The Xanthomonas oryzae pv. oryzae PilZ domain proteins function differentially in cyclic di-GMP binding and regulation of virulence and motility

Applied and Environmental Microbiology

Volumn 81, Issue 13, 2015, Pages 4358-4367

  Yang, Fenghuan ^a   Tian, Fang ^a   Chen, Huamin ^a   Hutchins, William ^b   Yang, Ching Hong ^b   He, Chenyang ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BINS; GENE EXPRESSION; GENES; MOLECULAR BIOLOGY; PROTEINS; TRANSCRIPTION;

EXOPOLYSACCHARIDES; GENE TRANSCRIPTIONS; OPEN READING FRAME; PATHOGENIC BACTERIUM; SIGNALING PATHWAYS; SUBCELLULAR LOCALIZATIONS; TYPE III SECRETION SYSTEM; XANTHOMONAS ORYZAE PV. ORYZAE;

GENE EXPRESSION REGULATION;

BACTERIUM; BIOENGINEERING; BIOFILM; CHEMICAL BINDING; FUNCTIONAL ROLE; MOTILITY; PATHOGEN; PHENOTYPE; PROTEIN; RICE; SECRETION; VIRULENCE;

BACTERIA (MICROORGANISMS); XANTHOMONAS ORYZAE PV. ORYZAE;

BACTERIAL PROTEIN; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CYCLIC GMP; PROTEIN BINDING;

ANALOGS AND DERIVATIVES; BINDING SITE; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; LOCOMOTION; METABOLISM; PATHOGENICITY; PHYSIOLOGY; PROTEIN MOTIF; VIRULENCE; XANTHOMONAS;

AMINO ACID MOTIFS; BACTERIAL PROTEINS; BINDING SITES; CYCLIC GMP; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; LOCOMOTION; PROTEIN BINDING; VIRULENCE; XANTHOMONAS;

EID: 84930794740     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.04044-14     Document Type: Article

References (55)

1. Romling U, Gomelsky M, Galperin MY. 2005. C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57:629-639. http://dx.doi.org/10.1111/j.1365-2958.2005.04697.x.
2. Hengge R. 2009. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263-273. http://dx.doi.org/10.1038/nrmicro2109.
3. Romling U, Galperin MY, Gomelsky M. 2013. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1-52. http://dx.doi.org/10.1128/MMBR.00043-12.
4. Schirmer T, Jenal U. 2009. Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7:724-735. http://dx.doi.org/10.1038/nrmicro2203.
5. Amikam D, Galperin MY. 2006. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22:3-6. http://dx.doi.org/10.1093/bioinformatics/bti739.
6. Hickman JW, Harwood CS. 2008. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69:376-389. http://dx.doi.org/10.1111/j.1365-2958.2008.06281.x.
7. Leduc JL, Roberts GP. 2009. Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J Bacteriol 191:7121-7122. http://dx.doi.org/10.1128/JB.00845-09.
8. Tao F, He YW, Wu DH, Swarup S, Zhang LH. 2010. The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J Bacteriol 192: 1020-1029. http://dx.doi.org/10.1128/JB.01253-09.
9. Navarro MV, De N, Bae N, Wang Q, Sondermann H. 2009. Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure 17:1104-1116. http://dx.doi.org/10.1016/j.str.2009.06.010.
10. Duerig A, Abel S, Folcher M, Nicollier M, Schwede T, Amiot N, Giese B, Jenal U. 2009. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 23:93-104. http://dx.doi.org/10.1101/gad.502409.
11. Yang FH, Tian F, Li XT, Fan SS, Chen HM, Wu MS, Yang CH, He CY. 2014. The degenerate EAL-GGDEF domain protein Filp functions as a cyclic di-GMP receptor and specifically interacts with the PilZ-domain protein PXO_02715 to regulate virulence in Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 6:578-589. http://dx.doi.org/10.1094/MPMI-12-13-0371-R.
12. Lee ER, Baker JL, Weinberg Z, Sudarsan N, Breaker RR. 2010. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329:845-848. http://dx.doi.org/10.1126/science.1190713.
13. Tuckerman JR, Gonzalez G, Gilles-Gonzalez MA. 2011. Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J Mol Biol 407:633-639. http://dx.doi.org/10.1016/j.jmb.2011.02.019.
14. Wang YC, Chin KH, Chuah ML, Liang ZX, Chou SH. 2012. Crystallization and preliminary X-ray diffraction studies of Xanthomonas campestris PNPase in the presence of c-di-GMP. Acta Crystallogr Sect F Struct Biol Cryst Commun 68:1247-1250. http://dx.doi.org/10.1107/S1744309112036202.
15. Ryjenkov DA, Simm R, Romling U, Gomelsky M. 2006. The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J Biol Chem 281:30310-30314. http://dx.doi.org/10.1074/jbc.C600179200.
16. Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, Ackermann M, Kaever V, Sourjik V, Roth V, Jenal U. 2010. Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141:107-116. http://dx.doi.org/10.1016/j.cell.2010.01.018.
17. Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM. 2010. The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a "backstop brake" mechanism. Mol Cell 38:128-139. http://dx.doi.org/10.1016/j.molcel.2010.03.001.
18. Pultz IS, Christen M, Kulasekara HD, Kennard A, Kulasekara B, Miller SI. 2012. The response threshold of Salmonella PilZ domain proteins is determined by their binding affinities for c-di-GMP. Mol Microbiol 86: 1424-1440. http://dx.doi.org/10.1111/mmi.12066.
19. Merighi M, Lee VT, Hyodo M, Hayakawa Y, Lory S. 2007. The second messenger bis-(3=-5=)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol Microbiol 65:876-895. http://dx.doi.org/10.1111/j.1365-2958.2007.05817.x.
20. Martinez-Granero F, Navazo A, Barahona E, Redondo-Nieto M, Gonzalez de Heredia E, Baena I, Martin-Martin I, Rivilla R, Martin M. 2014. Identification of flgZ as a flagellar gene encoding a PilZ domain protein that regulates swimming motility and biofilm formation in Pseudomonas. PLoS One 9:e87608. http://dx.doi.org/10.1371/journal.pone.0087608.
21. Pratt JT, Tamayo R, Tischler AD, Camilli A. 2007. PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae. J Biol Chem 282:12860-12870. http://dx.doi.org/10.1074/jbc.M61159 3200.
22. McCarthy Y, Ryan RP, O'Donovan K, He YQ, Jiang BL, Feng JX, Tang JL, Dow JM. 2008. The role of PilZ domain proteins in the virulence of Xanthomonas campestris pv. campestris. Mol Plant Pathol 9:819-824. http://dx.doi.org/10.1111/j.1364-3703.2008.00495.x.
23. Nino-Liu DO, Ronald PC, Bogdanove AJ. 2006. Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7:303-324. http://dx.doi.org/10.1111/j.1364-3703.2006.00344.x.
24. Das A, Rangaraj N, Sonti RV. 2009. Multiple adhesin-like functions of Xanthomonas oryzae pv. oryzae are involved in promoting leaf attachment, entry, and virulence on rice. Mol Plant Microbe Interact 22:73-85. http://dx.doi.org/10.1094/MPMI-22-1-0073.
25. Yang FH, Tian F, Sun L, Chen HM, Wu MS, Yang CH, He CY. 2012. A novel two-component system PdeK/PdeR regulates c-di-GMP turnover and virulence of Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 25:1361-1369. http://dx.doi.org/10.1094/MPMI-01-12-0014-R.
26. He YW, Wu J, Cha JS, Zhang LH. 2010. Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production. BMC Microbiol 10:187. http://dx.doi.org/10.1186/1471-2180-10-187.
27. Li B, Tian F, Chen HM, Wu MS, He CY. 2013. Binding of transcription regulator ClpXoo to promoter of endoglucanase gene engAXoo was inhibited by c-di-GMP in Xanthomonas oryzae pv. oryzae. Acta Microbiol Sin 53:1166-1171.
28. Salzberg SL, Sommer DD, Schatz MC, Phillippy AM, Rabinowicz PD, Tsuge S, Furutani A, Ochiai H, Delcher AL, Kelley D, Madupu R, Puiu D, Radune D, Shumway M, Trapnell C, Aparna G, Jha G, Pandey A, Patil PB, Ishihara H, Meyer DF, Szurek B, Verdier V, Koebnik R, Dow JM, Ryan RP, Hirata H, Tsuyumu S, Won Lee S, Seo YS, Sriariyanum M, Ronald PC, Sonti RV, Van Sluys MA, Leach JE, White FF, Bogdanove AJ. 2008. Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 9:204. http://dx.doi.org/10.1186/1471-2164-9-204.
29. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557-580. http://dx.doi.org/10.1016/S0022-2836 (83)80284-8.
30. Hopkins CM, White FF, Choi SH, Guo A, Leach JE. 1992. Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 5:451-459. http://dx.doi.org/10.1094/MPMI-5-451.
31. Schafer A, Tauch A, Jager W, Kalinowski J, Thierbach G, Puhler A. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69-73. http://dx.doi.org/10.1016/0378-1119(94)90324-7.
32. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM, Peterson KM. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176. http://dx.doi.org/10.1016/0378-1119(95)00584-1.
33. Ray SK, Rajeshwari R, Sonti RV. 2000. Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase. Mol Plant Microbe Interact 13:394-401. http://dx.doi.org/10.1094/MPMI.2000.13.4.394.
34. Shen Y, Chern M, Silva FG, Ronald P. 2001. Isolation of a Xanthomonas oryzae pv. oryzae flagellar operon region and molecular characterization of flhF. Mol Plant Microbe Interact 14:204-213. http://dx.doi.org/10.1094/MPMI.2001.14.2.204.
35. Guzzo CR, Salinas RK, Andrade MO, Farah CS. 2009. PILZ protein structure and interactions with PILB and the FIMX EAL domain: implications for control of type IV pilus biogenesis. J Mol Biol 393:848-866. http://dx.doi.org/10.1016/j.jmb.2009.07.065.
36. Tang JL, Feng JX, Li QQ, Wen HX, Zhou DL, Wilson TJ, Dow JM, Ma QS, Daniels MJ. 1996. Cloning and characterization of the rpfC gene of Xanthomonas oryzae pv. oryzae: involvement in exopolysaccharide production and virulence to rice. Mol Plant Microbe Interact 9:664-666. http://dx.doi.org/10.1094/MPMI-9-0664.
37. An S, Wu J, Zhang LH. 2010. Modulation of Pseudomonas aeruginosa biofilm dispersal by a cyclic-di-GMP phosphodiesterase with a putative hypoxia-sensing domain. Appl Environ Microbiol 76:8160-8173. http://dx.doi.org/10.1128/AEM.01233-10.
38. Furutanin A, Tsuge S, Oku T, Tsuno K, Inoue Y, Ochiai H, Kaku H, Kubo Y. 2003. HpaI secretion via type III secretion system in Xanthomonas oryzae pv. oryzae. J Gen Plant Pathol 69:271-275. http://dx.doi.org/10.1007/s10327-003-0042-2.
39. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402-408. http://dx.doi.org/10.1006/meth.2001.1262.
40. Tsuge S, Nakayama T, Terashima S, Ochiai H, Furutani A, Oku T, Tsuno K, Kubo Y, Kaku H. 2006. Gene involved in transcriptional activation of the hrp regulatory gene hrpG in Xanthomonas oryzae pv. oryzae. J Bacteriol 188:4158-4162. http://dx.doi.org/10.1128/JB.00 006-06.
41. Sondermann H, Shikuma NJ, Yildiz FH. 2012. You've come a long way: c-di-GMP signaling. Curr Opin Microbiol 15:140-146. http://dx.doi.org/10.1016/j.mib.2011.12.008.
42. Christen M, Christen B, Allan MG, Folcher M, Jeno P, Grzesiek S, Jenal U. 2007. DgrA is a member of a new family of cyclic diguanosine monophosphate receptors and controls flagellar motor function in Caulobacter crescentus. Proc Natl Acad Sci U S A 104:4112-4117. http://dx.doi.org/10.1073/pnas.0607738104.
43. Qi Y, Xu L, Dong X, Yau YH, Ho CL, Koh SL, Shochat SG, Chou SH, Tang K, Liang ZX. 2012. Functional divergence of FimX in PilZ binding and type IV pilus regulation. J Bacteriol 194:5922-5931. http://dx.doi.org/10.1128/JB.00767-12.
44. Kazmierczak BI, Lebron MB, Murray TS. 2006. Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol Microbiol 60:1026-1043. http://dx.doi.org/10.1111/j.1365-2958.2006.05156.x.
45. Viollier PH, Sternheim N, Shapiro L. 2002. A dynamically localized histidine kinase controls the asymmetric distribution of polar pili proteins. EMBO J 21:4420-4428. http://dx.doi.org/10.1093/emboj/cdf454.
46. Gao B, Lara-Tejero M, Lefebre M, Goodman AL, Galán JE. 2014. Novel components of the flagellar system in Epsilonproteobacteria. mBio 5(3): e01349-14. http://dx.doi.org/10.1128/mBio.01349-14.
47. Pitzer JE, Sultan SZ, Hayakawa Y, Hobbs G, Miller MR, Motaleb MA. 2011. Analysis of the Borrelia burgdorferi cyclic-di-GMP-binding protein PlzA reveals a role in motility and virulence. Infect Immun 79:1815-1825. http://dx.doi.org/10.1128/IAI.00075-11.
48. Bian J, Liu X, Cheng YQ, Li C. 2013. Inactivation of cyclic di-GMP binding protein TDE0214 affects the motility, biofilm formation, and virulence of Treponema denticola. J Bacteriol 195:3897-3905. http://dx.doi.org/10.1128/JB.00610-13.
49. Ryan RP. 2013. Cyclic di-GMP signalling and the regulation of bacterial virulence. Microbiology 159:1286-1297. http://dx.doi.org/10.1099/mic.0.068189-0.
50. Petersen E, Chaudhuri P, Gourley C, Harms J, Splitter G. 2011. Brucella melitensis cyclic di-GMP phosphodiesterase BpdA controls expression of flagellar genes. J Bacteriol 193:5683-5691. http://dx.doi.org/10.1128/JB.00428-11.
51. Comolli JC, Hauser AR, Waite L, Whitchurch CB, Mattick JS, Engel JN. 1999. Pseudomonas aeruginosa gene products PilT and PilU are required for cytotoxicity in vitro and virulence in a mouse model of acute pneumonia. Infect Immun 67:3625-3630.
52. Wairuri CK, van der Waals JE, van Schalkwyk A, Theron J. 2012. Ralstonia solanacearum needs Flp pili for virulence on potato. Mol Plant Microbe Interact 25:546-556. http://dx.doi.org/10.1094/MPMI-06-11-0166.
53. Mahdavi J, Royer PJ, Sjolinder HS, Azimi S, Self T, Stoof J, Wheldon LM, Brannstrom K, Wilson R, Moreton J, Moir JW, Sihlbom C, Boren T, Jonsson AB, Soultanas P, Ala'Aldeen DA. 2013. Proinflammatory cytokines can act as intracellular modulators of commensal bacterial virulence. Open Biol 3(10):130048. http://dx.doi.org/10.1098/rsob.130048.
54. Guzzo CR, Dunger G, Salinas RK, Farah CS. 2013. Structure of the PilZ-FimXEAL-c-di-GMP complex responsible for the regulation of bacterial type IV pilus biogenesis. J Mol Biol 425:2174-2197. http://dx.doi.org/10.1016/j.jmb.2013.03.021.
55. Burns C, Gregory KE, Kirby M, Cheung MK, Riquelme M, Elliott TJ, Challen MP, Bailey A, Foster GD. 2005. Efficient GFP expression in the mushroom Agaricus bisporus and Coprinus cinereus requires introns. Fungal Genet Biol 42:191-199. http://dx.doi.org/10.1016/j.fgb.2004.11.005.