Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum

Hui Liu, Sarah J. Coulthurst, Leighton Pritchard, Peter E. Hedley, Michael Ravensdale, Sonia Humphris, Tom Burr, Gunnhild Takle, May-Bente Brurberg, Paul R. J. Birch, George P. C. Salmond, Ian K. Toth

    Research output: Contribution to journalArticle

    143 Citations (Scopus)

    Abstract

    Quorum sensing (QS) in vitro controls production of plant cell wall degrading enzymes (PCWDEs) and other virulence factors in the soft rotting enterobacterial plant pathogen Pectobacterium atrosepticum (Pba). Here, we demonstrate the genome-wide regulatory role of QS in vivo during the Pba-potato interaction, using a Pba-specific microarray. We show that 26% of the Pba genome exhibited differential transcription in a QS (expl-) mutant, compared to the wild-type, suggesting that QS may make a greater contribution to pathogenesis than previously thought. We identify novel components of the QS regulon, including the Type I and II secretion systems, which are involved in the secretion of PCWDEs; a novel Type VI secretion system (T6SS) and its predicted substrates Hcp and VgrG; more than 70 known or putative regulators, some of which have been demonstrated to control pathogenesis and, remarkably, the Type III secretion system and associated effector proteins, and coronafacoyl-amide conjugates, both of which play roles in the manipulation of plant defences. We show that the T6SS and a novel potential regulator, VirS, are required for full virulence in Pba, and propose a model placing QS at the apex of a regulatory hierarchy controlling the later stages of disease progression in Pba. Our findings indicate that QS is a master regulator of phytopathogenesis, controlling multiple other regulators that, in turn, co-ordinately regulate genes associated with manipulation of host defences in concert with the destructive arsenal of PCWDEs that manifest the soft rot disease phenotype.

    Original languageEnglish
    Article numbere1000093
    Pages (from-to)-
    Number of pages11
    JournalPLoS Pathogens
    Volume4
    Issue number6
    DOIs
    Publication statusPublished - 2008

    Keywords

    • CAROTOVORA SUBSP-ATROSEPTICA
    • GRAM-NEGATIVE BACTERIA
    • III SECRETION SYSTEM
    • N-ACYLHOMOSERINE LACTONES
    • PV. TOMATO DC3000
    • SOFT-ROT ERWINIAE
    • PSEUDOMONAS-AERUGINOSA
    • PHYTOTOXIN CORONATINE
    • PROTEIN SECRETION
    • YERSINIA-ENTEROCOLITICA

    Cite this

    Liu, Hui ; Coulthurst, Sarah J. ; Pritchard, Leighton ; Hedley, Peter E. ; Ravensdale, Michael ; Humphris, Sonia ; Burr, Tom ; Takle, Gunnhild ; Brurberg, May-Bente ; Birch, Paul R. J. ; Salmond, George P. C. ; Toth, Ian K. / Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. In: PLoS Pathogens. 2008 ; Vol. 4, No. 6. pp. -.
    @article{4cf90d1e48c94c41bbcaf6714f1e0aac,
    title = "Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum",
    abstract = "Quorum sensing (QS) in vitro controls production of plant cell wall degrading enzymes (PCWDEs) and other virulence factors in the soft rotting enterobacterial plant pathogen Pectobacterium atrosepticum (Pba). Here, we demonstrate the genome-wide regulatory role of QS in vivo during the Pba-potato interaction, using a Pba-specific microarray. We show that 26{\%} of the Pba genome exhibited differential transcription in a QS (expl-) mutant, compared to the wild-type, suggesting that QS may make a greater contribution to pathogenesis than previously thought. We identify novel components of the QS regulon, including the Type I and II secretion systems, which are involved in the secretion of PCWDEs; a novel Type VI secretion system (T6SS) and its predicted substrates Hcp and VgrG; more than 70 known or putative regulators, some of which have been demonstrated to control pathogenesis and, remarkably, the Type III secretion system and associated effector proteins, and coronafacoyl-amide conjugates, both of which play roles in the manipulation of plant defences. We show that the T6SS and a novel potential regulator, VirS, are required for full virulence in Pba, and propose a model placing QS at the apex of a regulatory hierarchy controlling the later stages of disease progression in Pba. Our findings indicate that QS is a master regulator of phytopathogenesis, controlling multiple other regulators that, in turn, co-ordinately regulate genes associated with manipulation of host defences in concert with the destructive arsenal of PCWDEs that manifest the soft rot disease phenotype.",
    keywords = "CAROTOVORA SUBSP-ATROSEPTICA, GRAM-NEGATIVE BACTERIA, III SECRETION SYSTEM, N-ACYLHOMOSERINE LACTONES, PV. TOMATO DC3000, SOFT-ROT ERWINIAE, PSEUDOMONAS-AERUGINOSA, PHYTOTOXIN CORONATINE, PROTEIN SECRETION, YERSINIA-ENTEROCOLITICA",
    author = "Hui Liu and Coulthurst, {Sarah J.} and Leighton Pritchard and Hedley, {Peter E.} and Michael Ravensdale and Sonia Humphris and Tom Burr and Gunnhild Takle and May-Bente Brurberg and Birch, {Paul R. J.} and Salmond, {George P. C.} and Toth, {Ian K.}",
    year = "2008",
    doi = "10.1371/journal.ppat.1000093",
    language = "English",
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    Liu, H, Coulthurst, SJ, Pritchard, L, Hedley, PE, Ravensdale, M, Humphris, S, Burr, T, Takle, G, Brurberg, M-B, Birch, PRJ, Salmond, GPC & Toth, IK 2008, 'Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum', PLoS Pathogens, vol. 4, no. 6, e1000093, pp. -. https://doi.org/10.1371/journal.ppat.1000093

    Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. / Liu, Hui; Coulthurst, Sarah J.; Pritchard, Leighton; Hedley, Peter E.; Ravensdale, Michael; Humphris, Sonia; Burr, Tom; Takle, Gunnhild; Brurberg, May-Bente; Birch, Paul R. J.; Salmond, George P. C.; Toth, Ian K.

    In: PLoS Pathogens, Vol. 4, No. 6, e1000093, 2008, p. -.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum

    AU - Liu, Hui

    AU - Coulthurst, Sarah J.

    AU - Pritchard, Leighton

    AU - Hedley, Peter E.

    AU - Ravensdale, Michael

    AU - Humphris, Sonia

    AU - Burr, Tom

    AU - Takle, Gunnhild

    AU - Brurberg, May-Bente

    AU - Birch, Paul R. J.

    AU - Salmond, George P. C.

    AU - Toth, Ian K.

    PY - 2008

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    AB - Quorum sensing (QS) in vitro controls production of plant cell wall degrading enzymes (PCWDEs) and other virulence factors in the soft rotting enterobacterial plant pathogen Pectobacterium atrosepticum (Pba). Here, we demonstrate the genome-wide regulatory role of QS in vivo during the Pba-potato interaction, using a Pba-specific microarray. We show that 26% of the Pba genome exhibited differential transcription in a QS (expl-) mutant, compared to the wild-type, suggesting that QS may make a greater contribution to pathogenesis than previously thought. We identify novel components of the QS regulon, including the Type I and II secretion systems, which are involved in the secretion of PCWDEs; a novel Type VI secretion system (T6SS) and its predicted substrates Hcp and VgrG; more than 70 known or putative regulators, some of which have been demonstrated to control pathogenesis and, remarkably, the Type III secretion system and associated effector proteins, and coronafacoyl-amide conjugates, both of which play roles in the manipulation of plant defences. We show that the T6SS and a novel potential regulator, VirS, are required for full virulence in Pba, and propose a model placing QS at the apex of a regulatory hierarchy controlling the later stages of disease progression in Pba. Our findings indicate that QS is a master regulator of phytopathogenesis, controlling multiple other regulators that, in turn, co-ordinately regulate genes associated with manipulation of host defences in concert with the destructive arsenal of PCWDEs that manifest the soft rot disease phenotype.

    KW - CAROTOVORA SUBSP-ATROSEPTICA

    KW - GRAM-NEGATIVE BACTERIA

    KW - III SECRETION SYSTEM

    KW - N-ACYLHOMOSERINE LACTONES

    KW - PV. TOMATO DC3000

    KW - SOFT-ROT ERWINIAE

    KW - PSEUDOMONAS-AERUGINOSA

    KW - PHYTOTOXIN CORONATINE

    KW - PROTEIN SECRETION

    KW - YERSINIA-ENTEROCOLITICA

    U2 - 10.1371/journal.ppat.1000093

    DO - 10.1371/journal.ppat.1000093

    M3 - Article

    VL - 4

    SP - -

    JO - PLoS Pathogens

    JF - PLoS Pathogens

    SN - 1553-7366

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    ER -