Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants
Edited by Luis Herrera Estrella, Center for Research and Advanced Studies, Irapuato, Mexico, and approved March 17, 2011 (received for review May 13, 2010)
Abstract
Microorganisms and their hosts communicate with each other through an array of signals. The plant hormone auxin (indole-3-acetic acid; IAA) is central in many aspects of plant development. Cyclodipeptides and their derivative diketopiperazines (DKPs) constitute a large class of small molecules synthesized by microorganisms with diverse and noteworthy activities. Here, we present genetic, chemical, and plant-growth data showing that in Pseudomonas aeruginosa, the LasI quorum-sensing (QS) system controls the production of three DKPs—namely, cyclo(l-Pro-l-Val), cyclo(l-Pro-l-Phe), and cyclo(l-Pro-l-Tyr)—that are involved in plant growth promotion by this bacterium. Analysis of all three bacterial DKPs in Arabidopsis thaliana seedlings provided detailed information indicative of an auxin-like activity, based on their efficacy at modulating root architecture, activation of auxin-regulated gene expression, and response of auxin-signaling mutants tir1, tir1 afb2 afb3, arf7, arf19, and arf7arf19. The observation that QS-regulated bacterial production of DKPs modulates auxin signaling and plant growth promotion establishes an important function for DKPs mediating prokaryote/eukaryote transkingdom signaling.
Acknowledgments
We thank Drs. Peter Doerner, Christian Luschnig, Athanasios Theologis, Tom Guilfoyle, and Mark A. Estelle for kindly providing seeds of transgenic and mutant lines. Dr. Barbara Iglewski is acknowledged for her kind donation of WT P. aeruginosa and mutant strains. This work was supported by Consejo Nacional de Ciencia y Tecnología Grants 80916 and 106567, and the Consejo de la Investigación Científica 2.26 and 2.14.
Supporting Information
Supporting Information (PDF)
Supporting Information
- Download
- 1.71 MB
References
1
C Fuqua, SC Winans, EP Greenberg, Census and consensus in bacterial ecosystems: The LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu Rev Microbiol 50, 727–751 (1996).
2
G Telford, et al., The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-l-homoserine lactone has immunomodulatory activity. Infect Immun 66, 36–42 (1998).
3
U Mathesius, et al., Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100, 1444–1449 (2003).
4
V Sperandio, AG Torres, B Jarvis, JP Nataro, JB Kaper, Bacteria-host communication: The language of hormones. Proc Natl Acad Sci USA 100, 8951–8956 (2003).
5
MM Gao, M Teplitski, JB Robinson, WD Bauer, Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol Plant Microbe Interact 16, 827–834 (2003).
6
JP Pearson, et al., Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc Natl Acad Sci USA 91, 197–201 (1994).
7
JP Pearson, L Passador, BH Iglewski, EP Greenberg, A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92, 1490–1494 (1995).
8
MB Hussain, et al., The acyl-homoserine lactone-type quorum-sensing system modulates cell motility and virulence of Erwinia chrysanthemi pv. zeae. J Bacteriol 190, 1045–1053 (2008).
9
V Rosemeyer, J Michiels, C Verreth, J Vanderleyden, luxI- and luxR-homologous genes of Rhizobium etli CNPAF512 contribute to synthesis of autoinducer molecules and nodulation of Phaseolus vulgaris. J Bacteriol 180, 815–821 (1998).
10
U von Rad, et al., Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta 229, 73–85 (2008).
11
R Ortíz-Castro, M Martínez-Trujillo, J López-Bucio, 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 (2008).
12
S Spaepen, J Vanderleyden, R Remans, Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31, 425–448 (2007).
13
AW Woodward, B Bartel, Auxin: Regulation, action, and interaction. Ann Bot (Lond) 95, 707–735 (2005).
14
K Ström, J Sjögren, A Broberg, J Schnürer, Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo(l-Phe-l-Pro) and cyclo(l-Phe-trans-4-OH-l-Pro) and 3-phenyllactic acid. Appl Environ Microbiol 68, 4322–4327 (2002).
15
K Kanoh, et al., Antitumor activity of phenylahistin in vitro and in vivo. Biosci Biotechnol Biochem 63, 1130–1133 (1999).
16
DE Williams, et al., Ambewelamides A and B, antineoplastic epidithiopiperazinediones isolated from the lichen Usnea sp. Tetrahedron Lett 39, 9579–9582 (1998).
17
M Gondry, et al., Cyclodipeptide synthases are a family of tRNA-dependent peptide bond-forming enzymes. Nat Chem Biol 5, 414–420 (2009).
18
EC Pesci, JP Pearson, PC Seed, BH Iglewski, Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179, 3127–3132 (1997).
19
LI Calderón-Villalobos, X Tan, N Zheng, M Estelle, Auxin perception—structural insights. Cold Spring Harb Perspect Biol 2, a005546 (2010).
20
T Ulmasov, J Murfett, G Hagen, TJ Guilfoyle, Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9, 1963–1971 (1997).
21
Y Oono, QG Chen, PJ Overvoorde, C Köhler, A Theologis, age Mutants of Arabidopsis exhibit altered auxin-regulated gene expression. Plant Cell 10, 1649–1662 (1998).
22
N Dharmasiri, S Dharmasiri, M Estelle, The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445 (2005).
23
S Kepinski, O Leyser, The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451 (2005).
24
WM Gray, S Kepinski, D Rouse, O Leyser, M Estelle, Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414, 271–276 (2001).
25
LG Rahme, et al., Common virulence factors for bacterial pathogenicity in plants and animals. Science 268, 1899–1902 (1995).
26
JM Plotnikova, LG Rahme, FM Ausubel, Pathogenesis of the human opportunistic pathogen Pseudomonas aeruginosa PA14 in Arabidopsis. Plant Physiol 124, 1766–1774 (2000).
27
TS Walker, et al., Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol 134, 320–331 (2004).
28
GM Preston, Plant perceptions of plant growth-promoting Pseudomonas. Philos Trans R Soc Lond B Biol Sci 359, 907–918 (2004).
29
A Colón-Carmona, R You, T Haimovitch-Gal, P Doerner, Technical advance: Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20, 503–508 (1999).
30
T Sieberer, MT Hauser, GJ Seifert, C Luschnig, PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr Biol 13, 837–842 (2003).
31
C Boisnard-Lorig, et al., Dynamic analyses of the expression of the HISTONE:YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains. Plant Cell 13, 495–509 (2001).
32
MTG Holden, et al., Quorum-sensing cross talk: Isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol Microbiol 33, 1254–1266 (1999).
33
X Tan, et al., Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640–645 (2007).
34
N Dharmasiri, S Dharmasiri, AM Jones, M Estelle, Auxin action in a cell-free system. Curr Biol 13, 1418–1422 (2003).
35
G Degrassi, et al., Plant growth-promoting Pseudomonas putida WCS358 produces and secretes four cyclic dipeptides: Cross-talk with quorum sensing bacterial sensors. Curr Microbiol 45, 250–254 (2002).
36
N Dharmasiri, et al., Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9, 109–119 (2005).
37
Y Okushima, H Fukaki, M Onoda, A Theologis, M Tasaka, ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19, 118–130 (2007).
38
LL Li, JE Malone, BH Iglewski, Regulation of the Pseudomonas aeruginosa quorum-sensing regulator VqsR. J Bacteriol 189, 4367–4374 (2007).
39
H Zhang, A Jennings, PW Barlow, BG Forde, Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96, 6529–6534 (1999).
Information & Authors
Information
Published in
Classifications
Submission history
Published online: April 11, 2011
Published in issue: April 26, 2011
Keywords
Acknowledgments
We thank Drs. Peter Doerner, Christian Luschnig, Athanasios Theologis, Tom Guilfoyle, and Mark A. Estelle for kindly providing seeds of transgenic and mutant lines. Dr. Barbara Iglewski is acknowledged for her kind donation of WT P. aeruginosa and mutant strains. This work was supported by Consejo Nacional de Ciencia y Tecnología Grants 80916 and 106567, and the Consejo de la Investigación Científica 2.26 and 2.14.
Notes
*This Direct Submission article had a prearranged editor.
Authors
Competing Interests
The authors declare no conflict of interest.
Metrics & Citations
Metrics
Altmetrics
Citations
Cite this article
Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants, Proc. Natl. Acad. Sci. U.S.A.
108 (17) 7253-7258,
https://doi.org/10.1073/pnas.1006740108
(2011).
Copied!
Copying failed.
Export the article citation data by selecting a format from the list below and clicking Export.
Cited by
Loading...
View Options
View options
PDF format
Download this article as a PDF file
DOWNLOAD PDFLogin options
Check if you have access through your login credentials or your institution to get full access on this article.
Personal login Institutional LoginRecommend to a librarian
Recommend PNAS to a LibrarianPurchase options
Purchase this article to access the full text.