Genome-wide identification of Hfq-regulated small RNAs in the fire blight pathogen Erwinia amylovora discovered small RNAs with virulence regulatory function

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Zeng, Quan ^a   Sundin, George W ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Amylovoran; ArcZ; Biofilm; Motility; RNA seq; sRNA; Type III secretion system

Indexed keywords

AMYLOVORAN; BACTERIAL RNA; EXOPOLYSACCHARIDE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; HOST FACTOR 1; SMALL UNTRANSLATED RNA; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BIOFILM; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; ERWINIA AMYLOVORA; FIRE BLIGHT; GENE EXPRESSION; GENE IDENTIFICATION; GENE INDUCTION; GENETIC CODE; GENETIC TRAIT; HFQ GENE; NONHUMAN; NORTHERN BLOTTING; PEAR; REGULATOR GENE; RNA ANALYSIS; RNA SEQUENCE; SEQUENCE ANALYSIS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; TYPE III SECRETION SYSTEM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; PLANT DISEASE; PYRUS;

BACTERIA (MICROORGANISMS); ERWINIA; ERWINIA AMYLOVORA; PYRUS;

BACTERIAL PROTEINS; BIOFILMS; ERWINIA AMYLOVORA; GENE EXPRESSION REGULATION, BACTERIAL; HOST FACTOR 1 PROTEIN; PHYLOGENY; PLANT DISEASES; PYRUS; RNA, BACTERIAL; RNA, SMALL UNTRANSLATED; VIRULENCE FACTORS;

EID: 84904755624     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-414     Document Type: Article

References (63)

1. Norelli JL, Jones AL, Aldwinckle HS. Fire blight management in the twenty-first century: using new technologies that enhance host resistance in apple. Plant Dis 2003, 87:756-765.
2. Malnoy M, Martens S, Norelli JL, Barny MA, Sundin GW, Smits TH, Duffy B. Fire blight: applied genomic insights of the pathogen and host. Annu Rev Phytopathol 2012, 50:475-494. 10.1146/annurev-phyto-081211-172931, 22702352.
3. Castiblanco LF, Edmunds AC, Waters CM, Sundin GW. Characterization of quorum sensing and cyclic-di-GMP signaling systems in Erwinia amylovora. Phytopathology 2011, 101:S2.2.
4. Koczan JM, McGrath MJ, Zhao Y, Sundin GW. Contribution of Erwinia amylovora exopolysaccharides amylovoran and levan to biofilm formation: implications in pathogenicity. Phytopathology 2009, 99(11):1237-1244. 10.1094/PHYTO-99-11-1237, 19821727.
5. McNally RR, Toth IK, Cock PJ, Pritchard L, Hedley PE, Morris JA, Zhao Y, Sundin GW. Genetic characterization of the HrpL regulon of the fire blight pathogen Erwinia amylovora reveals novel virulence factors. Mol Plant Pathol 2012, 13(2):160-173. 10.1111/j.1364-3703.2011.00738.x, 21831138.
6. Oh CS, Kim JF, Beer SV. The Hrp pathogenicity island of Erwinia amylovora and identification of three novel genes required for systemic infectiondouble dagger. Mol Plant Pathol 2005, 6(2):125-138. 10.1111/j.1364-3703.2005.00269.x, 20565644.
7. Wang D, Korban SS, Pusey PL, Zhao Y. Characterization of the RcsC sensor kinase from Erwinia amylovora and other Enterobacteria. Phytopathology 2011, 101(6):710-717. 10.1094/PHYTO-09-10-0258, 21261468.
8. Zhao Y, Blumer SE, Sundin GW. Identification of Erwinia amylovora genes induced during infection of immature pear tissue. J Bacteriol 2005, 187(23):8088-8103. 10.1128/JB.187.23.8088-8103.2005, 1291285, 16291682.
9. Zhao Y, Wang D, Nakka S, Sundin GW, Korban SS. Systems level analysis of two-component signal transduction systems in Erwinia amylovora: role in virulence, regulation of amylovoran biosynthesis and swarming motility. BMC Genomics 2009, 10:245. 10.1186/1471-2164-10-245, 2698875, 19470164.
10. Edmunds AC, Castiblanco LF, Sundin GW, Waters CM. Cyclic Di-GMP modulates the disease progression of Erwinia amylovora. J Bacteriol 2013, 195(10):2155-2165. 10.1128/JB.02068-12, 3650540, 23475975.
11. Wei Z, Kim JF, Beer SV. Regulation of hrp genes and type III protein secretion in Erwinia amylovora by HrpX/HrpY, a novel two-component system, and HrpS. Mol Plant Microbe Interact 2000, 13(11):1251-1262. 10.1094/MPMI.2000.13.11.1251, 11059492.
12. Frohlich KS, Vogel J. Activation of gene expression by small RNA. Curr Opin Microbiol 2009, 12(6):674-682. 10.1016/j.mib.2009.09.009, 19880344.
13. Gottesman S, Storz G. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 2011, 3:a003798. 3225950, 20980440.
14. Storz G, Vogel J, Wassarman KM. Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 2011, 43(6):880-891. 10.1016/j.molcel.2011.08.022, 3176440, 21925377.
15. Vogel J, Luisi BF. Hfq and its constellation of RNA. Nat Rev Microbiol 2011, 9(8):578-589. 10.1038/nrmicro2615, 21760622.
16. Backofen R, Hess WR. Computational prediction of sRNAs and their targets in bacteria. RNA Biol 2010, 7(1):33-42. 10.4161/rna.7.1.10655, 20061798.
17. Pichon C, Felden B. Small RNA gene identification and mRNA target predictions in bacteria. Bioinformatics 2008, 24(24):2807-2813. 10.1093/bioinformatics/btn560, 18974076.
18. Huttenhofer A, Vogel J. Experimental approaches to identify non-coding RNAs. Nucleic Acids Res 2006, 34(2):635-646. 10.1093/nar/gkj469, 1351373, 16436800.
19. van Vliet AH. Next generation sequencing of microbial transcriptomes: challenges and opportunities. FEMS Microbiol Lett 2010, 302(1):1-7. 10.1111/j.1574-6968.2009.01767.x, 19735299.
20. Sorek R, Cossart P. Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nat Rev Genet 2010, 11(1):9-16.
21. Schmidtke C, Findeiss S, Sharma CM, Kuhfuss J, Hoffmann S, Vogel J, Stadler PF, Bonas U. Genome-wide transcriptome analysis of the plant pathogen Xanthomonas identifies sRNAs with putative virulence functions. Nucleic Acids Res 2012, 40(5):2020-2031. 10.1093/nar/gkr904, 3300014, 22080557.
22. Filiatrault MJ, Stodghill PV, Bronstein PA, Moll S, Lindeberg M, Grills G, Schweitzer P, Wang W, Schroth GP, Luo S, Khrebtukova I, Yang Y, Thannhauser T, Butcher BG, Cartinhour S, Schneider DJ. Transcriptome analysis of Pseudomonas syringae identifies new genes, noncoding RNAs, and antisense activity. J Bacteriol 2010, 192(9):2359-2372. 10.1128/JB.01445-09, 2863471, 20190049.
23. Wilms I, Overloper A, Nowrousian M, Sharma CM, Narberhaus F. Deep sequencing uncovers numerous small RNAs on all four replicons of the plant pathogen Agrobacterium tumefaciens. RNA Biol 2012, 9(4):446-457. 10.4161/rna.17212, 3384568, 22336765.
24. Raghavan R, Groisman EA, Ochman H. Genome-wide detection of novel regulatory RNAs in E. coli. Genome Res 2011, 21(9):1487-1497. 10.1101/gr.119370.110, 3166833, 21665928.
25. Shinhara A, Matsui M, Hiraoka K, Nomura W, Hirano R, Nakahigashi K, Tomita M, Mori H, Kanai A. Deep sequencing reveals as-yet-undiscovered small RNAs in Escherichia coli. BMC Genomics 2011, 12:428. 10.1186/1471-2164-12-428, 3175480, 21864382.
26. Hershberg R, Altuvia S, Margalit H. A survey of small RNA-encoding genes in Escherichia coli. Nucleic Acids Res 2003, 31(7):1813-1820. 10.1093/nar/gkg297, 152812, 12654996.
27. Kroger C, Dillon SC, Cameron AD, Papenfort K, Sivasankaran SK, Hokamp K, Chao Y, Sittka A, Hebrard M, Handler K, Colgan A, Leekitcharoenphon P, Langridge GC, Lohan AJ, Loftus B, Lucchini S, Ussery DW, Dorman CJ, Thomson NR, Vogel J, Hinton JCD. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci U S A 2012, 109(20):E1277-E1286. 10.1073/pnas.1201061109, 3356629, 22538806.
28. Koo JT, Alleyne TM, Schiano CA, Jafari N, Lathem WW. Global discovery of small RNAs in Yersinia pseudotuberculosis identifies Yersinia-specific small, noncoding RNAs required for virulence. Proc Natl Acad Sci U S A 2011, 108(37):E709-E717. 10.1073/pnas.1101655108, 3174644, 21876162.
29. Gomez-Lozano M, Marvig RL, Molin S, Long KS. Genome-wide identification of novel small RNAs in Pseudomonas aeruginosa. Environ Microbiol 2012, 14(8):2006-2016. 10.1111/j.1462-2920.2012.02759.x, 22533370.
30. Papenfort K, Vogel J. Regulatory RNA in bacterial pathogens. Cell Host Microbe 2010, 8(1):116-127. 10.1016/j.chom.2010.06.008, 20638647.
31. Bardill JP, Hammer BK. Non-coding sRNAs regulate virulence in the bacterial pathogen Vibrio cholerae. RNA Biol 2012, 9(4):392-401. 10.4161/rna.19975, 3384565, 22546941.
32. Bradley ES, Bodi K, Ismail AM, Camilli A. A genome-wide approach to discovery of small RNAs involved in regulation of virulence in Vibrio cholerae. PLoS Pathog 2011, 7(7):e1002126. 10.1371/journal.ppat.1002126, 3136459, 21779167.
33. Hammer BK, Bassler BL. Regulatory small RNAs circumvent the conventional quorum sensing pathway in pandemic Vibrio cholerae. Proc Natl Acad Sci U S A 2007, 104(27):11145-11149. 10.1073/pnas.0703860104, 1888797, 17556542.
34. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 2004, 118(1):69-82. 10.1016/j.cell.2004.06.009, 15242645.
35. Svenningsen SL, Tu KC, Bassler BL. Gene dosage compensation calibrates four regulatory RNAs to control Vibrio cholerae quorum sensing. EMBO J 2009, 28(4):429-439. 10.1038/emboj.2008.300, 2632942, 19165149.
36. Moon K, Gottesman S. A PhoQ/P-regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides. Mol Microbiol 2009, 74(6):1314-1330. 10.1111/j.1365-2958.2009.06944.x, 2841474, 19889087.
37. Pfeiffer V, Sittka A, Tomer R, Tedin K, Brinkmann V, Vogel J. A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome. Mol Microbiol 2007, 66(5):1174-1191. 10.1111/j.1365-2958.2007.05991.x, 17971080.
38. Wadler CS, Vanderpool CK. Characterization of homologs of the small RNA SgrS reveals diversity in function. Nucleic Acids Res 2009, 37(16):5477-5485. 10.1093/nar/gkp591, 2760806, 19620214.
39. Zeng Q, McNally RR, Sundin GW. Global small RNA chaperone Hfq and regulatory small RNAs are important virulence regulators in Erwinia amylovora. J Bacteriol 2013, 195(8):1706-1717. 10.1128/JB.02056-12, 3624556, 23378513.
40. Chao Y, Vogel J. The role of Hfq in bacterial pathogens. Curr Opin Microbiol 2010, 13(1):24-33. 10.1016/j.mib.2010.01.001, 20080057.
41. Sittka A, Pfeiffer V, Tedin K, Vogel J. The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol Microbiol 2007, 63(1):193-217. 10.1111/j.1365-2958.2006.05489.x, 1810395, 17163975.
42. Wilms I, Moller P, Stock AM, Gurski R, Lai EM, Narberhaus F. Hfq influences multiple transport systems and virulence in the plant pathogen Agrobacterium tumefaciens. J Bacteriol 2012, 194(19):5209-5217. 10.1128/JB.00510-12, 3457239, 22821981.
43. Huynh TV, Dahlbeck D, Staskawicz BJ. Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 1989, 245(4924):1374-1377. 10.1126/science.2781284, 2781284.
44. Sebaihia M, Bocsanczy AM, Biehl BS, Quail MA, Perna NT, Glasner JD, DeClerck GA, Cartinhour S, Schneider DJ, Bentley SD, Parkhill J, Beer SV. Complete genome sequence of the plant pathogen Erwinia amylovora strain ATCC 49946. J Bacteriol 2010, 192(7):2020-2021. 10.1128/JB.00022-10, 2838050, 20118253.
45. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. Artemis: sequence visualization and annotation. Bioinformatics 2000, 16(10):944-945. 10.1093/bioinformatics/16.10.944, 11120685.
46. Zeng Q, Ibekwe AM, Biddle E, Yang CH. Regulatory mechanisms of exoribonuclease PNPase and regulatory small RNA on T3SS of Dickeya dadantii. Mol Plant Microbe Interact 2010, 23(10):1345-1355. 10.1094/MPMI-03-10-0063, 20831411.
47. de Hoon MJ, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics 2004, 20(9):1453-1454. 10.1093/bioinformatics/bth078, 14871861.
48. Saldanha AJ. Java Treeview-extensible visualization of microarray data. Bioinformatics 2004, 20(17):3246-3248. 10.1093/bioinformatics/bth349, 15180930.
49. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 2000, 97(12):6640-6645. 10.1073/pnas.120163297, 18686, 10829079.
50. Bellemann P, Bereswill S, Berger S, Geider K. Visualization of capsule formation by Erwinia amylovora and assays to determine amylovoran synthesis. Int J Biol Macromol 1994, 16(6):290-296. 10.1016/0141-8130(94)90058-2, 7537077.
51. Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, Eddy SR, Gardner PP, Bateman A. Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 2013, 41(Database issue):D226-D232. 3531072, 23125362.
52. Vogel J, Sharma CM. How to find small non-coding RNAs in bacteria. Biol Chem 2005, 386(12):1219-1238.
53. Maxson-Stein K, McGhee GC, Smith JJ, Jones AL, Sundin GW. Genetic analysis of a pathogenic Erwinia sp. isolated from pear in Japan. Phytopathology 2003, 93(11):1393-1399. 10.1094/PHYTO.2003.93.11.1393, 18944067.
54. Wilms I, Voss B, Hess WR, Leichert LI, Narberhaus F. Small RNA-mediated control of the Agrobacterium tumefaciens GABA binding protein. Mol Microbiol 2011, 80(2):492-506. 10.1111/j.1365-2958.2011.07589.x, 21320185.
55. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, Altuvia S. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 2001, 11(12):941-950. 10.1016/S0960-9822(01)00270-6, 11448770.
56. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, Gottesman S. Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 2003, 50(4):1111-1124. 10.1046/j.1365-2958.2003.03734.x, 14622403.
57. Moon K, Gottesman S. Competition among Hfq-binding small RNAs in Escherichia coli. Mol Microbiol 2011, 82(6):1545-1562. 10.1111/j.1365-2958.2011.07907.x, 22040174.
58. De Lay N, Gottesman S. A complex network of small non-coding RNAs regulate motility in Escherichia coli. Mol Microbiol 2012, 86(3):524-538. 10.1111/j.1365-2958.2012.08209.x, 22925049.
59. Soper T, Mandin P, Majdalani N, Gottesman S, Woodson SA. Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci U S A 2010, 107(21):9602-9607. 10.1073/pnas.1004435107, 2906882, 20457943.
60. Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, Vogel J. Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 2009, 74(1):139-158. 10.1111/j.1365-2958.2009.06857.x, 19732340.
61. Hebrard M, Kroger C, Srikumar S, Colgan A, Handler K, Hinton JC. sRNAs and the virulence of Salmonella enterica serovar Typhimurium. RNA Biol 2012, 9(4):437-445. 10.4161/rna.20480, 3384567, 22546935.
62. Zhao Y, Sundin GW, Wang D. Construction and analysis of pathogenicity island deletion mutants of Erwinia amylovora. Can J Microbiol 2009, 55(4):457-464. 10.1139/W08-147, 19396246.
63. Labes M, Puhler A, Simon R. A new family of RSF1010-derived expression and lac-fusion broad-host-range vectors for gram-negative bacteria. Gene 1990, 89(1):37-46. 10.1016/0378-1119(90)90203-4, 2115488.