Home LiteratureArticle Details
PMID: 10811621 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A bacterial sensor of plant cell contact controls the transcriptional induction of Ralstonia solanacearum pathogenicity genes.

The EMBO journal ·Vol. 19 ·No. 10 ·2000-05-15 ·Pages 2304-14

Aldon D, Brito B, Boucher C, Genin S

Abstract

The hrp genes of the plant pathogen Ralstonia solanacearum are key pathogenicity determinants; they encode a type III protein secretion machinery involved in the secretion of mediators of the bacterium-plant interaction. These hrp genes are under the genetic control of the hrpB regulatory gene, expression of which is induced when bacteria are co-cultivated with plant cell suspensions. In this study, we used hrp-gfp transcriptional fusions to demonstrate that the expression of the hrpB and type III secretion genes is specifically induced in response to the bacterium-plant cell contact. This contact-dependent induction of hrpB gene expression requires the outer membrane protein PrhA, but not a functional type III secretion apparatus. Genetic evidence indicates that PrhA constitutes the first example of a bacterial receptor for a non-diffusible signal present in the plant cell wall and which triggers the transcriptional activation of bacterial virulence genes.

MeSH Terms
Arabidopsis/genetics,microbiology Arabidopsis Proteins Bacterial Proteins/genetics Betaproteobacteria/pathogenicity,physiology DNA-Binding Proteins Gene Expression Regulation, Bacterial Homeodomain Proteins/genetics Plant Proteins/genetics Repressor Proteins/genetics Transcription Factors Transcription, Genetic
Chemicals
Arabidopsis Proteins Bacterial Proteins DNA-Binding Proteins Homeodomain Proteins PRHA protein, Arabidopsis Plant Proteins Repressor Proteins Transcription Factors hrpB protein, Ralstonia solanacearum
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Aldon D
Laboratoire de Biologie Moléculaire des Relations Plantes-Microorganismes, INRA-CNRS, BP27, 31326 Castanet-Tolosan Cedex, France.
Brito B
Boucher C
Genin S
References (46)
46 references, click to expand
  1. The Yersinia deadly kiss.
    J Bacteriol. 1998 Nov;180(21):5495-504 PMID: 9791096
  2. Analysis of Sweet cherry (Prunus avium L.) Leaves for Plant Signal Molecules That Activate the syrB Gene Required for Synthesis of the Phytotoxin, Syringomycin, by Pseudomonas syringae pv syringae.
    Plant Physiol. 1995 Feb;107(2):603-612 PMID: 12228385
  3. Induction of gene expression in Escherichia coli after pilus-mediated adherence.
    Science. 1996 Aug 30;273(5279):1234-6 PMID: 8703059
  4. Contact with cultured epithelial cells stimulates secretion of Salmonella typhimurium invasion protein InvJ.
    Infect Immun. 1995 Oct;63(10):4024-8 PMID: 7558314
  5. Pseudomonas syringae pv. syringae harpinPss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants.
    Cell. 1993 Jul 2;73(7):1255-66 PMID: 8324821
  6. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes.
    Science. 1986 Aug 29;233(4767):977-80 PMID: 3738520
  7. A pathogenic bacterium triggers epithelial signals to form a functional bacterial receptor that mediates actin pseudopod formation.
    EMBO J. 1996 Jun 3;15(11):2613-24 PMID: 8654358
  8. Ralstonia solanacearum produces hrp-dependent pili that are required for PopA secretion but not for attachment of bacteria to plant cells.
    Mol Microbiol. 2000 Apr;36(2):249-60 PMID: 10792714
  9. Characterization of the Pseudomonas syringae pv. tomato AvrRpt2 protein: demonstration of secretion and processing during bacterial pathogenesis.
    Mol Microbiol. 1999 Jun;32(5):927-41 PMID: 10361296
  10. Type III secretion machines: bacterial devices for protein delivery into host cells.
    Science. 1999 May 21;284(5418):1322-8 PMID: 10334981
  11. Induction of type III secretion in Shigella flexneri is associated with differential control of transcription of genes encoding secreted proteins.
    EMBO J. 1998 May 15;17(10):2894-903 PMID: 9582283
  12. The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes.
    J Cell Biol. 1999 Nov 1;147(3):683-93 PMID: 10545510
  13. Requirement for exported proteins in secretion through the invasion-associated type III system of Salmonella typhimurium.
    Infect Immun. 1996 Sep;64(9):3524-31 PMID: 8751894
  14. Green fluorescent protein-based reporter systems for genetic analysis of bacteria including monocopy applications.
    Gene. 1997 Sep 1;196(1-2):69-74 PMID: 9322742
  15. Type III secretion by Salmonella typhimurium does not require contact with a eukaryotic host.
    Mol Microbiol. 1999 Jan;31(1):45-51 PMID: 9987108
  16. A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica.
    Science. 1997 Nov 7;278(5340):1140-3 PMID: 9353199
  17. Type III machines of pathogenic yersiniae secrete virulence factors into the extracellular milieu.
    Mol Microbiol. 1999 Mar;31(6):1619-29 PMID: 10209737
  18. Signal transfer through three compartments: transcription initiation of the Escherichia coli ferric citrate transport system from the cell surface.
    EMBO J. 1995 Apr 3;14(7):1430-8 PMID: 7729419
  19. Type III protein secretion systems in bacterial pathogens of animals and plants.
    Microbiol Mol Biol Rev. 1998 Jun;62(2):379-433 PMID: 9618447
  20. Evidence that the hrpB gene encodes a positive regulator of pathogenicity genes from Pseudomonas solanacearum.
    Mol Microbiol. 1992 Oct;6(20):3065-76 PMID: 1479894
  21. prhJ and hrpG, two new components of the plant signal-dependent regulatory cascade controlled by PrhA in Ralstonia solanacearum.
    Mol Microbiol. 1999 Jan;31(1):237-51 PMID: 9987125
  22. The Pseudomonas syringae pv. tomato HrpW protein has domains similar to harpins and pectate lyases and can elicit the plant hypersensitive response and bind to pectate.
    J Bacteriol. 1998 Oct;180(19):5211-7 PMID: 9748456
  23. HrpW of Erwinia amylovora, a new harpin that contains a domain homologous to pectate lyases of a distinct class.
    J Bacteriol. 1998 Oct;180(19):5203-10 PMID: 9748455
  24. Pilus-mediated adhesion of Neisseria meningitidis: the essential role of cell contact-dependent transcriptional upregulation of the PilC1 protein.
    Mol Microbiol. 1998 Jun;28(6):1153-63 PMID: 9680205
  25. Contact of Shigella with host cells triggers release of Ipa invasins and is an essential function of invasiveness.
    EMBO J. 1995 Jun 1;14(11):2461-70 PMID: 7781600
  26. The Xanthomonas Hrp type III system secretes proteins from plant and mammalian bacterial pathogens.
    Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9368-73 PMID: 10430949
  27. Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria.
    Trends Microbiol. 1993 Aug;1(5):175-80 PMID: 8143135
  28. PopA1, a protein which induces a hypersensitivity-like response on specific Petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum.
    EMBO J. 1994 Feb 1;13(3):543-53 PMID: 8313899
  29. Role for the outer membrane ferric siderophore receptor PupB in signal transduction across the bacterial cell envelope.
    EMBO J. 1994 Jun 15;13(12):2805-13 PMID: 8026465
  30. PrhA controls a novel regulatory pathway required for the specific induction of Ralstonia solanacearum hrp genes in the presence of plant cells.
    Mol Microbiol. 1998 Jan;27(2):437-53 PMID: 9484898
  31. Erwinia amylovora secretes DspE, a pathogenicity factor and functional AvrE homolog, through the Hrp (type III secretion) pathway.
    J Bacteriol. 1998 Apr;180(8):2244-7 PMID: 9555912
  32. Plant cell wall architecture.
    Cell. 1989 Jan 27;56(2):231-9 PMID: 2643477
  33. DspA, an essential pathogenicity factor of Erwinia amylovora showing homology with AvrE of Pseudomonas syringae, is secreted via the Hrp secretion pathway in a DspB-dependent way.
    Mol Microbiol. 1997 Dec;26(5):1057-69 PMID: 9426142
  34. Two novel proteins, PopB, which has functional nuclear localization signals, and PopC, which has a large leucine-rich repeat domain, are secreted through the hrp-secretion apparatus of Ralstonia solanacearum.
    Mol Microbiol. 2000 Apr;36(2):261-77 PMID: 10792715
  35. Modulation of virulence factor expression by pathogen target cell contact.
    Science. 1996 Aug 30;273(5279):1231-3 PMID: 8703058
  36. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora.
    Science. 1992 Jul 3;257(5066):85-8 PMID: 1621099
  37. In vitro and in vivo expression studies of yopE from Yersinia enterocolitica using the gfp reporter gene.
    Mol Microbiol. 1998 Nov;30(4):865-82 PMID: 10094634
  38. Isolation and analysis of cell walls from plant material.
    Methods Biochem Anal. 1987;32:25-153 PMID: 3574138
  39. The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD.
    EMBO J. 1994 Nov 15;13(22):5293-302 PMID: 7957095
  40. The Avr (effector) proteins HrmA (HopPsyA) and AvrPto are secreted in culture from Pseudomonas syringae pathovars via the Hrp (type III) protein secretion system in a temperature- and pH-sensitive manner.
    J Bacteriol. 1999 Aug;181(16):4790-7 PMID: 10438746
  41. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells.
    EMBO J. 1994 Feb 15;13(4):964-72 PMID: 8112310
  42. Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity.
    Science. 1989 Sep 22;245(4924):1374-7 PMID: 2781284
  43. hrp genes of Pseudomonas solanacearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria.
    Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):384-9 PMID: 1472716
  44. The TonB-dependent ferrichrome receptor FcuA of Yersinia enterocolitica: evidence against a strict co-evolution of receptor structure and substrate specificity.
    Mol Microbiol. 1993 Feb;7(3):383-93 PMID: 8384682
  45. Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000.
    Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3459-64 PMID: 9096416
  46. The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex.
    Mol Microbiol. 1995 Mar;15(6):1095-114 PMID: 7623665
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2000-05-15
Pages
2304-14
Language
English
Region
England
NLM ID
8208664
PMCID
PMC384368
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]