Abstract
Spiroplasmas are members of the Class Mollicutes, wall-less prokaryotes having a high adenosine–thymidine content in their small genomes. Spiroplasma citri is a plant pathogen that inhabits phloem. Like other phytopathogenic spiroplasmas and the related phytoplasmas, it is transmitted from plant to plant by phloem-feeding leafhoppers that serve as alternate hosts for the spiroplasma as well as vectors. Genetic information in spiroplasmas is carried on a circular chromosome, on plasmids and/or in virus genomes. A picture emerging from recent research on the S. citri genome is one of frequent and often extensive variation, resulting from a number of different mechanisms. Expansion and contraction events must continually be occurring in about equal proportions so that the net genome size varies within defined boundaries. Particularly impressive are large changes in genome size that can occur in only a few generations. As with most organisms, genetic variation in S. citri results from variation in extrachromosomal DNA content, changes due to DNA replication and repair processes and changes due to recombination. The implied flux of genetic information into and out of the S. citri genome should be beneficial to the bacterium, allowing it, with its small genome size, to adapt to new environments.
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References
Amikan D, Glaser G and Razin S (1984) Mycoplasmas (Mollicutes) have a low number of rRNA genes. J Bacteriol 158: 376-378
Andachi Y, Yamao F, Muto A and Osawa S (1989) Codon recognition patterns as deduced from sequences of the complete set of transfer RNA species in Mycoplasma capricolum. Resemblence to mitochondria. J Mol Biol 209: 37-54
Archer DB and Townsend R (1981) Immunoelectrophoretic separation of spiroplasma antigens. J Gen Microbiol 119: 413-422
Barber CE, Archer DB and Daniels MJ (1983) Molecular biology of spiroplasma plasmids. Yale J Biol Med 56: 777-781
Barroso G and Labarere J (1988) Chromosomal gene transfer in Spiroplasma citri. Science 241: 959-961
Bebear C-M, Aullo P, Bove J-M and Renaudin J (1996) Spiroplasma citri virus SpV1: characterization of viral sequences present in the spiroplasmal host chromosome. Curr Micro 32: 134-140
Behrens A, Heller M, Kirchhoff H, Yogev D and Rosengarten R (1994) A family of phase-and size-variant membrane surface lipoprotein antigens (Vsps) of Mycoplasma bovis. Inf and Immun 62: 5075-5084
Bhugra B and Dybvig K (1993) Identification and characterization of IS1138, a transposable element from Mycoplasma pulmonis that belongs to the IS3 family. Mol Microbiol 7: 577-584
Bhugra B, Voelker LL, Zou N, Yu H and Dybvig K (1995) Mechanism of antigenic variation in Mycoplasma pulmonis: interwoven, site-specific DNA inversions. Mol Microbiol 18: 703-714
Boesen T, Emmersen J, Jensen LT, Ladefoged S, Birkelund S and Christiansen G (1998) A mosaic gene structure is displayed by the vaa gene of Mycoplasma hominis. Proc 12th Int Conf, Int Org Mycoplasmol. (p 129) Sydney, Australia
Bove JM (1993) Molecular features of mollicutes. Clin Infect Dis 17: S10-S31
Bove JM, Foissac X and Saillard C (1993) Spiralins. In: Rottem S and Kahane I (eds) Mycoplasma Cell Membranes. (pp 203-223) Plenum, New York
Carle P, Laigret F, Tully JG and Bove JM (1995) Heterogeneity of genome sizes within the genus Spiroplasma. Int J Syst Bacteriol 45: 178-181
Chevalier C, Saillard C and Bove JM (1990) Organization and nucleotide sequences of the Spiroplasma citri genes for ribosomal protein S2, elongation factor Ts, spiralin, phosphofructokinase, pyruvate kinase, and an unidentified protein. J Bacteriol 172: 2693-2703
Christiansen G and Andersen H (1988) Heterogeneity among Mycoplasma hominis strains as detected by probes containing parts of ribosomal ribonucleic acid genes. Int J Syst Bacteriol 38: 108-115
Citti C and Wise KS (1995) Mycoplasma hyorhinis vlp gene-transcription: critical role in phase variation and expression of surface lipoproteins. Molec Microbiol 18: 649-660
Cordwell SJ, Basseal DJ and Humphery-Smith I (1997) Proteome analysis of Spiroplasma melliferum (A56) and protein characterisation across species boundaries. Electrophoresis 18: 1335-1346
Davis RE and Dally EL (1998) Distinction of plant pathogenic Spiroplasma species based on nucleotide sequences homologous with spiroplasmavirus SVTS2 DNA. Phytopathology 88: S20
Davis RE, Jomantiene R and Dally EL (1998) Interoperon sequence heterogeneity and differential PCR-mediated amplification of sequences from the two rRNA operons in phytoplasma. Proc 12th Int Conf, Int Org Mycoplasmol. (pp 176-177) Sydney, Australia
Dickinson MJ and Townsend R (1984) Integration of a temperate phage infecting Spiroplasma citri. Isr J Med Sci 20: 785-787
Dong Q, Sadouk A, van der Lelie D, Taghavi S, Ferhat A, Nuyten JM, Borremans B, Mergeay M and Toussaint A (1992) Cloning and sequencing of IS1086, an Alcaligenes eutrophus insertion element related to IS30 and IS4351. J Bacteriol 174: 8133-8138
Dybvig K and Cassell GH (1987) Transposition of gram-positive transposon Tn916 in Acholeplasma laidlawii and Mycoplasma pulmonis. Science 235: 1392-1394
Dybvig K and Voelker LL (1996) Molecular biology of mycoplasmas. Ann Rev Microbiol 50: 25-57
Dybvig K and Yu H (1994) Regulation of a restriction and modification system via DNA inversion in Mycoplasma pulmonis. Mol Microbiol 12: 547-560
Fletcher J, Schultz GA, Davis RE, Eastman CE and Goodman RE (1981) Brittle root disease of horseradish: evidence for an etiological role of Spiroplasma citri. Phytopathology 71: 1073-1080
Fletcher J, Shaw ME, Baker GR, Dugan KJ, Ye F, Sha Y, Zuck PD and Myers GD (1996) Molecular characterization of Spiroplasma citri BR3 lines that differ in transmissibility by the leafhopper Circulifer tenellus. Can J Microbiol 42: 124-131
Fletcher J, Wayadande A, Melcher U and Ye F (1998) The phytopathogenic mollicute-insect vector interface: a closer look. Phytopathology 88: 1351-1358
Foissac X, Danet JL, Saillard C, Gaurivaud P, Laigret F, Pare C and Bove JM (1997a) Mutagenesis by insertion of Tn4001 into the genome of Spiroplasma citri: characterization of mutants affected in plant pathogenicity and transmission to the plant by the leafhopper Circulifer haematoceps. Molec Pl Micr Interact 10: 454-461
Foissac X, Saillard C and Bove JM (1997b) Random insertion of transposon Tn4001 in the genome of Spiroplasma citri strain GII3. Plasmid 37: 80-86
Foissac X, Saillard C, Gandar J, Zreik L and Bove JM (1996) Spiralin polymorphism in strains of Spiroplasma citri is not due to differences in posttranslational palmitoylation. J Bacteriol 178: 2934-2940
Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM, Fritchman JL, Weidman JF, Small KV Sandusky M, Fughrmann J, Nguyen D, Utterback TR, Saudek DM, Phillips CA, Merrick JM, Tomb JF, Dougherty BA, Bott KF, Hu PC, Lucier TS, Peterson SN, Smith HO, Hutchison CA and Venter JC (1995) The minimal gene complement of Mycoplasma genitalium. Science 270: 397-403
French CT, Sitaraman R and Dybvig K (1998) Complex gene rearrangements regulate the phase variable expression of at least seven distinct restriction and modification enzymes in Mycoplasma pulmonis. Proc 12th Int Conf, Int Org Mycoplasmol. (p 144) Sydney, Australia
Frey J, Cheng X, Kuhnert P and Nicolet J (1995) Identification and characterization of IS1296 in Mycoplasma mycoides subsp. mycoides SC and presence in related mycoplasmas. Gene 160: 95-100
Fudl-Allah AEA, Calavan EC and Igwegbe ECK (1972) Culture of a mycoplasmalike organism associated with stubborn of citrus. Phytopathology 63: 403-408
Gadeau AP, Mouches C and Bove JM (1986) Probable insensitivity of mollicutes to rifampin and characterization of spiroplasmal DNA-dependent RNA polymerase. J Bacteriol 166: 824-828
Glass JI, Lefkowitz EJ, Glass JS, Heiner CR, Nguyen T, Chen EY and Cassell GH (1998) The Ureaplasma ureolyticum genome. Proc 12th Int Conf, Int Org Mycoplasmol. (p 148) Sydney, Australia
Glew MD, Bergonier D, Rosengarten R, and Citti C (1998) Analysis of the locus involved in the antigenic variation of the Mycoplasma bovis Vsp homologue in Mycoplasma agalactiae. Proc 12th Int Conf, Int Org Mycoplasmol. (p 126) Sydney, Australia
Grau O, Laigret F and Bove JM (1990) Analysis of ribosomal genes in two spiroplasmas, one acholeplasma and one unclassified mollicute. In Zbl Bakt Suppl 20: 895-897
Hackett KJ and Clark TB (1989) Ecology of spiroplasmas. In: Whitcomb RF and Tully JG (eds) The Mycoplasmas, Vol. V. (pp 113-200) Academic Press, New York
Hackett KJ, Whitcomb RF, Henegar RB, Wagner AG, Clark EA, Tully JG, Green F, McKay WH, Santini P, Rose DL, Anderson JJ and Lynn DE (1990) Mollicute diversity in arthropod hosts. In: Stanek G, Cassell GH, Tully JG and Whitcomb RF (eds) Recent Advances in Mycoplasmology. (pp 441-454) Gustav Fischer Verlag, NY
Himmelreich R, Hilbert H, Plagens H, Pirkl E, Li B-C and Herrmann R (1996) Complete sequence analysis of the genome of the bacterium Mycoplasma pneumoniae. Nucleic Acids Res 24: 4420-4449
Himmelreich R, Plagens H, Hilbert H, Reiner B and Herrmann R (1997) Comparative analysis of the genomes of the bacteria Mycoplasma pneumoniae and Mycoplasma genitalium. Nucleic Acids Res 25: 701-712
Humphery-Smith I, Grulet O, Le Goff F and Chastel C (1991) Spiroplasma (Mollicutes: Spiroplasmataceae) pathogenic for Aedes aegypti and Anopheles stephensi (Diptera: Culicidae). J Med Entomol 28: 219-222
Jacob C, Nouzi'res F, Duret S, Bove JM and Renaudin J (1997) Isolation, characterization and complementation of a motility mutant of Spiroplasma citri. J Bacteriol 179: 4802-4810
Labarere J and Barroso G (1989) Lethal and mutation frequency responses of Spiroplasma citri cells to UV irradiation. Mutat Res 210: 135-141
Laigret F, Gaurivaud P and Bove JM (1996) The unique organization of the rpoB region of Spiroplasma citri: a restriction and modification system gene is adjacent to rpoB. Gene 171: 95-98
Le Dantec L, Bove JM and Saillard C (1998a) Gene organization and transcriptional analysis of the Spiroplasma citri rpsB/tsf/x operon. Curr Microbiol 37: 269-273
Le Dantec L, Castroviejo M, Bove JM and Saillard C (1998b) Purification, cloning and preliminary characterization of a Spiroplasma citri ribosomal protein with DNA binding capacity. J Biol Chem 273: 24379-24386
Liefting LW, Andersen MT, Beever RE, Gardner RC and Forster RLS (1996) Sequence heterogeneity in the two 16S rRNA genes of Phormium yellow leaf phytoplasma. Appl Env Microbiol 62: 3133-3139
Lysnyansky I, Rosengarten R and Yogev D (1996) Phenotypic switching of variable surface lipoproteins in Mycoplasma bovis involves high-frequency chromosomal rearrangements. J Bacteriol 178: 5395-5401
Marais A, Bove JM and Renaudin J (1996a) Characterization of the recA gene regions of Spiroplasma citri and Spiroplasma melliferum. J Bacteriol 178: 7003-7009
Marais A, Bove JM and Renaudin J (1996b) Spiroplasma citri virus SpV1-derived cloning vector: deletion formation by illegitimate and homologous recombination in a spiroplasmal host strain which probably lacks a functional recA gene. J Bacteriol 178: 862-870
McCammon SL, Dally EL and Davis RE (1990) Electroporation and DNA methylation effects on the transfection of spiroplasma. Zentralbl Bakeriol Supp 20: 60-65
Melcher U, Sha Y, Ye F and Fletcher J (1999) Mechanisms of Spiroplasma genome variation associated with SpV1-like viral DNA's inferred from sequence comparisons. Micro Comp Genomics (accepted for publication)
Mouches C, Barroso G, Gadeau A and Bove JM (1984) Characterization of two cryptic plasmids from Spiroplasma citri and occurrence of their DNA sequences among various spiroplasmas. Ann Microbiol (Paris) 135A: 17-24
Mouches C, Vignault JC, Tully JG, Whitcomb RF and Bove JM (1979) Characterization of spiroplasmas by one-and two-dimensional protein analysis on polyacrylamide slab gels. Curr Microbiol 2: 69-74
Mowry TM (1986) Mechanisms of and barriers to Spiroplasma citri infection of Macrosteles fascifrons (Stal). Ph.D. thesis, Michigan State University, East Lansing, MI.
Nur I, LeBlanc DJ and Tully JG (1987) Short, interspersed, and repetitive DNA sequences in Spiroplasma species. Plasmid 17: 110-116
Nur I, Moshe S, Razin A, Glaser G, Rottem S and Razin S. (1985) Procaryotic and eucaryotic traits of DNA methylation in spiroplasmas (mycoplasmas). J Bacteriol 164: 19-24
Olasz F, Farkas T, Kiss J, Arini A and Arber W (1997a) Terminal inverted repeats of insertion sequence IS30 serve as targets for transposition. J Bacteriol 179: 7551-7558
Olasz F, Farkas T, Stalder R and Arber W (1997b) Mutations in the carboxy-terminal part of IS30 transposase affect the formation and dissolution of (IS30)2 dimer. FEBS Lett 413: 453-461
Olasz F, Stalder R and Arber W (1993) Formation of the tandem repeat (IS30)2 and its role in IS30-mediated transpositional DNA rearrangements. Mol Gen Genet 239: 177-187
Padovan AC and Gibb KS (1998) Progress in understanding phytopathogenic mollicute genome organization. Proc 12th Conf Int Org. Mycoplasmol, Jul 22–28: 130-131
Pascarel-Devilder MC, Renaudin J and Bove JM (1986) The spiroplasma virus 4 replicative form cloned in Escherichia coli transfects spiroplasmas. Virology 151: 390-393
Polard P, Ton-Hoang B, Haren L, Bétermier M, Walczak R and Chandler M (1996) IS911-mediated transpositional recombination in vitro. J Mol Biol 264: 68-81
Pollack JD, Williams MV and McElhaney RN (1997) The comparative metabolism of the mollicutes (Mycoplasmas): the utility for taxonomic classification and the relationship of putative gene annotation and phylogeny to enzymatic function in the smallest, free-living cells. Crit Rev Microbiol 23: 269-354
Purcell, AH (1982) Insect vector relationships with procaryotic plant pathogens. Ann Rev Phytopathol 20: 397-417
Ranhand JM, Nur I, Rose DL and Tully JG (1987) Spiroplasma species share common DNA sequences among their viruses, plasmids and genomes. Ann Inst Pasteur Microbiol 138: 509-522
Rascoe J, Melcher U and Fletcher J (1996) Evaluation of variations in gene presence and expression among lines of Spiroplasma citri using arbitrarily-primed PCR of cDNA. Phytopathology 86: S96
Rascoe J, Melcher U and Fletcher J (1998) Arbitrarily-primed PCR of cDNA for determination of differential gene presence and expression among lines of Spiroplasma citri. Phytopathology 88: S75
Razin S, Nur I and Glaser G (1987) Spiroplasma plasmids. Isr J Med Sci 23: 678-682
Razin S, Yogev D and Naot Y (1998) Molecular biology and pathogenicity of mycoplasmas. Microbiol Mol Biol Rev 62: 1094-1156
Renaudin J, Aullo P, Vignault JC and Bove JM (1990) Complete nucleotide sequence of the genome of Spiroplasma citri virus SpV1-R8A2 B. Nucl Acids Res 18: 1293
Renaudin J and Bove JM (1994) SpV1 and SpV4, spiroplasma viruses with circular single-stranded DNA genomes, and their contribution to the molecular biology of spiroplasmas. Adv Virus Res 44: 429-463
Renaudin J, Marais A, Verdin E, Duret S, Foissac X, Laigret F and Bove JM (1995) Integrative and free Spiroplasma citri oriC plasmids: expression of the Spiroplasma phoeniceum spiralin in Spiroplasma citri. J Bact 177: 2870-2877
Renbaum P, Abrahamove D, Fainsod A, Wilson GG, Rottem S and Razin A (1990) Cloning, characterization, and expression in Escherichia coli of the gene coding for the CpG DNA methylase from Spiroplasma sp. strain MQ1(M-SssI). Nucleic Acids Res 18: 1145-1152
Renbaum P and Razin A (1992) Mode of action of the Spiroplasma CpG methylase M.SssI. FEBS Lett 313: 243-247
Roberts MC and Kenny GE (1987) Conjugal transfer of transposon Tn916 from Streptococcus faecalis to Mycoplasma hominis. J Bacteriol 169: 3836-3839
Saglio P, LaFleche D, Bonissol C and Bove JM (1971) Isolement et culture in vitro des mycoplasmes associes au ‘stubborn’ des agrumes et leur observation au microscope electronique. Compte Rend Acad Sci Paris 272: 1387-1390
Salvado JC, Barroso G and Labarere J (1989) Involvement of a Spiroplasma citri plasmid in the erythromycin-resistance transfer. Plasmid 22: 151-159
Schneider B and Seemuller E (1994) Presence of two sets of ribosomal genes in phytopathogenic mollicutes. Appl Env Microbiol 60: 3409-3412
Sha YH, Melcher U, Davis RE and Fletcher J (1995) Resistance of Spiroplasma citri lines to the virus SVTS2 is associated with integration of viral DNA sequences into host chromosomal and extrachromosomal DNA. Appl Environ Microbiol 61: 3950-3959
Sha Y, Melcher U, Davis RE and Fletcher J (1998) SpV1-like Spiroplasma virus essential features suggested by SVTS2DNA sequence. Phytopathology 88: S80
Simmons WL, Zuhua C, Glass JI, Simecka JW, Cassell GH and Watson HL (1996) Sequence analysis of the chromosomal region around and within the V-1 encoding gene of Mycoplasma pulmonis: evidence for DNA inversion as a mechanism for V-1 variation. Infect Immun 64: 472-479
Simoneau P and Labarere J (1990) Construction of chimeric antibiotic resistance determinants and their use in the development of cloning vectors for spiroplasmas. Zentralbl Bakeriol Suppl. 20: 66-74
Sitaraman R and Dybvig K (1997) The hsd loci of Mycoplasma pulmonis: organization, rearrangements and expression of genes. Mol Microbiol 26: 109-120
Stephens MA (1982) Partial purification and cleavage specificity of a site-specific endonuclease, SciNI, isolated from Spiroplasma citri. J Bacteriol 149: 508-514
Taylor MA, Ferrell RV, Wise KS and McIntosh MA (1988) Reiterated DNA sequences defining genomic diversity within the species Mycoplasma hyorhinis. Mol Microbiol 2: 665-672
Theiss P, Karpas A and Wise KS (1996) Antigenic topology of the P29 surface lipoprotein of Mycoplasma fermentans: differential display of epitopes results in high-frequency phase variation. Infect Immun 64: 1800-1809
Theiss P and Wise KS (1997) Localized frameshift mutation generates selective, high-frequency phase variation of a surface lipoprotein encoded by a mycoplasma ABC transporter operon. J Bacteriol 179: 4013-4022
Wayadande AC and Fletcher J (1995) Transmission of Spiroplasma citri lines and their ability to cross gut and salivary gland barriers within the leafhopper vector Circulifer tenellus (Homoptera: Cicadellidae). Phytopathology 85: 1256-1259
Whitcomb RF, Chen TA, Williamson DL, Liao C, Tully JG, Bove JM, Mouches C, Rose DL, Coan ME and Clark TB (1986) Spiroplasma kunkelii sp. nov.: characterization of the etiological agent of corn stunt disease. Intl J Syst Bacteriol 36: 170-178
Whitcomb RF and Williamson DL (1979) Pathogenicity of mycoplasmas for arthropods. Zbl Bakt Hyg I Abt Orig A 245: 200-221
Whitcomb RF, Tully JG and Wroblewski H (1983) Spiralin: major membrane protein specific for subgroup I-1 spiroplasmas. Curr Microbiol 9: 7-12
Williamson DL, Hackett KJ, Wagner AG and Cohen AJ (1989) Pathogenicity of cultivated Drosophila willistoni spiroplasmas. Current Microbiol 19: 53-56
Williamson DL, Renaudin J and Bove JM (1991) Nucleotide sequence of the Spiroplasma citri fibril protein gene. J Bacteriol 173: 4352-4362
Woese CR, Maniloff J and Zablen LB (1980) Phylogenetic analysis of the mycoplasmas. Proc Natl Acad Sci USA 77: 494-498
Wroblewski H, Blanchard A, Nystrom S, Wieslander A and Thomas D (1987) Amphiphilic properties of spiralin, the major surface antigen of spiroplasmas. Isr J Med Sci 23: 439-441
Ye F, Laigret F and Bove JM (1994a) A physical and genomic map of the prokaryote Spiroplasma melliferum and its comparison with the Spiroplasma citri map. C R Acad Sci Paris 317: 392-398
Ye F, Laigret F, Carle P and Bove JM (1995) Chromosomal heterogeneity among various strains of Spiroplasma citri. Int J Syst Bact 45: 729-734
Ye F, Laigret F, Whitley JC, Citti C, Finch LR, Carle P, Renaudin J and Bove JM (1992) A physical and genetic map of the Spiroplasma citri genome. Nucleic Acids Res 20: 1559-1565
Ye F, Melcher U, Rascoe JE and Fletcher J (1996) Extensive chromosome aberrations in Spiroplasma citri strain BR3. Biochem Genet 34: 269-286
Ye F, Melcher U, Wayadande AC and Fletcher J (1997) Molecular characterization of a gene encoding a membrane protein of Spiroplasma citri. Gene 189: 95-100
Ye F, Renaudin J, Bove JM and Laigret F (1994b) Cloning and sequencing of the replication origin (oriC) of the Spiroplasma citri chromosome and construction of autonomously replicating artificial plasmids. Curr Microbiol 29: 23-29
Zaaria A, Fontenelle C, Le Henaff M and Wroblewski H (1990) Antigenic relatedness between the spiralins of Spiroplasma citri and Spiroplasma melliferum. J Bacteriol 172: 5494-5496
Zhang QJ and Wise KS (1996) Molecular basis of size and antigenic variation of a Mycoplasma hominis adhesin encoded by divergent vaa genes. Infect Immun 64: 2737-2744
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Melcher, U., Fletcher, J. Genetic Variation in Spiroplasma citri. European Journal of Plant Pathology 105, 519–533 (1999). https://doi.org/10.1023/A:1008757716803
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DOI: https://doi.org/10.1023/A:1008757716803