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

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 48, 2016, Pages 13917-13922

  Westfall, Corey S ^a   Sherp, Ashley M ^a   Zubieta, Chloe ^b   Alvarez, Sophie ^c   Schraft, Evelyn ^a   Marcellin, Romain ^d   Ramirez, Loren ^a   Jez, Joseph M ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b UNIV GRENOBLE ALPES   (France)

^c DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^d EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

Author keywords

Arabidopsis; Auxin; Plant biochemistry; Plant hormone; Protein structure

Indexed keywords

ACYLACID AMIDO SYNTHETASE; AUXIN; BENZOIC ACID; INDOLEACETIC ACID; PHENYLACETIC ACID; SALICYLIC ACID; SYNTHETASE; UNCLASSIFIED DRUG; AMINO ACID; ARABIDOPSIS PROTEIN; GH3.5 PROTEIN, ARABIDOPSIS; INDOLEACETIC ACID DERIVATIVE; LIGASE;

ARABIDOPSIS THALIANA; ARTICLE; BINDING SITE; BIOCHEMICAL ANALYSIS; ENZYME ACTIVITY; HOMEOSTASIS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY; ARABIDOPSIS; CHEMISTRY; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

AMINO ACIDS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; INDOLEACETIC ACIDS; LIGASES; SALICYLIC ACID; SUBSTRATE SPECIFICITY;

EID: 84999098905     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1612635113     Document Type: Article

References (44)

1. Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64(9):2541-2555.
2. Westfall CS, Muehler AM, Jez JM (2013) Enzyme action in the regulation of plant hormone responses. J Biol Chem 288(27):19304-19311.
3. Staswick PE, Tiryaki I, Rowe ML (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14(6):1405-1415.
4. Fonseca S, et al. (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5(5):344-350.
5. Meesters C, et al. (2014) A chemical inhibitor of jasmonate signaling targets JAR1 in Arabidopsis thaliana. Nat Chem Biol 10(10):830-836.
6. LeClere S, Tellez R, Rampey RA, Matsuda SP, Bartel B (2002) Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis. J Biol Chem 277(23):20446-20452.
7. Staswick PE, et al. (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17(2):616-627.
8. Westfall CS, Herrmann J, Chen Q, Wang S, Jez JM (2010) Modulating plant hormones by enzyme action: The GH3 family of acyl acid amido synthetases. Plant Signal Behav 5(12):1607-1612.
9. Westfall CS, et al. (2012) Structural basis for prereceptor modulation of plant hormones by GH3 proteins. Science 336(6089):1708-1711.
10. Gulick AM (2009) Conformational dynamics in the Acyl-CoA synthetases, adenylation domains of non-ribosomal peptide synthetases, and firefly luciferase. ACS Chem Biol 4(10):811-827.
11. Chen Q, Zhang B, Hicks LM, Wang S, Jez JM (2009) A liquid chromatography-tandem mass spectrometry-based assay for indole-3-acetic acid-amido synthetase. Anal Biochem 390(2):149-154.
12. Chen Q, Westfall CS, Hicks LM, Wang S, Jez JM (2010) Kinetic basis for the conjugation of auxin by a GH3 family indole-acetic acid-amido synthetase. J Biol Chem 285(39):29780-29786.
13. Peat TS, et al. (2012) Crystal structure of an indole-3-acetic acid amido synthetase from grapevine involved in auxin homeostasis. Plant Cell 24(11):4525-4538.
14. Round A, et al. (2013) Determination of the GH3.12 protein conformation through HPLC-integrated SAXS measurements combined with X-ray crystallography. Acta Crystallogr D Biol Crystallogr 69(Pt 10):2072-2080.
15. Takase T, et al. (2004) ydk1-D, an auxin-responsive GH3 mutant that is involved in hypocotyl and root elongation. Plant J 37(4):471-483.
16. Park JE, et al. (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282(13):10036-10046.
17. Zhang Z, et al. (2007) Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis-Pseudomonas syringae interaction. Plant Physiol 145(2):450-464.
18. Nakazawa M, et al. (2001) DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length. Plant J 25(2):213-221.
19. Khan S, Stone JM (2007) Arabidopsis thaliana GH3.9 influences primary root growth. Planta 226(1):21-34.
20. Zheng Z, et al. (2016) Local auxin metabolism regulates environment-induced hypocotyl elongation. Nat Plants 2:16025.
21. Park JE, et al. (2007) An Arabidopsis GH3 gene, encoding an auxin-conjugating enzyme, mediates phytochrome B-regulated light signals in hypocotyl growth. Plant Cell Physiol 48(8):1236-1241.
22. Zhang Z, Wang M, Li Z, Li Q, He Z (2008) Arabidopsis GH3.5 regulates salicylic acid-dependent and both NPR1-dependent and independent defense responses. Plant Signal Behav 3(8):537-542.
23. Chen Y, Shen H, Wang M, Li Q, He Z (2013) Salicyloyl-aspartate synthesized by the acetyl-amido synthetase GH3.5 is a potential activator of plant immunity in Arabidopsis. Acta Biochim Biophys Sin (Shanghai) 45(10):827-836.
24. Terol J, Domingo C, Talón M (2006) The GH3 family in plants: Genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371(2):279-290.
25. Okrent RA, Brooks MD, Wildermuth MC (2009) Arabidopsis GH3.12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate. J Biol Chem 284(15):9742-9754.
26. Reger AS, Carney JM, Gulick AM (2007) Biochemical and crystallographic analysis of substrate binding and conformational changes in acetyl-CoA synthetase. Biochemistry 46(22):6536-6546.
27. Yadavalli SS, Ibba M (2012) Quality control in aminoacyl-tRNA synthesis its role in translational fidelity. Adv Protein Chem Struct Biol 86:1-43.
28. Manandhar M, Cronan JE (2013) Proofreading of noncognate acyl adenylates by an acyl-coenzyme a ligase. Chem Biol 20(12):1441-1446.
29. Ding X, et al. (2008) Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell 20(1):228-240.
30. Domingo C, Andrés F, Tharreau D, Iglesias DJ, Talón M (2009) Constitutive expression of OsGH3.1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice. Mol Plant Microbe Interact 22(2):201-210.
31. Zhang SW, et al. (2009) Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant Physiol 151(4):1889-1901.
32. Sugawara S, et al. (2015) Distinct characteristics of indole-3-acetic acid and phenylacetic acid, two common auxins in plants. Plant Cell Physiol 56(8):1641-1654.
33. Cook SD, et al. (2016) Auxin biosynthesis: Are the indole-3-acetic acid and phenylacetic acid biosynthesis pathways mirror images? Plant Physiol 171(2):1230-1241.
34. Yan S, Dong X (2014) Perception of the plant immune signal salicylic acid. Curr Opin Plant Biol 20:64-68.
35. Widhalm JR, Dudareva N (2015) A familiar ring to it: Biosynthesis of plant benzoic acids. Mol Plant 8(1):83-97.
36. León J, Shulaev V, Yalpani N, Lawton MA, Raskin I (1995) Benzoic acid 2-hydroxylase, a soluble oxygenase from tobacco, catalyzes salicylic acid biosynthesis. Proc Natl Acad Sci USA 92(22):10413-10417.
37. Chong J, et al. (2001) Free and conjugated benzoic acid in tobacco plants and cell cultures. Induced accumulation upon elicitation of defense responses and role as salicylic acid precursors. Plant Physiol 125(1):318-328.
38. Kabsch W (2010) XDS. Acta Crystallogr D Biol Crystallogr 66(Pt 2):125-132.
39. de la Fortelle E, Bricogne G (1997) Maximum-likelihood heavy-atom parameter refinement for the multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol 276:472-494.
40. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: A web-based environment for protein structure homology modelling. Bioinformatics 22(2):195-201.
41. Blanc E, et al. (2004) Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1):2210-2221.
42. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1):2126-2132.
43. Adams PD, et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66(Pt 2):213-221.
44. Earley KW, et al. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45(4):616-629.