [PubMed]
     [Google Scholar]
  37. Marcone C., Jarausch B., Jarausch W. ( 2010). ‘Candidatus Phytoplasma prunorum’ the causal agent of European stone fruit yellows: an overview. J Plant Pathol 92:19–34
     [Google Scholar]
  38. Oshima K., Shiomi T., Kuboyama T., Sawayanagi T., Nishigawa H., Kakizawa S., Miyata S., Ugaki M., Namba S. ( 2001). Isolation and characterization of derivative lines of the Onion Yellows phytoplasma that do not cause stunting or phloem hyperplasia. Phytopathology 91:1024–1029 [View Article] [PubMed]
     [Google Scholar]
  39. Oshima K., Kakizawa S., Nishigawa H., Jung H.-Y., Wei W., Suzuki S., Arashida R., Nakata D., Miyata S. & other authors ( 2004). Reductive evolution suggested from the complete genome sequence of a plant-pathogenic phytoplasma. Nat Genet 36:27–29 [View Article] [PubMed]
     [Google Scholar]
  40. Osler R., Firrao G., Carraro L., Loi N., Musetti R., Chen T. A. ( 1994). Biodiversity of plant MLOs in a well defined ecological area. IOM Lett 3:286–287
     [Google Scholar]
  41. Peterlongo P., Chikhi R. ( 2012). Mapsembler, targeted and micro assembly of large NGS datasets on a desktop computer. BMC Bioinformatics 13:48 [View Article] [PubMed]
     [Google Scholar]
  42. Poptsova M. S., Gogarten J. P. ( 2007). BranchClust: a phylogenetic algorithm for selecting gene families. BMC Bioinformatics 8:120 [View Article] [PubMed]
     [Google Scholar]
  43. Seemüller E., Kampmann M., Kiss E., Schneider B. ( 2011). HflB gene-based phytopathogenic classification of ‘Candidatus Phytoplasma mali’ strains and evidence that strain composition determines virulence in multiply infected apple trees. Mol Plant Microbe Interact 24:1258–1266 [PubMed] [CrossRef]
     [Google Scholar]
  44. Sugio A., Kingdom H. N., MacLean A. M., Grieve V. M., Hogenhout S. A. ( 2011). Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proc Natl Acad Sci U S A 108:E1254–E1263 [View Article] [PubMed]
     [Google Scholar]
  45. Tran-Nguyen L. T., Gibb K. S. ( 2007). Optimizing phytoplasma DNA purification for genome analysis. J Biomol Tech 18:104–112 [PubMed]
     [Google Scholar]
  46. Tran-Nguyen L. T., Kube M., Schneider B., Reinhardt R., Gibb K. S. ( 2008). Comparative genome analysis of “Candidatus Phytoplasma australiense” (subgroup tuf-Australia I; rp-A) and “Ca. Phytoplasma asteris” strains OY-M and AY-WB. J Bacteriol 190:3979–3991 [PubMed] [CrossRef]
     [Google Scholar]
  47. Valiunas D., Samuitiene M., Rasomavicius V., Navalinskiene M., Staniulis J., Davis R. E. ( 2007). Subgroup 16SrIII-F phytoplasma strains in an invasive plant, Heracleum sosnowskyi, and an ornamental, Dictamnus albus . J Plant Pathol 89:137–140
     [Google Scholar]
  48. Vincent C. D., Friedman J. R., Jeong K. C., Buford E. C., Miller J. L., Vogel J. P. ( 2006). Identification of the core transmembrane complex of the Legionella Dot/Icm type IV secretion system. Mol Microbiol 62:1278–1291 [View Article] [PubMed]
     [Google Scholar]
  49. Wall D. P., Fraser H. B., Hirsh A. E. ( 2003). Detecting putative orthologs. Bioinformatics 19:1710–1711 [View Article] [PubMed]
     [Google Scholar]
  50. Wei W., Davis R. E., Lee I.-M., Zhao Y. ( 2007). Computer-simulated RFLP analysis of 16S rRNA genes: identification of ten new phytoplasma groups. Int J Syst Evol Microbiol 57:1855–1867 [PubMed] [CrossRef]
     [Google Scholar]
  51. Zerbino D. R., Birney E. ( 2008). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829 [View Article] [PubMed]
     [Google Scholar]
  52. Zhao Y., Wei W., Lee I.-M., Shao J., Suo X., Davis R. E. ( 2009). Construction of an interactive online phytoplasma classification tool, iPhyClassifier, and its application in analysis of the peach X-disease phytoplasma group (16SrIII). Int J Syst Evol Microbiol 59:2582–2593 [View Article] [PubMed]
     [Google Scholar]
  53. Zonneveld B. J. M., Leitch I. J., Bennett M. D. ( 2005). First nuclear DNA amounts in more than 300 angiosperms. Ann Bot (Lond) 96:229–244 [PubMed] [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.061432-0
Loading
Genome drafts of four phytoplasma strains of the ribosomal group 16SrIII
Microbiology 158, 2805 (2012); https://doi.org/10.1099/mic.0.061432-0
/content/journal/micro/10.1099/mic.0.061432-0
/content/journal/micro/10.1099/mic.0.061432-0
Loading

Data & Media loading...

Most cited 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