Crystal Structure of an Indole-3-Acetic Acid Amido Synthetase from Grapevine Involved in Auxin Homeostasis

Peat, Thomas S.; Böttcher, Christine; Newman, Janet; Lucent, Del; Cowieson, Nathan; Davies, Christopher

doi:10.1105/tpc.112.102921

Cited by 83 publications

(88 citation statements)

References 57 publications

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“…2B). The architecture of the AMP binding site is nearly identical to those described for previously reported GH3 protein structures (9,13,14). Sequence comparison of AtGH3.5 with the IAA-conjugating AtGH3.1, AtGH3.2, AtGH3.17, and VvGH3.1, the JA-Ile biosynthesis enzyme AtGH3.11, and the benzoate-conjugating AtGH3.12 emphasizes the similarity of this site across GH3 proteins that recognize diverse acyl acid substrates (Fig.…”

Section: Resultsmentioning

confidence: 53%

“…This orientation would be a catalytically nonproductive binding orientation and likely results from charge repulsion between the negatively charged carboxylate of IAA and the phosphate of AMP. Peat et al (13) reported the structure of VvGH3.1 in complex with an inhibitor (adenosine-5′-[2-(1H-indol-3-yl)ethyl]phosphate; AIEP) that mimics the IAA reaction intermediate. An overlay of VvGH3.1 and AtGH3.5 highlights the similarity in IAA binding ( Fig.…”

Section: Resultsmentioning

confidence: 99%

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Arabidopsis thaliana GH3.5 acyl acid amido synthetase mediates metabolic crosstalk in auxin and salicylic acid homeostasis

Westfall

Sherp

Zubieta

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

142

170

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InArabidopsis thaliana, the acyl acid amido synthetase Gretchen Hagen 3.5 (AtGH3.5) conjugates both indole-3-acetic acid (IAA) and salicylic acid (SA) to modulate auxin and pathogen response pathways. To understand the molecular basis for the activity of AtGH3.5, we determined the X-ray crystal structure of the enzyme in complex with IAA and AMP. Biochemical analysis demonstrates that the substrate preference of AtGH3.5 is wider than originally described and includes the natural auxin phenylacetic acid (PAA) and the potential SA precursor benzoic acid (BA). Residues that determine IAA versus BA substrate preference were identified. The dual functionality of AtGH3.5 is unique to this enzyme although multiple IAA-conjugating GH3 proteins share nearly identical acyl acid binding sites.In plantaanalysis of IAA, PAA, SA, and BA and their respective aspartyl conjugates were determined in wild-type and overexpressing lines ofA.thaliana. This study suggests that AtGH3.5 conjugates auxins (i.e., IAA and PAA) and benzoates (i.e., SA and BA) to mediate crosstalk between different metabolic pathways, broadening the potential roles for GH3 acyl acid amido synthetases in plants.

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Section: Resultsmentioning

confidence: 53%

Section: Resultsmentioning

confidence: 99%

Arabidopsis thaliana GH3.5 acyl acid amido synthetase mediates metabolic crosstalk in auxin and salicylic acid homeostasis

Westfall

Sherp

Zubieta

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

142

170

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“…They show the protein complex in an unanticipated conformation leading to reorganization of the substrate-binding site, which may aid the nucleophilic attack during catalysis. To substantiate this theory, we superposed the FIN219 structure with open-form AtGH3.12 and closed-form VvGH3.1 (PDB ID code 4B2G) from grapevine (Vitis vinifera) (39). An ATP analog, α,β-methylene adenosine 5′-triphosphate (AMPCPP) in the AtGH3.12 structure, shows a similar binding position to the inhibitor adenosine-5′-[2-(1H-indol-3-yl)ethyl]phosphate (AIEP) in the VvGH3.1 structure.…”

Section: Resultsmentioning

confidence: 99%

Structural basis of jasmonate-amido synthetase FIN219 in complex with glutathione S-transferase FIP1 during the JA signal regulation

Chen

Kuo

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Far-red (FR) light-coupled jasmonate (JA) signaling is necessary for plant defense and development. FR insensitive 219 (FIN219) is a member of the Gretchen Hagen 3 (GH3) family of proteins in Arabidopsis and belongs to the adenylate-forming family of enzymes. It directly controls biosynthesis of jasmonoyl-isoleucine in JA-mediated defense responses and interacts with FIN219-interacting protein 1 (FIP1) under FR light conditions. FIN219 and FIP1 are involved in FR light signaling and are regulators of the interplay between light and JA signaling. However, how their interactions affect plant physiological functions remains unclear. Here, we demonstrate the crystal structures of FIN219-FIP1 while binding with substrates at atomic resolution. Our results show an unexpected FIN219 conformation and demonstrate various differences between this protein and other members of the GH3 family. We show that the rotated C-terminal domain of FIN219 alters ATP binding and the core structure of the active site. We further demonstrate that this unique FIN219-FIP1 structure is crucial for increasing FIN219 activity and determines the priority of substrate binding. We suggest that the increased FIN219 activity resulting from the complex form, a conformation for domain switching, allows FIN219 to switch to its high-affinity mode and thereby enhances JA signaling under continuous FR light conditions. jasmonate response | far-red light | signaling cross-talk | adenylation enzyme | phytohormone F ar-red (FR) insensitive 219 (FIN219) (1), also known as jasmonate (JA) resistant 1 (JAR1; AtGH3.11) (2), is a member of the auxin-regulated Gretchen Hagen 3 (GH3) family of proteins (3). The GH3 family in Arabidopsis is composed of 19 distinct proteins and is also conserved in plants such as rice (4-6), tomato (7,8), and maize (9), with 13, 15, and 13 members, respectively. Phylogenetically, the GH3 family is classified as part of the adenylate-forming enzyme superfamily, which contains proteins such as firefly luciferase-like enzymes (10). This diverse group of enzymes catalyzes the addition of AMP to carboxyl groups on a wide variety of substrates and typically contains three conserved motifs that form a binding pocket for ATP and AMP substrate intermediates (11). GH3 proteins regulate the activity of plant hormones through amino acid conjugation and have a substantial effect on plant metabolism and physiology (12). For example, FIN219 catalyzes the conjugation of isoleucine (Ile) to JA, forming jasmonoyl-isoleucine (JA-Ile). This reaction results in the degradation of the transcriptional repressor JA-ZIM (zinc-finger protein expressed in inflorescence meristem) domain (JAZ) proteins and the subsequent activation of downstream transcriptional responses (13).FIN219 has been identified in suppressor screenings using a temperature sensitive constitutive photomorphogenic 1 (cop1) mutant line. It is involved in FR light-mediated inhibition of hypocotyl elongation and regulates light inactivation of COP1 activity (1). Furthermore, FIN219 acts as a ...

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“…Although mutants of AtGH3.12/PBS3 display SA-related phenotypes in Arabidopsis, SA is not a substrate of this protein, and the physiologically relevant substrate is not known (94). The grapevine protein (VvGH3.1) conjugates IAA with aspartate (96). These structures define the overall GH3 fold as a large N-terminal domain with a ␤-barrel and two ␤-sheets flanked by ␣-helices and a smaller C-terminal domain consisting of a single four-stranded ␤-sheet flanked by two ␣-helices on each side (Fig.…”

Section: Plant Hormone-amino Acid Conjugationmentioning

confidence: 99%

“…Across the structures, the nucleotide site is identical to residues conserved in not only GH3 proteins but also the ANL superfamily (83,95,96). Three motifs define this site.…”

Section: Plant Hormone-amino Acid Conjugationmentioning

confidence: 99%

Enzyme Action in the Regulation of Plant Hormone Responses

Westfall

Muehler

Jez

2013

Journal of Biological Chemistry

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Plants synthesize a chemically diverse range of hormones that regulate growth, development, and responses to environmental stresses. The major classes of plant hormones are specialized metabolites with exquisitely tailored perception and signaling systems, but equally important are the enzymes that control the dose and exposure to the bioactive forms of these molecules. Here, we review new insights into the role of enzyme families, including the SABATH methyltransferases, the methylesterases, the GH3 acyl acid-amido synthetases, and the hormone peptidyl hydrolases, in controlling the biosynthesis and modifications of plant hormones and how these enzymes contribute to the network of chemical signals responsible for plant growth, development, and environmental adaptation.

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Crystal Structure of an Indole-3-Acetic Acid Amido Synthetase from Grapevine Involved in Auxin Homeostasis

Cited by 83 publications

References 57 publications

Arabidopsis thaliana GH3.5 acyl acid amido synthetase mediates metabolic crosstalk in auxin and salicylic acid homeostasis

Arabidopsis thaliana GH3.5 acyl acid amido synthetase mediates metabolic crosstalk in auxin and salicylic acid homeostasis

Structural basis of jasmonate-amido synthetase FIN219 in complex with glutathione S-transferase FIP1 during the JA signal regulation

Enzyme Action in the Regulation of Plant Hormone Responses

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