title: Conservation and clade-specific diversification of pathogen-inducible tryptophan and indole glucosinolate metabolism in Arabidopsis thaliana relatives.
abstract: • 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).
authors.affiliation: Max Planck Institute for Plant Breeding Research, Department of Plant Microbe Interactions, Köln, Germany. bednarek@ibch.poznan.pl
authors.forename: Paweł
authors.initials: P
authors.lastname: Bednarek
authors.forename: Mariola
authors.initials: M
authors.lastname: Piślewska-Bednarek
authors.forename: Emiel
authors.initials: E
authors.lastname: Ver Loren van Themaat
authors.forename: Ravi Kumar
authors.initials: RK
authors.lastname: Maddula
authors.forename: Aleš
authors.initials: A
authors.lastname: Svatoš
authors.forename: Paul
authors.initials: P
authors.lastname: Schulze-Lefert
mesh_terms: D000042:Absorption / Q000528:radiation effects; D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000276:immunology / Q000378:metabolism* / Q000382:microbiology / Q000528:radiation effects; D001203:Ascomycota / Q000502:physiology / Q000528:radiation effects; D020171:Botrytis / Q000502:physiology / Q000528:radiation effects; D019607:Brassicaceae / Q000276:immunology / Q000378:metabolism* / Q000382:microbiology*; D014644:Genetic Variation; D005961:Glucosinolates / Q000737:chemistry / Q000378:metabolism*; D007113:Immunity, Innate / Q000528:radiation effects; D007211:Indoles / Q000737:chemistry / Q000378:metabolism*; D008969:Molecular Sequence Data; D010802:Phylogeny; D010935:Plant Diseases / Q000382:microbiology; D010940:Plant Proteins / Q000737:chemistry; D017386:Sequence Homology, Amino Acid; D013045:Species Specificity; D013844:Thiazoles / Q000378:metabolism; D014364:Tryptophan / Q000737:chemistry / Q000378:metabolism*; D014466:Ultraviolet Rays; D000094162:Phytoalexins
chemical_list: D005961:Glucosinolates; D007211:Indoles; D010940:Plant Proteins; D013844:Thiazoles; D014364:Tryptophan; C102405:camalexin; D000094162:Phytoalexins; C036025:4-methoxy-3-indolylmethyl glucosinolate