Variable Suites of Non-effector Genes Are Co-regulated in the Type III Secretion Virulence Regulon across the Pseudomonas syringae Phylogeny

PLoS Pathogens

Volumn 10, Issue 1, 2014, Pages

  Mucyn, Tatiana S ^a   Yourstone, Scott ^a   Lind, Abigail L ^a,e   Biswas, Surojit ^a   Nishimura, Marc T ^a   Baltrus, David A ^b   Cumbie, Jason S ^c   Chang, Jeff H ^c   Jones, Corbin D ^a   Dangl, Jeffery L ^a,d   Grant, Sarah R ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c OREGON STATE UNIVERSITY   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA BINDING PROTEIN; HRPL PROTEIN, PSEUDOMONAS SYRINGAE; SIGMA FACTOR; VIRULENCE FACTOR;

BACTERIAL SECRETION SYSTEM; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; OPERON; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; PSEUDOMONAS SYRINGAE;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; DNA-BINDING PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; OPERON; PHYLOGENY; PSEUDOMONAS SYRINGAE; SIGMA FACTOR; VIRULENCE FACTORS;

EID: 84893720690     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003807     Document Type: Article

References (91)

1. Troisfontaines P, Cornelis GR, (2005) Type III secretion: more systems than you think. Physiology (Bethesda) 20: 326-339.
2. Naum M, Brown EW, Mason-Gamer RJ, (2009) Phylogenetic evidence for extensive horizontal gene transfer of type III secretion system genes among enterobacterial plant pathogens. Microbiology 155: 3187-3199.
3. Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS, et al. (2011) Dynamic Evolution of Pathogenicity Revealed by Sequencing and Comparative Genomics of 19 Pseudomonas syringae Isolates. PLoS Pathog 7: e1002132.
4. Hirano SS, Upper CD, (2000) Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte. Microbiol Mol Biol Rev 64: 624-653.
5. Morris CE, Monteil CL, Berge O, (2013) The Life History of Pseudomonas syringae: Linking Agriculture to Earth System Processes. Annu Rev Phytopathol 51: 85-104.
6. O'Brien HE, Desveaux D, Guttman DS, (2011) Next-generation genomics of Pseudomonas syringae. Curr Opin Microbiol 14: 24-30.
7. Alfano JR, Charkowski AO, Deng WL, Badel JL, Petnicki-Ocwieja T, et al. (2000) The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc Natl Acad Sci U S A 97: 4856-4861.
8. Stavrinides J, McCann HC, Guttman DS, (2008) Host-pathogen interplay and the evolution of bacterial effectors. Cell Microbiol 10: 285-292.
9. Rohmer L, Guttman DS, Dangl JL, (2004) Diverse evolutionary mechanisms shape the type III effector virulence factor repertoire in the plant pathogen Pseudomonas syringae. Genetics 167: 1341-1360.
10. Lindeberg M, Myers CR, Collmer A, Schneider DJ, (2008) Roadmap to new virulence determinants in Pseudomonas syringae: insights from comparative genomics and genome organization. Mol Plant Microbe Interact 21: 685-700.
11. Jones JD, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
12. Xiao Y, Heu S, Yi J, Lu Y, Hutcheson SW, (1994) Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J Bacteriol 176: 1025-1036.
13. Tang X, Xiao Y, Zhou JM, (2006) Regulation of the type III secretion system in phytopathogenic bacteria. Mol Plant Microbe Interact 19: 1159-1166.
14. Xiao Y, Hutcheson SW, (1994) A single promoter sequence recognized by a newly identified alternate sigma factor directs expression of pathogenicity and host range determinants in Pseudomonas syringae. J Bacteriol 176: 3089-3091.
15. Fouts DE, Abramovitch RB, Alfano JR, Baldo AM, Buell CR, et al. (2002) Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc Natl Acad Sci U S A 99: 2275-2280.
16. Lan L, Deng X, Zhou J, Tang X, (2006) Genome-wide gene expression analysis of Pseudomonas syringae pv. tomato DC3000 reveals overlapping and distinct pathways regulated by hrpL and hrpRS. Mol Plant Microbe Interact 19: 976-987.
17. Ferreira AO, Myers CR, Gordon JS, Martin GB, Vencato M, et al. (2006) Whole-genome expression profiling defines the HrpL regulon of Pseudomonas syringae pv. tomato DC3000, allows de novo reconstruction of the Hrp cis clement, and identifies novel coregulated genes. Mol Plant Microbe Interact 19: 1167-1179.
18. Vencato M, Tian F, Alfano JR, Buell CR, Cartinhour S, et al. (2006) Bioinformatics-enabled identification of the HrpL regulon and type III secretion system effector proteins of Pseudomonas syringae pv. phaseolicola 1448A. Mol Plant Microbe Interact 19: 1193-1206.
19. Chang JH, Urbach JM, Law TF, Arnold LW, Hu A, et al. (2005) A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proc Natl Acad Sci U S A 102: 2549-2554.
20. McNally RR, Toth IK, Cock PJ, Pritchard L, Hedley PE, et al. (2012) Genetic characterization of the HrpL regulon of the fire blight pathogen Erwinia amylovora reveals novel virulence factors. Mol Plant Pathol 13: 160-173.
21. Occhialini A, Cunnac S, Reymond N, Genin S, Boucher C, (2005) Genome-wide analysis of gene expression in Ralstonia solanacearum reveals that the hrpB gene acts as a regulatory switch controlling multiple virulence pathways. Mol Plant Microbe Interact 18: 938-949.
22. Noel L, Thieme F, Nennstiel D, Bonas U, (2001) cDNA-AFLP analysis unravels a genome-wide hrpG-regulon in the plant pathogen Xanthomonas campestris pv. vesicatoria. Mol Microbiol 41: 1271-1281.
23. Schmidtke C, Findeiss S, Sharma CM, Kuhfuss J, Hoffmann S, et al. (2012) Genome-wide transcriptome analysis of the plant pathogen Xanthomonas identifies sRNAs with putative virulence functions. Nucleic Acids Res 40: 2020-2031.
24. Hogan CS, Mole BM, Grant SR, Willis DK, Charkowski AO, (2013) The Type III Secreted Effector DspE Is Required Early in Solanum tuberosum Leaf Infection by Pectobacterium carotovorum to Cause Cell Death, and Requires Wx(3-6)D/E Motifs. PLoS One 8: e65534.
25. Sreedharan A, Penaloza-Vazquez A, Kunkel BN, Bender CL, (2006) CorR regulates multiple components of virulence in Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact 19: 768-779.
26. Ullrich M, Penaloza-Vazquez A, Bailey AM, Bender CL, (1995) A modified two-component regulatory system is involved in temperature-dependent biosynthesis of the Pseudomonas syringae phytotoxin coronatine. J Bacteriol 177: 6160-6169.
27. Hwang MS, Morgan RL, Sarkar SF, Wang PW, Guttman DS, (2005) Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Appl Environ Microbiol 71: 5182-5191.
28. Bull CT, Manceau C, Lydon J, Kong H, Vinatzer BA, et al. (2010) Pseudomonas cannabina pv. cannabina pv. nov., and Pseudomonas cannabina pv. alisalensis (Cintas Koike and Bull, 2000) comb. nov., are members of the emended species Pseudomonas cannabina (ex Sutic & Dowson 1959) Gardan, Shafik, Belouin, Brosch, Grimont & Grimont 1999. Syst Appl Microbiol 33: 105-115.
29. Joardar V, Lindeberg M, Jackson RW, Selengut J, Dodson R, et al. (2005) Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. J Bacteriol 187: 6488-6498.
30. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, et al. (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A 100: 10181-10186.
31. Feil H, Feil WS, Chain P, Larimer F, DiBartolo G, et al. (2005) Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc Natl Acad Sci U S A 102: 11064-11069.
32. Butler MI, Stockwell PA, Black MA, Day RC, Lamont IL, et al. (2013) Pseudomonas syringae pv. actinidiae from recent outbreaks of kiwifruit bacterial canker belong to different clones that originated in China. PLoS One 8: e57464.
33. O'Brien HE, Thakur S, Gong Y, Fung P, Zhang J, et al. (2012) Extensive remodeling of the Pseudomonas syringae pv. avellanae type III secretome associated with two independent host shifts onto hazelnut. BMC Microbiol 12: 141.
34. Green S, Studholme DJ, Laue BE, Dorati F, Lovell H, et al. (2010) Comparative genome analysis provides insights into the evolution and adaptation of Pseudomonas syringae pv. aesculi on Aesculus hippocastanum. PLoS One 5: e10224.
35. Sarris PF, Trantas EA, Baltrus DA, Bull CT, Wechter WP, et al. (2013) Comparative genomics of multiple strains of Pseudomonas cannabina pv. alisalensis, a potential model pathogen of both monocots and dicots. PLoS One 8: e59366.
36. Reinhardt JA, Baltrus DA, Nishimura MT, Jeck WR, Jones CD, et al. (2009) De novo assembly using low-coverage short read sequence data from the rice pathogen Pseudomonas syringae pv. oryzae. Genome Res 19: 294-305.
37. Cai R, Lewis J, Yan S, Liu H, Clarke CR, et al. (2011) The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog 7: e1002130.
38. Studholme DJ, Ibanez SG, MacLean D, Dangl JL, Chang JH, et al. (2009) A draft genome sequence and functional screen reveals the repertoire of type III secreted proteins of Pseudomonas syringae pathovar tabaci 11528. BMC Genomics 10: 395.
39. McCann HC, Rikkerink EHA, Bertels F, Fiers M, Lu A, et al. (2013) Genomic Analysis of the Kiwifruit Pathogen Pseudomonas syringae pv. actinidiae Provides Insight into the Origins of an Emergent Plant Disease. PLoS Pathog 9: e1003503.
40. Clarke CR, Cai R, Studholme DJ, Guttman DS, Vinatzer BA, (2010) Pseudomonas syringae strains naturally lacking the classical P. syringae hrp/hrc Locus are common leaf colonizers equipped with an atypical type III secretion system. Mol Plant Microbe Interact 23: 198-210.
41. Filiatrault MJ, Stodghill PV, Myers CR, Bronstein PA, Butcher BG, et al. (2011) Genome-wide identification of transcriptional start sites in the plant pathogen Pseudomonas syringae pv. tomato str. DC3000. PLoS One 6: e29335.
42. Filiatrault MJ, Stodghill PV, Bronstein PA, Moll S, Lindeberg M, et al. (2010) Transcriptome analysis of Pseudomonas syringae identifies new genes, noncoding RNAs, and antisense activity. J Bacteriol 192: 2359-2372.
43. Greenwald JW, Greenwald CJ, Philmus BJ, Begley TP, Gross DC, (2012) RNA-seq analysis reveals that an ECF sigma factor, AcsS, regulates achromobactin biosynthesis in Pseudomonas syringae pv. syringae B728a. PLoS One 7: e34804.
44. Hockett KL, Burch AY, Lindow SE, (2013) Thermo-regulation of genes mediating motility and plant interactions in Pseudomonas syringae. PLoS One 8: e59850.
45. Cumbie JS, Kimbrel JA, Di Y, Schafer DW, Wilhelm LJ, et al. (2011) GENE-counter: a computational pipeline for the analysis of RNA-Seq data for gene expression differences. PLoS One 6: e25279.
46. Bushley KE, Raja R, Jaiswal P, Cumbie JS, Nonogaki M, et al. (2013) The genome of Tolypocladium inflatum: evolution, organization, and expression of the cyclosporin biosynthetic gene cluster. PLoS Genet 9: e1003496.
47. Filichkin SA, Mockler TC, (2012) Unproductive alternative splicing and nonsense mRNAs: a widespread phenomenon among plant circadian clock genes. Biol Direct 7: 20.
48. Huynh TV, Dahlbeck D, Staskawicz BJ, (1989) Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245: 1374-1377.
49. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
50. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
51. Greene W, (2008) Functional forms for the negative binomial model for count data. Economics Letters 99: 585-590.
52. Greene W, (2005) Functional Form and Heterogeneity in Models for Count Data. Foundations and Trends® in Econometrics 1: 113-218.
53. Di Y, Schafer D, Cumbie J, Chang J, (2011) The NBP Negative Binomial Model for Assessing Differential Gene Expression from RNA-Seq. Stat Appl Genet Mol Biol 10Article 24.
54. Kvitko BH, Park DH, Velasquez AC, Wei CF, Russell AB, et al. (2009) Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog 5: e1000388.
55. Mukaihara T, Tamura N, (2009) Identification of novel Ralstonia solanacearum type III effector proteins through translocation analysis of hrpB-regulated gene products. Microbiology 155: 2235-2244.
56. Guttman DS, Vinatzer BA, Sarkar SF, Ranall MV, Kettler G, et al. (2002) A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295: 1722-1726.
57. Cunnac S, Chakravarthy S, Kvitko BH, Russell AB, Martin GB, et al. (2011) Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc Natl Acad Sci U S A 108: 2975-2980.
58. Lindeberg M, Stavrinides J, Chang JH, Alfano JR, Collmer A, et al. (2005) Proposed guidelines for a unified nomenclature and phylogenetic analysis of type III Hop effector proteins in the plant pathogen Pseudomonas syringae. Mol Plant Microbe Interact 18: 275-282.
59. Lindow SE, (1985) Ecology of Pseudomonas syringae relevant to the field use of Ice- deletion mutants constructed in vitro for plant frost control. Engineered Organisms in the Environment: Scientific Issues pp. 23-35.
60. Mohr TJ, Liu H, Yan S, Morris CE, Castillo JA, et al. (2008) Naturally occurring nonpathogenic isolates of the plant pathogen Pseudomonas syringae lack a type III secretion system and effector gene orthologues. J Bacteriol 190: 2858-2870.
61. Morris CE, Sands DC, Vanneste JL, Montarry J, Oakley B, et al. (2010) Inferring the evolutionary history of the plant pathogen Pseudomonas syringae from its biogeography in headwaters of rivers in North America, Europe, and New Zealand. MBio 1: e00107-10.
62. Morris CE, Sands DC, Vinatzer BA, Glaux C, Guilbaud C, et al. (2008) The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle. ISME J 2: 321-334.
63. Baltrus DA, Yourstone S, Lind A, Guilbaud C, Sands DC, et al. (2013) Draft Genomes for a Phylogenetically Diverse Suite of Pseudomonas syringae Isolates From Multiple Source Populations. J Bacteriol in press.
64. Schechter LM, Vencato M, Jordan KL, Schneider SE, Schneider DJ, et al. (2006) Multiple approaches to a complete inventory of Pseudomonas syringae pv. tomato DC3000 type III secretion system effector proteins. Mol Plant Microbe Interact 19: 1180-1192.
65. Keen NT, Tamaki S, Kobayashi D, Gerhold D, Stayton M, et al. (1990) Bacteria expressing avirulence gene D produce a specific elicitor of the soybean hypersensitive reaction. Mol Plant Microbe Interact 3: 112-121.
66. Kobayashi DY, Tamaki SJ, Keen NT, (1989) Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc Natl Acad Sci U S A 86: 157-161.
67. Kobayashi DY, Tamaki SJ, Keen NT, (1990) Molecular characterization of avirulence gene D from Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 3: 94-102.
68. Loper JE, Hassan KA, Mavrodi DV, Davis EW 2nd, Lim CK, et al. (2012) Comparative genomics of plant-associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet 8: e1002784.
69. Stavrinides J, Ma W, Guttman DS, (2006) Terminal reassortment drives the quantum evolution of type III effectors in bacterial pathogens. PLoS Pathog 2: e104.
70. Gazi AD, Sarris PF, Fadouloglou VE, Charova SN, Mathioudakis N, et al. (2012) Phylogenetic analysis of a gene cluster encoding an additional, rhizobial-like type III secretion system that is narrowly distributed among Pseudomonas syringae strains. BMC Microbiol 12: 188.
71. Badel JL, Shimizu R, Oh HS, Collmer A, (2006) A Pseudomonas syringae pv. tomato avrE1/hopM1 mutant is severely reduced in growth and lesion formation in tomato. Mol Plant Microbe Interact 19: 99-111.
72. Macho AP, Zumaquero A, Gonzalez-Plaza JJ, Ortiz-Martin I, Rufian JS, et al. (2012) Genetic analysis of the individual contribution to virulence of the type III effector inventory of Pseudomonas syringae pv. phaseolicola. PLoS One 7: e35871.
73. Melotto M, Underwood W, Koczan J, Nomura K, He SY, (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969-980.
74. Glass NL, Kosuge T, (1986) Cloning of the gene for indoleacetic acid-lysine synthetase from Pseudomonas syringae subsp. savastanoi. J Bacteriol 166: 598-603.
75. Denance N, Sanchez-Vallet A, Goffner D, Molina A, (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4: 155.
76. Oh CS, Kim JF, Beer SV, (2005) The Hrp pathogenicity island of Erwinia amylovora and identification of three novel genes required for systemic infectiondouble dagger. Mol Plant Pathol 6: 125-138.
77. Beck BJ, Downs DM, (1998) The apbE gene encodes a lipoprotein involved in thiamine synthesis in Salmonella typhimurium. J Bacteriol 180: 885-891.
78. Skovran E, Lauhon CT, Downs DM, (2004) Lack of YggX results in chronic oxidative stress and uncovers subtle defects in Fe-S cluster metabolism in Salmonella enterica. J Bacteriol 186: 7626-7634.
79. Boyd JM, Endrizzi JA, Hamilton TL, Christopherson MR, Mulder DW, et al. (2011) FAD binding by ApbE protein from Salmonella enterica: a new class of FAD-binding proteins. J Bacteriol 193: 887-895.
80. Silby MW, Cerdeno-Tarraga AM, Vernikos GS, Giddens SR, Jackson RW, et al. (2009) Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol 10: R51.
81. Burnens AP, Stanley J, Sack R, Hunziker P, Brodard I, et al. (1997) The flagellin N-methylase gene fliB and an adjacent serovar-specific IS200 element in Salmonella typhimurium. Microbiology 143 (Pt 5):: 1539-1547.
82. Oldenburg M, Kruger A, Ferstl R, Kaufmann A, Nees G, et al. (2012) TLR13 recognizes bacterial 23S rRNA devoid of erythromycin resistance-forming modification. Science 337: 1111-1115.
83. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, et al. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764-767.
84. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
85. Murillo J, Shen H, Gerhold D, Sharma A, Cooksey DA, et al. (1994) Characterization of pPT23B, the plasmid involved in syringolide production by Pseudomonas syringae pv. tomato PT23. Plasmid 31: 275-287.
86. Atkinson MM, Midland SL, Sims JJ, Keen NT, (1996) Syringolide 1 Triggers Ca2+ Influx, K+ Efflux, and Extracellular Alkalization in Soybean Cells Carrying the Disease-Resistance Gene Rpg4. Plant Physiol 112: 297-302.
87. Yucel I, Midland SL, Sims JJ, Keen NT, (1994) Class I and class II avrD alleles direct the production of different products in gram-negative bacteria. Mol Plant Microbe Interact 7: 148-150.
88. Gust B, Chandra G, Jakimowicz D, Yuqing T, Bruton CJ, et al. (2004) Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces. Adv Appl Microbiol 54: 107-128.
89. Earl AM, Desjardins CA, Fitzgerald MG, Arachchi HM, Zeng Q, et al. (2011) High quality draft genome sequence of Segniliparus rugosus CDC 945(T) = (ATCC BAA-974(T)). Stand Genomic Sci 5: 389-397.
90. Wernisch L, Kendall SL, Soneji S, Wietzorrek A, Parish T, et al. (2003) Analysis of whole-genome microarray replicates using mixed models. Bioinformatics 19: 53-61.
91. Marco ML, Legac J, Lindow SE, (2005) Pseudomonas syringae genes induced during colonization of leaf surfaces. Environ Microbiol 7: 1379-1391.