Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000

Tanja Petnicki-Ocwieja, David J. Schneider, Vincent C. Tam, Scott T. Chancey, Libo Shan, Yashitola Jamir, Lisa M. Schechter, Misty D. Janes, C. Robin Buell, Xiaoyan Tang, Alan Collmer, James R. Alfano

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219 Citations (Scopus)

Abstract

The ability of Pseudomonas syringae pv. tomato DC3000 to be pathogenic on plants depends on the Hrp (hypersensitive response and pathogenicity) type III protein secretion system and the effector proteins it translocates into plant cells. Through iterative application of experimental and computational techniques, the DC3000 effector inventory has been substantially enlarged. Five homologs of known avirulence (Avr) proteins and five effector candidates, encoded by genes with putative Hrp promoters and signatures of horizontal acquisition, were demonstrated to be secreted in culture and/or translocated into Arabidopsis in a Hrp-dependent manner. These 10 Hrp-dependent outer proteins (Hops) were designated HopPtoC (Avr-PpiC2 homolog), HopPtoD1 and HopPtoD2 (AvrPphD homologs), HopPtoK (AvrRps4 homolog), HopPtoJ (AvrXv3 homolog), HopPtoE, HopPtoG, HopPtoH, HopPtol, and HopPtoS1 (an ADP-ribosyltransferase homolog). Analysis of the enlarged collection of proteins traveling the Hrp pathway in P. syringae revealed an export-associated pattern of equivalent solvent-exposed amino acids in the N-terminal five positions, a lack of Asp or Glu residues in the first 12 positions, and amphipathicity in the first 50 positions. These characteristics were used to search the unfinished DC3000 genome, yielding 32 additional candidate effector genes that predicted proteins with Hrp export signals and that also possessed signatures of horizontal acquisition. Among these were genes encoding additional ADP-ribosyltransferases, a homolog of SrfC (a candidate effector in Salmonella enterica), a catalase, and a glucokinase. One ADP-ribosyl-transferase and the SrfC homolog were tested and shown to be secreted in a Hrp-dependent manner. These proteins, designated HopPtoS2 and HopPtoL, respectively, bring the DC3000 Hrp-secreted protein inventory to 22.

Original languageEnglish (US)
Pages (from-to)7652-7657
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume99
Issue number11
DOIs
StatePublished - May 28 2002

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Pseudomonas syringae
Lycopersicon esculentum
Virulence
Proteins
ADP Ribose Transferases
Glucokinase
Equipment and Supplies
Salmonella enterica
Type III Secretion Systems
Protein Translocation Systems
Plant Cells
Transferases
Arabidopsis
Catalase
Adenosine Diphosphate
Genes
Genome
Amino Acids

ASJC Scopus subject areas

  • General

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Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. / Petnicki-Ocwieja, Tanja; Schneider, David J.; Tam, Vincent C.; Chancey, Scott T.; Shan, Libo; Jamir, Yashitola; Schechter, Lisa M.; Janes, Misty D.; Robin Buell, C.; Tang, Xiaoyan; Collmer, Alan; Alfano, James R.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 99, No. 11, 28.05.2002, p. 7652-7657.

Research output: Contribution to journalArticle

Petnicki-Ocwieja, T, Schneider, DJ, Tam, VC, Chancey, ST, Shan, L, Jamir, Y, Schechter, LM, Janes, MD, Robin Buell, C, Tang, X, Collmer, A & Alfano, JR 2002, 'Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000', Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 11, pp. 7652-7657. https://doi.org/10.1073/pnas.112183899
Petnicki-Ocwieja, Tanja ; Schneider, David J. ; Tam, Vincent C. ; Chancey, Scott T. ; Shan, Libo ; Jamir, Yashitola ; Schechter, Lisa M. ; Janes, Misty D. ; Robin Buell, C. ; Tang, Xiaoyan ; Collmer, Alan ; Alfano, James R. / Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. In: Proceedings of the National Academy of Sciences of the United States of America. 2002 ; Vol. 99, No. 11. pp. 7652-7657.
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abstract = "The ability of Pseudomonas syringae pv. tomato DC3000 to be pathogenic on plants depends on the Hrp (hypersensitive response and pathogenicity) type III protein secretion system and the effector proteins it translocates into plant cells. Through iterative application of experimental and computational techniques, the DC3000 effector inventory has been substantially enlarged. Five homologs of known avirulence (Avr) proteins and five effector candidates, encoded by genes with putative Hrp promoters and signatures of horizontal acquisition, were demonstrated to be secreted in culture and/or translocated into Arabidopsis in a Hrp-dependent manner. These 10 Hrp-dependent outer proteins (Hops) were designated HopPtoC (Avr-PpiC2 homolog), HopPtoD1 and HopPtoD2 (AvrPphD homologs), HopPtoK (AvrRps4 homolog), HopPtoJ (AvrXv3 homolog), HopPtoE, HopPtoG, HopPtoH, HopPtol, and HopPtoS1 (an ADP-ribosyltransferase homolog). Analysis of the enlarged collection of proteins traveling the Hrp pathway in P. syringae revealed an export-associated pattern of equivalent solvent-exposed amino acids in the N-terminal five positions, a lack of Asp or Glu residues in the first 12 positions, and amphipathicity in the first 50 positions. These characteristics were used to search the unfinished DC3000 genome, yielding 32 additional candidate effector genes that predicted proteins with Hrp export signals and that also possessed signatures of horizontal acquisition. Among these were genes encoding additional ADP-ribosyltransferases, a homolog of SrfC (a candidate effector in Salmonella enterica), a catalase, and a glucokinase. One ADP-ribosyl-transferase and the SrfC homolog were tested and shown to be secreted in a Hrp-dependent manner. These proteins, designated HopPtoS2 and HopPtoL, respectively, bring the DC3000 Hrp-secreted protein inventory to 22.",
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AU - Petnicki-Ocwieja, Tanja

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AU - Tam, Vincent C.

AU - Chancey, Scott T.

AU - Shan, Libo

AU - Jamir, Yashitola

AU - Schechter, Lisa M.

AU - Janes, Misty D.

AU - Robin Buell, C.

AU - Tang, Xiaoyan

AU - Collmer, Alan

AU - Alfano, James R.

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N2 - The ability of Pseudomonas syringae pv. tomato DC3000 to be pathogenic on plants depends on the Hrp (hypersensitive response and pathogenicity) type III protein secretion system and the effector proteins it translocates into plant cells. Through iterative application of experimental and computational techniques, the DC3000 effector inventory has been substantially enlarged. Five homologs of known avirulence (Avr) proteins and five effector candidates, encoded by genes with putative Hrp promoters and signatures of horizontal acquisition, were demonstrated to be secreted in culture and/or translocated into Arabidopsis in a Hrp-dependent manner. These 10 Hrp-dependent outer proteins (Hops) were designated HopPtoC (Avr-PpiC2 homolog), HopPtoD1 and HopPtoD2 (AvrPphD homologs), HopPtoK (AvrRps4 homolog), HopPtoJ (AvrXv3 homolog), HopPtoE, HopPtoG, HopPtoH, HopPtol, and HopPtoS1 (an ADP-ribosyltransferase homolog). Analysis of the enlarged collection of proteins traveling the Hrp pathway in P. syringae revealed an export-associated pattern of equivalent solvent-exposed amino acids in the N-terminal five positions, a lack of Asp or Glu residues in the first 12 positions, and amphipathicity in the first 50 positions. These characteristics were used to search the unfinished DC3000 genome, yielding 32 additional candidate effector genes that predicted proteins with Hrp export signals and that also possessed signatures of horizontal acquisition. Among these were genes encoding additional ADP-ribosyltransferases, a homolog of SrfC (a candidate effector in Salmonella enterica), a catalase, and a glucokinase. One ADP-ribosyl-transferase and the SrfC homolog were tested and shown to be secreted in a Hrp-dependent manner. These proteins, designated HopPtoS2 and HopPtoL, respectively, bring the DC3000 Hrp-secreted protein inventory to 22.

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