1887

Abstract

Phytoplasmas classified in group 16SrXII infect a wide range of plants and are transmitted by polyphagous planthoppers of the family Cixiidae. Based on 16S rRNA gene sequence identity and biological properties, group 16SrXII encompasses several species, including ‘ Phytoplasma australiense ’, ‘ Phytoplasma japonicum ’ and ‘ Phytoplasma fragariae ’. Other group 16SrXII phytoplasma strains are associated with stolbur disease in wild and cultivated herbaceous and woody plants and with bois noir disease in grapevines ( L.). Such latter strains have been informally proposed to represent a separate species, ‘ Phytoplasma solani’, but a formal description of this taxon has not previously been published. In the present work, stolbur disease strain STOL11 (STOL) was distinguished from reference strains of previously described species of the ‘ Phytoplasma ’ genus based on 16S rRNA gene sequence similarity and a unique signature sequence in the 16S rRNA gene. Other stolbur- and bois noir-associated (‘ Phytoplasma solani’) strains shared >99 % 16S rRNA gene sequence similarity with strain STOL11 and contained the signature sequence. ‘ Phytoplasma solani’ is the only phytoplasma known to be transmitted by . Insect vectorship and molecular characteristics are consistent with the concept that diverse ‘ Phytoplasma solani’ strains share common properties and represent an ecologically distinct gene pool. Phylogenetic analyses of 16S rRNA, , and gene sequences supported this view and yielded congruent trees in which ‘ Phytoplasma solani’ strains formed, within the group 16SrXII clade, a monophyletic subclade that was most closely related to, but distinct from, that of ‘ Phytoplasma australiense ’-related strains. Based on distinct molecular and biological properties, stolbur- and bois noir-associated strains are proposed to represent a novel species level taxon, ‘ Phytoplasma solani’; STOL11 is designated the reference strain.

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2013-08-01
2020-01-23
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References

  1. Andersen M. T., Longmore J., Liefting L. W., Wood G. A., Sutherland P. W., Beck D. L., Forster R. L. S.. ( 1998;). Phormium yellow leaf phytoplasma is associated with strawberry lethal yellows disease in New Zealand. . Plant Disease 82:, 606–609. [CrossRef]
    [Google Scholar]
  2. Arocha Y., López M., Piñol B., Fernández M., Picornell B., Almeida R., Palenzuela I., Wilson M. R., Jones P.. ( 2005;). Candidatus Phytoplasma graminis’ and ‘Candidatus Phytoplasma caricae’, two novel phytoplasmas associated with diseases of sugarcane, weeds and papaya in Cuba. . Int J Syst Evol Microbiol 55:, 2451–2463. [CrossRef][PubMed]
    [Google Scholar]
  3. Batlle A., Altabella N., Sabate J., Lavina A.. ( 2008;). Study of the transmission of stolbur phytoplasma to different crop species, by Macrosteles quadripunctulatus. . Ann Appl Biol 152:, 235–242. [CrossRef]
    [Google Scholar]
  4. Belli G., Bianco P. A., Conti M.. ( 2010;). Grapevine yellows in Italy: past, present and future. . J Plant Pathol 92:, 303–326.
    [Google Scholar]
  5. Berger J., Dalla Via J., Baric S.. ( 2009;). Development of a TaqMan allelic discrimination assay for the distinction of two major subtypes of the grapevine yellows phytoplasma Bois noir. . Eur J Plant Pathol 124:, 521–526. [CrossRef]
    [Google Scholar]
  6. Brcak J.. ( 1979;). Leafhopper and planthopper vectors of plant disease agents in central and southern Europe. . In Leafhopper Vectors and Plant Disease Agents, pp. 97–146. Edited by Maramorosch K., Harris K. F... London:: Academic Press;.
    [Google Scholar]
  7. Choueiri E., Jreijiri F., El-Zammar S., Verdin E., Salar P., Danet J. L., Bove J., Garnier M.. ( 2002;). First report of grapevine “bois noir” disease and a new phytoplasma infecting solanaceous plants in Lebanon. . Plant Disease 86:, 697. [CrossRef]
    [Google Scholar]
  8. 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. [CrossRef][PubMed]
    [Google Scholar]
  9. Davis R. E., Dally E. L.. ( 2001;). Revised subgroup classification of group 16SrV phytoplasmas and placement of Flavescence dorée-associated phytoplasmas in two distinct subgroups. . Plant Disease 85:, 790–797. [CrossRef]
    [Google Scholar]
  10. Davis R. E., Dally E. L., Gundersen D. E., Lee I.-M., Habili N.. ( 1997;). Candidatus Phytoplasma australiense’, a new phytoplasma taxon associated with Australian grapevine yellows. . Int J Syst Bacteriol 47:, 262–269. [CrossRef][PubMed]
    [Google Scholar]
  11. Davis R. E., Jomantiene R., Zhao Y., Dally E. L.. ( 2003;). Folate biosynthesis pseudogenes, PsifolP and PsifolK, and an O-sialoglycoprotein endopeptidase gene homolog in the phytoplasma genome. . DNA Cell Biol 22:, 697–706. [CrossRef][PubMed]
    [Google Scholar]
  12. Davis R. I., Jones P., Holman T. J., Halsey K., Amice R., Tupouniua S. K. M., Seth M.. ( 2006;). Phytoplasma disease surveys in Tonga, New Caledonia and Vanuatu. . Australas Plant Pathol 35:, 335–340. [CrossRef]
    [Google Scholar]
  13. Davis R. E., Zhao Y., Dally E., 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 Bacteriol 63:, 766–776. [CrossRef]
    [Google Scholar]
  14. Duduk B., Bertaccini A.. ( 2006;). Corn with symptoms of reddening: new host of stolbur phytoplasma. . Plant Disease 90:, 1313–1319. [CrossRef]
    [Google Scholar]
  15. Duduk B., Tian J., Contaldo N., Fan X., Paltrinieri S., Chen Q., Zhao Q., Bertaccini A.. ( 2010;). Occurrence of phytoplasmas related to stolbur and to ‘Candidatus Phytoplasma japonicum’ in woody host plants in China. . J Phytopathol 158:, 100–104. [CrossRef]
    [Google Scholar]
  16. Eroglu S., Ozbek H., Sahin F.. ( 2010;). First report of group 16SrXII phytoplasma causing stolbur disease in potato plants in the eastern and southern Anatolia regions of Turkey. . Plant Disease 94:, 1374. [CrossRef]
    [Google Scholar]
  17. Fránová J., Navratil M., Jakesova H.. ( 2009;). Molecular identification of stolbur phytoplasma associated with red clover dwarf disease symptoms. . J Phytopathol 157:, 502–506. [CrossRef]
    [Google Scholar]
  18. Gasteiger E., Gattiker A., Hoogland C., Ivanyi I., Appel R. D., Bairoch A.. ( 2003;). ExPASy: The proteomics server for in-depth protein knowledge and analysis. . Nucleic Acids Res 31:, 3784–3788. [CrossRef][PubMed]
    [Google Scholar]
  19. Gatineau F., Larrue J., Clair D., Lorton F., Richard-Molard M., Boudon-Padieu E.. ( 2001;). A new natural planthopper vector of stolbur phytoplasma in the genus Pentastiridius (Hemiptera: Cixiidae). . Eur J Plant Pathol 107:, 263–271. [CrossRef]
    [Google Scholar]
  20. Gera A., Mawassi M., Zeidan M., Spiegel S., Bar-Joseph M.. ( 2005;). An isolate of 'Candidatus Phytoplasma australiense' group associated with Nivun Haamir dieback disease of papaya in Israel. . Plant Pathol 54:, 560. [CrossRef]
    [Google Scholar]
  21. Girsova N., Bottner K. D., Mozhaeva K. A., Kastalyeva T. B., Owens R. A., Lee I.-M.. ( 2008;). Molecular detection and identification of group 16SrI and 16SrXII phytoplasmas associated with diseased potatoes in Russia. . Plant Disease 92:, 654. [CrossRef]
    [Google Scholar]
  22. 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]
  23. Hosseini P., Bahar M., Madani G., Zirak L.. ( 2011;). Molecular characterization of phytoplasmas associated with potato purple top disease in Iran. . J Phytopathol 159:, 241–246. [CrossRef]
    [Google Scholar]
  24. Iriti M., Quaglino F., Maffi D., Casati P., Bianco P. A., Faoro F.. ( 2008;). Solanum malacoxylon, a new natural host of Stolbur phytoplasma. . J Phytopathol 156:, 8–14.
    [Google Scholar]
  25. 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. [CrossRef][PubMed]
    [Google Scholar]
  26. Jones P., Arocha Y., Antesana O., Montilliano E., Franco P.. ( 2005;). First report of an isolate of ‘Candidatus Phytoplasma australiense’ associated with a yellow leaf roll disease of peach (Prunus persicae) in Bolivia. . Plant Pathol 54:, 558. [CrossRef]
    [Google Scholar]
  27. Jović J., Cvrković T., Mitrović M., Krnjajić S., Redinbaugh M. G., Pratt R. C., Gingery R. E., Hogenhout S. A., Toševski I.. ( 2007;). Roles of stolbur phytoplasma and Reptalus panzeri (Cixiinae, Auchenorrhyncha) in the epidemiology of Maize redness in Serbia. . Eur J Plant Pathol 118:, 85–89. [CrossRef]
    [Google Scholar]
  28. 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]
  29. Karimi M., Contaldo N., Mahmoudi B., Duduk B., Bertaccini A.. ( 2009;). Identification of stolbur-related phytoplasmas in grapevine showing decline symptoms in Iran. . Le Progrès agricole et viticole, Hors Série, Extended abstract of the 16th Meeting ICVG, Dijion, France, 31 August–4 September, pp. 208–209.
  30. Kumar S., Nei M., Dudley J., Tamura K.. ( 2008;). mega: a biologist-centric software for evolutionary analysis of DNA and protein sequences. . Brief Bioinform 9:, 299–306. [CrossRef][PubMed]
    [Google Scholar]
  31. Langer M., Maixner M.. ( 2004;). Molecular characterisation of Grapevine yellows associated phytoplasmas of the stolbur group based on RFLP-analysis of non-ribosomal DNA. . Vitis 43:, 191–200.
    [Google Scholar]
  32. Lee I.-M., Davis R. E., Gundersen-Rindal D. E.. ( 2000;). Phytoplasma: phytopathogenic mollicutes. . Annu Rev Microbiol 54:, 221–255. [CrossRef][PubMed]
    [Google Scholar]
  33. Lee I.-M., Martini M., Marcone C., Zhu S. F.. ( 2004;). Classification of phytoplasma strains in the elm yellows group (16SrV) and proposal of ‘Candidatus Phytoplasma ulmi’ for the phytoplasma associated with elm yellows. . Int J Syst Evol Microbiol 54:, 337–347. [CrossRef][PubMed]
    [Google Scholar]
  34. Lee I.-M., Bottner K. D., Secor G., Rivera-Varas V.. ( 2006;). Candidatus Phytoplasma americanum’, a phytoplasma associated with a potato purple top wilt disease complex. . Int J Syst Evol Microbiol 56:, 1593–1597. [CrossRef][PubMed]
    [Google Scholar]
  35. Lee I.-M., Bottner-Parker K. D., Zhao Y., Davis R. E., Harrison N. A.. ( 2010;). Phylogenetic analysis and delineation of phytoplasmas based on secY gene sequences. . Int J Syst Evol Microbiol 60:, 2887–2897. [CrossRef][PubMed]
    [Google Scholar]
  36. Liefting L. W., Beever R. E., Winks C. J., Pearson M. N., Forster R. L. S.. ( 1997;). Planthopper transmission of Phormium yellow leaf phytoplasma. . Australas Plant Pathol 26:, 148–154. [CrossRef]
    [Google Scholar]
  37. Liefting L. W., Veerakone S., Ward L. I., Clover G. R. G.. ( 2009;). First report of ‘Candidatus Phytoplasma australiense’ in potato. . Plant Disease 93:, 969. [CrossRef]
    [Google Scholar]
  38. Maixner M.. ( 1994;). Transmission of German grapevine yellows (Vergilbungskrankheit) by the planthopper Hyalesthes obsoletus (Auchenorrhyncha: Cixiidae). . Vitis 33:, 103–104.
    [Google Scholar]
  39. Malembic-Maher S., Salar P., Filippin L., Carle P., Angelini E., Foissac X.. ( 2011;). Genetic diversity of European phytoplasmas of the 16SrV taxonomic group and proposal of ‘Candidatus Phytoplasma rubi’. . Int J Syst Evol Microbiol 61:, 2129–2134. [CrossRef][PubMed]
    [Google Scholar]
  40. Marcone C., Ragozzino A., Seemüller E.. ( 1997;). Detection and identification of phytoplasmas infecting vegetable, ornamental and forage crops in southern Italy. . J Plant Pathol 79:, 211–217.
    [Google Scholar]
  41. Martini M., Lee I.-M., Bottner K. D., Zhao Y., Botti S., Bertaccini A., Harrison N. A., Carraro L., Marcone C.. & other authors ( 2007;). Ribosomal protein gene-based phylogeny for finer differentiation and classification of phytoplasmas. . Int J Syst Evol Microbiol 57:, 2037–2051. [CrossRef][PubMed]
    [Google Scholar]
  42. Martini M., Marcone C., Mitrović J., Maixner M., Delić D., Myrta A., Ermacora P., Bertaccini A., Duduk B.. ( 2012;). Candidatus Phytoplasma convolvuli’, a new phytoplasma taxon associated with bindweed yellows in four European countries. . Int J Syst Evol Microbiol 62:, 2910–2915. [CrossRef][PubMed]
    [Google Scholar]
  43. Mertelik J., Kloudova K., Vanc P., Mokra V., Sediva J., Navratil M., Valova P.. ( 2004;). First detection of phytoplasmas in rhododendron in the Czech Republic. . Plant Disease 88:, 906. [CrossRef]
    [Google Scholar]
  44. Minucci C., Boccardo G.. ( 1997;). Genetic diversity in the stolbur phytoplasma group. . Phytopathol Mediterr 36:, 45–49.
    [Google Scholar]
  45. 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]
  46. Padovan A. C., Gibb K. S., Bertaccini A., Vibio M., Bonfiglioli R. E., Magarey P. A., Sears B. B.. ( 1995;). Molecular detection of the Australian grapevine yellows phytoplasma and comparison with grapevine yellows phytoplasmas from Italy. . Aust J Grape Wine Res 1:, 25–31. [CrossRef]
    [Google Scholar]
  47. 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. [CrossRef]
    [Google Scholar]
  48. Quaglino F., Zhao Y., Bianco P. A., Wei W., Casati P., Durante G., Davis R. E.. ( 2009;). New 16Sr subgroups and distinct single nucleotide polymorphism lineages among grapevine Bois noir phytoplasma populations. . Ann Appl Biol 154:, 279–289. [CrossRef]
    [Google Scholar]
  49. Radonjić S., Hrnčić S., Jović J., Cvrković T., Krstić O., Krnjajić S., Toševski I.. ( 2009;). Occurrence and distribution of grapevine yellows caused by Stolbur phytoplasma in Montenegro. . J Phytopathol 157:, 682–685. [CrossRef]
    [Google Scholar]
  50. Riedle-Bauer M., Sara A., Regner F.. ( 2008;). Transmission of a Stolbur phytoplasma by the Agalliinae leafhopper Anaceratagallia ribauti (Hemiptera, Auchenorrhyncha, Cicadellidae). . J Phytopathol 156:, 687–690. [CrossRef]
    [Google Scholar]
  51. Sawayanagi T., Horikoshi N., Kanehira T., Shinohara M., Bertaccini A., Cousin M. T., Hiruki C., Namba S.. ( 1999;). Candidatus phytoplasma japonicum’, a new phytoplasma taxon associated with Japanese Hydrangea phyllody. . Int J Syst Bacteriol 49:, 1275–1285. [CrossRef][PubMed]
    [Google Scholar]
  52. Seemüller E., Schneider B.. ( 2004;). Candidatus Phytoplasma mali’, ‘Candidatus Phytoplasma pyri’ and ‘Candidatus Phytoplasma prunorum’, the causal agents of apple proliferation, pear decline and European stone fruit yellows, respectively. . Int J Syst Evol Microbiol 54:, 1217–1226. [CrossRef][PubMed]
    [Google Scholar]
  53. Seemüller E., Schneider B., Mäurer R., Ahrens U., Daire X., Kison H., Lorenz K. H., Firrao G., Avinent L.. & other authors ( 1994;). Phylogenetic classification of phytopathogenic mollicutes by sequence analysis of 16S ribosomal DNA. . Int J Syst Bacteriol 44:, 440–446. [CrossRef][PubMed]
    [Google Scholar]
  54. Šeruga M., Ćurkovic Perica M., Škorić D., Kozina B., Mirošević N., Šarić A., Bertaccini A., Krajačić M.. ( 2000;). Geographic distribution of Bois Noir phytoplasmas infecting grapevines in Croatia. . J Phytopathol 148:, 239–242. [CrossRef]
    [Google Scholar]
  55. Streten C., Gibb K. S.. ( 2005;). Genetic variation in Candidatus Phytoplasma australiense. . Plant Pathol 54:, 8–14. [CrossRef]
    [Google Scholar]
  56. 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]
  57. Terlizzi F., Babini A. R., Credi R.. ( 2006;). First report of stolbur phytoplasma (16SrXII-A) on strawberry in northern Italy. . Plant Disease 90:, 831. [CrossRef]
    [Google Scholar]
  58. Torres E., Botti E., Rahola J., Martin M. P., Bertaccini A.. ( 2005;). Grapevine yellows diseases in Spain: eight year survey of disease spread and molecular characterization of phytoplasmas involved. . An Jard Bot Madr 62:, 127–133. [CrossRef]
    [Google Scholar]
  59. 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. [CrossRef][PubMed]
    [Google Scholar]
  60. Weisburg W. G., Tully J. G., Rose D. L., Petzel J. P., Oyaizu H., Yang D., Mandelco L., Sechrest J., Lawrence T. G.. & other authors ( 1989;). A phylogenetic analysis of the mycoplasmas: basis for their classification. . J Bacteriol 171:, 6455–6467.[PubMed]
    [Google Scholar]
  61. White D. T., Blackall L. L., Scott P. T., Walsh K. B.. ( 1998;). Phylogenetic positions of phytoplasmas associated with dieback, yellow crinkle and mosaic diseases of papaya, and their proposed inclusion in ‘Candidatus Phytoplasma australiense’ and a new taxon, ‘Candidatus Phytoplasma australasia’. . Int J Syst Bacteriol 48:, 941–951. [CrossRef][PubMed]
    [Google Scholar]
  62. Zirak L., Bahar M., Ahoonmanesh A.. ( 2009;). Molecular characterization of phytoplasmas related to peanut witches broom and stolbur groups infecting plum in Iran. . J Plant Pathol 91:, 713–716.
    [Google Scholar]
  63. Zirak L., Bahar M., Ahoonmanesh A.. ( 2010;). Molecular characterization of phytoplasmas associated with peach diseases in Iran. . J Phytopathol 158:, 105–110. [CrossRef]
    [Google Scholar]
  64. Zwolinska A., Krawczyk K., Pospieszny H.. ( 2012;). Molecular characterization of stolbur phytoplasma associated with pea plants in Poland. . J Phytopathol 160:, 317–323. [CrossRef]
    [Google Scholar]
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