Response of Arabidopsis thaliana to N-hexanoyl-dl-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere

Planta, Sep 2008

The bacterial quorum sensing signals N-acyl-l-homoserine lactones enable bacterial cells to regulate gene expression depending on population density, in order to undertake collective actions such as the infection of host cells. Only little is known about the molecular ways of plants reacting to these bacterial signals. In this study we show that the contact of Arabidopsis thaliana roots with N-hexanoyl-dl-homoserine-lactone (C6-HSL) resulted in distinct transcriptional changes in roots and shoots, respectively. Interestingly, unlike most other bacterial signals, C6-HSL influenced only a few defense-related transcripts. Instead, several genes associated with cell growth as well as genes regulated by growth hormones showed changes in their expression after C6-HSL treatment. C6-HSL did not induce plant systemic resistance against Pseudomonas syringae. The inoculation of roots with different types of AHLs led predominantly for short chain N-butyryl-dl-homoserine lactone and C6-HSL to root elongation. Determination of plant hormone concentrations in root and shoot tissues supported alterations of auxin to cytokinin ratio. Finally, we provide evidence that Arabidopsis takes up bacterial C6-HSL and allows systemic distribution throughout the plant. In sum, the bacterial quorum sensing signal C6-HSL does induce transcriptional changes in Arabidopsis and may contribute to tuning plant growth to the microbial composition of the rhizosphere.

Article PDF cannot be displayed. You can download it here:

https://link.springer.com/content/pdf/10.1007%2Fs00425-008-0811-4.pdf

Response of Arabidopsis thaliana to N-hexanoyl-dl-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere

Planta December 2008, Volume 229, Issue 1, pp 73–85 | Cite as Response of Arabidopsis thaliana to N-hexanoyl-dl-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere AuthorsAuthors and affiliations Uta von RadIlona KleinPetre I. DobrevJana KottovaEva ZazimalovaAgnes FeketeAnton HartmannPhilippe Schmitt-KopplinJörg Durner Original Article First Online: 03 September 2008 1 Shares 986 Downloads 84 Citations Abstract The bacterial quorum sensing signals N-acyl-l-homoserine lactones enable bacterial cells to regulate gene expression depending on population density, in order to undertake collective actions such as the infection of host cells. Only little is known about the molecular ways of plants reacting to these bacterial signals. In this study we show that the contact of Arabidopsis thaliana roots with N-hexanoyl-dl-homoserine-lactone (C6-HSL) resulted in distinct transcriptional changes in roots and shoots, respectively. Interestingly, unlike most other bacterial signals, C6-HSL influenced only a few defense-related transcripts. Instead, several genes associated with cell growth as well as genes regulated by growth hormones showed changes in their expression after C6-HSL treatment. C6-HSL did not induce plant systemic resistance against Pseudomonas syringae. The inoculation of roots with different types of AHLs led predominantly for short chain N-butyryl-dl-homoserine lactone and C6-HSL to root elongation. Determination of plant hormone concentrations in root and shoot tissues supported alterations of auxin to cytokinin ratio. Finally, we provide evidence that Arabidopsis takes up bacterial C6-HSL and allows systemic distribution throughout the plant. In sum, the bacterial quorum sensing signal C6-HSL does induce transcriptional changes in Arabidopsis and may contribute to tuning plant growth to the microbial composition of the rhizosphere. KeywordsQuorum sensing Plant defense Plant hormones Rhizosphere  Abbreviations AHL N-acyl-l-homoserine lactones ARR Arabidopsis response regulators C4-HSL N-butyryl-dl-HSL C6-HSL N-hexanoyl-dl-HSL C10-HSL N-decanoyl-dl-homoserine lactone IAA Indole-3-acetic acid 3-Oxo-C12-HSL N-3-oxo-dodecanoyl homoserine lactone PGPR Plant growth promoting rhizobacteria SA Salicylic acid U. von Rad and I. Klein contributed equally. Electronic supplementary material The online version of this article (doi: 10.1007/s00425-008-0811-4) contains supplementary material, which is available to authorized users. This is a preview of subscription content, log in to check access. Notes Acknowledgments This work was supported by Deutsche Forschungsgeeinschaft (IK, UvR, JD) and by the Ministry of Education of the Czech Republic, project LC06034 (PID, JK, EZ). The authors thank Elke Mattes for excellent technical assistance and J. Malbeck for accomplishment of MS analyses. Supplementary material 425_2008_811_MOESM1_ESM.pdf (14 kb) Total number of differentially transcribed genes (PDF 13 kb) 425_2008_811_MOESM2_ESM.pdf (73 kb) Genes implicated in plant hormone response by HHL treatment (PDF 73 kb) 425_2008_811_MOESM3_ESM.pdf (81 kb) Frequently occurring gene families in leaf tissue (PDF 80 kb) 425_2008_811_MOESM4_ESM.pdf (86 kb) Frequently occurring gene families in root tissue (PDF 85 kb) 425_2008_811_MOESM5_ESM.pdf (167 kb) Regulated genes after HHL treatment in leaf tissue (PDF 166 kb) 425_2008_811_MOESM6_ESM.pdf (211 kb) Regulated genes after HHL treatment in root tissue (PDF 211 kb) References Battke F, Schramel P, Ernst D (2003) A novel method for in vitro culture of plants: cultivation of barley in a floating hydroponic system. Plant Mol Biol Rep 21:405–409CrossRefGoogle Scholar Bauer WD, Mathesius U (2004) Plant responses to bacterial quorum sensing signals. Curr Opin Plant Biol 7:429–433PubMedCrossRefGoogle Scholar Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602PubMedCrossRefGoogle Scholar Charlton TS, de Nys R, Netting A, Kumar N, Hentzer M, Givskov M, Kjelleberg S (2000) A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. Environ Microbiol 2:530–541PubMedCrossRefGoogle Scholar Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159PubMedCrossRefGoogle Scholar Cleveland WS (1981) Lowess—a program for smoothing scatterplots by robust locally weighted regression. Am Stat 35:54–62CrossRefGoogle Scholar Cosgrove DJ, Li LC, Cho HT, Hoffmann-Benning S, Moore RC, Blecker D (2002) The growing world of expansins. Plant Cell Physiol 43:1436–1444PubMedCrossRefGoogle Scholar D’Agostino IB, Deruere J, Kieber JJ (2000) Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol 124:1706–1717PubMedCrossRefGoogle Scholar Degrassi G, Devescovi G, Solis R, Steindler L, Venturi V (2007) Oryza sativa rice plants contain molecules that activate different quorum-sensing N-acyl homoserine lactone biosensors and are sensitive to the specific AiiA lactonase. FEMS Microbiol Lett 269:213–220PubMedCrossRefGoogle Scholar Dobrev PI, Havlicek L, Vagner M, Malbeck J, Kaminek M (2005) Purification and determination of plant hormones auxin and abscisic acid using solid phase extraction and two-dimensional high performance liquid chromatography. J Chromatogr A 1075:159–166PubMedCrossRefGoogle Scholar Dobrev PI, Kaminek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A 950:21–29PubMedCrossRefGoogle Scholar Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Curr Opin Plant Biol 8:518–525PubMedCrossRefGoogle Scholar Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439–468PubMedCrossRefGoogle Scholar Gao M, Teplitski M, Robinson JB, Bauer WD (2003) Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol Plant Microbe Interact 16:827–834PubMedCrossRefGoogle Scholar Gotz C, Fekete A, Gebefuegi I, Forczek ST, Fuksova K, Li X, Englmann M, Gryndler M, Hartmann A, Matucha M, Schmitt-Kopplin P, Schroder P (2007) Uptake, degradation and chiral discrimination of N-acyl-d:/l: -homoserine lactones by barley (Hordeum vulgare) and yam bean (Pachyrhizus erosus) plants. Anal Bioanal Chem 389:1447–1457PubMedCrossRefGoogle Scholar Hense BA, Kuttler C, Müller J, Rothballer M, Hartmann A, Kreft JU (2007) Does efficiency sensing unify diffusion and quorum sensing? Nat Rev Microbiol 5:230–239PubMedCrossRefGoogle Scholar Joseph C, Philli (...truncated)


This is a preview of a remote PDF: https://link.springer.com/content/pdf/10.1007%2Fs00425-008-0811-4.pdf
Article home page: http://link.springer.com/article/10.1007/s00425-008-0811-4

Uta von Rad, Ilona Klein, Petre I. Dobrev, Jana Kottova, Eva Zazimalova, Agnes Fekete, Anton Hartmann, Philippe Schmitt-Kopplin, Jörg Durner. Response of Arabidopsis thaliana to N-hexanoyl-dl-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere, Planta, 2008, pp. 73-85, Volume 229, Issue 1, DOI: 10.1007/s00425-008-0811-4