Inactive methyl indole-3-acetic acid ester can be hydrolyzed and activated by several esterases belonging to the AtMES esterase family of arabidopsis

Plant Physiology

Volumn 147, Issue 3, 2008, Pages 1034-1045

  Yang, Yue ^a,c   Xu, Richard ^a   Ma, Choong Je ^a,d   Vlot, A Corina ^b,e   Klessig, Daniel F ^b   Pichersky, Eran ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

^d Kangwon National University   (South Korea)

^e MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA TABACUM;

ARABIDOPSIS PROTEIN; AXR1 PROTEIN, ARABIDOPSIS; BETA GLUCURONIDASE; INDOLEACETIC ACID DERIVATIVE; METHYL ETHERASE; O DEMETHYLASE; PHYTOHORMONE; SYNTHETIC DNA;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; HYDROLYSIS; METABOLISM; MOLECULAR GENETICS; PHENOTYPE; PLANT GROWTH; PLANT ROOT; REPORTER GENE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION; GENES, REPORTER; GENES, SYNTHETIC; GENOME, PLANT; GLUCURONIDASE; HYDROLYSIS; HYPOCOTYL; INDOLEACETIC ACIDS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; OXIDOREDUCTASES, O-DEMETHYLATING; PHENOTYPE; PLANT GROWTH REGULATORS; PLANT ROOTS; SUBSTRATE SPECIFICITY;

EID: 51549107429     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.118224     Document Type: Article

References (62)

1. Bartel B, Fink G (1995) ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. Science 268: 1745-1748
2. Baudouin E, Charpenteau M, Roby D, Marco Y, Ranjeva R, Ranty B (1997) Functional expression of a tobacco gene related to the serine hydrolase family-esterase activity towards short-chain dinitrophenyl acylesters. Eur J Biochem 248: 700-706
3. Boerjan W, Cervera MT, Delarue M, Beeckman T, Dewitte W, Bellini C, Caboche M, Onckelen HV, Montagu MV, Inze D (1995) superroot, A recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7: 1405-1419
4. Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318: 801-806
5. Chen F, D'Auria JC, Tholl D, Ross JR, Gershenzon J, Noel JP, Pichersky E (2003) An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J 36: 577-588
6. Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19: 2430-2439
7. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
8. Collett CE, Harberd NP, Leyser O (2000) Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol 124: 553-562
9. D'Auria JC, Chen F, Pichersky E (2002) Characterization of an acyltransferase capable of synthesizing benzylbenzoate and other volatile esters in flowers and damaged leaves of Clarkia breweri. Plant Physiol 130: 466-476
10. Delker C, Raschke A, Quint M (2008) Auxin dynamics: the dazzling complexity of a small molecule's message. Planta 227: 929-941
11. Ding X, Cao Y, Huang L, Zhao J, Xu C, Li X, Wang S (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: 228-240
12. Dogru E, Warzecha H, Seibel F, Haebel S, Lottspeich F, Stöckigt J (2000) The gene encoding polyneuridine aldehyde esterase of monoterpenoid indole alkaloid biosynthesis in plants is an ortholog of the alpha/beta hydrolase super family. Eur J Biochem 267: 1397-1406
13. Evans ML (1985) The action of auxin on plant-cell elongation. Crc Crit Rev Plant Sci 2: 317-365
14. Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang Y, Acton TB, Montelione GT, Pichersky E, et al (2005) Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc Natl Acad Sci USA 102: 1773-1778
15. Fridman E, Wang J, Iijima Y, Froehlich JE, Gang DR, Ohlrogge J, Pichersky E (2005) Metabolic, genomic, and biochemical analyses of glandular trichomes from the wild tomato species Lycopersicon hirsutum identify a key enzyme in the biosynthesis of methylketones. Plant Cell 17: 1252-1267
16. Hartley JL, Temple GF, Brasch MA (2000) DNA cloning using in vitro site-specific recombination. Genome Res 10: 1788-1795
17. Hikage T, Saitoh Y, Tanaka-Saito C, Hagami H, Satou F, Shimotai Y, Nakano Y, Takahashi M, Takahata Y, Tsutsumi K (2007) Structure and allele-specific expression variation of novel alpha/beta hydrolase fold proteins in gentian plants. Mol Genet Genomics 278: 95-104
18. Holmquist M (2000) Alpha beta-hydrolase fold enzymes structures, functions and mechanisms. Curr Protein Pept Sci 1: 209-235
19. Ichinose Y, Hisayasu Y, Sanematsu S, Ishiga Y, Seki H, Toyoda K, Shiraishi T, Yamada T (2001) Molecular cloning and functional analysis of pea cDNA E86 encoding homologous protein to hypersensitivity-related hsr203J. Plant Sci 160: 997-1006
20. Jackson RG, Lim EK, Li Y, Kowalczyk M, Sandberg G, Hoggett J, Ashford DA, Bowles DJ (2001) Identification and biochemical characterization of an Arabidopsis indole-3-acetic acid glucosyltransferase. J Biol Chem 276: 4350-4356
21. Jensen PJ, Hangarter RP, Estelle M (1998) Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis. Plant Physiol 116: 455-462
22. Ko MK, Jeon WB, Kim KS, Lee HH, Seo HH, Kim YS, Oh BJ (2005) A Colletotrichum gloeosporioides-induced esterase gene of nonclimacteric pepper (Capsicum annuum) fruit during ripening plays a role in resistance against fungal infection. Plant Mol Biol 58: 529-541
23. Kumar D, Klessig DF (2003) High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proc Natl Acad Sci USA 100: 16101-16106
24. LeClere S, Tellez R, Rampey RA, Matsuda SPT, Bartel B (2002) Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis. J Biol Chem 277: 20446-20452
25. Leyser HM, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle M (1993) Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364: 161-164
26. Li L, Hou X, Tsuge T, Ding M, Aoyama T, Oka A, Gu H, Zhao Y, Qu LJ (2008) The possible action mechanisms of indole-3-acetic acid methyl ester in Arabidopsis. Plant Cell Rep 27: 575-584
27. Lincoln C, Britton JH, Estelle M (1990) Growth and development of the Axr1 mutants of Arabidopsis. Plant Cell 2: 1071-1080
28. Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol 50: 309-332
29. Marshall SG, Putterill J, Plummer K, Newcomb R (2003) The carboxylesterase gene family from Arabidopsis thaliana. J Mol Evol V57: 487-500
30. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473-497
31. Nakamura A, Higuchi K, Goda H, Fujiwara MT, Sawa S, Koshiba T, Shimada Y, Yoshida S (2003) Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol 133: 1843-1853
32. Nam KH, Dudareva N, Pichersky E (1999) Characterization of benzylalcohol acetyltransferases in scented and non-scented Clarkia species. Plant Cell Physiol 40: 916-923
33. Narasimhan K, Basheer C, Bajic VB, Swarup S (2003) Enhancement of plant-microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132: 146-153
34. Nardini M, Dijkstra BW (1999) Alpha/beta hydrolase fold enzymes: the family keeps growing. Curr Opin Struct Biol 9: 732-737
35. Normanly J (1997) Auxin metabolism. Physiol Plant 100: 431-442
36. Nowacki J, Bandurski RS (1980) Myoinositol esters of indole-3-acetic-acid as seed auxin precursors of Zea Mays L. Plant Physiol 65: 422-427
37. Ottenschlager I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, Ishikawa H, Evans M, Palme K (2003) Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci USA 100: 2987-2991
38. Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318: 113-116
39. Pontier D, Godiard L, Marco Y, Roby D (1994) Hsr203j, A tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions. Plant J 5: 507-521
40. Pontier D, Tronchet M, Rogowsky P, Lam E, Roby D (1998) Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death. Mol Plant Microbe Interact 11: 544-554
41. Qin G, Gu H, Zhao Y, Ma Z, Shi G, Yang Y, Pichersky E, Chen H, Liu M, Chen Z, et al (2005) Regulation of Arabidopsis leaf development by an indole-3-acetic acid carboxyl methyltransferase in Arabidopsis. Plant Cell 17: 2693-2704
42. Rampey RA, LeClere S, Kowalczyk M, Ljung K, Sandberg G, Bartel B (2004) A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol 135: 978-988
43. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37: 501-506
44. Shulaev V, Silverman P, Raskin I (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385: 718-721
45. Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17: 616-627
46. Stuhlfelder C, Mueller MJ, Warzecha H (2004) Cloning and expression of a tomato cDNA encoding a methyl jasmonate cleaving esterase. Eur J Biochem 271: 2976-2983
47. Tan X, Calderon-Villalobos LIA, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446: 640-645
48. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7: 847-859
49. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The clustalx windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24: 4876-4882
50. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971
51. Vandenbussche F, Verbelen P, Van Der Straeten D (2005) Of light and length: regulation of hypocotyl growth in Arabidopsis. Bioessays 27: 275-284
52. Varbanova M, Yamaguchi S, Yang Y, McKelvey K, Hanada A, Borochov R, Yu F, Jikumaru Y, Ross J, Cortes D, et al (2007) Methylation of gibberellins by Arabidopsis GAMT1 and GAMT2. Plant Cell 19: 32-45
53. Walden AR, Walter C, Gardner RC (1999) Genes expressed in Pinus radiata male cones include homologs to anther-specific and pathogenesis response genes. Plant Physiol 121: 1103-1116
54. Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot (Lond) 95: 707-735
55. Wu J, Wang L, Baldwin I (2008) Methyl jasmonate-elicited herbivore resistance: does MeJA function as a signal without being hydrolyzed to JA? Planta 227: 1161-1168
56. Yang Y, Varbanova M, Ross J, Wang G, Cortes D, Fridman E, Shulaev V, Noel JP, Pichersky E (2006a) Methylation and demethylation of plant signaling molecules. In JT Romeo, ed, Recent Advances in Phytochemistry, Ed 1, Vol 40. Elsevier Science, Oxford, p 253
57. Yang Y, Yuan JS, Ross J, Noel JP, Pichersky E, Chen F (2006b) An Arabidopsis thaliana methyltransferase capable of methylating farnesoic acid. Arch Biochem Biophys 448: 123-132
58. Zhao N, Ferrer J, Ross J, Guan J, Yang Y, Pichersky E, Noel JP, Chen F (2008) Structural, biochemical and phylogenetic analyses suggest that indole-3-acetic acid methyltransferase is an evolutionarily ancient member of the SABATH family. Plant Physiol 146: 455-467
59. Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16: 3100-3112
60. Zhao YD, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291: 306-309
61. Zimmerman P, Hitchcock AE (1937) Comparative effectiveness of acids, esters, and salts as growth substances and methods of evaluating them. Contrib. Boyce Thompson Inst 8: 337-350
62. Zubieta C, Ross JR, Koscheski P, Yang Y, Pichersky E, Noel JP (2003) Structural basis for substrate recognition in the salicylic acid carboxyl methyltransferase family. Plant Cell 15: 1704-1716