Plant responses to bacterial N-acyl l-homoserine lactones are dependent on enzymatic degradation to l-homoserine

ACS Chemical Biology

Volumn 9, Issue 8, 2014, Pages 1834-1845

  Palmer, Andrew G ^a,b   Senechal, Amanda C ^a   Mukherjee, Arijit ^a,c   Ané, Jean Michel ^a   Blackwell, Helen E ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Department of Agronomy University of Wisconsin Madison ^*  (United States)

^c UNIVERSITY OF CENTRAL ARKANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ETHYLENE; FATTY ACID AMIDASE; HOMOSERINE; N ACYLHOMOSERINE LACTONE; VIRULENCE FACTOR; AMIDASE; FATTY-ACID AMIDE HYDROLASE; GAMMA BUTYROLACTONE DERIVATIVE;

ARABIDOPSIS THALIANA; ARTICLE; BARREL MEDIC; BIOFILM; BIOLUMINESCENCE; CELL DENSITY; CONTROLLED STUDY; ENZYMATIC DEGRADATION; EUKARYOTE; EVAPOTRANSPIRATION; GRAM NEGATIVE BACTERIUM; NODULATION; NONHUMAN; PHENOTYPE; PLANT GROWTH; PLANT RESPONSE; PRIORITY JOURNAL; QUORUM SENSING; HYDROLYSIS; METABOLISM;

ACYL-BUTYROLACTONES; AMIDOHYDROLASES; HOMOSERINE; HYDROLYSIS; QUORUM SENSING;

EID: 84906280585     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500191a     Document Type: Article

References (66)

1. Bassler, B. L. (2012) Microbes as menaces, mates, and marvels Daedalus 141, 67-76
2. Bassler, B. L. and Losick, R. (2006) Bacterially speaking Cell 125, 237-246
3. Fuqua, C. and Greenberg, E. P. (2002) Listening in on bacteria: Acyl-homoserine lactone signalling Nat. Rev. Mol. Cell Biol. 3, 685-695
4. Schuster, M., Sexton, D. J., Diggle, S. P., Greenberg, E. P., and Gottesman, S. (2013) Acyl-homoserine lactone quorum sensing: From evolution to application Annu. Rev. Microbiol. 67, 43-63
5. Bjarnsholt, T. and Givskov, M. (2007) The role of quorum sensing in the pathogenicity of the cunning aggressor Pseudomonas aeruginosa Anal. Bioanal. Chem. 387, 409-414
6. Rumbaugh, K. P., Griswold, J. A., Iglewski, B. H., and Hamood, A. N. (1999) Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections Infect. Immun. 67, 5854-5862
7. Gurich, N. and Gonzalez, J. E. (2009) Role of quorum sensing in Sinorhizobium meliloti -alfalfa symbiosis J. Bacteriol. 191, 4372-4382
8. Stacy, D. M., Welsh, M. A., Rather, P. N., and Blackwell, H. E. (2012) Attenuation of quorum sensing in the pathogen Acinetobacter baumannii using non-native N -acyl homoserine lactones ACS Chem. Biol. 7, 1719-1728
9. Palmer, A. G., Streng, E., and Blackwell, H. E. (2011) Attenuation of virulence in pathogenic bacteria using synthetic quorum-sensing modulators under native conditions on plant hosts ACS Chem. Biol. 6, 1348-1356
10. Palmer, A. G., Streng, E., Jewell, K. A., and Blackwell, H. E. (2011) Quorum sensing in bacterial species that use degenerate autoinducers can be tuned by using structurally identical non-native ligands ChemBioChem. 12, 138-147
11. Geske, G. D., O'Neill, J. C., and Blackwell, H. E. (2007) N -phenylacetanoyl- l -homoserine lactones can strongly antagonize or superagonize quorum sensing in Vibrio fischeri ACS Chem. Biol. 2, 315-319
12. Galloway, W. R. J. D., Hodgkinson, J. T., Bowden, S. D., Welch, M., and Spring, D. R. (2011) Quorum sensing in gram-negative bacteria: Small-molecule modulation of AHL and Al-2 quorum sensing pathways Chem. Rev. 111, 28-67
13. Amara, N., Mashiach, R., Amar, D., Krief, P., Spieser, S. A. H., Bottomley, M. J., Aharoni, A., and Meijler, M. M. (2009) Covalent inhibition of bacterial quorum sensing J. Am. Chem. Soc. 131, 10610-10619
14. Teplitski, M., Mathesius, U., and Rumbaugh, K. P. (2011) Perception and degradation of N -acyl homoserine lactone quorum sensing signals by mammalian and plant cells Chem. Rev. 111, 100-116
15. Bryan, A., Watters, C., Koenig, L., Youn, E., Olmos, A., Li, G., Williams, S. C., and Rumbaugh, K. P. (2010) Human transcriptome analysis reveals a potential role for active transport in the metabolism of Pseudomonas aeruginosa autoinducers Microbes Infect. 12, 1042-1050
16. Kravchenko, V. V., Kaufmann, G. F., Mathison, J. C., Scott, D. A., Katz, A. Z., Grauer, D. C., Lehmann, M., Meijler, M. M., Janda, K. D., and Ulevitch, R. J. (2008) Modulation of gene expression via disruption of NF-KB signaling by a bacterial small molecule Science 321, 259-263
17. Ritchie, A. J., Jansson, A., Stallberg, J., Nilsson, P., Lysaght, P., and Cooley, M. A. (2005) The Pseudomonas aeruginosa quorum-sensing molecule N -3-(oxododecanoyl)- l -homoserine lactone inhibits T-cell differentiation and cytokine production by a mechanism involving an early step in T-cell activation Infect. Immun. 73, 1648-1655
18. Telford, G., Wheeler, D., Williams, P., Tomkins, P. T., Appleby, P., Sewell, H., Stewart, G. S., Bycroft, B. W., and Pritchard, D. I. (1998) The Pseudomonas aeruginosa quorum-sensing signal molecule N -(3-oxododecanoyl)- l -homoserine lactone has immunomodulatory activity Infect. Immun. 66, 36-42
19. Venturi, V., Fuqua, C., and VanAlfen, N. K. (2013) Chemical signaling between plants and plant-pathogenic bacteria Annu. Rev. Phytopathol. 51, 17-37
20. Ortíz-Castro, R., Contreras-Cornejo, H. A., Macias-Rodriguez, L., and Lopez-Bucio, J. (2009) The role of microbial signals in plant growth and development Plant Signal Behav. 4, 701-712
21. Schaefer, A. L., Lappala, C. R., Morlen, R. P., Pelletier, D. A., Lu, T. Y. S., Lankford, P. K., Harwood, C. S., and Greenberg, E. P. (2013) LuxR- and LuxI-type quorum-sensing circuits are prevalent in members of the Populus deltoides microbiome Appl. Environ. Microbiol. 79, 5745-5752
22. Joint, I., Tait, K., Callow, M. E., Callow, J. A., Milton, D., Williams, P., and Camara, M. (2002) Cell-to-cell communication across the prokaryote-eukaryote boundary Science 298, 1207
23. Licciardello, G., Bertani, I., Steindler, L., Bella, P., Venturi, V., and Catara, V. (2007) Pseudomonas corrugata contains a conserved N -acyl homoserine lactone quorum sensing system; its role in tomato pathogenicity and tobacco hypersensitivity response FEMS Microbiol. Ecol. 61, 222-234
24. Schuhegger, R., Ihring, A., Gantner, S., Bahnweg, G., Knappe, C., Vogg, G., Hutzler, P., Schmid, M., Van Breusegem, F., Eberl, L., Hartmann, A., and Langebartels, C. (2006) Induction of systemic resistance in tomato by N -acyl- l -homoserine lactone-producing rhizosphere bacteria Plant Cell Environ. 29, 909-918
25. von Rad, U., Klein, I., Dobrev, P. I., Kottova, J., Zazimalova, E., Fekete, A., Hartmann, A., Schmitt-Kopplin, P., and Durner, J. (2008) Response of Arabidopsis thaliana to N -hexanoyl- dl -homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere Planta 229, 73-85
26. Ortíz-Castro, R., Martinez-Trujillo, M., and Lopez-Bucio, J. (2008) N -acyl- l -homoserine lactones: A class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana Plant Cell Environ. 31, 1497-1509
27. Mathesius, U., Mulders, S., Gao, M., Teplitski, M., Caetano-Anolles, G., Rolfe, B. G., and Bauer, W. D. (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals Proc. Natl. Acad. Sci. U.S.A. 100, 1444-1449
28. Gonzalez, J. F. and Venturi, V. (2013) A novel widespread interkingdom signaling circuit Trends Plant Sci. 18, 167-174
29. Wang, Y. J. and Leadbetter, J. R. (2005) Rapid acyl-homoserine lactone quorum signal biodegradation in diverse soils Appl. Environ. Microbiol. 71, 1291-1299
30. Jin, G., Liu, F., Ma, H., Hao, S., Zhao, Q., Bian, Z., Jia, Z., and Song, S. (2012) Two G-protein-coupled-receptor candidates, Cand2 and Cand7, are involved in Arabidopsis root growth mediated by the bacterial quorum-sensing signals N -acyl-homoserine lactones Biochem. Biophys. Res. Commun. 417, 991-995
31. Liu, F., Bian, Z., Jia, Z., Zhao, Q., and Song, S. (2012) The GCR1 and GPA1 participate in promotion of Arabidopsis primary root elongation induced by N -acyl-homoserine lactones, the bacterial quorum-sensing signals Mol. Plant-Microbe Interact. 25, 677-683
32. McKinney, M. K. and Cravatt, B. F. (2005) Structure and function of fatty acid amide hydrolase Annu. Rev. Biochem. 74, 411-432
33. Shrestha, R., Kim, S. C., Dyer, J. M., Dixon, R. A., and Chapman, K. D. (2006) Plant fatty acid (ethanol) amide hydrolases Biochim. Biophys. Acta 1761, 324-334
34. Williams, P. (2007) Quorum sensing, communication, and cross-kingdom signalling in the bacterial world Microbiol-Sgm 153, 3923-3938
35. Schaefer, A. L., Greenberg, E. P., Oliver, C. M., Oda, Y., Huang, J. J., Bittan-Banin, G., Peres, C. M., Schmidt, S., Juhaszova, K., Sufrin, J. R., and Harwood, C. S. (2008) A new class of homoserine lactone quorum-sensing signals Nature 454, 595-600
36. Glansdorp, F. G., Thomas, G. L., Lee, J. J. K., Dutton, J. M., Salmond, G. P. C., Welch, M., and Spring, D. R. (2004) Synthesis and stability of small molecule probes for Pseudomonas aeruginosa quorum sensing modulation Org. Biomol. Chem. 2, 3329-3336
37. Yang, F., Wang, L. H., Wang, J., Dong, Y. H., Hu, J. Y., and Zhang, L. H. (2005) Quorum quenching enzyme activity is widely conserved in the sera of mammalian species FEBS Lett. 579, 3713-3717
38. Sio, C. F., Otten, L. G., Cool, R. H., Diggle, S. P., Braun, P. G., Bos, R., Daykin, M., Camara, M., Williams, P., and Quax, W. J. (2006) Quorum quenching by an N -acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1 Infect. Immun. 74, 1673-1682
39. Palmer, A. G., Chen, M. C., Kinger, N. P., and Lynn, D. G. (2009) Parasitic angiosperms, semagenesis, and general strategies for plant-plant signaling in the rhizosphere Pest Manage. Sci. 65, 512-519
40. Dunand, C., Crevecoeur, M., and Penel, C. (2007) Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: Possible interaction with peroxidases New Phytol. 174, 332-341
41. Danhorn, T. and Fuqua, C. (2007) Biofilm formation by plant-associated bacteria Annu. Rev. Microbiol. 61, 401-422
42. Smith, R. M. and Hansen, D. E. (1998) The pH-rate profile for the hydrolysis of a peptide bond J. Am. Chem. Soc. 120, 8910-8913
43. Wang, Y. S., Shrestha, R., Kilaru, A., Wiant, W., Venables, B. J., Chapman, K. D., and Blancaflor, E. B. (2006) Manipulation of Arabidopsis fatty acid amide hydrolase expression modifies plant growth and sensitivity to N -acylethanolamines Proc. Natl. Acad. Sci. U.S.A. 103, 12197-12202
44. Shrestha, R., Dixon, R. A., and Chapman, K. D. (2003) Molecular identification of a functional homologue of the mammalian fatty acid amide hydrolase in Arabidopsis thaliana J. Biol. Chem. 278, 34990-34997
45. Sieper, T., Forczek, S., Matucha, M., Kramer, P., Hartmann, A., and Schroder, P. (2014) N -Acyl-homoserine lactone uptake and systemic transport in barley rest upon active parts of the plant New Phytol. 201, 545-555
46. Stein, S., Bohlen, P., Stone, J., Dairman, W., and Udenfriend, S. (1973) Amino acid analysis with fluorescamine at the picomole level Arch. Biochem. Biophys. 155, 202-212
47. Joseph, C. M. and Phillips, D. A. (2003) Metabolites from soil bacteria affect plant water relations Plant Physiol. Biochem. 41, 189-192
48. Iqbal, N., Nazar, R., Syeed, S., Masood, A., and Khan, N. A. (2011) Exogenously-sourced ethylene increases stomatal conductance, photosynthesis, and growth under optimal and deficient nitrogen fertilization in mustard J. Exp. Bot. 62, 4955-4963
49. Kuromori, T., Sugimoto, E., and Shinozaki, K. (2011) Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility Plant J. 67, 885-894
50. Tanaka, Y., Sano, T., Tamaoki, M., Nakajima, N., Kondo, N., and Hasezawa, S. (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis Plant Physiol. 138, 2337-2343
51. Stepanova, A. N., Yun, J., Likhacheva, A. V., and Alonso, J. M. (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots Plant Cell 19, 2169-2185
52. Alarcon, M. V., Lloret-Salamanca, A., Lloret, P. G., Iglesias, D. J., Talon, M., and Salguero, J. (2009) Effects of antagonists and inhibitors of ethylene biosynthesis on maize root elongation Plant Signal Behav. 4, 1154-1156
53. Penmetsa, R. V., Uribe, P., Anderson, J., Lichtenzveig, J., Gish, J. C., Nam, Y. W., Engstrom, E., Xu, K., Sckisel, G., Pereira, M., Baek, J. M., Lopez-Meyer, M., Long, S. R., Harrison, M. J., Singh, K. B., Kiss, G. B., and Cook, D. R. (2008) The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations Plant J. 55, 580-595
54. Chauvaux, N., VanDongen, W., Esmans, E. L., and VanOnckelen, H. A. (1997) Quantitative analysis of 1-aminocyclopropane-1-carboxylic acid by liquid chromatography coupled to electrospray tandem mass spectrometry J. Chromatogr. A 775, 143-150
55. Elasri, M., Delorme, S., Lemanceau, P., Stewart, G., Laue, B., Glickmann, E., Oger, P. M., and Dessaux, Y. (2001) Acyl-homoserine lactone production is more common among plant-associated Pseudomonas spp. than among soilborne Pseudomonas spp Appl. Environ. Microbiol. 67, 1198-1209
56. van Damme, M., Zeilmaker, T., Elberse, J., Andel, A., de Sain-van der Velden, M., and van den Ackerveken, G. (2009) Downy mildew resistance in Arabidopsis by mutation of homoserine kinase Plant Cell 21, 2179-2189
57. Song, S., Jia, Z., Xu, J., Zhang, Z., and Bian, Z. (2011) N -Butyryl-homoserine lactone, a bacterial quoum-sensing signaling molecule, induces intracellular calcium elevation in Arabidopsis root cells Biochem. Biophys. Res. Commun. 414, 355-360
58. Ma, W., Penrose, D. M., and Glick, B. R. (2002) Strategies used by rhizobia to lower plant ethylene levels and increase nodulation Can. J. Microbiol. 48, 947-954
59. Giang, D. K. and Cravatt, B. F. (1997) Molecular characterization of human and mouse fatty acid amide hydrolases Proc. Natl. Acad. Sci. U.S.A. 94, 2238-2242
60. Kai, K., Tani, A., and Hayashi, H. (2010) Facile preparation of deuterium-labeled N -acylhomoserine lactones as internal standards for isotope dilution mass spectrometry Bioorg. Med. Chem. 18, 3776-3782
61. Hodgkinson, J. T., Galloway, W. R. J. D., Casoli, M., Keane, H., Su, X. B., Salmond, G. P. C., Welch, M., and Spring, D. R. (2011) Robust routes for the synthesis of N -acylated- l -homoserine lactone (AHL) quorum sensing molecules with high levels of enantiomeric purity Tetrahedron Lett. 52, 3291-3294
62. Pomini, A. M. and Marsaioli, A. J. (2008) Absolute configuration and antimicrobial activity of acylhomoserine lactones J. Nat. Prod. 71, 1032-1036
63. Catoira, R., Galera, C., de Billy, F., Penmetsa, R. V., Journet, E. P., Maillet, F., Rosenberg, C., Cook, D., Gough, C., and Denarie, J. (2000) Four genes of Medicago truncatula controlling components of a nod factor transduction pathway Plant Cell 12, 1647-1665
64. 2+ environments Plant Cell 21, 4018-4030
65. Kim, S.-C., Kang, L., Nagaraj, S., Blancaflor, E. B., Mysore, K. S., and Chapman, K. D. (2009) Mutations in Arabidopsis fatty acid amide hydrolase reveal that catalytic activity influences growth but not sensitivity to abscisic acid or pathogens J. Biol. Chem. 284, 34065-34074
66. Kim, K. W., Franceschi, V. R., Davin, L. B., and Lewis, N. G. (2006) β-Glucuronidase as reporter gene: Advantages and limitations Methods Mol. Biol. 323, 263-273