1887

Abstract

Phytoplasmas are unculturable, cell-wall-less bacteria that parasitize plants and insects. This transkingdom life cycle requires rapid responses to vastly different environments, including transitions from plant phloem sieve elements to various insect tissues and alternations among diverse plant hosts. Features that enable such flexibility in other microbes include simple sequence repeats (SSRs) — mutation-prone, phase-variable short DNA tracts that function as ‘evolutionary rheostats’ and enhance rapid adaptations. To gain insights into the occurrence, distribution and potentially functional roles of SSRs in phytoplasmas, we performed computational analysis on the genomes of five completely sequenced phytoplasma strains, ‘ Phytoplasma asteris’-related strains OYM and AYWB, ‘ Phytoplasma australiense’-related strains CBWB and SLY and ‘ Phytoplasma mali’-related strain AP-AT. The overall density of SSRs in phytoplasma genomes was higher than in representative strains of other prokaryotes. While mono- and trinucleotide SSRs were significantly overrepresented in the phytoplasma genomes, dinucleotide SSRs and other higher-order SSRs were underrepresented. The occurrence and distribution of long SSRs in the prophage islands and phytoplasma-unique genetic loci indicated that SSRs played a role in compounding the complexity of sequence mosaics in individual genomes and in increasing allelic diversity among genomes. Findings from computational analyses were further complemented by an examination of SSRs in varied additional phytoplasma strains, with a focus on potential contingency genes. Some SSRs were located in regions that could profoundly alter the regulation of transcription and translation of affected genes and/or the composition of protein products.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.000273
2015-08-01
2020-01-20
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/65/8/2748.html?itemId=/content/journal/ijsem/10.1099/ijs.0.000273&mimeType=html&fmt=ahah

References

  1. Ahrens U., Seemüller E.. ( 1992;). Detection of DNA of plant pathogenic mycoplasma like organisms by a polymerase chain reaction that amplifies a sequence of the 16S rRNA gene. Phytopathology 82: 828–832 [CrossRef].
    [Google Scholar]
  2. Andersen M.T., Liefting L.W., Havukkala I., Beever R.E.. ( 2013;). Comparison of the complete genome sequence of two closely related isolates of ‘Candidatus Phytoplasma australiense’ reveals genome plasticity. BMC Genomics 14: 529 [CrossRef] [PubMed].
    [Google Scholar]
  3. Arashida R., Kakizawa S., Hoshi A., Ishii Y., Jung H.Y., Kagiwada S., Yamaji Y., Oshima K., Namba S.. ( 2008a;). Heterogeneic dynamics of the structures of multiple gene clusters in two pathogenetically different lines originating from the same phytoplasma. DNA Cell Biol 27: 209–217 [CrossRef] [PubMed].
    [Google Scholar]
  4. Arashida R., Kakizawa S., Ishii Y., Hoshi A., Jung H.Y., Kagiwada S., Yamaji Y., Oshima K., Namba S.. ( 2008b;). Cloning and characterization of the antigenic membrane protein (Amp) gene and in situ detection of Amp from malformed flowers infected with Japanese hydrangea phyllody phytoplasma. Phytopathology 98: 769–775 [CrossRef] [PubMed].
    [Google Scholar]
  5. 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 [CrossRef] [PubMed].
    [Google Scholar]
  6. Bayliss C.D., Field D., Moxon E.R.. ( 2001;). The simple sequence contingency loci of Haemophilus influenzae Neisseria meningitidis. J Clin Invest 107: 657–666 [CrossRef] [PubMed].
    [Google Scholar]
  7. Boonrod K., Munteanu B., Jarausch B., Jarausch W., Krczal G.. ( 2012;). An immunodominant membrane protein (Imp) of ‘Candidatus Phytoplasma mali’ binds to plant actin. Mol Plant Microbe Interact 25: 889–895 [CrossRef] [PubMed].
    [Google Scholar]
  8. Bukata L., Altabe S., de Mendoza D., Ugalde R.A., Comerci D.J.. ( 2008;). Phosphatidylethanolamine synthesis is required for optimal virulence of Brucella abortus. J Bacteriol 190: 8197–8203 [CrossRef] [PubMed].
    [Google Scholar]
  9. Chen Y.L., Montedonico A.E., Kauffman S., Dunlap J.R., Menn F.M., Reynolds T.B.. ( 2010;). Phosphatidylserine synthase and phosphatidylserine decarboxylase are essential for cell wall integrity and virulence in Candida albicans. Mol Microbiol 75: 1112–1132 [CrossRef] [PubMed].
    [Google Scholar]
  10. Chistiakov D.A., Hellemans B., Haley C.S., Law A.S., Tsigenopoulos C.S., Kotoulas G., Bertotto D., Libertini A., Volckaert F.A.. ( 2005;). A microsatellite linkage map of the European sea bass Dicentrarchus labrax L. Genetics 170: 1821–1826 [CrossRef] [PubMed].
    [Google Scholar]
  11. Coenye T., Vandamme P.. ( 2005;). Characterization of mononucleotide repeats in sequenced prokaryotic genomes. DNA Res 12: 221–233 [CrossRef] [PubMed].
    [Google Scholar]
  12. Conde-Alvarez R., Grilló M.J., Salcedo S.P., de Miguel M.J., Fugier E., Gorvel J.P., Moriyón I., Iriarte M.. ( 2006;). Synthesis of phosphatidylcholine, a typical eukaryotic phospholipid, is necessary for full virulence of the intracellular bacterial parasite Brucella abortus. Cell Microbiol 8: 1322–1335 [CrossRef] [PubMed].
    [Google Scholar]
  13. Davis R.E., Jomantiene R., Zhao Y., Dally E.L.. ( 2003;). Folate biosynthesis pseudogenes, (folP and (folK, and an O-sialoglycoprotein endopeptidase gene homolog in the phytoplasma genome. DNA Cell Biol 22: 697–706 [CrossRef] [PubMed].
    [Google Scholar]
  14. Davis R.E., Jomantiene R., Zhao Y.. ( 2005;). Lineage-specific decay of folate biosynthesis genes suggests ongoing host adaptation in phytoplasmas. DNA Cell Biol 24: 832–840 [CrossRef] [PubMed].
    [Google Scholar]
  15. Doi Y.M., Teranaka M., Yora K., Asuyama H.. ( 1967;). Mycoplasma or PLT group-like microorganisms found in the phloem elements of plants infected with mulberry dwarf, potato witches'-broom, aster yellows, or paulownia witches'-broom. Ann Phytopathol Soc Jpn 33: 259–266 [CrossRef].
    [Google Scholar]
  16. Ellegren H.. ( 2004;). Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5: 435–445 [CrossRef] [PubMed].
    [Google Scholar]
  17. Field D., Wills C.. ( 1998;). Abundant microsatellite polymorphism in Saccharomyces cerevisiae, and the different distributions of microsatellites in eight prokaryotes and S. cerevisiae, result from strong mutation pressures and a variety of selective forces. Proc Natl Acad Sci U S A 95: 1647–1652 [CrossRef] [PubMed].
    [Google Scholar]
  18. Gedvilaite A., Jomantiene R., Dabrisius J., Norkiene M., Davis R.E.. ( 2014;). Functional analysis of a lipolytic protein encoded in phytoplasma phage based genomic island. Microbiol Res 169: 388–394 [CrossRef] [PubMed].
    [Google Scholar]
  19. Gundersen D.E., Lee I.-M., Rehner S.A., Davis R.E., Kingsbury D.T.. ( 1994;). Phylogeny of mycoplasmalike organisms (phytoplasmas): a basis for their classification. J Bacteriol 176: 5244–5254 [PubMed].
    [Google Scholar]
  20. Gur-Arie R., Cohen C.J., Eitan Y., Shelef L., Hallerman E.M., Kashi Y.. ( 2000;). Simple sequence repeats in Escherichia coli: abundance, distribution, composition, and polymorphism. Genome Res 10: 62–71 [PubMed].
    [Google Scholar]
  21. Harrison N., Davis R.E., Oropeza C., Helmick E., Narvaez M., Eden-Green S., Dollet M., Dickinson M.. ( 2014;). Candidatus Phytoplasma palmicola’, associated with a lethal yellowing-type disease of coconut (Cocos nucifera L.) in Mozambique. Int J Syst Evol Microbiol 64: 1890–1899 [CrossRef].
    [Google Scholar]
  22. Heringa J., Taylor W.R.. ( 1997;). Three-dimensional domain duplication, swapping and stealing. Curr Opin Struct Biol 7: 416–421 [CrossRef] [PubMed].
    [Google Scholar]
  23. Jomantiene R., Davis R.E.. ( 2006;). Clusters of diverse genes existing as multiple, sequence-variable mosaics in a phytoplasma genome. FEMS Microbiol Lett 255: 59–65 [CrossRef] [PubMed].
    [Google Scholar]
  24. Jomantiene R., Zhao Y., Davis R.E.. ( 2007;). Sequence-variable mosaics: composites of recurrent transposition characterizing the genomes of phylogenetically diverse phytoplasmas. DNA Cell Biol 26: 557–564 [CrossRef] [PubMed].
    [Google Scholar]
  25. Kakizawa S., Oshima K., Nishigawa H., Jung H.Y., Wei W., Suzuki S., Tanaka M., Miyata S., Ugaki M., Namba S.. ( 2004;). Secretion of immunodominant membrane protein from onion yellows phytoplasma through the Sec protein-translocation system in Escherichia coli. Microbiology 150: 135–142 [CrossRef] [PubMed].
    [Google Scholar]
  26. Karlin S., Brocchieri L., Bergman A., Mrazek J., Gentles A.J.. ( 2002;). Amino acid runs in eukaryotic proteomes and disease associations. Proc Natl Acad Sci U S A 99: 333–338 [CrossRef] [PubMed].
    [Google Scholar]
  27. Kashi Y., King D.G.. ( 2006;). Simple sequence repeats as advantageous mutators in evolution. Trends Genet 22: 253–259 [CrossRef] [PubMed].
    [Google Scholar]
  28. Kashi Y., King D., Soller M.. ( 1997;). Simple sequence repeats as a source of quantitative genetic variation. Trends Genet 13: 74–78 [CrossRef] [PubMed].
    [Google Scholar]
  29. Katti M.V., Ranjekar P.K., Gupta V.S.. ( 2001;). Differential distribution of simple sequence repeats in eukaryotic genome sequences. Mol Biol Evol 18: 1161–1167 [CrossRef] [PubMed].
    [Google Scholar]
  30. King D.G.. ( 1994;). Triple repeat DNA as a highly mutable regulatory mechanism. Science 263: 595–596 [CrossRef] [PubMed].
    [Google Scholar]
  31. 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 [CrossRef] [PubMed].
    [Google Scholar]
  32. Kube M., Mitrovic J., Duduk B., Rabus R., Seemüller E.. ( 2012;). Current view on phytoplasma genomes and encoded metabolism. ScientificWorldJournal 2012: 185942 [CrossRef] [PubMed].
    [Google Scholar]
  33. Leclercq S., Rivals E., Jarne P.. ( 2010;). DNA slippage occurs at microsatellite loci without minimal threshold length in humans: a comparative genomic approach. Genome Biol Evol 2: 325–335 [CrossRef] [PubMed].
    [Google Scholar]
  34. Lee I.-M., Davis R.E., Gundersen-Rindal D.E.. ( 2000;). Phytoplasma: phytopathogenic mollicutes. Annu Rev Microbiol 54: 221–255 [CrossRef] [PubMed].
    [Google Scholar]
  35. Li Y.C., Korol A.B., Fahima T., Beiles A., Nevo E.. ( 2002;). Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11: 2453–2465 [CrossRef] [PubMed].
    [Google Scholar]
  36. Li Y.C., Korol A.B., Fahima T., Nevo E.. ( 2004;). Microsatellites within genes: structure, function, and evolution. Mol Biol Evol 21: 991–1007 [CrossRef] [PubMed].
    [Google Scholar]
  37. Liu L., Panangala V.S., Dybvig K.. ( 2002;). Trinucleotide GAA repeats dictate pMGA gene expression in Mycoplasma gallisepticum by affecting spacing between flanking regions. J Bacteriol 184: 1335–1339 [CrossRef] [PubMed].
    [Google Scholar]
  38. Loire E., Higuet D., Netter P., Achaz G.. ( 2013;). Evolution of coding microsatellites in primate genomes. Genome Biol Evol 5: 283–295 [CrossRef] [PubMed].
    [Google Scholar]
  39. Morton A., Davies D.L., Blomquist C.L., Barbara D.J.. ( 2003;). Characterization of homologues of the apple proliferation immunodominant membrane protein gene from three related phytoplasmas. Mol Plant Pathol 4: 109–114 [CrossRef] [PubMed].
    [Google Scholar]
  40. Moxon R., Bayliss C., Hood D.. ( 2006;). Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40: 307–333 [CrossRef] [PubMed].
    [Google Scholar]
  41. Mrázek J.. ( 2006;). Analysis of distribution indicates diverse functions of simple sequence repeats in Mycoplasma genomes. Mol Biol Evol 23: 1370–1385 [CrossRef] [PubMed].
    [Google Scholar]
  42. Mrázek J., Guo X., Shah A.. ( 2007;). Simple sequence repeats in prokaryotic genomes. Proc Natl Acad Sci U S A 104: 8472–8477 [CrossRef] [PubMed].
    [Google Scholar]
  43. 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 [CrossRef] [PubMed].
    [Google Scholar]
  44. Oshima K., Kakizawa S., Arashida R., Ishii Y., Hoshi A., Hayashi Y., Kagiwada S., Namba S.. ( 2007;). Presence of two glycolytic gene clusters in a severe pathogenic line of Candidatus Phytoplasma asteris. Mol Plant Pathol 8: 481–489 [CrossRef] [PubMed].
    [Google Scholar]
  45. Rocha E.P.C., Blanchard A.. ( 2002;). Genomic repeats, genome plasticity and the dynamics of Mycoplasma evolution. Nucleic Acids Res 30: 2031–2042 [CrossRef] [PubMed].
    [Google Scholar]
  46. Rocha E.P.C., Matic I., Taddei F.. ( 2002;). Over-representation of repeats in stress response genes: a strategy to increase versatility under stressful conditions?. Nucleic Acids Res 30: 1886–1894 [CrossRef] [PubMed].
    [Google Scholar]
  47. Shuman S.. ( 1994;). Novel approach to molecular cloning and polynucleotide synthesis using vaccinia DNA topoisomerase. J Biol Chem 269: 32678–32684 [PubMed].
    [Google Scholar]
  48. Simmons W.L., Denison A.M., Dybvig K.. ( 2004;). Resistance of Mycoplasma pulmonis to complement lysis is dependent on the number of Vsa tandem repeats: shield hypothesis. Infect Immun 72: 6846–6851 [CrossRef] [PubMed].
    [Google Scholar]
  49. Suzuki S., Oshima K., Kakizawa S., Arashida R., Jung H.Y., Yamaji Y., Nishigawa H., Ugaki M., Namba S.. ( 2006;). Interaction between the membrane protein of a pathogen and insect microfilament complex determines insect-vector specificity. Proc Natl Acad Sci U S A 103: 4252–4257 [CrossRef] [PubMed].
    [Google Scholar]
  50. Tran-Nguyen L.T.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 [CrossRef] [PubMed].
    [Google Scholar]
  51. Trivedi S.. ( 2006;). Comparison of simple sequence repeats in 19 archaea. Genet Mol Res 5: 741–772 [PubMed].
    [Google Scholar]
  52. Trivedi S.. ( 2013;). Repeats in transforming acidic coiled-coil (TACC) genes. Biochem Genet 51: 458–473 [CrossRef] [PubMed].
    [Google Scholar]
  53. Tsai J.H.. ( 1979;). Vector transmission of mycoplasmal agents of plant diseases. . In The Mycoplasmas, pp. 265–307. Edited by Whitcomb R. F, Tully J. G. San Diego: [CrossRef] Academic Press;.
    [Google Scholar]
  54. van Belkum A., Scherer S., van Alphen L., Verbrugh H.. ( 1998;). Short-sequence DNA repeats in prokaryotic genomes. Microbiol Mol Biol Rev 62: 275–293 [PubMed].
    [Google Scholar]
  55. 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 [CrossRef] [PubMed].
    [Google Scholar]
  56. Wei W., Davis R.E., Jomantiene R., Zhao Y.. ( 2008;). Ancient, recurrent phage attacks and recombination shaped dynamic sequence-variable mosaics at the root of phytoplasma genome evolution. Proc Natl Acad Sci U S A 105: 11827–11832 [CrossRef] [PubMed].
    [Google Scholar]
  57. Young E.T., Sloan J.S., Van Riper K.. ( 2000;). Trinucleotide repeats are clustered in regulatory genes in Saccharomyces cerevisiae. Genetics 154: 1053–1068 [PubMed].
    [Google Scholar]
  58. 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 [CrossRef] [PubMed].
    [Google Scholar]
  59. Zhao Y., Wei W., Davis R.E., Lee I.-M.. ( 2010;). Recent advances in 16S rRNA gene-based phytoplasma differentiation, classification and taxonomy. . In Phytoplasmas: Genomes, Plant Hosts and Vector, pp. 64–92. Edited by Weintraub P, Jones P. Wallingford, UK: CABI Publishing;.
    [Google Scholar]
  60. Zhao Y., Davis R.E., Wei W., Shao J., Jomantiene R.. ( 2014;). Phytoplasma genomes: evolution through mutually complementary mechanisms, gene loss and horizontal acquisition. . In Genomics of Plant-Associated Bacteria, pp. 235–271. Edited by Gross D, Lichens-Park A, Kole C. Heidelberg: [CrossRef] Springer;.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.000273
Loading
/content/journal/ijsem/10.1099/ijs.0.000273
Loading

Data & Media loading...

Supplements

Supplementary Data



PDF

Most cited articles

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