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Plant Physiol. 2015 Jul;168(3):814-27. doi: 10.1104/pp.15.00182. Epub 2015 May 28.

Mutant Allele-Specific Uncoupling of PENETRATION3 Functions Reveals Engagement of the ATP-Binding Cassette Transporter in Distinct Tryptophan Metabolic Pathways.

Author information

1
Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany (X.L., J.Di., M.P.-B., P.B., P.S.-L.);Institute of Bioorganic Chemistry, Polish Academy of Sciences, 61-704 Poznan, Poland (M.P.-B., P.B.);Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, 28223 Madrid, Spain (A.M.); Research Groups on Biosynthesis/Nuclear Magnetic Resonance (B.S.) and Mass Spectrometry/Proteomics (A.S., J.Do.), Max Planck Institute for Chemical Ecology, 07745 Jena, Germany; andDepartment of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tuebingen, Germany (K.S., D.W.).
2
Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany (X.L., J.Di., M.P.-B., P.B., P.S.-L.);Institute of Bioorganic Chemistry, Polish Academy of Sciences, 61-704 Poznan, Poland (M.P.-B., P.B.);Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, 28223 Madrid, Spain (A.M.); Research Groups on Biosynthesis/Nuclear Magnetic Resonance (B.S.) and Mass Spectrometry/Proteomics (A.S., J.Do.), Max Planck Institute for Chemical Ecology, 07745 Jena, Germany; andDepartment of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tuebingen, Germany (K.S., D.W.) bednarek@ibch.poznan.pl schlef@mpipz.mpg.de.

Abstract

Arabidopsis (Arabidopsis thaliana) penetration (PEN) genes quantitatively contribute to the execution of different forms of plant immunity upon challenge with diverse leaf pathogens. PEN3 encodes a plasma membrane-resident pleiotropic drug resistance-type ATP-binding cassette transporter and is thought to act in a pathogen-inducible and PEN2 myrosinase-dependent metabolic pathway in extracellular defense. This metabolic pathway directs the intracellular biosynthesis and activation of tryptophan-derived indole glucosinolates for subsequent PEN3-mediated efflux across the plasma membrane at pathogen contact sites. However, PEN3 also functions in abiotic stress responses to cadmium and indole-3-butyric acid (IBA)-mediated auxin homeostasis in roots, raising the possibility that PEN3 exports multiple functionally unrelated substrates. Here, we describe the isolation of a pen3 allele, designated pen3-5, that encodes a dysfunctional protein that accumulates in planta like wild-type PEN3. The specific mutation in pen3-5 uncouples PEN3 functions in IBA-stimulated root growth modulation, callose deposition induced with a conserved peptide epitope of bacterial flagellin (flg22), and pathogen-inducible salicylic acid accumulation from PEN3 activity in extracellular defense, indicating the engagement of multiple PEN3 substrates in different PEN3-dependent biological processes. We identified 4-O-β-D-glucosyl-indol-3-yl formamide (4OGlcI3F) as a pathogen-inducible, tryptophan-derived compound that overaccumulates in pen3 leaf tissue and has biosynthesis that is dependent on an intact PEN2 metabolic pathway. We propose that a precursor of 4OGlcI3F is the PEN3 substrate in extracellular pathogen defense. These precursors, the shared indole core present in IBA and 4OGlcI3F, and allele-specific uncoupling of a subset of PEN3 functions suggest that PEN3 transports distinct indole-type metabolites in distinct biological processes.

PMID:
26023163
PMCID:
PMC4741342
DOI:
10.1104/pp.15.00182
[Indexed for MEDLINE]
Free PMC Article

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