Endoplasmic reticulum-associated inactivation of the hormone jasmonoyl-L-isoleucine by multiple members of the cytochrome P450 94 family in Arabidopsis

Journal of Biological Chemistry

Volumn 289, Issue 43, 2014, Pages 29728-29738

  Koo, Abraham J ^a,d,e   Thireault, Caitlin ^a   Zemelis, Starla ^a   Poudel, Arati N ^d,e   Zhang, Tong ^d,e   Kitaoka, Naoki ^c   Brandizzi, Federica ^a   Matsuura, Hideyuki ^c   Howe, Gregg A ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c HOKKAIDO UNIVERSITY   (Japan)

^d University of Missouri   (United States)

^e UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; ENZYMES; METABOLISM; PHYSIOLOGY;

BIOSYNTHETIC PATHWAY; CYTOCHROMES P450; ENDOPLASMIC RETICULUM; INTRACELLULAR LEVELS; LOSS-OF-FUNCTION MUTANTS; PLANT IMMUNITIES; RECEPTOR COMPLEX; SUBCELLULAR LOCALIZATIONS;

PLANTS (BOTANY);

CYTOCHROME P450; CYTOCHROME P450 94 B1; CYTOCHROME P450 94 B3; JASMONOYL LEVO ISOLEUCINE; PHYTOHORMONE; PROTEIN COI1; PROTEIN JAZ; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ARABIDOPSIS PROTEIN; BACTERIAL DNA; CYCLOPENTANE DERIVATIVE; ISOLEUCINE; JASMONIC ACID; JASMONOYL-ISOLEUCINE; OXYLIPIN; PROTEIN BINDING; T-DNA;

AMINO ACID SEQUENCE; ARABIDOPSIS THALIANA; ARTICLE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; CYP94B1 GENE; ENDOPLASMIC RETICULUM; GROWTH INHIBITION; HOMEOSTASIS; HYDROXYLATION; IN VITRO STUDY; NONHUMAN; PLANT GENE; PLANT LEAF; POLLINATION; PROTEIN ASSEMBLY; PROTEIN DEPLETION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; ROOT GROWTH; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANTIBODY SPECIFICITY; ARABIDOPSIS; BIOCATALYSIS; CELL FRACTIONATION; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HYDROLYSIS; METABOLISM; MULTIGENE FAMILY; MUTATION; OXIDATION REDUCTION REACTION; PHENOTYPE; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOCATALYSIS; CYCLOPENTANES; CYTOCHROME P-450 ENZYME SYSTEM; DNA, BACTERIAL; ENDOPLASMIC RETICULUM; HOMEOSTASIS; HYDROLYSIS; ISOLEUCINE; METABOLIC NETWORKS AND PATHWAYS; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; MUTATION; ORGAN SPECIFICITY; OXIDATION-REDUCTION; OXYLIPINS; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; SUBCELLULAR FRACTIONS;

EID: 84908158261     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.603084     Document Type: Article

References (67)

1. Glazebrook, J. (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227
2. Wasternack, C., and Hause, B. (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Ann. Bot. 111, 1021-1058
3. McConn, M., and Browse, J. (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8, 403-416
4. Li, L., Zhao, Y., McCaig, B. C., Wingerd, B. A., Wang, J., Whalon, M. E., Pichersky, E., and Howe, G. A. (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16, 126-143
5. Zhang, Y., and Turner, J. (2008) Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PLoS ONE 3, e3699
6. Song, S., Qi, T., Wasternack, C., and Xie, D. (2014) Jasmonate signaling and crosstalk with gibberellin and ethylene. Curr. Opin. Plant Biol. 21, 112-119
7. Vanstraelen, M., and Benková, E. (2012) Hormonal interactions in the regulation of plant development. Annu. Rev. Cell Dev. Biol. 28, 463-487
8. Browse, J. (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu. Rev. Plant Biol. 60, 183-205
9. Koo, A. J., and Howe, G. A. (2009) The wound hormone jasmonate. Phytochemistry 70, 1571-1580
10. Fonseca, S., Chini, A., Hamberg, M., Adie, B., Porzel, A., Kramell, R., Miersch, O., Wasternack, C., and Solano, R. (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol. 5, 344-350
11. Schaller, A., and Stintzi, A. (2009) Enzymes in jasmonate biosynthesis - structure, function, regulation. Phytochemistry 70, 1532-1538
12. Westfall, C. S., Zubieta, C., Herrmann, J., Kapp, U., Nanao, M. H., and Jez, J. M. (2012) Structural basis for prereceptor modulation of plant hormones by GH3 proteins. Science 336, 1708-1711
13. Yan, Y., Stolz, S., Chételat, A., Reymond, P., Pagni, M., Dubugnon, L., and Farmer, E. E. (2007) A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19, 2470-2483
14. Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G., Nomura, K., He, S. Y., Howe, G. A., and Browse, J. (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448, 661-665
15. Chini, A., Fonseca, S., Fernández, G., Adie, B., Chico, J. M., Lorenzo, O., García-Casado, G., López-Vidriero, I., Lozano, F. M., Ponce, M. R., Micol, J. L., and Solano, R. (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666-671
16. Katsir, L., Schilmiller, A. L., Staswick, P. E., He, S. Y., and Howe, G. A. (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc. Natl. Acad. Sci. U.S.A. 105, 7100-7105
17. Yang, D. L., Yao, J., Mei, C. S., Tong, X. H., Zeng, L. J., Li, Q., Xiao, L. T., Sun, T. P., Li, J., Deng, X. W., Lee, C. M., Thomashow, M. F., Yang, Y., He, Z., and He, S. Y. (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc. Natl. Acad. Sci. U.S.A. 109, E1192-E1200
18. Noir, S., Bömer, M., Takahashi, N., Ishida, T., Tsui, T. L., Balbi, V., Shanahan, H., Sugimoto, K., and Devoto, A. (2013) Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode. Plant Physiol. 161, 1930-1951
19. Ullmann-Zeunert, L., Stanton, M. A., Wielsch, N., Bartram, S., Hummert, C., Svatoš, A., Baldwin, I. T., and Groten, K. (2013) Quantification of growth-defense trade-offs in a common currency: nitrogen required for phenolamide biosynthesis is not derived from ribulose-1,5-bisphosphate carboxylase/oxygenase turnover. Plant J. 75, 417-429
20. Koo, A. J., and Howe, G. A. (2012) Catabolism and deactivation of the lipid-derived hormone jasmonoyl-isoleucine. Front. Plant Sci. 3, 19
21. Huot, B., Yao, J., Montgomery, B. L., and He, S. Y. (2014) Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7, 1267-1287
22. Campos, M. L., Kang, J. H., and Howe, G. A. (2014) Jasmonate-triggered plant immunity. J. Chem. Ecol. 40, 657-675
23. Chung, H. S., Koo, A. J., Gao, X., Jayanty, S., Thines, B., Jones, A. D., and Howe, G. A. (2008) Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol. 146, 952-964
24. Moreno, J. E., Shyu, C., Campos, M. L., Patel, L. C., Chung, H. S., Yao, J., He, S. Y., and Howe, G. A. (2013) Negative feedback control of jasmonate signaling by an alternative splice variant of JAZ10. Plant Physiol. 162, 1006-1017
25. Chung, H. S., and Howe, G. A. (2009) A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Plant Cell 21, 131-145
26. Chung, H. S., Niu, Y., Browse, J., and Howe, G. A. (2009) Top hits in contemporary JAZ: an update on jasmonate signaling. Phytochemistry 70, 1547-1559
27. Shyu, C., Figueroa, P., Depew, C. L., Cooke, T. F., Sheard, L. B., Moreno, J. E., Katsir, L., Zheng, N., Browse, J., and Howe, G. A. (2012) JAZ8 lacks a canonical degron and has an EAR motif that mediates transcriptional repression of jasmonate responses in Arabidopsis. Plant Cell 24, 536-550
28. Nakata, M., Mitsuda, N., Herde, M., Koo, A. J., Moreno, J. E., Suzuki, K., Howe, G. A., and Ohme-Takagi, M. (2013) A bHLH-type transcription factor, ABA-inducible BHLH-type transcription factor/JA-associated MYC2-like1, acts as a repressor to negatively regulate jasmonate signaling in Arabidopsis. Plant Cell 25, 1641-1656
29. Sasaki-Sekimoto, Y., Jikumaru, Y., Obayashi, T., Saito, H., Masuda, S., Kamiya, Y., Ohta, H., and Shirasu, K. (2013) Basic helix-loop-helix transcription factors Jasmonate-associated MYC2-like1 (JAM1), JAM2, and JAM3 are negative regulators of jasmonate responses in Arabidopsis. Plant Physiol. 163, 291-304
30. Song, S., Qi, T., Fan, M., Zhang, X., Gao, H., Huang, H., Wu, D., Guo, H., and Xie, D. (2013) The bHLH subgroup IIId factors negatively regulate jasmonate-mediated plant defense and development. PLoS Genet. 9, e1003653
31. Fonseca, S., Fernández-Calvo, P., Fernández, G. M., Díez-Díaz, M., Gimenez-Ibanez, S., Lopez-Vidriero, I., Godoy, M., Fernández-Barbero, G., Van Leene, J., De Jaeger, G., Franco-Zorrilla, J. M., and Solano, R. (2014) bHLH003, bHLH013 and bHLH017 are new targets of JAZ repressors negatively regulating JA responses. PLoS ONE 9, e86182
32. Woldemariam, M. G., Onkokesung, N., Baldwin, I. T., and Galis, I. (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulates jasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores. Plant J. 72, 758-767
33. Bhosale, R., Jewell, J. B., Hollunder, J., Koo, A. J., Vuylsteke, M., Michoel, T., Hilson, P., Goossens, A., Howe, G. A., Browse, J., and Maere, S. (2013) Predicting gene function from uncontrolled expression variation among individual wild-type Arabidopsis plants. Plant Cell 25, 2865-2877
34. Widemann, E., Miesch, L., Lugan, R., Holder, E., Heinrich, C., Aubert, Y., Miesch, M., Pinot, F., and Heitz, T. (2013) The amidohydrolases IAR3 and ILL6 contribute to jasmonoyl-isoleucine hormone turnover and generate 12-hydroxyjasmonic acid upon wounding in Arabidopsis leaves. J. Biol. Chem. 288, 31701-31714
35. Glauser, G., Grata, E., Dubugnon, L., Rudaz, S., Farmer, E. E., and Wolfender, J. L. (2008) Spatial and temporal dynamics of jasmonate synthesis and accumulation in Arabidopsis in response to wounding. J. Biol. Chem. 283, 16400-16407
36. Guranowski, A., Miersch, O., Staswick, P. E., Suza, W., and Wasternack, C. (2007) Substrate specificity and products of side-reactions catalyzed by jasmonate:amino acid synthetase (JAR1). FEBS Lett. 581, 815-820
37. Kitaoka, N., Kawaide, H., Amano, N., Matsubara, T., Nabeta, K., Takahashi, K., and Matsuura, H. (2014) CYP94B3 activity against jasmonic acid amino acid conjugates and the elucidation of 12-O-β-glucopyranosyl-jasmonoyl-L-isoleucine as an additional metabolite. Phytochemistry 99, 6-13
38. Koo, A. J., Cooke, T. F., and Howe, G. A. (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine. Proc. Natl. Acad. Sci. U.S.A. 108, 9298-9303
39. Kitaoka, N., Matsubara, T., Sato, M., Takahashi, K., Wakuta, S., Kawaide, H., Matsui, H., Nabeta, K., and Matsuura, H. (2011) Arabidopsis CYP94B3 encodes jasmonyl-L-isoleucine 12-hydroxylase, a key enzyme in the oxidative catabolism of jasmonate. Plant Cell Physiol. 52, 1757-1765
40. Heitz, T., Widemann, E., Lugan, R., Miesch, L., Ullmann, P., Désaubry, L., Holder, E., Grausem, B., Kandel, S., Miesch, M., Werck-Reichhart, D., and Pinot, F. (2012) Cytochromes P450 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone Jasmonoyl-isoleucine for catabolic turnover. J. Biol. Chem. 287, 6296-6306
41. Koo, A. J. K., Chung, H. S., Kobayashi, Y., and Howe, G. A. (2006) Identification of a peroxisomal acyl-activating enzyme involved in the biosynthesis of jasmonic acid in Arabidopsis. J. Biol. Chem. 281, 33511-33520
42. Herde, M., Koo, A. K., and Howe, G. (2013) Elicitation of jasmonate-mediated defense responses by mechanical wounding and insect herbivory in Jasmonate Signaling (Goossens, A., and Pauwels, L. eds), pp. 51-61, Humana Press
43. Schilmiller, A. L., Koo, A. J., and Howe, G. A. (2007) Functional diversification of acyl-coenzyme A oxidases in jasmonic acid biosynthesis and action. Plant Physiol. 143, 812-824
44. Brandizzi, F., Hanton, S., DaSilva, L. L., Boevink, P., Evans, D., Oparka, K., Denecke, J., and Hawes, C. (2003) ER quality control can lead to retrograde transport from the ER lumen to the cytosol and the nucleoplasm in plants. Plant J. 34, 269-281
45. Brandizzi, F., Fricker, M., and Hawes, C. (2002) A greener world: The revolution in plant bioimaging. Nat. Rev. Mol. Cell Biol. 3, 520-530
46. Pompon, D., Louerat, B., Bronine, A., and Urban, P. (1996) Yeast expression of animal and plant P450s in optimized redox environments. Methods Enzymol. 272, 51-64
47. Koo, A. J., Gao, X., Jones, A. D., and Howe, G. A. (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J. 59, 974-986
48. Kramell, R., Schmidt, J., Schneider, G., Sembdner, G., and Schreiber, K. (1988) Synthesis of N-(jasmonoyl) amino acid conjugates. Tetrahedron 44, 5791-5807
49. Werck-Reichhart, D. l., Bak, S. r., and Paquette, S. (2009) Cytochromes P450 in The Arabidopsis Book, The American Society of Plant Biologists, pp. 1-28
50. Sheard, L. B., Tan, X., Mao, H., Withers, J., Ben-Nissan, G., Hinds, T. R., Kobayashi, Y., Hsu, F. F., Sharon, M., Browse, J., He, S. Y., Rizo, J., Howe, G. A., and Zheng, N. (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468, 400-405
51. Hsieh, H. L., Okamoto, H., Wang, M., Ang, L. H., Matsui, M., Goodman, H., and Deng, X. W. (2000) FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Dev. 14, 1958-1970
52. Withers, J., Yao, J., Mecey, C., Howe, G. A., Melotto, M., and He, S. Y. (2012) Transcription factor-dependent nuclear localization of a transcriptional repressor in jasmonate hormone signaling. Proc. Natl. Acad. Sci. U.S.A. 109, 20148-20153
53. Yamamoto, K., Gildenberg, M., Ahuja, S., Im, S.-C., Pearcy, P., Waskell, L., and Ramamoorthy, A. (2013) Probing the transmembrane structure and topology of cicrosomal cytochrome-P450 by solid-state NMR on temperature-resistant bicelles. Sci. Rep. 3, 2556
54. Benveniste, I., Salaün, J.-P., and Durst, F. (1978) Phytochrome-mediated regulation of a monooxygenase hydroxylating cinnamic acid in etiolated pea seedlings. Phytochemistry 17, 359-363
55. Okuda, K. I. (1994) Liver mitochondrial P450 involved in cholesterol catabolism and vitamin D activation. J. Lipid Res. 35, 361-372
56. Froehlich, J. E., Itoh, A., and Howe, G. A. (2001) Tomato allene oxide synthase and fatty acid hydroperoxide lyase, two cytochrome P450s involved in oxylipin metabolism, are targeted to different membranes of chloroplast envelope. Plant Physiol. 125, 306-317
57. Helliwell, C. A., Sullivan, J. A., Mould, R. M., Gray, J. C., Peacock, W. J., and Dennis, E. S. (2001) A plastid envelope location of Arabidopsis entkaurene oxidase links the plastid and endoplasmic reticulum steps of the gibberellin biosynthesis pathway. Plant J. 28, 201-208
58. Hardwick, J. P. (2008) Cytochrome P450 omega hydroxylase (CYP4) function in fatty acid metabolism and metabolic diseases. Biochem. Pharmacol. 75, 2263-2275
59. Pinot, F., and Beisson, F. (2011) Cytochrome P450 metabolizing fatty acids in plants: characterization and physiological roles. FEBS J. 278, 195-205
60. Goldberg, M. W., and Allen, T. D. (1995) Structural and functional organization of the nuclear envelope. Curr. Opin. Cell Biol. 7, 301-309
61. Yoshihara, T., Omer, E.-L., Koshino, H., Sakamura, S., Kikuta, Y., and Koda, Y. (1989) Structure of a tuber-inducing stimulus from potato leaves (Solanum tuberosum L.). Agric. Biol. Chem. 53, 2835-2837
62. Nakamura, Y., Mithöfer, A., Kombrink, E., Boland, W., Hamamoto, S., Uozumi, N., Tohma, K., and Ueda, M. (2011) 12-Hydroxyjasmonic acid glucoside is a COI1-JAZ-independent activator of leaf-closing movement in samanea saman. Plant Physiol. 155, 1226-1236
63. Bell, E. M., Lin, W. C., Husbands, A. Y., Yu, L., Jaganatha, V., Jablonska, B., Mangeon, A., Neff, M. M., Girke, T., and Springer, P. S. (2012) Arabidopsis lateral organ boundaries negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc. Natl. Acad. Sci. U.S.A. 109, 21146-21151
64. Mizutani, M., and Ohta, D. (2010) Diversification of P450 genes during land plant evolution. Annu. Rev. Plant Biol. 61, 291-315
65. Bartel, B., and Fink G. R. (1995) ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. Science 268, 1745-1748
66. Ludwig-Müller, J. (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J. Exp. Bot. 62, 1757-1773
67. Campanella, J. J., Larko, D., and Smalley, J. (2003) A molecular phylogenomic analysis of the ILR1-like family of IAA amidohydrolase genes. Comp. Funct. Genomics 4, 584-600