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Title: Show me your secret(ed) weapons: a multifaceted approach reveals a wide arsenal of type III‐secreted effectors in the cucurbit pathogenic bacterium Acidovorax citrulli and novel effectors in the Acidovorax genus

Abstract

Summary The cucurbit pathogenic bacterium Acidovorax citrulli requires a functional type III secretion system (T3SS) for pathogenicity. In this bacterium, as with Xanthomonas and Ralstonia spp . , an AraC‐type transcriptional regulator, HrpX, regulates expression of genes encoding T3SS components and type III‐secreted effectors (T3Es) . The annotation of a sequenced A. citrulli strain revealed 11 T3E genes. Assuming that this could be an underestimation, we aimed to uncover the T3E arsenal of the A. citrulli model strain, M6. Thorough sequence analysis revealed 51 M6 genes whose products are similar to known T3Es. Furthermore, we combined machine learning and transcriptomics to identify novel T3Es. The machine‐learning approach ranked all A. citrulli M6 genes according to their propensity to encode T3Es. RNA‐Seq revealed differential gene expression between wild‐type M6 and a mutant defective in HrpX: 159 and 28 genes showed significantly reduced and increased expression in the mutant relative to wild‐type M6, respectively. Data combined from these approaches led to the identification of seven novel T3E candidates that were further validated using a T3SS‐dependent translocation assay. These T3E genes encode hypothetical proteins that seem to be restricted to plant pathogenic Acidovorax species. Transient expression in Nicotiana benthamiana revealed that two ofmore » these T3Es localize to the cell nucleus and one interacts with the endoplasmic reticulum. This study places A. citrulli among the ‘richest’ bacterial pathogens in terms of T3E cargo. It also revealed novel T3Es that appear to be involved in the pathoadaptive evolution of plant pathogenic Acidovorax species.« less

Authors:
 [1];  [2];  [1];  [3];  [3];  [4];  [5];  [5];  [4];  [6];  [3]; ORCiD logo [1]
  1. Department of Plant Pathology and Microbiology The Robert H. Smith Faculty of Agriculture, Food and Environment The Hebrew University of Jerusalem Rehovot Israel
  2. Department of Plant Pathology and Microbiology The Robert H. Smith Faculty of Agriculture, Food and Environment The Hebrew University of Jerusalem Rehovot Israel, Department of Microbiology University of Seville Seville Spain
  3. The School of Molecular Cell Biology and Biotechnology The George S. Wise Faculty of Life Sciences Tel Aviv University Tel Aviv Israel
  4. Department of Plant Pathology University of Georgia Athens GA USA
  5. Department of Plant Pathology and Weed Research Agricultural Research Organization The Volcani Center Bet Dagan Israel
  6. School of Plant Sciences and Food Security The George S. Wise Faculty of Life Sciences Tel Aviv University Tel Aviv Israel
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1571542
Alternate Identifier(s):
OSTI ID: 1571543
Resource Type:
Published Article
Journal Name:
Molecular Plant Pathology
Additional Journal Information:
Journal Name: Molecular Plant Pathology Journal Volume: 21 Journal Issue: 1; Journal ID: ISSN 1464-6722
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Jiménez‐Guerrero, Irene, Pérez‐Montaño, Francisco, Da Silva, Gustavo Mateus, Wagner, Naama, Shkedy, Dafna, Zhao, Mei, Pizarro, Lorena, Bar, Maya, Walcott, Ron, Sessa, Guido, Pupko, Tal, and Burdman, Saul. Show me your secret(ed) weapons: a multifaceted approach reveals a wide arsenal of type III‐secreted effectors in the cucurbit pathogenic bacterium Acidovorax citrulli and novel effectors in the Acidovorax genus. United Kingdom: N. p., 2019. Web. doi:10.1111/mpp.12877.
Jiménez‐Guerrero, Irene, Pérez‐Montaño, Francisco, Da Silva, Gustavo Mateus, Wagner, Naama, Shkedy, Dafna, Zhao, Mei, Pizarro, Lorena, Bar, Maya, Walcott, Ron, Sessa, Guido, Pupko, Tal, & Burdman, Saul. Show me your secret(ed) weapons: a multifaceted approach reveals a wide arsenal of type III‐secreted effectors in the cucurbit pathogenic bacterium Acidovorax citrulli and novel effectors in the Acidovorax genus. United Kingdom. https://doi.org/10.1111/mpp.12877
Jiménez‐Guerrero, Irene, Pérez‐Montaño, Francisco, Da Silva, Gustavo Mateus, Wagner, Naama, Shkedy, Dafna, Zhao, Mei, Pizarro, Lorena, Bar, Maya, Walcott, Ron, Sessa, Guido, Pupko, Tal, and Burdman, Saul. Wed . "Show me your secret(ed) weapons: a multifaceted approach reveals a wide arsenal of type III‐secreted effectors in the cucurbit pathogenic bacterium Acidovorax citrulli and novel effectors in the Acidovorax genus". United Kingdom. https://doi.org/10.1111/mpp.12877.
@article{osti_1571542,
title = {Show me your secret(ed) weapons: a multifaceted approach reveals a wide arsenal of type III‐secreted effectors in the cucurbit pathogenic bacterium Acidovorax citrulli and novel effectors in the Acidovorax genus},
author = {Jiménez‐Guerrero, Irene and Pérez‐Montaño, Francisco and Da Silva, Gustavo Mateus and Wagner, Naama and Shkedy, Dafna and Zhao, Mei and Pizarro, Lorena and Bar, Maya and Walcott, Ron and Sessa, Guido and Pupko, Tal and Burdman, Saul},
abstractNote = {Summary The cucurbit pathogenic bacterium Acidovorax citrulli requires a functional type III secretion system (T3SS) for pathogenicity. In this bacterium, as with Xanthomonas and Ralstonia spp . , an AraC‐type transcriptional regulator, HrpX, regulates expression of genes encoding T3SS components and type III‐secreted effectors (T3Es) . The annotation of a sequenced A. citrulli strain revealed 11 T3E genes. Assuming that this could be an underestimation, we aimed to uncover the T3E arsenal of the A. citrulli model strain, M6. Thorough sequence analysis revealed 51 M6 genes whose products are similar to known T3Es. Furthermore, we combined machine learning and transcriptomics to identify novel T3Es. The machine‐learning approach ranked all A. citrulli M6 genes according to their propensity to encode T3Es. RNA‐Seq revealed differential gene expression between wild‐type M6 and a mutant defective in HrpX: 159 and 28 genes showed significantly reduced and increased expression in the mutant relative to wild‐type M6, respectively. Data combined from these approaches led to the identification of seven novel T3E candidates that were further validated using a T3SS‐dependent translocation assay. These T3E genes encode hypothetical proteins that seem to be restricted to plant pathogenic Acidovorax species. Transient expression in Nicotiana benthamiana revealed that two of these T3Es localize to the cell nucleus and one interacts with the endoplasmic reticulum. This study places A. citrulli among the ‘richest’ bacterial pathogens in terms of T3E cargo. It also revealed novel T3Es that appear to be involved in the pathoadaptive evolution of plant pathogenic Acidovorax species.},
doi = {10.1111/mpp.12877},
journal = {Molecular Plant Pathology},
number = 1,
volume = 21,
place = {United Kingdom},
year = {Wed Oct 23 00:00:00 EDT 2019},
month = {Wed Oct 23 00:00:00 EDT 2019}
}

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https://doi.org/10.1111/mpp.12877

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