The developmental selector AS1 is an evolutionarily conserved regulator of the plant immune response

Pedro L. Nurmberg, Kirsten A. Knox, Byung Wook Yun, Peter C. Morris, Reza Shafiei, Andrew Hudson, Gary J. Loake

    Research output: Contribution to journalArticle

    Abstract

    The MYB-related gene ASYMMETRIC LEAVES 1 (AS1) and its orthologs have an evolutionarily conserved role in specification of leaf cell identity. AS1 is expressed in leaf founder cells, where it functions as a heterodimer with the structurally unrelated AS2 proteins to repress activity of KNOTTED 1-like homeobox (KNOX) genes. AS1 therefore confines KNOX activity to the shoot apical meristem, where it promotes stem cell function through the regulation of phytohormone activities. Here, we show that loss-of-function mutations in AS1 unexpectedly convey heightened protection against necrotrophic fungi. AS1 operates as a negative regulator of inducible resistance against these pathogens by selectively binding to the promoters of genes controlled by the immune activator, jasmonic acid (JA), damping the defense response. In contrast, AS1 is a positive regulator of salicylic acid (SA)-independent extracellular defenses against bacterial pathogens. Neither the absence of AS2 nor ERECTA function, which enhances the morphological phenotype of as1, nor the conditional or constitutive expression of KNOX genes impacted disease resistance. Thus, the function of AS1 in responses to phytopathogens is independent of its AS2-associated role in development. Loss of function in the AS1 orthologs PHAN in Antirrhinum majus and NSPHAN in Nicotiana sylvestris produced pathogen-response phenotypes similar to as1 plants, and therefore the defense function of AS1 is evolutionarily conserved in plant species with a divergence time of ˜125 million years. © 2007 by The National Academy of Sciences of the USA.

    Original languageEnglish
    Pages (from-to)18795-18800
    Number of pages6
    JournalProceedings of the National Academy of Sciences
    Volume104
    Issue number47
    DOIs
    Publication statusPublished - 20 Nov 2007

    Fingerprint

    Plant Immunity
    Antirrhinum
    Phenotype
    Disease Resistance
    Plant Growth Regulators
    Salicylic Acid
    Meristem
    Homeobox Genes
    Genes
    Tobacco
    Fungi
    Stem Cells
    Gene Expression
    Mutation
    Proteins

    Keywords

    • Arabidopsis thaliana
    • Asymmetric leaves 1
    • Disease resistance
    • Plant defense response

    Cite this

    Nurmberg, Pedro L. ; Knox, Kirsten A. ; Yun, Byung Wook ; Morris, Peter C. ; Shafiei, Reza ; Hudson, Andrew ; Loake, Gary J. / The developmental selector AS1 is an evolutionarily conserved regulator of the plant immune response. In: Proceedings of the National Academy of Sciences. 2007 ; Vol. 104, No. 47. pp. 18795-18800.
    @article{d86f02f740964be6ab162e66a8568967,
    title = "The developmental selector AS1 is an evolutionarily conserved regulator of the plant immune response",
    abstract = "The MYB-related gene ASYMMETRIC LEAVES 1 (AS1) and its orthologs have an evolutionarily conserved role in specification of leaf cell identity. AS1 is expressed in leaf founder cells, where it functions as a heterodimer with the structurally unrelated AS2 proteins to repress activity of KNOTTED 1-like homeobox (KNOX) genes. AS1 therefore confines KNOX activity to the shoot apical meristem, where it promotes stem cell function through the regulation of phytohormone activities. Here, we show that loss-of-function mutations in AS1 unexpectedly convey heightened protection against necrotrophic fungi. AS1 operates as a negative regulator of inducible resistance against these pathogens by selectively binding to the promoters of genes controlled by the immune activator, jasmonic acid (JA), damping the defense response. In contrast, AS1 is a positive regulator of salicylic acid (SA)-independent extracellular defenses against bacterial pathogens. Neither the absence of AS2 nor ERECTA function, which enhances the morphological phenotype of as1, nor the conditional or constitutive expression of KNOX genes impacted disease resistance. Thus, the function of AS1 in responses to phytopathogens is independent of its AS2-associated role in development. Loss of function in the AS1 orthologs PHAN in Antirrhinum majus and NSPHAN in Nicotiana sylvestris produced pathogen-response phenotypes similar to as1 plants, and therefore the defense function of AS1 is evolutionarily conserved in plant species with a divergence time of ˜125 million years. {\circledC} 2007 by The National Academy of Sciences of the USA.",
    keywords = "Arabidopsis thaliana, Asymmetric leaves 1, Disease resistance, Plant defense response",
    author = "Nurmberg, {Pedro L.} and Knox, {Kirsten A.} and Yun, {Byung Wook} and Morris, {Peter C.} and Reza Shafiei and Andrew Hudson and Loake, {Gary J.}",
    year = "2007",
    month = "11",
    day = "20",
    doi = "10.1073/pnas.0705586104",
    language = "English",
    volume = "104",
    pages = "18795--18800",
    journal = "Proceedings of the National Academy of Sciences",
    issn = "0027-8424",
    number = "47",

    }

    The developmental selector AS1 is an evolutionarily conserved regulator of the plant immune response. / Nurmberg, Pedro L.; Knox, Kirsten A.; Yun, Byung Wook; Morris, Peter C.; Shafiei, Reza; Hudson, Andrew; Loake, Gary J.

    In: Proceedings of the National Academy of Sciences, Vol. 104, No. 47, 20.11.2007, p. 18795-18800.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - The developmental selector AS1 is an evolutionarily conserved regulator of the plant immune response

    AU - Nurmberg, Pedro L.

    AU - Knox, Kirsten A.

    AU - Yun, Byung Wook

    AU - Morris, Peter C.

    AU - Shafiei, Reza

    AU - Hudson, Andrew

    AU - Loake, Gary J.

    PY - 2007/11/20

    Y1 - 2007/11/20

    N2 - The MYB-related gene ASYMMETRIC LEAVES 1 (AS1) and its orthologs have an evolutionarily conserved role in specification of leaf cell identity. AS1 is expressed in leaf founder cells, where it functions as a heterodimer with the structurally unrelated AS2 proteins to repress activity of KNOTTED 1-like homeobox (KNOX) genes. AS1 therefore confines KNOX activity to the shoot apical meristem, where it promotes stem cell function through the regulation of phytohormone activities. Here, we show that loss-of-function mutations in AS1 unexpectedly convey heightened protection against necrotrophic fungi. AS1 operates as a negative regulator of inducible resistance against these pathogens by selectively binding to the promoters of genes controlled by the immune activator, jasmonic acid (JA), damping the defense response. In contrast, AS1 is a positive regulator of salicylic acid (SA)-independent extracellular defenses against bacterial pathogens. Neither the absence of AS2 nor ERECTA function, which enhances the morphological phenotype of as1, nor the conditional or constitutive expression of KNOX genes impacted disease resistance. Thus, the function of AS1 in responses to phytopathogens is independent of its AS2-associated role in development. Loss of function in the AS1 orthologs PHAN in Antirrhinum majus and NSPHAN in Nicotiana sylvestris produced pathogen-response phenotypes similar to as1 plants, and therefore the defense function of AS1 is evolutionarily conserved in plant species with a divergence time of ˜125 million years. © 2007 by The National Academy of Sciences of the USA.

    AB - The MYB-related gene ASYMMETRIC LEAVES 1 (AS1) and its orthologs have an evolutionarily conserved role in specification of leaf cell identity. AS1 is expressed in leaf founder cells, where it functions as a heterodimer with the structurally unrelated AS2 proteins to repress activity of KNOTTED 1-like homeobox (KNOX) genes. AS1 therefore confines KNOX activity to the shoot apical meristem, where it promotes stem cell function through the regulation of phytohormone activities. Here, we show that loss-of-function mutations in AS1 unexpectedly convey heightened protection against necrotrophic fungi. AS1 operates as a negative regulator of inducible resistance against these pathogens by selectively binding to the promoters of genes controlled by the immune activator, jasmonic acid (JA), damping the defense response. In contrast, AS1 is a positive regulator of salicylic acid (SA)-independent extracellular defenses against bacterial pathogens. Neither the absence of AS2 nor ERECTA function, which enhances the morphological phenotype of as1, nor the conditional or constitutive expression of KNOX genes impacted disease resistance. Thus, the function of AS1 in responses to phytopathogens is independent of its AS2-associated role in development. Loss of function in the AS1 orthologs PHAN in Antirrhinum majus and NSPHAN in Nicotiana sylvestris produced pathogen-response phenotypes similar to as1 plants, and therefore the defense function of AS1 is evolutionarily conserved in plant species with a divergence time of ˜125 million years. © 2007 by The National Academy of Sciences of the USA.

    KW - Arabidopsis thaliana

    KW - Asymmetric leaves 1

    KW - Disease resistance

    KW - Plant defense response

    UR - http://www.scopus.com/inward/record.url?scp=36749100622&partnerID=8YFLogxK

    U2 - 10.1073/pnas.0705586104

    DO - 10.1073/pnas.0705586104

    M3 - Article

    C2 - 18003921

    VL - 104

    SP - 18795

    EP - 18800

    JO - Proceedings of the National Academy of Sciences

    JF - Proceedings of the National Academy of Sciences

    SN - 0027-8424

    IS - 47

    ER -