Diversity and plasticity of the intracellular plant pathogen and insect symbiont "Candidatus Liberibacter asiaticus" as revealed by hypervariable prophage genes with intragenic tandem repeats

Applied and Environmental Microbiology

Volumn 77, Issue 18, 2011, Pages 6663-6673

  Zhou, Lijuan ^a   Powell, Charles A ^a   Hoffman, Michele T ^b   Li, Wenbin ^c   Fan, Guocheng ^d   Liu, Bo ^d   Lin, Hong ^e   Duan, Yongping ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b U S DEPARTMENT OF AGRICULTURE   (United States)

^c USDA APHISPPQ CPHST NPGBL   (United States)

^d INSTITUTE OF PLANT PROTECTION   (China)

^e AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POPULATION; FLORIDA; GEOGRAPHICAL ORIGINS; HUANGLONGBING; MULTISOURCES; OPEN READING FRAME; PHYLOGENETIC TREES; PLANT PATHOGEN; PROPHAGE GENES; PROPHAGES; SEQUENCE ANALYSIS; SEQUENCE CONSERVATION; SINGLE ORIGIN; TANDEM REPEATS;

BACTERIA; GENES; PLASTICITY;

CALCIUM;

BACTERIAL DISEASE; BACTERIUM; COEXISTENCE; HOMOLOGY; HOST-PATHOGEN INTERACTION; INSECT; PHYLOGENETICS; SAMPLING; SPECIES DIVERSITY; SYMBIONT;

ANIMAL; ARTICLE; CITRUS; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETIC POLYMORPHISM; GENETICS; INSECT; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGEOGRAPHY; PLANT DISEASE; PROPHAGE; RHIZOBIACEAE; TANDEM REPEAT; UNITED STATES;

ANIMALS; CITRUS; CLUSTER ANALYSIS; FLORIDA; INSECTS; MOLECULAR SEQUENCE DATA; PHYLOGEOGRAPHY; PLANT DISEASES; POLYMORPHISM, GENETIC; PROPHAGES; RHIZOBIACEAE; SEQUENCE ANALYSIS, DNA; TANDEM REPEAT SEQUENCES;

FLORIDA [UNITED STATES]; UNITED STATES;

BACTERIA (MICROORGANISMS); CANDIDATUS LIBERIBACTER; CANDIDATUS LIBERIBACTER ASIATICUS; CITRUS; HEXAPODA; PSYLLIDAE;

EID: 80052801990     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.05111-11     Document Type: Article

References (57)

1. Abascal, F., R. Zardoya, and D. Posada. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104-2105.
2. Altschul, S. F., et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Bastianel, C., M. Garnier-Semancik, J. Renaudin, J. M. Bové, and S. Eveillard. 2005. Diversity of "Candidatus Liberibacter asiaticus," based on the omp gene sequence. Appl. Environ. Microbiol. 71:6473-6478.
4. Benson, G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27:573-580.
5. Boch, J., et al. 2009. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:1509-1512.
6. Bové, J. M. 2006. Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J. Plant Pathol. 88:7-37.
7. Boyd, E. F., and H. Brüssow. 2002. Common themes among bacteriophageencoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 10:521-529.
8. Bruce, D. S., et al. 2005. Detection and identification of citrus Huanglongbing (greening) in Florida, abstr. H-11, p. 59. Proceedings of the Second International Citrus Canker and Huanglongbing Research Workshop. Orlando, FL.
9. Brunings, A. M., and D. W. Gabriel. 2003. Xanthomonas citri: breaking the surface. Mol. Plant Pathol. 4:141-157.
10. Casjens, S. 2003. Prophages and bacterial genomics: what have we learned so far? Mol. Microbiol. 49:277-300.
11. Chen, J., et al. 2010. Guangdong and Florida populations of 'Candidatus Liberibacter asiaticus' distinguished by a genomic locus with short tandem repeats. Phytopathology 100:567-572.
12. Ding, F., et al. 2009. Phylogenetic analysis of the citrus Huanglongbing (HLB) bacterium based on the sequences of 16S rDNA and 16S/23S rDNA intergenic regions among isolates in China. Eur. J. Plant Pathol. 124:495-503.
13. Drummond, A., and K. Strimmer. 2001. PAL: an object-oriented programming library for molecular evolution and phylogenetics. Bioinformatics 17: 662-663.
14. Duan, Y. P., A. Castaneda, G. Zhao, G. Erdos, and D. W. Gabriel. 1999. Expression of a single, host-specific, bacterial pathogenicity gene in plant cells elicits division, enlargement and cell death. Mol. Plant Microbe Interact. 12:556-560.
15. Duan, Y. P., T. Gottwald, L. J. Zhou, and D. W. Gabriel. 2008. First report of dodder transmission of 'Candidatus Liberibacter asiaticus' to tomato (Lycopersicon esculentum). Plant Dis. 92:831.
16. Duan, Y. P., et al. 2009. Complete genome sequence of citrus huanglongbing bacterium, 'Candidatus Liberibacter asiaticus' obtained through metagenomics. Mol. Plant Microbe Interact. 22:1011-1020.
17. Furuya, N., et al. 2010. Sequence homogeneity of the ψserA-trmU-tufBsecE- nusG-rplKAJL-rpoB gene cluster and the flanking regions of 'Candidatus Liberibacter asiaticus' isolates around Okinawa Main Island in Japan. J. Gen. Plant Pathol. 76:122-131.
18. Gottwald, T. R., J. V. Da Graca, and R. B. Bassanezi. 2007. Citrus huanglongbing: the pathogen and its impact. Plant Health Progr. http://www.plantmanagementnetwork.org/pub/php/review/2007/huanglongbing/.
19. Gottwald, T. R. 2010. Current epidemiological understanding of citrus huanglongbing. Annu. Rev. Phytopathol. 48:119-139.
20. Gravekamp, C., B. Rosner, and L. C. Madoff. 1998. Deletion of repeats in the alpha C protein enhances the pathogenicity of group B streptococci in immune mice. Infect. Immun. 66:4347-4354.
21. Guindon, S., O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
22. Halbert, S. E., and K. L. Manjunath. 2004. Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Fla. Entomol. 87:330-353.
23. Ikegami, A., K. Honma, A. Sharma, and H. K. Kuramitsu. 2004. Multiple functions of the leucine-rich repeat protein LrrA of Treponema denticola. Infect. Immun. 72:4619-4627.
24. Irey, M. S., T. Gast, and T. Gottwald. 2006. Comparison of visual assessment and PCR assay testing to estimate the incidence of the huanglongbin pathogen in commercial Florida citrus. Proc. Fla. State Hortic. Soc. 42:17-21.
25. Jagoueix, S., J. M. Bové, and M. Garnier. 1994. The phloem-limited bacterium of greening disease of citrus is a member of the subdivision of the proteobacteria. Int. J. Syst. Bacteriol. 44:379-386.
26. Jagoueix, S., J. M. Bové, and M. Garnier. 1997. Comparison of the 16S/23S ribosomal intergenic regions of "Candidatus Liberobacter asiaticum" and "Candidatus Liberobacter africanum," the two species associated with citrus huanglongbing (greening) disease. Int. J. Syst. Bacteriol. 47:224-227.
27. Jones, D. T., W. R. Taylor, and J. M. Thornton. 1992. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. (Camb.) 8:275-282.
28. Katoh, H., et al. 2011. Differentiation of "Candidatus Liberibacter asiaticus" isolates by variable number of tandem repeat analysis. Appl. Environ. Microbiol. 77:1910-1917.
29. Levdansky, E., et al. 2007. Coding tandem repeats generate diversity in Aspergillus fumigatus genes. Eukaryot. Cell 6:1380-1391.
30. Levinson, G., and G. A. Gutman. 1987. Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol. Biol. Evol. 4:203-221.
31. Li, W., J. S. Hartung, and L. Levy. 2006. Quantitative real-time PCR for detection and identification of Candidatus Liberibacter species associated with citrus huanglongbing. J. Microbiol. Methods 66:104-115.
32. Li, W., D. Li, E. Twieg, J. S. Hartung, and L. Levy. 2008. Optimized quantification of unculturable Candidatus Liberibacter spp. in host plants using real-time PCR. Plant Dis. 92:854-861.
33. Liu, R., et al. 2011. Analysis of a prophage gene frequency revealed population variation of 'Candidatus Liberibacter asiaticus' from two citrus-growing provinces in China. Plant Dis. 95:431-435.
34. Maddison, W. P., and D. R. Maddison. 2010. Mesquite: a modular system for evolutionary analysis. Version 2.73. http://mesquiteproject.org.
35. Madoff, L. C., J. L. Michel, E. W. Gong, D. E. Kling, and D. L. Kasper. 1996. Group B streptococci escape host immunity by deletion of tandem repeat elements of the alpha C protein. Proc. Natl. Acad. Sci. U. S. A. 93:4131-4136.
36. Michel, J. L., et al. 1992. Large, identical, tandem repeating units in the C protein alpha antigen gene, bca, of group B streptococci. Proc. Natl. Acad. Sci. U. S. A. 89:10060-10064.
37. Miller, M. A., W. Pfeiffer, and T. Schwartz. 2010. Creating the CIPRES gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop, New Orleans, LA.
38. Planet, P., S. Jagoueix, J. M. Bové, and M. Garnier. 1995. Detection and characterization of the African citrus greening Liberibacter by amplification, cloning and sequencing of the rplKAJL-rpoBC operon. Curr. Microbiol. 30:137-141.
39. Romero, D., and R. Palacios. 1997. Gene amplification and genomic plasticity in prokaryotes. Annu. Rev. Genet. 31:91-111.
40. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
41. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
42. Subandiyah, S., et al. 2000. Comparison of 16S rDNA and 16S/23S intergenic region sequences among citrus greening organisms in Asia. Plant Dis. 84:15-18.
43. Swofford, D. L. 2002. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4b10. Sinauer Associates, Sunderland, MA.
44. Teixeira, D. C., et al. 2005. First report of a huanglongbing-like disease of citrus in Sao Paulo State, Brazil, and association of a new liberibacter species, 'Candidatus Liberibacter americanus', with the disease. Plant Dis. 89:107.
45. Teixeira, D. C., et al. 2005. Citrus huanglongbing in São Paulo, Brazil: PCR detection of the 'Candidatus' Liberibacter species associated with the disease, Mol. Cell. Probes 19:173-179.
46. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
47. Tomimura, K., et al. 2009. Evaluation of genetic diversity among 'Candidatus Liberibacter asiaticus' isolates collected in southeast Asia. Phytopathology 99:1062-1069.
48. Verstrepen, K. J., A. Jansen, F. Lewitter, and G. R. Fink. 2005. Intragenic tandem repeats generate functional variability. Nat. Genet. 37:986-990.
49. Villechanoux, S., M. Garnier, F. Laigret, J. Renaudin, and J. M. Bové. 1993. The genome of the non-cultured, bacterial-like organism associated with citrus greening disease contains the nusG-rplKAJLrpoBC gene cluster and the gene for a bacteriophage type DNA polymerase. Curr. Microbiol. 26: 161-166.
50. Yang, Y., R. De Feyter, and D. W. Gabriel. 1994. Host-specific symptoms and increased release of Xanthomonas citri and X. campestris pv. malvacearum from leaves are determined by the 102-bp tandem repeats of pthA and avrb6, respectively. Mol. Plant Microbe Interact. 7:345-355.
51. Yang, Y., and D. W. Gabriel. 1995. Xanthomonas avirulence/pathogenicity gene family encodes functional plant nuclear targeting signals. Mol. Plant Microbe Interact. 8:627-631.
52. Yang, Y., and D. W. Gabriel. 1995. Intragenic recombination of a single plant pathogen gene provides a mechanism for the evolution of new host specificities. J. Bacteriol. 177:4963-4968.
53. Zhang, M. Q., et al. 2010. Screening molecules for control of citrus huanglongbing using an optimized regeneration system for 'Candidatus Liberibacter asiaticus' infected periwinkle (Catharanthus roseus) cuttings. Phytopathology 100:239-245.
54. Zhang, S. J., et al. 2011. Ca. Liberibacter asiaticus carries an excision plasmid prophage and a chromosomally integrated prophage that becomes lytic in plant. Mol. Plant Microbe Interact. 24:458-468.
55. Zhao, X. 1981. Citrus yellow shoot disease (Huanglongbing) - a review. Proc. Int. Soc. Citric. 1:466-469.
56. Zhou, L. J., D. W. Gabriel, Y. P. Duan, S. E. Halbert, and W. N. Dixon. 2007. First report of dodder transmission of Huanglongbing from naturally infected Murraya paniculata to citrus. Plant Dis. 91:227.
57. Zhou, L. J., and Y. P. Duan. 2008. Genetic diversity of citrus huanglongbing bacterium 'Candidatus Liberibacter asiaticus,' p. 172-175. Proceedings of the International Research Conference on Huanglongbing, Orlando, FL.