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Brassicaceae-specific Gretchen Hagen 3 acyl acid amido synthetases conjugate amino acids to chorismate, a precursor of aromatic amino acids and salicylic acid.
J Biol Chem. 2019 11 08; 294(45):16855-16864.JB

Abstract

To modulate responses to developmental or environmental cues, plants use Gretchen Hagen 3 (GH3) acyl acid amido synthetases to conjugate an amino acid to a plant hormone, a reaction that regulates free hormone concentration and downstream responses. The model plant Arabidopsis thaliana has 19 GH3 proteins, of which 8 have confirmed biochemical functions. One Brassicaceae-specific clade of GH3 proteins was predicted to use benzoate as a substrate and includes AtGH3.7 and AtGH3.12/PBS3. Previously identified as a 4-hydroxybenzoic acid-glutamate synthetase, AtGH3.12/PBS3 influences pathogen defense responses through salicylic acid. Recent work has shown that AtGH3.12/PBS3 uses isochorismate as a substrate, forming an isochorismate-glutamate conjugate that converts into salicylic acid. Here, we show that AtGH3.7 and AtGH3.12/PBS3 can also conjugate chorismate to cysteine and glutamate, which act as precursors to aromatic amino acids and salicylic acid, respectively. The X-ray crystal structure of AtGH3.12/PBS3 in complex with AMP and chorismate at 1.94 Å resolution, along with site-directed mutagenesis, revealed how the active site potentially accommodates this substrate. Examination of Arabidopsis knockout lines indicated that the gh3.7 mutants do not alter growth and showed no increased susceptibility to the pathogen Pseudomonas syringae, unlike gh3.12 mutants, which were more susceptible than WT plants, as was the gh3.7/gh3.12 double mutant. The findings of our study suggest that GH3 proteins can use metabolic precursors of aromatic amino acids as substrates.

Authors+Show Affiliations

Department of Biology, Washington University, St. Louis, Missouri 63130.Department of Biology, Washington University, St. Louis, Missouri 63130.Department of Biology, Washington University, St. Louis, Missouri 63130.Department of Biology, Washington University, St. Louis, Missouri 63130.Laboratoire de Physiologie Cellulaire & Végétale, University Grenoble Alpes, CNRS, CEA, INRA, IRIG, Grenoble, France.Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, Nebraska 68583.Department of Biology, Washington University, St. Louis, Missouri 63130 jjez@wustl.edu.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

31575658

Citation

Holland, Cynthia K., et al. "Brassicaceae-specific Gretchen Hagen 3 Acyl Acid Amido Synthetases Conjugate Amino Acids to Chorismate, a Precursor of Aromatic Amino Acids and Salicylic Acid." The Journal of Biological Chemistry, vol. 294, no. 45, 2019, pp. 16855-16864.
Holland CK, Westfall CS, Schaffer JE, et al. Brassicaceae-specific Gretchen Hagen 3 acyl acid amido synthetases conjugate amino acids to chorismate, a precursor of aromatic amino acids and salicylic acid. J Biol Chem. 2019;294(45):16855-16864.
Holland, C. K., Westfall, C. S., Schaffer, J. E., De Santiago, A., Zubieta, C., Alvarez, S., & Jez, J. M. (2019). Brassicaceae-specific Gretchen Hagen 3 acyl acid amido synthetases conjugate amino acids to chorismate, a precursor of aromatic amino acids and salicylic acid. The Journal of Biological Chemistry, 294(45), 16855-16864. https://doi.org/10.1074/jbc.RA119.009949
Holland CK, et al. Brassicaceae-specific Gretchen Hagen 3 Acyl Acid Amido Synthetases Conjugate Amino Acids to Chorismate, a Precursor of Aromatic Amino Acids and Salicylic Acid. J Biol Chem. 2019 11 8;294(45):16855-16864. PubMed PMID: 31575658.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Brassicaceae-specific Gretchen Hagen 3 acyl acid amido synthetases conjugate amino acids to chorismate, a precursor of aromatic amino acids and salicylic acid. AU - Holland,Cynthia K, AU - Westfall,Corey S, AU - Schaffer,Jason E, AU - De Santiago,Alejandro, AU - Zubieta,Chloe, AU - Alvarez,Sophie, AU - Jez,Joseph M, Y1 - 2019/10/01/ PY - 2019/06/25/received PY - 2019/09/29/revised PY - 2019/10/3/pubmed PY - 2020/6/11/medline PY - 2019/10/3/entrez KW - Arabidopsis thaliana KW - X-ray crystallography KW - enzyme KW - plant biochemistry KW - substrate specificity SP - 16855 EP - 16864 JF - The Journal of biological chemistry JO - J Biol Chem VL - 294 IS - 45 N2 - To modulate responses to developmental or environmental cues, plants use Gretchen Hagen 3 (GH3) acyl acid amido synthetases to conjugate an amino acid to a plant hormone, a reaction that regulates free hormone concentration and downstream responses. The model plant Arabidopsis thaliana has 19 GH3 proteins, of which 8 have confirmed biochemical functions. One Brassicaceae-specific clade of GH3 proteins was predicted to use benzoate as a substrate and includes AtGH3.7 and AtGH3.12/PBS3. Previously identified as a 4-hydroxybenzoic acid-glutamate synthetase, AtGH3.12/PBS3 influences pathogen defense responses through salicylic acid. Recent work has shown that AtGH3.12/PBS3 uses isochorismate as a substrate, forming an isochorismate-glutamate conjugate that converts into salicylic acid. Here, we show that AtGH3.7 and AtGH3.12/PBS3 can also conjugate chorismate to cysteine and glutamate, which act as precursors to aromatic amino acids and salicylic acid, respectively. The X-ray crystal structure of AtGH3.12/PBS3 in complex with AMP and chorismate at 1.94 Å resolution, along with site-directed mutagenesis, revealed how the active site potentially accommodates this substrate. Examination of Arabidopsis knockout lines indicated that the gh3.7 mutants do not alter growth and showed no increased susceptibility to the pathogen Pseudomonas syringae, unlike gh3.12 mutants, which were more susceptible than WT plants, as was the gh3.7/gh3.12 double mutant. The findings of our study suggest that GH3 proteins can use metabolic precursors of aromatic amino acids as substrates. SN - 1083-351X UR - https://www.unboundmedicine.com/medline/citation/31575658/Brassicaceae_specific_Gretchen_Hagen_3_acyl_acid_amido_synthetases_conjugate_amino_acids_to_chorismate_a_precursor_of_aromatic_amino_acids_and_salicylic_acid_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0021-9258(20)30528-7 DB - PRIME DP - Unbound Medicine ER -