Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle

Julietta Jupe, Remco Stam, Andrew J.M. Howden, Jenny A. Morris, Runxuan Zhang, Pete E. Hedley (Lead / Corresponding author), Edgar Huitema (Lead / Corresponding author)

    Research output: Contribution to journalArticle

    54 Citations (Scopus)

    Abstract

    Background
    Plant-microbe interactions feature complex signal interplay between pathogens and their hosts. Phytophthora species comprise a destructive group of fungus-like plant pathogens, collectively affecting a wide range of plants important to agriculture and natural ecosystems. Despite the availability of genome sequences of both hosts and microbes, little is known about the signal interplay between them during infection. In particular, accurate descriptions of coordinate relationships between host and microbe transcriptional programs are lacking.

    Results
    Here, we explore the molecular interaction between the hemi-biotrophic broad host range pathogen Phytophthora capsici and tomato. Infection assays and use of a composite microarray allowed us to unveil distinct changes in both P. capsici and tomato transcriptomes, associated with biotrophy and the subsequent switch to necrotrophy. These included two distinct transcriptional changes associated with early infection and the biotrophy to necrotrophy transition that may contribute to infection and completion of the P. capsici lifecycle.?

    Conclusions
    Our results suggest dynamic but highly regulated transcriptional programming in both host and pathogen that underpin P. capsici disease and hemi-biotrophy. Dynamic expression changes of both effector-coding genes and host factors involved in immunity, suggests modulation of host immune signaling by both host and pathogen. With new unprecedented detail on transcriptional reprogramming, we can now explore the coordinate relationships that drive host-microbe interactions and the basic processes that underpin pathogen lifestyles. Deliberate alteration of lifestyle-associated transcriptional changes may allow prevention or perhaps disruption of hemi-biotrophic disease cycles and limit damage caused by epidemics.
    Original languageEnglish
    Article numberR63
    Pages (from-to)R63
    JournalGenome Biology
    Volume14
    Issue number6
    Early online date25 Jun 2013
    DOIs
    Publication statusPublished - 2013

    Fingerprint

    Phytophthora
    Phytophthora capsici
    Lycopersicon esculentum
    lifestyle
    gene expression
    Life Style
    tomatoes
    Gene Expression
    pathogen
    Infection
    pathogens
    microorganisms
    Host Specificity
    Agriculture
    Transcriptome
    infection
    Ecosystem
    Immunity
    Fungi
    Genome

    Keywords

    • Gene Expression Regulation
    • Host-Pathogen Interactions
    • Lycopersicon esculentum
    • Phytophthora
    • Plant Diseases
    • Plant Immunity
    • Plant Leaves
    • Plant Proteins
    • Signal Transduction
    • Transcription Factors
    • Transcription, Genetic

    Cite this

    Jupe, Julietta ; Stam, Remco ; Howden, Andrew J.M. ; Morris, Jenny A. ; Zhang, Runxuan ; Hedley, Pete E. ; Huitema, Edgar. / Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. In: Genome Biology. 2013 ; Vol. 14, No. 6. pp. R63.
    @article{9f1afeedd8df41a6a7f8ed0086f8832f,
    title = "Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle",
    abstract = "BackgroundPlant-microbe interactions feature complex signal interplay between pathogens and their hosts. Phytophthora species comprise a destructive group of fungus-like plant pathogens, collectively affecting a wide range of plants important to agriculture and natural ecosystems. Despite the availability of genome sequences of both hosts and microbes, little is known about the signal interplay between them during infection. In particular, accurate descriptions of coordinate relationships between host and microbe transcriptional programs are lacking.ResultsHere, we explore the molecular interaction between the hemi-biotrophic broad host range pathogen Phytophthora capsici and tomato. Infection assays and use of a composite microarray allowed us to unveil distinct changes in both P. capsici and tomato transcriptomes, associated with biotrophy and the subsequent switch to necrotrophy. These included two distinct transcriptional changes associated with early infection and the biotrophy to necrotrophy transition that may contribute to infection and completion of the P. capsici lifecycle.?ConclusionsOur results suggest dynamic but highly regulated transcriptional programming in both host and pathogen that underpin P. capsici disease and hemi-biotrophy. Dynamic expression changes of both effector-coding genes and host factors involved in immunity, suggests modulation of host immune signaling by both host and pathogen. With new unprecedented detail on transcriptional reprogramming, we can now explore the coordinate relationships that drive host-microbe interactions and the basic processes that underpin pathogen lifestyles. Deliberate alteration of lifestyle-associated transcriptional changes may allow prevention or perhaps disruption of hemi-biotrophic disease cycles and limit damage caused by epidemics.",
    keywords = "Gene Expression Regulation, Host-Pathogen Interactions, Lycopersicon esculentum, Phytophthora, Plant Diseases, Plant Immunity, Plant Leaves, Plant Proteins, Signal Transduction, Transcription Factors, Transcription, Genetic",
    author = "Julietta Jupe and Remco Stam and Howden, {Andrew J.M.} and Morris, {Jenny A.} and Runxuan Zhang and Hedley, {Pete E.} and Edgar Huitema",
    year = "2013",
    doi = "10.1186/gb-2013-14-6-r63",
    language = "English",
    volume = "14",
    pages = "R63",
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    Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. / Jupe, Julietta; Stam, Remco; Howden, Andrew J.M.; Morris, Jenny A.; Zhang, Runxuan; Hedley, Pete E. (Lead / Corresponding author); Huitema, Edgar (Lead / Corresponding author).

    In: Genome Biology, Vol. 14, No. 6, R63, 2013, p. R63.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle

    AU - Jupe, Julietta

    AU - Stam, Remco

    AU - Howden, Andrew J.M.

    AU - Morris, Jenny A.

    AU - Zhang, Runxuan

    AU - Hedley, Pete E.

    AU - Huitema, Edgar

    PY - 2013

    Y1 - 2013

    N2 - BackgroundPlant-microbe interactions feature complex signal interplay between pathogens and their hosts. Phytophthora species comprise a destructive group of fungus-like plant pathogens, collectively affecting a wide range of plants important to agriculture and natural ecosystems. Despite the availability of genome sequences of both hosts and microbes, little is known about the signal interplay between them during infection. In particular, accurate descriptions of coordinate relationships between host and microbe transcriptional programs are lacking.ResultsHere, we explore the molecular interaction between the hemi-biotrophic broad host range pathogen Phytophthora capsici and tomato. Infection assays and use of a composite microarray allowed us to unveil distinct changes in both P. capsici and tomato transcriptomes, associated with biotrophy and the subsequent switch to necrotrophy. These included two distinct transcriptional changes associated with early infection and the biotrophy to necrotrophy transition that may contribute to infection and completion of the P. capsici lifecycle.?ConclusionsOur results suggest dynamic but highly regulated transcriptional programming in both host and pathogen that underpin P. capsici disease and hemi-biotrophy. Dynamic expression changes of both effector-coding genes and host factors involved in immunity, suggests modulation of host immune signaling by both host and pathogen. With new unprecedented detail on transcriptional reprogramming, we can now explore the coordinate relationships that drive host-microbe interactions and the basic processes that underpin pathogen lifestyles. Deliberate alteration of lifestyle-associated transcriptional changes may allow prevention or perhaps disruption of hemi-biotrophic disease cycles and limit damage caused by epidemics.

    AB - BackgroundPlant-microbe interactions feature complex signal interplay between pathogens and their hosts. Phytophthora species comprise a destructive group of fungus-like plant pathogens, collectively affecting a wide range of plants important to agriculture and natural ecosystems. Despite the availability of genome sequences of both hosts and microbes, little is known about the signal interplay between them during infection. In particular, accurate descriptions of coordinate relationships between host and microbe transcriptional programs are lacking.ResultsHere, we explore the molecular interaction between the hemi-biotrophic broad host range pathogen Phytophthora capsici and tomato. Infection assays and use of a composite microarray allowed us to unveil distinct changes in both P. capsici and tomato transcriptomes, associated with biotrophy and the subsequent switch to necrotrophy. These included two distinct transcriptional changes associated with early infection and the biotrophy to necrotrophy transition that may contribute to infection and completion of the P. capsici lifecycle.?ConclusionsOur results suggest dynamic but highly regulated transcriptional programming in both host and pathogen that underpin P. capsici disease and hemi-biotrophy. Dynamic expression changes of both effector-coding genes and host factors involved in immunity, suggests modulation of host immune signaling by both host and pathogen. With new unprecedented detail on transcriptional reprogramming, we can now explore the coordinate relationships that drive host-microbe interactions and the basic processes that underpin pathogen lifestyles. Deliberate alteration of lifestyle-associated transcriptional changes may allow prevention or perhaps disruption of hemi-biotrophic disease cycles and limit damage caused by epidemics.

    KW - Gene Expression Regulation

    KW - Host-Pathogen Interactions

    KW - Lycopersicon esculentum

    KW - Phytophthora

    KW - Plant Diseases

    KW - Plant Immunity

    KW - Plant Leaves

    KW - Plant Proteins

    KW - Signal Transduction

    KW - Transcription Factors

    KW - Transcription, Genetic

    U2 - 10.1186/gb-2013-14-6-r63

    DO - 10.1186/gb-2013-14-6-r63

    M3 - Article

    VL - 14

    SP - R63

    JO - Genome Biology

    JF - Genome Biology

    SN - 1474-7596

    IS - 6

    M1 - R63

    ER -