Conservation and clade-specific diversification of pathogen-inducible tryptophan and indole glucosinolate metabolism in Arabidopsis thaliana relatives

Authors

  • Paweł Bednarek,

    1. Max Planck Institute for Plant Breeding Research, Department of Plant Microbe Interactions, Carl-von-Linné-Weg 10, D-50829 Köln, Germany
    2. Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12/14, 61-704 Poznań, Poland
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  • Mariola Piślewska-Bednarek,

    1. Max Planck Institute for Plant Breeding Research, Department of Plant Microbe Interactions, Carl-von-Linné-Weg 10, D-50829 Köln, Germany
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  • Emiel Ver Loren van Themaat,

    1. Max Planck Institute for Plant Breeding Research, Department of Plant Microbe Interactions, Carl-von-Linné-Weg 10, D-50829 Köln, Germany
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  • Ravi Kumar Maddula,

    1. Max Planck Institute for Chemical Ecology, Beutenberg Campus, Hans- Knöll-Straße 8, D-07745 Jena, Germany
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  • Aleš Svatoš,

    1. Max Planck Institute for Chemical Ecology, Beutenberg Campus, Hans- Knöll-Straße 8, D-07745 Jena, Germany
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  • Paul Schulze-Lefert

    1. Max Planck Institute for Plant Breeding Research, Department of Plant Microbe Interactions, Carl-von-Linné-Weg 10, D-50829 Köln, Germany
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Authors for correspondence:
Paweł Bednarek
Tel: +48 618528503
Email: bednarek@ibch.poznan.pl
Paul Schulze-Lefert
Tel: +49 2215062351
Email: schlef@mpiz-koeln.mpg.de

Summary

  • A hallmark of the innate immune system of plants is the biosynthesis of low-molecular-weight compounds referred to as secondary metabolites. Tryptophan-derived branch pathways contribute to the capacity for chemical defense against microbes in Arabidopsis thaliana.
  • Here, we investigated phylogenetic patterns of this metabolic pathway in relatives of A. thaliana following inoculation with filamentous fungal pathogens that employ contrasting infection strategies.
  • The study revealed unexpected phylogenetic conservation of the pathogen-induced indole glucosinolate (IG) metabolic pathway, including a metabolic shift of IG biosynthesis to 4-methoxyindol-3-ylmethylglucosinolate and IG metabolization. By contrast, indole-3-carboxylic acid and camalexin biosyntheses are clade-specific innovations within this metabolic framework. A Capsella rubella accession was found to be devoid of any IG metabolites and to lack orthologs of two A. thaliana genes needed for 4-methoxyindol-3-ylmethylglucosinolate biosynthesis or hydrolysis. However, C. rubella was found to retain the capacity to deposit callose after treatment with the bacterial flagellin-derived epitope flg22 and pre-invasive resistance against a nonadapted powdery mildew fungus.
  • We conclude that pathogen-inducible IG metabolism in the Brassicaceae is evolutionarily ancient, while other tryptophan-derived branch pathways represent relatively recent manifestations of a plant–pathogen arms race. Moreover, at least one Brassicaceae lineage appears to have evolved IG-independent defense signaling and/or output pathway(s).

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