1887

Abstract

Phytoplasmas (species of the genus ‘ ’) are insect-vectored phytopathogenic bacteria associated with economically and ecologically important crop diseases. Strawberry production represents an important part of agricultural activity in Mexico and elsewhere, and infection of plants with phytoplasma renders the fruit inedible by altering plant development, resulting in virescence and phyllody. In this study we examined samples taken from four strawberry plants showing symptoms associated with strawberry green petal disease and from two periwinkle plants showing virescence, sampled in different areas of Mexico. Analysis of the 16S rRNA-encoding sequences showed that the plants were infected with a phytoplasma previously identified as Mexican periwinkle virescence (MPV; 16SrXIII). Examination of bacterial sequences from these samples revealed that two distinct 16S rRNA gene sequences were present in each sample along with a single chaperonin-60 (60) sequence and a single B sequence, suggesting that this strain displays 16S rRNA gene sequence heterogeneity. Two distinct operons, identified with subgroup 16SrXIII-A and the newly described subgroup 16SrXIII-I, were identified from the six samples analyzed, delineating the novel subgroup 16SrXIII-(A/I)I, following the nomenclature proposed for heterogeneous subgroups.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.001365
2016-11-01
2021-08-01
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/66/11/4406.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.001365&mimeType=html&fmt=ahah

References

  1. Bonfield J. K., Whitwham A. 2010; Gap5-editing the billion fragment sequence assembly. Bioinformatics 26:1699–1703 [View Article][PubMed]
    [Google Scholar]
  2. Botti S., Bertaccini A. 2003; Variability and functional role of chromosomal sequences in 16SrI-B subgroup phytoplasmas including aster yellows and related strains. J Appl Microbiol 94:103–110 [View Article][PubMed]
    [Google Scholar]
  3. Bouffard K. 2012; Florida strawberry farmers face increasing competition from Mexico. In The Ledger Lakeland, Florida: Ledger Publishing Company;
    [Google Scholar]
  4. Contaldo N., Mejia J. F., Paltrinieri S., Calari A., Bertaccini A. 2012; Identification and GroEl gene characterization of green petal phytoplasma infecting strawberry in Italy. Phytopathogenic Mollicutes 2:59–62 [View Article]
    [Google Scholar]
  5. Davis R. E., Jomantiene R., Dally E. L. 1998; Interoperon sequence heterogeneity and differential PCR-mediated amplification of sequences from the two rRNA operons in phytoplasma. In Proceedings of the 12th International Conference , pp. 176–177 Sydney, Australia: International Organization of Mycoplasmology;
    [Google Scholar]
  6. Davis R. E., Jomantiene R., Kalvelyte A., Dally E. L. 2003; Differential amplification of sequence heterogeneous ribosomal RNA genes and classification of the Fragaria multicipita’ phytoplasma. Microbiol Res 158:229–236 [View Article][PubMed]
    [Google Scholar]
  7. Davis R. E., Zhao Y., Dally E. L., Lee I. M., Jomantiene R., Douglas S. M. 2013; ‘Candidatus phytoplasma pruni’, a novel taxon associated with X-disease of stone fruits, Prunus spp.: multilocus characterization based on 16S rRNA, secY, and ribosomal protein genes. Int J Syst Evol Microbiol 63:766–776 [View Article][PubMed]
    [Google Scholar]
  8. Dumonceaux T. J., Hill J. E., Hemmingsen S. M., Van Kessel A. G. 2006; Characterization of intestinal microbiota and response to dietary virginiamycin supplementation in the broiler chicken. Appl Environ Microbiol 72:2815–2823 [View Article][PubMed]
    [Google Scholar]
  9. Dumonceaux T. J., Green M., Hammond C., Perez E., Olivier C. 2014; Molecular diagnostic tools for detection and differentiation of phytoplasmas based on chaperonin-60 reveal differences in host plant infection patterns. PLoS One 9:e116039 [View Article][PubMed]
    [Google Scholar]
  10. Fernández F. D., Conci V. C., Kirschbaum D. S., Conci L. R. 2013; Molecular characterization of a phytoplasma of the ash yellows group occurring in strawberry (Fragaria x ananassa Duch.) plants in Argentina. Eur J Plant Pathol 135:1–4 [View Article]
    [Google Scholar]
  11. Fernández F. D., Meneguzzi N. G., Guzmán F. A., Kirschbaum D. S., Conci V. C., Nome C. F., Conci L. R. 2015; Detection and identification of a novel 16SrXIII subgroup phytoplasma associated with strawberry red leaf disease in Argentina. Int J Syst Evol Microbiol 65:2741–2747 [View Article][PubMed]
    [Google Scholar]
  12. Goh S. H., Potter S., Wood J. O., Hemmingsen S. M., Reynolds R. P., Chow A. W. 1996; HSP60 gene sequences as universal targets for microbial species identification: studies with coagulase-negative staphylococci. J Clin Microbiol 34:818–823[PubMed]
    [Google Scholar]
  13. Gundersen D. E., Lee I.-M. 1996; Ultrasensitive detection of phytoplasmas by nested-PCR assays using two universal primer pairs. Phytopathol Mediterr 35:144–151
    [Google Scholar]
  14. 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 Sys Bacteriol 46:64–75 [View Article]
    [Google Scholar]
  15. Harrison N. A., Legard D. E., DiBonito R., Richardson P. A. 1997; Detection and differentiation of phytoplasmas associated with diseases of strawberry in Florida. Plant Dis 81:230 [View Article]
    [Google Scholar]
  16. Harrison N. A., Boa E., Carpio M. L. 2003; Characterization of phytoplasmas detected in Chinaberry trees with symptoms of leaf yellowing and decline in Bolivia. Plant Pathol 52:147–157 [View Article]
    [Google Scholar]
  17. Hodgetts J., Boonham N., Mumford R., Harrison N., Dickinson M. 2008; Phytoplasma phylogenetics based on analysis of secA and 23S rRNA gene sequences for improved resolution of candidate species of ‘Candidatus phytoplasma’. Int J Syst Evol Microbiol 58:1826–1837 [View Article][PubMed]
    [Google Scholar]
  18. Honetšlegrová J. F., Vibio M., Bertaccinc A. 1996; Electron microscopy and molecular identification of phytoplasmas associated with strawberry green petals in the Czech Republic. Eur J Plant Pathol 102:831–835 [View Article]
    [Google Scholar]
  19. IRPCM 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]
  20. Jomantiene R., Davis R. E., Maas J., Dally E. L. 1998; Classification of new phytoplasmas associated with diseases of strawberry in Florida, based on analysis of 16S rRNA and ribosomal protein gene operon sequences. Int J Sys Bacteriol 48:269–277 [View Article]
    [Google Scholar]
  21. Jomantiene R., Maas J. L., Dally E. L., Davis R. E. 1999; First report of clover yellow edge and STRAWB2 phytoplasmas in strawberry in Maryland. Plant Dis 83:1072 [View Article]
    [Google Scholar]
  22. Jomantiene R. J., Maas L., Davis R. E., Dally E. L. 2001; Molecular identification and classification of a phytoplasma associated with phyllody of strawberry fruit in Maryland. Plant Dis 85:335 [CrossRef]
    [Google Scholar]
  23. Jomantiene R., Davis R. E., Valiunas D., Alminaite A. 2002; New group 16SrIII phytoplasma lineages in Lithuania exhibit rRNA interoperon sequence heterogeneity. Eur J Plant Pathol 108:507–517 [CrossRef]
    [Google Scholar]
  24. Lee I.-M., Hammond R. W., Davis R. E., Gundersen D. E. 1993; Universal amplification and analysis of pathogen 16S rDNA for classification and identification of mycoplasmalike organisms. Phytopathology 83:834–842 [View Article]
    [Google Scholar]
  25. Lee I-M., Gundersen-Rindal D. E., Davis R. E., Bartoszyk I. M. 1998; Revised classification scheme of phytoplasmas based on RFLP analyses of 16S rRNA and ribosomal protein gene sequences. Int J Syst Bacteriol 48:1153–1169 [View Article]
    [Google Scholar]
  26. Lee I.-M., Davis R. E., Gundersen-Rindal D. E. 2000; Phytoplasma: phytopathogenic mollicutes. Annu Rev Microbiol 54:221–255 [View Article][PubMed]
    [Google Scholar]
  27. Lee I.-M., Gundersen-Rindal D. E., Davis R. E., Bottner K. D., Marcone C., Seemüller E. 2004; ‘Candidatus phytoplasma asteris’, a novel phytoplasma taxon associated with aster yellows and related diseases. Int J Syst Evol Microbiol 54:1037–1048 [View Article][PubMed]
    [Google Scholar]
  28. Lee I.-M., Zhao Y., Bottner K. D. 2006; SecY gene sequence analysis for finer differentiation of diverse strains in the aster yellows phytoplasma group. Mol Cell Prob 20:87–91 [View Article]
    [Google Scholar]
  29. Liefting L. W., Andersen M. T., Beever R. E., Gardner R. C., Forster R. L. 1996; Sequence heterogeneity in the two 16S rRNA genes of Phormium yellow leaf phytoplasma. Appl Environ Microbiol 62:3133–3139[PubMed]
    [Google Scholar]
  30. Links M. G., Chaban B., Hemmingsen S. M., Muirhead K., Hill J. E. 2013; mPUMA: a computational approach to microbiota analysis by de novo assembly of operational taxonomic units based on protein-coding barcode sequences. Microbiome 1:23 [View Article][PubMed]
    [Google Scholar]
  31. Links M. G., Demeke T., Gräfenhan T., Hill J. E., Hemmingsen S. M., Dumonceaux T. J. 2014; Simultaneous profiling of seed-associated bacteria and fungi reveals antagonistic interactions between microorganisms within a shared epiphytic microbiome on Triticum and Brassica seeds. New Phytol 202:542–553 [View Article][PubMed]
    [Google Scholar]
  32. Marcone C., Lee I.-M., Davis R. E., Ragozzino A., Seemüller E. 2000; Classification of aster yellows-group phytoplasmas based on combined analyses of rRNA and tuf gene sequences. Int J Syst Evol Microbiol 50:1703–1713 [View Article][PubMed]
    [Google Scholar]
  33. McKenney E. A., Ashwell M., Lambert J. E., Fellner V. 2014; Fecal microbial diversity and putative function in captive western lowland gorillas (Gorilla gorilla gorilla), common chimpanzees (Pan troglodytes), Hamadryas baboons (Papio hamadryas) and binturongs (Arctictis binturong). Integr Zool 9:557–569 [View Article][PubMed]
    [Google Scholar]
  34. Mello A. A. P. O., Bedendo I. P., Camargo L. E. A. 2006; Sequence heterogeneity in the 16S rDNA of tomato big bud phytoplasma belonging to group 16SrIII. J Phytopathol 154:245–249 [CrossRef]
    [Google Scholar]
  35. Mitrović J., Kakizawa S., Duduk B., Oshima K., Namba S., Bertaccini A. 2011; The groEL gene as an additional marker for finer differentiation of ‘Candidatus phytoplasma asteris’-related strains. Ann Appl Biol 159:41–48 [View Article]
    [Google Scholar]
  36. Mitrović J., Smiljković M., Seemüller E., Reinhardt R., Hüttel B., Büttner C., Bertaccini A., Kube M., Duduk B. 2015; Differentiation of ‘Candidatus phytoplasma cynodontis’ based on 16S rRNA and groEL genes and dentification of a new subgroup, 16SrXIV-C. Plant Disease 99:1578–1583 [View Article]
    [Google Scholar]
  37. Murray R. G., Stackebrandt E. 1995; Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol 45:186–187 [View Article][PubMed]
    [Google Scholar]
  38. Olivier C. Y., Séguin-Swartz G., Hegedus D., Barasubiye T. 2006; First report of ‘Candidatus phytoplasma asteris’-related strains in Brassica rapa in Saskatchewan, Canada. Plant Disease 90:832 [View Article]
    [Google Scholar]
  39. Padovan A., Gibb K., Persley D. 2000; Association of ‘Candidatus phytoplasma australiense’ with green petal and lethal yellows diseases in strawberry. Plant Pathol 49:362–369 [View Article]
    [Google Scholar]
  40. Pérez-López E., Luna-Rodríguez M., Olivier C. Y., Dumonceaux T. J. 2016a; The underestimated diversity of phytoplasmas in Latin America. Int J Syst Evol Microbiol 66:492–513 [View Article][PubMed]
    [Google Scholar]
  41. Pérez-López E., Olivier C. Y., Luna-Rodríguez M., Rodríguez Y., Iglesias L. G., Castro-Luna A., Adame-García J., Dumonceaux T. J. 2016b; Maize bushy stunt phytoplasma affects native corn at high elevations in Southeast Mexico. Eur J For Pathol 145:963–971 [View Article]
    [Google Scholar]
  42. Santos-Cervantes M. E., Chávez-Medina J. A., Acosta-Pardini J., Flores-Zamora G. L., Méndez-Lozano J., Leyva-López N. E. 2010; Genetic diversity and geographical distribution of phytoplasmas associated with potato purple top disease in Mexico. Plant Dis 94:388–395 [View Article]
    [Google Scholar]
  43. Sugawara K., Himeno M., Keima T., Kitazawa Y., Maejima K., Oshima K., Namba S. 2012; Rapid and reliable detection of phytoplasma by loop-mediated isothermal amplification targeting a housekeeping gene. J Gen Plant Pathol 78:389–397 [View Article]
    [Google Scholar]
  44. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013; mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  45. Torres L., Galdeano E., Docampo D., Conci L. 2004; Characterization of an aster yellows phytoplasma associated with catharanthus little leaf in Argentina. J Plant Pathol 86:209–214
    [Google Scholar]
  46. Valiunas D., Staniulis J., Davis R. E. 2006; Candidatus phytoplasma fragariae’, a novel phytoplasma taxon discovered in yellows diseased strawberry, Fragaria x ananassa. Int J Syst Evol Microbiol 56:277–281 [View Article][PubMed]
    [Google Scholar]
  47. Valiunas D., Jomantiene R., Davis R. E. 2013; Evaluation of the DNA-dependent RNA polymerase β-subunit gene (rpoB) for phytoplasma classification and phylogeny. Int J Syst Evol Microbiol 63:3904–3914 [View Article][PubMed]
    [Google Scholar]
  48. Verbeke T. J., Sparling R., Hill J. E., Links M. G., Levin D., Dumonceaux T. J. 2011; Predicting relatedness of bacterial genomes using the chaperonin-60 universal target (cpn60 UT): application to Thermoanaerobacter species. Syst Appl Microbiol 34:171–179 [View Article][PubMed]
    [Google Scholar]
  49. Wei W., Lee I. M., Davis R. E., Suo X., Zhao Y. 2008; Automated RFLP pattern comparison and similarity coefficient calculation for rapid delineation of new and distinct phytoplasma 16Sr subgroup lineages. Int J Syst Evol Microbiol 58:2368–2377 [View Article][PubMed]
    [Google Scholar]
  50. Wei W., Wu W., Davis R. E., Lee I.-M., Zhao Y. 2016; Development of molecular markers and a diagnostic tool for investigation of coinfections by and interactions between potato purple top and potato witches’-broom phytoplasmas in tomato. Ann Appl Biol 168:133–141 [CrossRef]
    [Google Scholar]
  51. 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]
  52. 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. C., Lichens-Park A., Kole C. Heidelberg: Springer;
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.001365
Loading
/content/journal/ijsem/10.1099/ijsem.0.001365
Loading

Data & Media loading...

Supplements

Supplementary File 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