COI1-Regulated Hydroxylation of Jasmonoyl-l-isoleucine Impairs Nicotiana attenuata's Resistance to the Generalist Herbivore Spodoptera litura

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 14, 2016, Pages 2822-2831

  Luo, Ji ^a,c   Wei, Kun ^a   Wang, Shuanghua ^a,c   Zhao, Weiye ^a   Ma, Canrong ^a,c   Hettenhausen, Christian ^a   Wu, Jinsong ^a   Cao, Guoyan ^a   Sun, Guiling ^a   Baldwin, Ian T ^b   Wu, Jianqiang ^a   Wang, Lei ^a  

^a KUNMING INSTITUTE OF BOTANY   (China)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

catabolism; cytochrome P450; defense; JA Ile; Nicotiana attenuata; plant insect interaction; Spodoptera litura

Indexed keywords

AMINO ACIDS; FORESTRY; GENES; HYDROXYLATION; MOLECULES; PLANT CELL CULTURE;

CATABOLISM; CYTOCHROME P450; DEFENSE; JA-ILE; NICOTIANA ATTENUATA; PLANT-INSECT INTERACTIONS; SPODOPTERA LITURA;

METABOLISM;

CYCLOPENTANE DERIVATIVE; CYTOCHROME P450; ISOLEUCINE; JASMONOYL-ISOLEUCINE; PLANT PROTEIN;

ANALOGS AND DERIVATIVES; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; HERBIVORY; HYDROXYLATION; IMMUNOLOGY; METABOLISM; PARASITOLOGY; PHYSIOLOGY; SPODOPTERA; TOBACCO; TRANSGENIC PLANT;

ANIMALS; CYCLOPENTANES; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION REGULATION, PLANT; HERBIVORY; HYDROXYLATION; ISOLEUCINE; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SPODOPTERA; TOBACCO;

EID: 84964664237     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b06056     Document Type: Article

References (43)

1. Kessler, A.; Halitschke, R.; Baldwin, I. T. Silencing the jasmonate cascade: induced plant defenses and insect populations Science 2004, 305, 665-668 10.1126/science.1096931
2. Wang, L.; Wu, J. The essential role of jasmonic acid in plant-herbivore interactions-using the wild tobacco Nicotiana attenuata as a model J. Genet. Genomics 2013, 40, 597-606 10.1016/j.jgg.2013.10.001
3. Halitschke, R.; Schittko, U.; Pohnert, G.; Boland, W.; Baldwin, I. T. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses Plant Physiol. 2001, 125, 711-717 10.1104/pp.125.2.711
4. Wasternack, C.; Hause, B. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany Ann. Bot. 2013, 111, 1021-1058 10.1093/aob/mct067
5. Staswick, P. E.; Tiryaki, I. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis Plant Cell 2004, 16, 2117-2127 10.1105/tpc.104.023549
6. Xie, D. X.; Feys, B. F.; James, S.; Nieto-Rostro, M.; Turner, J. G. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility Science 1998, 280, 1091-1094 10.1126/science.280.5366.1091
7. COI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis Plant Cell 2002, 14, 1919-1935 10.1105/tpc.003368
8. Chini, A.; Fonseca, S.; Fernandez, G.; Adie, B.; Chico, J. M.; Lorenzo, O.; Garcia-Casado, G.; Lopez-Vidriero, I.; Lozano, F. M.; Ponce, M. R.; Micol, J. L.; Solano, R. The JAZ family of repressors is the missing link in jasmonate signalling Nature 2007, 448, 666-671 10.1038/nature06006
9. COI1 complex during jasmonate signalling Nature 2007, 448, 661-665 10.1038/nature05960
10. Wang, L.; Allmann, S.; Wu, J.; Baldwin, I. T. Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata Plant Physiol. 2008, 146, 904-915 10.1104/pp.107.109264
11. Kang, J. H.; Wang, L.; Giri, A.; Baldwin, I. T. Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta Plant Cell 2006, 18, 3303-3320 10.1105/tpc.106.041103
12. Mikkelsen, M. D.; Petersen, B. L.; Glawischnig, E.; Jensen, A. B.; Andreasson, E.; Halkier, B. A. Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways Plant Physiol. 2003, 131, 298-308 10.1104/pp.011015
13. Steppuhn, A.; Gase, K.; Krock, B.; Halitschke, R.; Baldwin, I. T. Nicotine's defensive function in nature PLoS Biol. 2004, 2, e217 10.1371/journal.pbio.0020217
14. Zavala, J. A.; Patankar, A. G.; Gase, K.; Hui, D.; Baldwin, I. T. Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses Plant Physiol. 2004, 134, 1181-1190 10.1104/pp.103.035634
15. Jassbi, A. R.; Gase, K.; Hettenhausen, C.; Schmidt, A.; Baldwin, I. T. Silencing geranylgeranyl diphosphate synthase in Nicotiana attenuata dramatically impairs resistance to tobacco hornworm Plant Physiol. 2008, 146, 974-986 10.1104/pp.107.108811
16. Heinrich, M.; Hettenhausen, C.; Lange, T.; Wunsche, H.; Fang, J.; Baldwin, I. T.; Wu, J. High levels of jasmonic acid antagonize the biosynthesis of gibberellins and inhibit the growth of Nicotiana attenuata stems Plant J. 2013, 73, 591-606 10.1111/tpj.12058
17. Zhang, Y.; Turner, J. G. Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis PLoS One 2008, 3, e3699 10.1371/journal.pone.0003699
18. Baldwin, I. T. Jasmonate-induced responses are costly but benefit plants under attack in native populations Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 8113-8118 10.1073/pnas.95.14.8113
19. Woldemariam, M. G.; Onkokesung, N.; Baldwin, I. T.; Galis, I. Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulates jasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores Plant J. 2012, 72, 758-767 10.1111/j.1365-313X.2012.05117.x
20. Koo, A. J.; Cooke, T. F.; Howe, G. A. Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 9298-9303 10.1073/pnas.1103542108
21. Heitz, T.; Widemann, E.; Lugan, R.; Miesch, L.; Ullmann, P.; Desaubry, L.; Holder, E.; Grausem, B.; Kandel, S.; Miesch, M.; Werck-Reichhart, D.; Pinot, F. Cytochromes P450 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone Jasmonoyl-isoleucine for catabolic turnover J. Biol. Chem. 2012, 287, 6296-6306 10.1074/jbc.M111.316364
22. Koo, A. J.; Howe, G. A. Catabolism and deactivation of the lipid-derived hormone jasmonoyl-isoleucine Front. Plant Sci. 2012, 3, 19 10.3389/fpls.2012.00019
23. Koo, A. J.; Thireault, C.; Zemelis, S.; Poudel, A. N.; Zhang, T.; Kitaoka, N.; Brandizzi, F.; Matsuura, H.; Howe, G. A. Endoplasmic Reticulum-associated Inactivation of the Hormone Jasmonoyl-l-Isoleucine by Multiple Members of the Cytochrome P450 94 Family in Arabidopsis J. Biol. Chem. 2014, 289, 29728-29738 10.1074/jbc.M114.603084
24. Aubert, Y.; Widemann, E.; Miesch, L.; Pinot, F.; Heitz, T. CYP94-mediated jasmonoyl-isoleucine hormone oxidation shapes jasmonate profiles and attenuates defence responses to Botrytis cinerea infection J. Exp. Bot. 2015, 66, 3879-3892 10.1093/jxb/erv190
25. Hwang, I. S.; Hwang, B. K. Role of the pepper cytochrome P450 gene CaCYP450A in defense responses against microbial pathogens Planta 2010, 232, 1409-1421 10.1007/s00425-010-1266-y
26. Krugel, T.; Lim, M.; Gase, K.; Halitschke, R.; Baldwin, I. T. Agrobacterium-mediated transformation of Nicotiana attenuata, a model ecological expression system Chemoecology 2002, 12, 177-183 10.1007/PL00012666
27. Kallenbach, M.; Bonaventure, G.; Gilardoni, P. A.; Wissgott, A.; Baldwin, I. T. Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent manner and identify jasmonate mutants in natural populations Proc. Natl. Acad. Sci. U. S. A. 2012, 109, E1548-1557 10.1073/pnas.1200363109
28. Paschold, A.; Halitschke, R.; Baldwin, I. T. Co(i)-ordinating defenses: NaCOI1 mediates herbivore- induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses Plant J. 2007, 51, 79-91 10.1111/j.1365-313X.2007.03119.x
29. Kramell, R.; Schmidt, J.; Schneider, G.; Sembdner, G.; Schreiber, K. Synthesis of N-(Jasmonoyl)Amino Acid Conjugates Tetrahedron 1988, 44, 5791-5807 10.1016/S0040-4020(01)81437-X
30. Sun, H.; Hu, X.; Ma, J.; Hettenhausen, C.; Wang, L.; Sun, G.; Wu, J.; Wu, J. Requirement of ABA signalling-mediated stomatal closure for resistance of wild tobacco to Alternaria alternata Plant Pathol. 2014, 63, 1070-1077 10.1111/ppa.12181
31. Saedler, R.; Baldwin, I. T. Virus-induced gene silencing of jasmonate-induced direct defences, nicotine and trypsin proteinase-inhibitors in Nicotiana attenuata J. Exp. Bot. 2004, 55, 151-157 10.1093/jxb/erh004
32. Keinanen, M.; Oldham, N. J.; Baldwin, I. T. Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in Nicotiana attenuata J. Agric. Food Chem. 2001, 49, 3553-3558 10.1021/jf010200+
33. van Dam, N. M.; Horn, M.; Mares, M.; Baldwin, I. T. Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata J. Chem. Ecol. 2001, 27, 547-568 10.1023/A:1010341022761
34. Heiling, S.; Schuman, M. C.; Schoettner, M.; Mukerjee, P.; Berger, B.; Schneider, B.; Jassbi, A. R.; Baldwin, I. T. Jasmonate and ppHsystemin regulate key Malonylation steps in the biosynthesis of 17-Hydroxygeranyllinalool Diterpene Glycosides, an abundant and effective direct defense against herbivores in Nicotiana attenuata Plant Cell 2010, 22, 273-292 10.1105/tpc.109.071449
35. Paschold, A.; Bonaventure, G.; Kant, M. R.; Baldwin, I. T. Jasmonate perception regulates jasmonate biosynthesis and JA-Ile metabolism: the case of COI1 in Nicotiana attenuata Plant Cell Physiol. 2008, 49, 1165-1175 10.1093/pcp/pcn091
36. Mizutani, M.; Ohta, D. Diversification of P450 genes during land plant evolution Annu. Rev. Plant Biol. 2010, 61, 291-315 10.1146/annurev-arplant-042809-112305
37. Miersch, O.; Neumerkel, J.; Dippe, M.; Stenzel, I.; Wasternack, C. Hydroxylated jasmonates are commonly occurring metabolites of jasmonic acid and contribute to a partial switch-off in jasmonate signaling New Phytol. 2008, 177, 114-127 10.1111/j.1469-8137.2007.02252.x
38. 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.; Zheng, N. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor Nature 2010, 468, 400-405 10.1038/nature09430
39. Yan, J.; Zhang, C.; Gu, M.; Bai, Z.; Zhang, W.; Qi, T.; Cheng, Z.; Peng, W.; Luo, H.; Nan, F.; Wang, Z.; Xie, D. The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor Plant Cell 2009, 21, 2220-2236 10.1105/tpc.109.065730
40. Devoto, A.; Ellis, C.; Magusin, A.; Chang, H. S.; Chilcott, C.; Zhu, T.; Turner, J. G. Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions Plant Mol. Biol. 2005, 58, 497-513 10.1007/s11103-005-7306-5
41. Jiang, W.; Zhou, H.; Bi, H.; Fromm, M.; Yang, B.; Weeks, D. P. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice Nucleic Acids Res. 2013, 41, e188 10.1093/nar/gkt780
42. Miao, J.; Guo, D. S.; Zhang, J. Z.; Huang, Q. P.; Qin, G. J.; Zhang, X.; Wan, J. M.; Gu, H. Y.; Qu, L. J. Targeted mutagenesis in rice using CRISPR-Cas system Cell Res. 2013, 23, 1233-1236 10.1038/cr.2013.123
43. Liang, Z.; Zhang, K.; Chen, K.; Gao, C. Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system J. Genet. Genomics 2014, 41, 63-68 10.1016/j.jgg.2013.12.001