• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jbacterPermissionsJournals.ASM.orgJournalJB ArticleJournal InfoAuthorsReviewers
J Bacteriol. Sep 1997; 179(18): 5655–5662.
PMCID: PMC179450

The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death.

Full Text

The Full Text of this article is available as a PDF (230K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Alfano JR, Bauer DW, Milos TM, Collmer A. Analysis of the role of the Pseudomonas syringae pv. syringae HrpZ harpin in elicitation of the hypersensitive response in tobacco using functionally non-polar hrpZ deletion mutations, truncated HrpZ fragments, and hrmA mutations. Mol Microbiol. 1996 Feb;19(4):715–728. [PubMed]
  • Alfano JR, Collmer A. Bacterial Pathogens in Plants: Life up against the Wall. Plant Cell. 1996 Oct;8(10):1683–1698. [PMC free article] [PubMed]
  • Alfano JR, Klm HS, Delaney TP, Collmer A. Evidence that the Pseudomonas syringae pv. syringae hrp-linked hrmA gene encodes an Avr-like protein that acts in an hrp-dependent manner within tobacco cells. Mol Plant Microbe Interact. 1997 Jul;10(5):580–588. [PubMed]
  • Arlat M, Van Gijsegem F, Huet JC, Pernollet JC, Boucher CA. 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):543–553. [PMC free article] [PubMed]
  • Bauer DW, Bogdanove AJ, Beer SV, Collmer A. Erwinia chrysanthemi hrp genes and their involvement in soft rot pathogenesis and elicitation of the hypersensitive response. Mol Plant Microbe Interact. 1994 Sep-Oct;7(5):573–581. [PubMed]
  • Bauer DW, Wei ZM, Beer SV, Collmer A. Erwinia chrysanthemi harpinEch: an elicitor of the hypersensitive response that contributes to soft-rot pathogenesis. Mol Plant Microbe Interact. 1995 Jul-Aug;8(4):484–491. [PubMed]
  • Bogdanove AJ, Beer SV, Bonas U, Boucher CA, Collmer A, Coplin DL, Cornelis GR, Huang HC, Hutcheson SW, Panopoulos NJ, et al. Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria. Mol Microbiol. 1996 May;20(3):681–683. [PubMed]
  • Bogdanove AJ, Wei ZM, Zhao L, Beer SV. Erwinia amylovora secretes harpin via a type III pathway and contains a homolog of yopN of Yersinia spp. J Bacteriol. 1996 Mar;178(6):1720–1730. [PMC free article] [PubMed]
  • Bonas U. hrp genes of phytopathogenic bacteria. Curr Top Microbiol Immunol. 1994;192:79–98. [PubMed]
  • Carpenter PB, Ordal GW. Bacillus subtilis FlhA: a flagellar protein related to a new family of signal-transducing receptors. Mol Microbiol. 1993 Mar;7(5):735–743. [PubMed]
  • Charkowski AO, Huang HC, Collmer A. Altered localization of HrpZ in Pseudomonas syringae pv. syringae hrp mutants suggests that different components of the type III secretion pathway control protein translocation across the inner and outer membranes of gram-negative bacteria. J Bacteriol. 1997 Jun;179(12):3866–3874. [PMC free article] [PubMed]
  • Chen Y, Smith MR, Thirumalai K, Zychlinsky A. A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J. 1996 Aug 1;15(15):3853–3860. [PMC free article] [PubMed]
  • Collazo CM, Galán JE. The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol Microbiol. 1997 May;24(4):747–756. [PubMed]
  • Cornelis GR, Wolf-Watz H. The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol. 1997 Mar;23(5):861–867. [PubMed]
  • Cui Y, Madi L, Mukherjee A, Dumenyo CK, Chatterjee AK. The RsmA- mutants of Erwinia carotovora subsp. carotovora strain Ecc71 overexpress hrpNEcc and elicit a hypersensitive reaction-like response in tobacco leaves. Mol Plant Microbe Interact. 1996 Sep;9(7):565–573. [PubMed]
  • Dangl JL. The enigmatic avirulence genes of phytopathogenic bacteria. Curr Top Microbiol Immunol. 1994;192:99–118. [PubMed]
  • Dangl JL, Dietrich RA, Richberg MH. Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. Plant Cell. 1996 Oct;8(10):1793–1807. [PMC free article] [PubMed]
  • Fenselau S, Balbo I, Bonas U. Determinants of pathogenicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in secretion in bacterial pathogens of animals. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):390–396. [PubMed]
  • Frederick RD, Majerczak DR, Coplin DL. Erwinia stewartii WtsA, a positive regulator of pathogenicity gene expression, is similar to Pseudomonas syringae pv. phaseolicola HrpS. Mol Microbiol. 1993 Aug;9(3):477–485. [PubMed]
  • Fullner KJ, Lara JC, Nester EW. Pilus assembly by Agrobacterium T-DNA transfer genes. Science. 1996 Aug 23;273(5278):1107–1109. [PubMed]
  • Galán JE. Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol. 1996 Apr;20(2):263–271. [PubMed]
  • Genin S, Boucher CA. A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Mol Gen Genet. 1994 Apr;243(1):112–118. [PubMed]
  • Genin S, Gough CL, Zischek C, Boucher CA. Evidence that the hrpB gene encodes a positive regulator of pathogenicity genes from Pseudomonas solanacearum. Mol Microbiol. 1992 Oct;6(20):3065–3076. [PubMed]
  • Gopalan S, Bauer DW, Alfano JR, Loniello AO, He SY, Collmer A. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell. 1996 Jul;8(7):1095–1105. [PMC free article] [PubMed]
  • Gough CL, Genin S, Zischek C, Boucher CA. 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):384–389. [PubMed]
  • He SY, Huang HC, Collmer A. 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):1255–1266. [PubMed]
  • Heu S, Hutcheson SW. Nucleotide sequence and properties of the hrmA locus associated with the Pseudomonas syringae pv. syringae 61 hrp gene cluster. Mol Plant Microbe Interact. 1993 Sep-Oct;6(5):553–564. [PubMed]
  • Huang HC, He SY, Bauer DW, Collmer A. The Pseudomonas syringae pv. syringae 61 hrpH product, an envelope protein required for elicitation of the hypersensitive response in plants. J Bacteriol. 1992 Nov;174(21):6878–6885. [PMC free article] [PubMed]
  • Huang HC, Lin RH, Chang CJ, Collmer A, Deng WL. The complete hrp gene cluster of Pseudomonas syringae pv. syringae 61 includes two blocks of genes required for harpinPss secretion that are arranged colinearly with Yersinia ysc homologs. Mol Plant Microbe Interact. 1995 Sep-Oct;8(5):733–746. [PubMed]
  • Huang HC, Schuurink R, Denny TP, Atkinson MM, Baker CJ, Yucel I, Hutcheson SW, Collmer A. Molecular cloning of a Pseudomonas syringae pv. syringae gene cluster that enables Pseudomonas fluorescens to elicit the hypersensitive response in tobacco plants. J Bacteriol. 1988 Oct;170(10):4748–4756. [PMC free article] [PubMed]
  • Huguet E, Bonas U. hrpf of Xanthomonas campestris pv. vesicatoria encodes an 87-kDa protein with homology to NoIX of Rhizobium fredii. Mol Plant Microbe Interact. 1997 May;10(4):488–498. [PubMed]
  • Keen NT. Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet. 1990;24:447–463. [PubMed]
  • Kim JF, Wei ZM, Beer SV. The hrpA and hrpC operons of Erwinia amylovora encode components of a type III pathway that secretes harpin. J Bacteriol. 1997 Mar;179(5):1690–1697. [PMC free article] [PubMed]
  • Kobayashi DY, Tamaki SJ, Keen NT. Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc Natl Acad Sci U S A. 1989 Jan;86(1):157–161. [PMC free article] [PubMed]
  • Leach JE, White FF. Bacterial avirulence genes. Annu Rev Phytopathol. 1996;34:153–179. [PubMed]
  • Leister RT, Ausubel FM, Katagiri F. Molecular recognition of pathogen attack occurs inside of plant cells in plant disease resistance specified by the Arabidopsis genes RPS2 and RPM1. Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15497–15502. [PMC free article] [PubMed]
  • Li J, Ochman H, Groisman EA, Boyd EF, Solomon F, Nelson K, Selander RK. Relationship between evolutionary rate and cellular location among the Inv/Spa invasion proteins of Salmonella enterica. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7252–7256. [PMC free article] [PubMed]
  • Lindgren PB, Peet RC, Panopoulos NJ. Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants. J Bacteriol. 1986 Nov;168(2):512–522. [PMC free article] [PubMed]
  • Lonetto MA, Brown KL, Rudd KE, Buttner MJ. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7573–7577. [PMC free article] [PubMed]
  • Lorang JM, Keen NT. Characterization of avrE from Pseudomonas syringae pv. tomato: a hrp-linked avirulence locus consisting of at least two transcriptional units. Mol Plant Microbe Interact. 1995 Jan-Feb;8(1):49–57. [PubMed]
  • Mansfield J, Jenner C, Hockenhull R, Bennett MA, Stewart R. Characterization of avrPphE, a gene for cultivar-specific avirulence from Pseudomonas syringae pv. phaseolicola which is physically linked to hrpY, a new hrp gene identified in the halo-blight bacterium. Mol Plant Microbe Interact. 1994 Nov-Dec;7(6):726–739. [PubMed]
  • Niepold F, Anderson D, Mills D. Cloning determinants of pathogenesis from Pseudomonas syringae pathovar syringae. Proc Natl Acad Sci U S A. 1985 Jan;82(2):406–410. [PMC free article] [PubMed]
  • Oku T, Alvarez AM, Kado CI. Conservation of the hypersensitivity-pathogenicity regulatory gene hrpX of Xanthomonas campestris and X. oryzae. DNA Seq. 1995;5(4):245–249. [PubMed]
  • Pirhonen MU, Lidell MC, Rowley DL, Lee SW, Jin S, Liang Y, Silverstone S, Keen NT, Hutcheson SW. Phenotypic expression of Pseudomonas syringae avr genes in E. coli is linked to the activities of the hrp-encoded secretion system. Mol Plant Microbe Interact. 1996 May;9(4):252–260. [PubMed]
  • Plano GV, Barve SS, Straley SC. LcrD, a membrane-bound regulator of the Yersinia pestis low-calcium response. J Bacteriol. 1991 Nov;173(22):7293–7303. [PMC free article] [PubMed]
  • Preston G, Huang HC, He SY, Collmer A. The HrpZ proteins of Pseudomonas syringae pvs. syringae, glycinea, and tomato are encoded by an operon containing Yersinia ysc homologs and elicit the hypersensitive response in tomato but not soybean. Mol Plant Microbe Interact. 1995 Sep-Oct;8(5):717–732. [PubMed]
  • Roine E, Wei W, Yuan J, Nurmiaho-Lassila EL, Kalkkinen N, Romantschuk M, He SY. 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):3459–3464. [PMC free article] [PubMed]
  • Rosqvist R, Magnusson KE, Wolf-Watz H. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 1994 Feb 15;13(4):964–972. [PMC free article] [PubMed]
  • Russel M. Moving through the membrane with filamentous phages. Trends Microbiol. 1995 Jun;3(6):223–228. [PubMed]
  • Salmeron JM, Staskawicz BJ. Molecular characterization and hrp dependence of the avirulence gene avrPto from Pseudomonas syringae pv. tomato [corrected]. Mol Gen Genet. 1993 May;239(1-2):6–16. [PubMed]
  • Salmond GP, Reeves PJ. Membrane traffic wardens and protein secretion in gram-negative bacteria. Trends Biochem Sci. 1993 Jan;18(1):7–12. [PubMed]
  • Scofield SR, Tobias CM, Rathjen JP, Chang JH, Lavelle DT, Michelmore RW, Staskawicz BJ. Molecular Basis of Gene-for-Gene Specificity in Bacterial Speck Disease of Tomato. Science. 1996 Dec 20;274(5295):2063–2065. [PubMed]
  • Sory MP, Cornelis GR. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol. 1994 Nov;14(3):583–594. [PubMed]
  • Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JD. Molecular genetics of plant disease resistance. Science. 1995 May 5;268(5211):661–667. [PubMed]
  • Staskawicz BJ, Dahlbeck D, Keen NT. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6024–6028. [PMC free article] [PubMed]
  • Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, Martin GB. Initiation of Plant Disease Resistance by Physical Interaction of AvrPto and Pto Kinase. Science. 1996 Dec 20;274(5295):2060–2063. [PubMed]
  • Van den Ackerveken G, Marois E, Bonas U. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell. 1996 Dec 27;87(7):1307–1316. [PubMed]
  • Van Gijsegem F, Genin S, Boucher C. Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria. Trends Microbiol. 1993 Aug;1(5):175–180. [PubMed]
  • Van Gijsegem F, Gough C, Zischek C, Niqueux E, Arlat M, Genin S, Barberis P, German S, Castello P, Boucher C. 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):1095–1114. [PubMed]
  • Wattiau P, Woestyn S, Cornelis GR. Customized secretion chaperones in pathogenic bacteria. Mol Microbiol. 1996 Apr;20(2):255–262. [PubMed]
  • Wei ZM, Beer SV. HrpI of Erwinia amylovora functions in secretion of harpin and is a member of a new protein family. J Bacteriol. 1993 Dec;175(24):7958–7967. [PMC free article] [PubMed]
  • Wei ZM, Beer SV. hrpL activates Erwinia amylovora hrp gene transcription and is a member of the ECF subfamily of sigma factors. J Bacteriol. 1995 Nov;177(21):6201–6210. [PMC free article] [PubMed]
  • Wei ZM, Laby RJ, Zumoff CH, Bauer DW, He SY, Collmer A, Beer SV. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science. 1992 Jul 3;257(5066):85–88. [PubMed]
  • Wengelnik K, Marie C, Russel M, Bonas U. Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction ofthe hypersensitive reaction. J Bacteriol. 1996 Feb;178(4):1061–1069. [PMC free article] [PubMed]
  • Wengelnik K, Van den Ackerveken G, Bonas U. HrpG, a key hrp regulatory protein of Xanthomonas campestris pv. vesicatoria is homologous to two-component response regulators. Mol Plant Microbe Interact. 1996 Nov;9(8):704–712. [PubMed]
  • Wengelnik K, Bonas U. HrpXv, an AraC-type regulator, activates expression of five of the six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. J Bacteriol. 1996 Jun;178(12):3462–3469. [PMC free article] [PubMed]
  • Whalen MC, Stall RE, Staskawicz BJ. Characterization of a gene from a tomato pathogen determining hypersensitive resistance in non-host species and genetic analysis of this resistance in bean. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6743–6747. [PMC free article] [PubMed]
  • Wood MW, Rosqvist R, Mullan PB, Edwards MH, Galyov EE. SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol Microbiol. 1996 Oct;22(2):327–338. [PubMed]
  • Xiao Y, Heu S, Yi J, Lu Y, Hutcheson SW. Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J Bacteriol. 1994 Feb;176(4):1025–1036. [PMC free article] [PubMed]
  • Yang Y, Gabriel DW. Xanthomonas avirulence/pathogenicity gene family encodes functional plant nuclear targeting signals. Mol Plant Microbe Interact. 1995 Jul-Aug;8(4):627–631. [PubMed]
  • Young SA, White FF, Hopkins CM, Leach JE. AVRXa10 protein is in the cytoplasm of Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact. 1994 Nov-Dec;7(6):799–804. [PubMed]
  • Yuan J, He SY. The Pseudomonas syringae Hrp regulation and secretion system controls the production and secretion of multiple extracellular proteins. J Bacteriol. 1996 Nov;178(21):6399–6402. [PMC free article] [PubMed]
  • Zupan JR, Zambryski P. Transfer of T-DNA from Agrobacterium to the plant cell. Plant Physiol. 1995 Apr;107(4):1041–1047. [PMC free article] [PubMed]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


  • PubMed
    PubMed citations for these articles

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...