Transcriptional responses of Pseudomonas syringae to growth in epiphytic versus apoplastic leaf sites

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 5, 2013, Pages

  Yu, Xilan ^a   Lund, Steven P ^b   Scott, Russell A ^c   Greenwald, Jessica W ^d   Records, Angela H ^d   Nettleton, Dan ^b   Lindow, Steven E ^c   Gross, Dennis C ^d   Beattie, Gwyn A ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b Department of Statistics Center for Statistics and Applications in Forensic Evidence Iowa State University 2438 Osborn Dr Ames   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Endophyte; Epiphyte; Phyllosphere

Indexed keywords

INDOLEACETIC ACID; IRON; NITROGEN; PHENYLALANINE; PLANT TOXIN; SYRINGOLIN A; TRYPTOPHAN; UNCLASSIFIED DRUG;

4 AMINOBUTYRIC ACID METABOLISM; AMINO ACID METABOLISM; APOPLAST; ARTICLE; BACTERIAL VIRULENCE; CATABOLISM; CHEMOTAXIS; ENVIRONMENTAL STRESS; FLAGELLUM; GENE EXPRESSION; HABITAT; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PLANT LEAF; PLANT STRESS; PRIORITY JOURNAL; PSEUDOMONAS SYRINGAE; WATER AVAILABILITY;

BACTERIAL PROTEINS; CELL WALL; CLUSTER ANALYSIS; ECOSYSTEM; EXTRACELLULAR SPACE; FLAGELLA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; MOVEMENT; NITROGEN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEPTIDES, CYCLIC; PHENYLALANINE; PLANT EPIDERMIS; PLANT LEAVES; PSEUDOMONAS SYRINGAE; VIRULENCE; WATER;

EID: 84873182174     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1221892110     Document Type: Article

References (50)

1. Monier JM, Lindow SE (2003) Pseudomonas syringae responds to the environment on leaves by cell size reduction. Phytopathology 93(10):1209-1216. (Pubitemid 37171726)
2. Scholz-Schroeder BK, Hutchison ML, Grgurina I, Gross DC (2001) The contribution of syringopeptin and syringomycin to virulence of Pseudomonas syringae pv. syringae strain B301D on the basis of sypA and syrB1 biosynthesis mutant analysis. Mol Plant Microbe Interact 14(3):336-348. (Pubitemid 32176728)
3. Hirano SS, Charkowski AO, Collmer A, Willis DK, Upper CD (1999) Role of the Hrp type III protein secretion system in growth of Pseudomonas syringae pv. syringae B728a on host plants in the field. Proc Natl Acad Sci USA 96(17):9851-9856. (Pubitemid 29398821)
4. Yu J, Peñaloza-Vázquez A, Chakrabarty AM, Bender CL (1999) Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol Microbiol 33(4):712-720. (Pubitemid 29392652)
5. Joyner DC, Lindow SE (2000) Heterogeneity of iron bioavailability on plants assessed with a whole-cell GFP-based bacterial biosensor. Microbiology 146(Pt 10):2435-2445.
6. Leveau JHJ, Lindow SE (2001) Appetite of an epiphyte: Quantitative monitoring of bacterial sugar consumption in the phyllosphere. Proc Natl Acad Sci USA 98(6):3446-3453. (Pubitemid 32220865)
7. Boch J, et al. (2002) Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol Microbiol 44(1):73-88. (Pubitemid 34429766)
8. Marco ML, Legac J, Lindow SE (2005) Pseudomonas syringae genes induced during colonization of leaf surfaces. Environ Microbiol 7(9):1379-1391. (Pubitemid 41204932)
9. Panopoulous NJ, Schroth MN (1974) Role of flagellar motility in invasion of bean leaves by Pseudomonas phaseolicola. Phytopathology 64(11):1389-1397.
10. Kroupitski Y, et al. (2009) Internalization of Salmonella enterica in leaves is induced by light and involves chemotaxis and penetration through open stomata. Appl Environ Microbiol 75(19):6076-6086.
11. Haefele DM, Lindow SE (1987) Flagellar motility confers epiphytic fitness advantages upon Pseudomonas syringae. Appl Environ Microbiol 53(10):2528-2533.
12. Burch AY, et al. (2012) Pseudomonas syringae coordinates production of a motilityenabling surfactant with flagellar assembly. J Bacteriol 194(6):1287-1298.
13. Cuppels DA (1988) Chemotaxis by Pseudomonas syringae pv. tomato. Appl Environ Microbiol 54(3):629-632.
14. Kim HE, Shitashiro M, Kuroda A, Takiguchi N, Kato J (2007) Ethylene chemotaxis in Pseudomonas aeruginosa and other Pseudomonas species. Microbes Environ 22(2):186-189.
15. Monier JM, Lindow SE (2004) Frequency, size, and localization of bacterial aggregates on bean leaf surfaces. Appl Environ Microbiol 70(1):346-355. (Pubitemid 38090224)
16. Arias-Barrau E, et al. (2004) The homogentisate pathway: A central catabolic pathway involved in the degradation of L-phenylalanine, L-tyrosine, and 3-hydroxyphenylacetate in Pseudomonas putida. J Bacteriol 186(15):5062-5077. (Pubitemid 38970833)
17. Ward JL, et al. (2010) The metabolic transition during disease following infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Plant J 63:443-457.
18. Truman W, de Zabala MT, Grant M (2006) Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J 46(1):14-33. (Pubitemid 43773576)
19. Molina-Henares MA, et al. (2009) Functional analysis of aromatic biosynthetic pathways in Pseudomonas putida KT2440. Microb Biotechnol 2(1):91-100.
20. Mazzola M, White FF (1994) A mutation in the indole-3-acetic acid biosynthesis pathway of Pseudomonas syringae pv. syringae affects growth in Phaseolus vulgaris and syringomycin production. J Bacteriol 176(5):1374-1382. (Pubitemid 24080053)
21. Howden AJ, Rico A, Mentlak T, Miguet L, Preston GM (2009) Pseudomonas syringae pv. syringae B728a hydrolyses indole-3-acetonitrile to the plant hormone indole-3-acetic acid. Mol Plant Pathol 10(6):857-865.
22. Park DH, et al. (2010) Mutations in β-aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. Plant J 64(2):318-330.
23. Rico A, Preston GM (2008) Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol Plant Microbe Interact 21(2):269-282.
24. Hernández-Morales A, et al. (2009) Transcriptional profile of Pseudomonas syringae pv. phaseolicola NPS3121 in response to tissue extracts from a susceptible Phaseolus vulgaris L. cultivar. BMC Microbiol 9:257.
25. Mo YY, Gross DC (1991) Plant signal molecules activate the syrB gene, which is required for syringomycin production by Pseudomonas syringae pv. syringae. J Bacteriol 173(18):5784-5792.
26. Waspi U, Blanc D, Winkler T, Ruedi P, Dudler R (1998) Syringolin, a novel peptide elicitor from Pseudomonas syringae pv. syringae that induces resistance to Pyricularia oryzae in rice. Mol Plant Microbe Interact 11(8):727-733.
27. Schellenberg B, Ramel C, Dudler R (2010) Pseudomonas syringae virulence factor syringolin A counteracts stomatal immunity by proteasome inhibition. Mol Plant Microbe Interact 23(10):1287-1293.
28. Berti AD, Greve NJ, Christensen QH, Thomas MG (2007) Identification of a biosynthetic gene cluster and the six associated lipopeptides involved in swarming motility of Pseudomonas syringae pv. tomato DC3000. J Bacteriol 189(17):6312-6323. (Pubitemid 47378639)
29. Burch AY, Browne PJ, Dunlap CA, Price NP, Lindow SE (2011) Comparison of biosurfactant detection methods reveals hydrophobic surfactants and contactregulated production. Environ Microbiol 13(10):2681-2691.
30. Chang WS, et al. (2007) Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J Bacteriol 189(22):8290-8299.
31. Kurz M, Burch AY, Seip B, Lindow SE, Gross H (2010) Genome-driven investigation of compatible solute biosynthesis pathways of Pseudomonas syringae pv. syringae and their contribution to water stress tolerance. Appl Environ Microbiol 76(16):5452-5462.
32. Jones AM, Wildermuth MC (2011) The phytopathogen Pseudomonas syringae pv. tomato DC3000 has three high-affinity iron-scavenging systems functional under iron limitation conditions but dispensable for pathogenesis. J Bacteriol 193(11):2767-2775.
33. Voigt B, et al. (2007) The glucose and nitrogen starvation response of Bacillus licheniformis. Proteomics 7(3):413-423. (Pubitemid 46293985)
34. Krol E, Becker A (2011) ppGpp in Sinorhizobium meliloti: Biosynthesis in response to sudden nutritional downshifts and modulation of the transcriptome. Mol Microbiol 81(5):1233-1254.
35. Morgan JV, Tukey HB (1964) Characterization of leachate from plant foliage. Plant Physiol 39(4):590-593.
36. Cabral MP, et al. (2011) Proteomic and functional analyses reveal a unique lifestyle for Acinetobacter baumannii biofilms and a key role for histidine metabolism. J Proteome Res 10(8):3399-3417.
37. Montalbini P (1992) Changes in xanthine oxidase activity in bean leaves induced by Uromyces phaseoli infection. J Phytopathol 134(1):63-74.
38. Chen C, Beattie GA (2008) Pseudomonas syringae BetT is a low-affinity choline transporter that is responsible for superior osmoprotection by choline over glycine betaine. J Bacteriol 190(8):2717-2725. (Pubitemid 351508172)
39. Lee J, et al. (2012) Type III secretion and effectors shape the survival and growth pattern of Pseudomonas syringae on leaf surfaces. Plant Physiol 158(4):1803-1818.
40. Koskella BKB, Thompson JN, Preston GM, Buckling A (2011) Local biotic environment shapes the spatial scale of bacteriophage adaptation to bacteria. Am Nat 177(4):440-451.
41. Freeman BC, Beattie GA (2009) Bacterial growth restriction during host resistance to Pseudomonas syringae is associated with leaf water loss and localized cessation of vascular activity in Arabidopsis thaliana. Mol Plant Microbe Interact 22(7):857-867.
42. Feil H, et al. (2005) Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc Natl Acad Sci USA 102(31):11064-11069. (Pubitemid 41105993)
43. Loper JE, Lindow SE (1987) Lack of evidence for in situ fluorescent pigment production by Pseudomonas syringae pv. syringae on bean leaf surfaces. Phytopathology 77(10):1449-1454.
44. King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44(2):301-307.
45. Huynh TV, Dahlbeck D, Staskawicz BJ (1989) Bacterial blight of soybean: Regulation of a pathogen gene determining host cultivar specificity. Science 245(4924):1374-1377.
46. Khodursky AB, et al. (2003) Escherichia coli spotted double-strand DNA microarrays: RNA extraction, labeling, hybridization, quality control, and data management. Methods Mol Biol 224:61-78.
47. Livny J, Teonadi H, Livny M, Waldor MK (2008) High-throughput, kingdomwide prediction and annotation of bacterial non-coding RNAs. PLoS ONE 3(9):e3197.
48. Irizarry RA, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4(2):249-264.
49. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Art 3.
50. Nettleton D, Hwang JTG, Caldo RA, Wise RP (2006) Estimating the number of true null hypotheses from a histogram of P values. J Agric Biol Environ Stat 11(3):337-356. (Pubitemid 44383308)