Transcriptome-based analysis of the Pantoea stewartii quorum-sensing regulon and identification of EsaR direct targets

Applied and Environmental Microbiology

Volumn 80, Issue 18, 2014, Pages 5790-5800

  Ramachandran, Revathy ^a,c   Burke, Alison Kernell ^a   Cormier, Guy ^b   Jensen, Roderick V ^a   Stevens, Ann M ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; ELECTROPHORETIC MOBILITY; POLYMERASE CHAIN REACTION; PROTEINS; RNA; TRANSCRIPTION;

DIFFERENTIALLY EXPRESSED GENE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HOMOSERINE LACTONES; NEXT-GENERATION SEQUENCING; PHYSIOLOGICAL RESPONSE; PROTEOMIC APPROACHES; TRANSCRIPTIONAL REGULATION; TRANSCRIPTIONAL REGULATOR;

GENE EXPRESSION REGULATION;

ADHESION; BACTERIUM; CROP PLANT; DISEASE; GENE EXPRESSION; MAIZE; MOBILITY; MOTILITY; PROTEIN; RNA;

BACTERIAL DNA; BACTERIAL PROTEIN; ESAR PROTEIN, PANTOEA STEWARTII; PROTEIN BINDING; TRANSCRIPTION FACTOR;

GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GENETICS; HIGH THROUGHPUT SEQUENCING; MAIZE; METABOLISM; MICROBIOLOGY; PANTOEA; PHYSIOLOGY; PLANT DISEASE; PROMOTER REGION; QUORUM SENSING; REAL TIME POLYMERASE CHAIN REACTION; REGULON;

BACTERIAL PROTEINS; DNA, BACTERIAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; PANTOEA; PLANT DISEASES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; QUORUM SENSING; REAL-TIME POLYMERASE CHAIN REACTION; REGULON; TRANSCRIPTION FACTORS; ZEA MAYS;

EID: 84906330891     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01489-14     Document Type: Article

References (36)

1. Pataky J. 2003. Stewart's wilt of corn. APSnet Feature 2003:0703. http: //dx.doi.org/10.1094/APSnetFeature-2003-0703.
2. Ham JH, Majerczak D, Ewert S, Sreerekha M-V, Mackey D, Coplin D. 2008. WtsE, an AvrE-family type III effector protein of Pantoea stewartii subsp. stewartii, causes cell death in non-host plants. Mol. Plant Pathol. 9:633-643. http://dx.doi.org/10.1111/j.1364-3703.2008.00489.x.
3. Roper MC. 2011. Pantoea stewartii subsp. stewartii: lessons learned from a xylem-dwelling pathogen of sweet corn. Mol. Plant Pathol. 12:628-637. http://dx.doi.org/10.1111/j.1364-3703.2010.00698.x.
4. Sasu MA, Seidl-Adams I, Wall K, Winsor JA, Stephenson AG. 2010. Floral transmission of Erwinia tracheiphila by cucumber beetles in a wild Cucurbita pepo. Environ. Entomol. 39:140-148. http://dx.doi.org/10.1603 /EN09190.
5. Crossman L, Dow JM. 2004. Biofilm formation and dispersal in Xanthomonas campestris. Microbes Infect. 6:623-629. http://dx.doi.org/10.1016/j.micinf.2004.01.013.
6. Nunney L, Yuan X, Bromley R, Hartung J, Montero-Astúa M, Moreira L, Ortiz B, Stouthamer R. 2010. Population genomic analysis of a bacterial plant pathogen: novel insight into the origin of Pierce's disease of grapevine in the U.S. PLoS One 5:e15488. http://dx.doi.org/10.1371 /journal.pone.0015488.
7. Peeters N, Guidot A, Vailleau F, Valls M. 2013. Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol. Plant Pathol. 14:651-662. http://dx.doi.org/10.1111/mpp.12038.
8. Minogue TD, Wehland-von Trebra M, Bernhard F, von Bodman SB. 2002. The autoregulatory role of EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: evidence for a repressor function. Mol. Microbiol. 44:1625- 1635. http://dx.doi.org/10.1046/j.1365-2958.2002.02987.x.
9. Glasner JD. 2003. ASAP, a systematic annotation package for community analysis of genomes. Nucleic Acids Res. 31:147-151. http://dx.doi.org/10.1093/nar/gkg125.
10. Beck von Bodman S, Farrand SK. 1995. Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an Nacylhomoserine lactone autoinducer. J. Bacteriol. 177:5000-5008.
11. Coplin DL, Rowan RG, Chisholm DA, Whitmoyer RE. 1981. Characterization of plasmids in Erwinia stewartii. Appl. Environ. Microbiol. 42: 599-604.
12. von Bodman SB, Majerczak DR, Coplin DL. 1998. A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc. Natl. Acad. Sci. U. S. A. 95:7687- 7692. http://dx.doi.org/10.1073/pnas.95.13.7687.
13. Ramachandran R, Stevens AM. 2013. Proteomic analysis of the quorumsensing regulon in Pantoea stewartii and identification of direct targets of EsaR. Appl. Environ. Microbiol. 79:6244-6252. http://dx.doi.org/10.1128 /AEM.01744-13.
14. Cock PJA, Antao T, Chang JT, Chapman BA, Cox CJ, Dalke A, Friedberg I, Hamelryck T, Kauff F, Wilczynski B, de Hoon MJL. 2009. Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25:1422-1423. http://dx.doi.org /10.1093/bioinformatics/btp163.
15. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410. http://dx.doi.org/10.1016/S0022-2836(05)80360-2.
16. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421. http://dx.doi.org/10.1186/1471-2105-10-421.
17. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinformatics 25:1754-1760. http://dx.doi.org/10.1093/bioinformatics/btp324.
18. Mane SP, Evans C, Cooper KL, Crasta OR, Folkerts O, Hutchison SK, Harkins TT, Thierry-Mieg D, Thierry-Mieg J, Jensen RV. 2009. Transcriptome sequencing of the microarray quality control (MAQC) RNA reference samples using next generation sequencing. BMC Genomics 10:264. http://dx.doi.org/10.1186/1471-2164-10-264.
19. Schu DJ, Carlier AL, Jamison KP, von Bodman SB, Stevens AM. 2009. Structure/function analysis of the Pantoea stewartii quorum-sensing regulator EsaR as an activator of transcription. J. Bacteriol. 191:7402-7409. http://dx.doi.org/10.1128/JB.00994-09.
20. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45. http://dx.doi.org/10.1093 /nar/29.9.e45.
21. Hertz GZ, Stormo GD. 1999. Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics 15:563-577. http://dx.doi.org/10.1093/bioinformatics/15.7.563.
22. Liu H, Coulthurst SJ, Pritchard L, Hedley PE, Ravensdale M, Humphris S, Burr T, Takle G, Brurberg MB, Birch PR, Salmond GP, Toth IK. 2008. Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog. 4:e1000093. http://dx.doi.org/10.1371/journal.ppat.1000093.
23. Carlier AL, von Bodman SB. 2006. The rcsA promoter of Pantoea stewartii subsp. stewartii features a low-level constitutive promoter and an EsaR quorum-sensing-regulated promoter. J. Bacteriol. 188:4581-4584. http://dx.doi.org/10.1128/JB.00211-06.
24. Wang X, Yang F, von Bodman SB. 2012. The genetic and structural basis of two distinct terminal side branch residues in stewartan and amylovoran exopolysaccharides and their potential role in host adaptation. Mol. Microbiol. 83:195-207. http://dx.doi.org/10.1111/j.1365-2958.2011.07926.x.
25. Koutsoudis MD, Tsaltas D, Minogue TD, von Bodman SB. 2006. Quorum-sensing regulation governs bacterial adhesion, biofilm development, and host colonization in Pantoea stewartii subspecies stewartii. Proc. Natl. Acad. Sci. U. S. A. 103:5983-5988. http://dx.doi.org/10.1073/pnas.0509860103.
26. Carlier A, Burbank L, von Bodman SB. 2009. Identification and characterization of three novel EsaI/EsaR quorum-sensing controlled stewartan exopolysaccharide biosynthetic genes in Pantoea stewartii ssp. stewartii. Mol. Microbiol. 74:903-913. http://dx.doi.org/10.1111/j.1365-2958.2009.06906.x.
27. Mangan S, Zaslaver A, Alon U. 2003. The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks. J. Mol. Biol. 334:197-204. http://dx.doi.org/10.1016/j.jmb.2003.09.049.
28. Ferrieres L, Aslam SN, Cooper RM, Clarke DJ. 2007. The yjbEFGH locus in Escherichia coli K-12 is an operon encoding proteins involved in exopolysaccharide production. Microbiology 153:1070-1080. http://dx.doi.org /10.1099/mic.0.2006/002907-0.
29. Herrera CM, Koutsoudis MD, Wang X, Bodman SB von. 2008. Pantoea stewartii subsp. stewartii exhibits surface motility, which is a critical aspect of Stewart's wilt disease development on maize. Mol. Plant Microbe Interact. 21:1359-1370. http://dx.doi.org/10.1094/MPMI-21-10-1359.
30. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R. 2005. Genomewide analysis of the general stress response network in Escherichia coli: Sdependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187: 1591-1603. http://dx.doi.org/10.1128/JB.187.5.1591-1603.2005.
31. González Barrios AF, Zuo R, Hashimoto Y, Yang L, Bentley WE, Wood TK. 2006. Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J. Bacteriol. 188:305-316. http://dx.doi.org/10.1128/JB.188.1.305-316.2006.
32. Yim HH, Brems RL, Villarejo M. 1994. Molecular characterization of the promoter of osmY, an rpoS-dependent gene. J. Bacteriol. 176:100-107.
33. Yoshida H, Maki Y, Furuike S, Sakai A, Ueta M, Wada A. 2012. YqjD is an inner membrane protein associated with stationary-phase ribosomes in Escherichia coli. J. Bacteriol. 194:4178-4183. http://dx.doi.org/10.1128/JB.00396-12.
34. Chapalain A, Vial L, Laprade N, Dekimpe V, Perreault J, Déziel E. 2013. Identification of quorum sensing-controlled genes in Burkholderia ambifaria. Microbiologyopen 2:226-242. http://dx.doi.org/10.1002/mbo3.67.
35. Lee J, Hiibel SR, Reardon KF, Wood TK. 2010. Identification of stressrelated proteins in Escherichia coli using the pollutant cisdichloroethylene. J. Appl. Microbiol. 108:2088-2102. http://dx.doi.org /10.1111/j.1365-2672.2009.04611.x.
36. Tkaczuk KL, Shumilin IA, Chruszcz M, Evdokimova E, Savchenko A, Minor W. 2013. Structural and functional insight into the universal stress protein family. Evol. Appl. 6:434-449. http://dx.doi.org/10.1111/eva.12057.