1887

Abstract

Phytoplasmas are plant-pathogenic, phloem-colonizing, cell wall-less microorganisms that are primarily dependent on insect transmission for their spread and survival. The life cycle of phytoplasmas involves replication in insects and host plants. Until recently, phytoplasmas have resisted all attempts at cultivation in cell-free media, making these pathogens poorly characterized on a physiological and biochemical basis. However, host–pathogen relationships can be studied by investigating immunodominant membrane proteins (IDPs), which are located on the exterior surfaces of phytoplasma cells and are the most abundant proteins of the cell membrane. These membrane proteins come in direct contact with both insect and plant hosts and are thought to play a crucial role in phytoplasma spread both within the plant and by insect vectors. Therefore, there is great interest in studying this class of proteins. We summarize and discuss important investigations about these membrane proteins, which have already provided a better understanding of the host–phytoplasma relationship.

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2016-08-01
2024-04-18
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References

  1. Arashida R., Kakizawa S., Ishii Y., Hoshi A., Jung H. Y., Kagiwada S., Yamaji Y., Oshima K., Namba S. 2008; 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 [View Article][PubMed]
    [Google Scholar]
  2. Bai X., Zhang J., Ewing A., Miller S. A., Jancso Radek A., Shevchenko D., Tsukerman K., Walunas T., Lapidus A. et al. 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]
  3. Barbara D. J., Morton A., Clark M. F., Davies D. L. 2002; Immunodominant membrane proteins from two phytoplasmas in the aster yellows clade (chlorante aster yellows and clover phyllody) are highly divergent in the major hydrophilic region. Microbiology 148:157–167 [View Article][PubMed]
    [Google Scholar]
  4. Berg M., Davies D. L., Clark M. F., Vetten H. J., Maier G., Marcone C., Seemüller E. 1999; Isolation of the gene encoding an immunodominant membrane protein of the apple proliferation phytoplasma, and expression and characterization of the gene product. Microbiology 145:1937–1943 [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 [View Article][PubMed]
    [Google Scholar]
  6. Boonrod K., Galetzka D., Nagy P. D., Conrad U., Krczal G. 2004; Single-chain antibodies against a plant viral RNA-dependent RNA polymerase confer virus resistance. Nat Biotechnol 22:856–862 [View Article][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 [View Article][PubMed]
    [Google Scholar]
  8. Bosco D., Galetto L., Leoncini P., Saracco P., Raccah B., Marzachì C. 2007; Interrelationships between ‘Candidatus Phytoplasma asteris’ and its leafhopper vectors (Homoptera: Cicadellidae). J Econ Entomol 100:1504–1511 [View Article][PubMed]
    [Google Scholar]
  9. Buxa S. V., Degola F., Polizzotto R., De Marco F., Loschi A., Kogel K. H., di Toppi L. S., van Bel A. J., Musetti R. 2015; Phytoplasma infection in tomato is associated with re-organization of plasma membrane, ER stacks, and actin filaments in sieve elements. Front Plant Sci 6:650 [View Article][PubMed]
    [Google Scholar]
  10. Contaldo N., Bertaccini A., Paltrinieri S., Windsor H. M., Windsor G. D. 2012; Axenic culture of plant pathogenic phytoplasmas. Phytopathol. Mediterr 51:607–617
    [Google Scholar]
  11. Duan C. G., Wang C. H., Guo H. S. 2012; Application of RNA silencing to plant disease resistance. Silence 3:5 [View Article][PubMed]
    [Google Scholar]
  12. Economou A. 1999; Following the leader: bacterial protein export through the Sec pathway. Trends Microbiol 7:315–320 [View Article][PubMed]
    [Google Scholar]
  13. Galetto L., Fletcher J., Bosco D., Turina M., Wayadande A., Marzachì C. 2008; Characterization of putative membrane protein genes of the ‘Candidatus Phytoplasma asteris’, chrysanthemum yellows isolate. Can J Microbiol 54:341–351 [View Article][PubMed]
    [Google Scholar]
  14. Galetto L., Bosco D., Balestrini R., Genre A., Fletcher J., Marzachì C. 2011; The major antigenic membrane protein of ‘Candidatus Phytoplasma asteris’ selectively interacts with ATP synthase and actin of leafhopper vectors. PLoS One 6:e22571 [View Article][PubMed]
    [Google Scholar]
  15. Galetto L., Siampour M., Marzachì C. 2013; Preparation of phytoplasma membrane recombinant proteins. Methods Mol Biol 938:351–369 [View Article][PubMed]
    [Google Scholar]
  16. Hong Y., Davies D. L., van Wezel R., Ellerker B. E., Morton A., Barbara D. 2001; Expression of the immunodominant membrane protein of chlorantie-aster yellows phytoplasma in Nicotiana benthamiana from a potato virus X-based vector. Acta Horticulturae 550:409–416 [View Article]
    [Google Scholar]
  17. Kakizawa S., Oshima K., Kuboyama T., Nishigawa H., Jung H., Sawayanagi T., Tsuchizaki T., Miyata S., Ugaki M., Namba S. 2001; Cloning and expression analysis of Phytoplasma protein translocation genes. Mol Plant Microbe Interact 14:1043–1050 [View Article][PubMed]
    [Google Scholar]
  18. 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 [View Article][PubMed]
    [Google Scholar]
  19. Kakizawa S., Oshima K., Jung H. -Y., Suzuki S., Nishigawa H., Arashida R., Miyata S.-i., Ugaki M., Kishino H., Namba S. 2006a; Positive selection acting on a surface membrane protein of the plant-pathogenic phytoplasmas. J Bacteriol 188:3424–3428 [View Article]
    [Google Scholar]
  20. Kakizawa S., Oshima K., Namba S. 2006b; Diversity and functional importance of phytoplasma membrane proteins. Trends Microbiol 14:254–256 [View Article]
    [Google Scholar]
  21. Kakizawa S., Oshima K., Ishii Y., Hoshi A., Maejima K., Jung H. Y., Yamaji Y., Namba S. 2009; Cloning of immunodominant membrane protein genes of phytoplasmas and their in planta expression. FEMS Microbiol Lett 293:92–101 [View Article][PubMed]
    [Google Scholar]
  22. Kato K., Ishiwa A. 2015; The role of carbohydrates in infection strategies of enteric pathogens. Trop Med Health 43:41–52 [View Article][PubMed]
    [Google Scholar]
  23. Killiny N., Castroviejo M., Saillard C. 2005; Spiroplasma citri spiralin acts in vitro as a lectin binding to glycoproteins from its insect vector circulifer haematoceps. Phytopathology 95:541–548 [View Article][PubMed]
    [Google Scholar]
  24. 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 [View Article][PubMed]
    [Google Scholar]
  25. Le Gall F., Bove J. M., Garnier M. 1998; Engineering of a single-chain variable-fragment (scFv) antibody specific for the stolbur phytoplasma (Mollicute) and its expression in Escherichia coli and tobacco plants. Appl Environ Microbiol 64:4566–4572[PubMed]
    [Google Scholar]
  26. 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]
  27. Lin X., Kim Y. A., Lee B. L., Söderhäll K., Söderhäll I. 2009; Identification and properties of a receptor for the invertebrate cytokine astakine, involved in hematopoiesis. Exp Cell Res 315:1171–1180 [View Article][PubMed]
    [Google Scholar]
  28. Martinez L. O., Jacquet S., Esteve J. P., Rolland C., Cabezón E., Champagne E., Pineau T., Georgeaud V., Walker J. E. et al. 2003; Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature 421:75–79 [View Article][PubMed]
    [Google Scholar]
  29. Mergenthaler E., Viczián O., Fodor M., Süle S. 2001; Isolation and expression of an immunodominant membrane protein gene of the ESFY phytoplasma for antiserum production. Acta Horticulturae 550:355–360 [CrossRef]
    [Google Scholar]
  30. Mori H., Ito K. 2001; The Sec protein-translocation pathway. Trends Microbiol 9:494–500 [View Article][PubMed]
    [Google Scholar]
  31. 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 [View Article][PubMed]
    [Google Scholar]
  32. Moser T. L., Stack M. S., Asplin I., Enghild J. J., Højrup P., Everitt L., Hubchak S., Schnaper H. W., Pizzo S. V. 1999; Angiostatin binds ATP synthase on the surface of human endothelial cells. Proc Natl Acad Sci U S A 96:2811–2816 [View Article][PubMed]
    [Google Scholar]
  33. Mounsey K. E., Streten C., Gibb K. S. 2006; Sequence characterization of four putative membrane-associated proteins from sweet potato little leaf strain V4 phytoplasma. Plant Pathol 55:29–35 [View Article]
    [Google Scholar]
  34. Narayanasamy P. 2011; Detection of Bacterial and Phytoplasmal pathogens. In Microbial Plant Pathogens-Detection and Disease Diagnosis: Bacterial and Phytoplasmal Pathogens vol. 2 pp. 75–76 Dordrecht/Heidelberg/London/New York: Springer;
    [Google Scholar]
  35. Nejat N., Vadamalai G. 2010; Phytoplasma detection in coconut palm and other tropical crops. Plant Pathol J 9:112–121 [CrossRef]
    [Google Scholar]
  36. Neriya Y., Sugawara K., Maejima K., Hashimoto M., Komatsu K., Minato N., Miura C., Kakizawa S., Yamaji Y. et al. 2011; Cloning, expression analysis, and sequence diversity of genes encoding two different immunodominant membrane proteins in poinsettia branch-inducing phytoplasma (PoiBI). FEMS Microbiol Lett 324:38–47 [View Article][PubMed]
    [Google Scholar]
  37. Oshima K., Kakizawa S., Nishigawa H., Jung H. Y., Wei W., Suzuki S., Arashida R., Nakata D., Miyata S. et al. 2004; Reductive evolution suggested from the complete genome sequence of a plant-pathogenic phytoplasma. Nat Genet 36:27–29 [View Article][PubMed]
    [Google Scholar]
  38. Pacifico D., Galetto L., Rashidi M., Abbà S., Palmano S., Firrao G., Bosco D., Marzachì C. 2015; Decreasing global transcript levels over time suggest that phytoplasma cells enter stationary phase during plant and insect colonization. Appl Environ Microbiol 81:2591–2602 [View Article][PubMed]
    [Google Scholar]
  39. Paingankar M. S., Gokhale M. D., Deobagkar D. N. 2010; Dengue-2-virus-interacting polypeptides involved in mosquito cell infection. Arch Virol 155:1453–1461 [View Article][PubMed]
    [Google Scholar]
  40. Peschen D., Li H. P., Fischer R., Kreuzaler F., Liao Y. C. 2004; Fusion proteins comprising a Fusarium-specific antibody linked to antifungal peptides protect plants against a fungal pathogen. Nat Biotechnol 22:732–738 [View Article][PubMed]
    [Google Scholar]
  41. Rashidi M., Galetto L., Bosco D., Bulgarelli A., Vallino M., Veratti F., Marzachì C. 2015; Role of the major antigenic membrane protein in phytoplasma transmission by two insect vector species. BMC Microbiol 15:193 [View Article][PubMed]
    [Google Scholar]
  42. Siampour M., Izadpanah K., Galetto L., Salehi M., Marzachí C. 2013; Molecular characterization, phylogenetic comparison and serological relationship of the Imp protein of several ‘Candidatus Phytoplasma aurantifolia’ strains. Plant Pathol 62:452–459 [View Article]
    [Google Scholar]
  43. Sugio A., MacLean A. M., Kingdom H. N., Grieve V. M., Manimekalai R., Hogenhout S. A. 2011; Diverse targets of phytoplasma effectors: from plant development to defense against insects. Annu Rev Phytopathol 49:175–195 [View Article][PubMed]
    [Google Scholar]
  44. 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 [View Article][PubMed]
    [Google Scholar]
  45. Tümmler B., Cornelis P. 2005; Pyoverdine receptor: a case of positive Darwinian selection in Pseudomonas aeruginosa . J Bacteriol 187:3289–3292 [View Article][PubMed]
    [Google Scholar]
  46. Wagner S., Klepsch M. M., Schlegel S., Appel A., Draheim R., Tarry M., Högbom M., van Wijk K. J., Slotboom D. J. et al. 2008; Tuning Escherichia coli for membrane protein overexpression. Proc Natl Acad Sci U S A 105:14371–14376 [View Article][PubMed]
    [Google Scholar]
  47. Yu Y. L., Yeh K. W., Lin C. P. 1998; An antigenic protein gene of a phytoplasma associated with sweet potato witches' broom. Microbiology 144:1257–1262 [View Article][PubMed]
    [Google Scholar]
  48. Yu J., Wayadande A. C., Fletcher J. 2000; Spiroplasma citri surface protein P89 implicated in adhesion to cells of the vector circulifer tenellus. Phytopathology 90:716–722 [View Article][PubMed]
    [Google Scholar]
  49. Zalewska M., Kochman A., Estève J. P., Lopez F., Chaoui K., Susini C., Ozyhar A., Kochman M. 2009; Juvenile hormone binding protein trafficinteraction with ATP synthase and lipid transfer proteins. Biochim Biophys Acta 1788:1695–1705 [View Article][PubMed]
    [Google Scholar]
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