Light induces jasmonate-isoleucine conjugation via OsJAR1-dependent and -independent pathways in rice

Plant, Cell and Environment

Volumn 37, Issue 4, 2014, Pages 827-839

  Svyatyna, Katharina ^a   Jikumaru, Yusuke ^b   Brendel, Rita ^a   Reichelt, Michael ^c   Mithöfer, Axel ^c   Takano, Makoto ^d   Kamiya, Yuji ^b   Nick, Peter ^a   Riemann, Michael ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b RIKEN   (Japan)

^c MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^d NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

GH3; JAR1; Jasmonate; Mechanical wounding; Oryza sativaL.; Photomorphogenesis

Indexed keywords

AMINO ACID; BIOCHEMICAL COMPOSITION; MORPHOGENESIS; MUTATION; PHENOTYPE; RICE; SEEDLING; SUBSTRATE;

ARABIDOPSIS; ORYZA; ORYZA SATIVA;

CYCLOPENTANE DERIVATIVE; DRUG DERIVATIVE; ISOLEUCINE; JASMONIC ACID; JASMONOYL ISOLEUCINE; JASMONOYL-ISOLEUCINE; OXYLIPIN; VEGETABLE PROTEIN;

ARTICLE; BIOSYNTHESIS; ENZYME SPECIFICITY; ETIOLATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GH3; JAR1; LIGHT; MECHANICAL WOUNDING; METABOLISM; MORPHOGENESIS; MUTATION; ORYZA SATIVA L.; PHENOTYPE; PHOTOMORPHOGENESIS; RADIATION EXPOSURE; RICE; SEEDLING; SIGNAL TRANSDUCTION;

GH3; JAR1; JASMONATE; MECHANICAL WOUNDING; ORYZA SATIVA L.; PHOTOMORPHOGENESIS;

BIOSYNTHETIC PATHWAYS; CYCLOPENTANES; ETIOLATION; GENE EXPRESSION REGULATION, PLANT; ISOLEUCINE; LIGHT; MORPHOGENESIS; MUTATION; ORYZA SATIVA; OXYLIPINS; PHENOTYPE; PLANT PROTEINS; SEEDLING; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 84896712025     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12201     Document Type: Article

References (50)

1. Bricchi I., Leitner M., Foti M., Mithöfer A., Boland W. & Maffei M.E. (2010) Robotic mechanical wounding (MecWorm) versus herbivore-induced responses: early signaling and volatile emission in lima bean (Phaseolus lunatus L. Planta 232, 719-729.
2. Caldana C., Scheible W.-R., Bernd Mueller-Roeber B. & Ruzicic S. (2007) A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods 3, 7.
3. Chen I.-C., Huang I.C., Liu M.-J., Wang Z.-G., Chung S.-S. & Hsieh H.-L. (2007) Glutathione S-transferase interacting with far-red insensitive 219 is involved in phytochrome A-mediated signaling in Arabidopsis. Plant Physiology 143, 1189-1202.
4. Chini A., Fonseca S., Fernandez G., etal. (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666-671.
5. Fonseca S., Chini A., Hamberg M., Adie B., Porzel A., Kramell R., Miersch O., Wasternack C. & Solano R. (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5, 344-350.
6. Fukumoto K., Alamgir K.M., Yamashita Y., Mori I.C., Matsuura H. & Galis I. (2013) Response of rice to insect elicitors and the role of OsJAR1 in wound and herbivory-induced JA-Ile accumulation. Journal of Integrative Plant Biology 55, 775-784.
7. Guilfoyle T.J. (1999) Auxin-regulated genes and promoters. Biochemistry and Molecular Biology of Plant Hormones 33, 423-459.
8. Gutjahr C., Banba M., Croset V., An K., Miyao A., An G., Hirochika H., Imaizumi-Anraku H. & Paszkowski U. (2008) Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. The Plant Cell 20, 2989-3005.
9. Haga K. & Iino M. (2004) Phytochrome-mediated transcriptional up-regulation of allene oxide synthase in rice seedlings. Plant and Cell Physiology 45, 119-128.
10. Hagen G. & Guilfoyle T. (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Molecular Biology 49, 373-385.
11. Hagen G., Kleinschmidt A. & Guilfoyle T. (1984) Auxin-regulated gene expression in intact soybean glycine-max cultivar wayne hypocotyl and excised hypocotyl sections. Planta 162, 147-153.
12. Hellemans J., Mortier G., De Paepe A., Speleman F. & Vandesompele J. (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology 8, R19.
13. Hsieh H.-L., Okamoto H., Wang M., Ang L.-H., Matsui M., Goodman H. & 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 and Development 14, 1958-1970.
14. Jain M., Kaur N., Tyagi A.K. & Khurana J.P. (2006) The auxin-responsive GH3 gene family in rice (Oryza sativa). Functional & Integrative Genomics 6, 36-46.
15. Kramell R., Schmidt J., Schneider G., Sembdner G. & Schreiber K. (1988) Synthesis of N-(jasmonoyl)amino acid conjugates. Tetrahedron 44, 5791-5807.
16. Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T-4. Nature 227, 680-685.
17. Larmande P., Gay C., Lorieux M., etal. (2008) Oryza Tag Line, a phenotypic mutant database for the Genoplante rice insertion line library. Nucleic Acid Research 36, D1022-D1027.
18. Livak K.J. & Schmittgen T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
19. Mithöfer A., Wanner G. & Boland W. (2005) Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiology 137, 1160-1168.
20. Miyao A., Tanaka K., Murata K., Sawaki H., Takeda S., Abe K., Shinozuka Y., Onosato K. & Hirochika H. (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. The Plant Cell 15, 1771-1780.
21. Moreno J.E., Tao Y., Chory J. & Ballare C.L. (2009) Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proceedings of the National Academy of Sciences of the United States of America 106, 4935-4940.
22. Pauwels L., Barbero G.F., Geerinck J., etal. (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464, 788-791.
23. Peat T.S., Bottcher C., Newman J., Lucent D., Cowieson N. & Davies C. (2012) Crystal structure of an indole-3-acetic acid amido synthetase from grapevine involved in auxin homeostasis. The Plant Cell 24, 4525-4538.
24. Qiao F., Petrasek J. & Nick P. (2010) Light can rescue auxin-dependent synchrony of cell division in a tobacco cell line. Journal of Experimental Botany 61, 503-510.
25. Radhika V., Kost C., Mithöfer A. & Boland W. (2010) Regulation of extrafloral nectar secretion by jasmonates in lima bean is light dependent. Proceedings of the National Academy of Sciences of the United States of America 107, 17228-17233.
26. Riemann M., Muller A., Korte A., Furuya M., Weiler E.W. & Nick P. (2003) Impaired induction of the jasmonate pathway in the rice mutant hebiba. Plant Physiology 133, 1820-1830.
27. Riemann M., Riemann M. & Takano M. (2008) Rice JASMONATE RESISTANT 1 is involved in phytochrome and jasmonate signalling. Plant, Cell & Environment 31, 783-792.
28. Riemann M., Haga K., Shimizu T., etal. (2013) Identification of rice ALLENE OXIDE CYCLASE mutants and the function of jasmonate for defence against Magnaporthe oryzae. The Plant Journal 74, 226-238.
29. Robson F., Okamoto H., Patrick E., Harris S.-R., Wasternack C., Brearley C. & Turner J.G. (2010) Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability. The Plant Cell 22, 1143-1160.
30. Roux C. & Perrot-Rechenmann C. (1997) Isolation by differential display and characterization of a tobacco auxin-responsive cDNA Nt-gh3, related to GH3. FEBS Letters 419, 131-136.
31. Roux C., Bilang J., Theunissen B.H. & Perrot-Rechenmann C. (1998) Identification of new early auxin markers in tobacco by mRNA differential display. Plant Molecular Biology 37, 385-389.
32. Rozen S. & Skaletsky H.J. (2000) Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols: Methods in Molecular Biology (eds S. Krawetz & S. Misener ), pp. 365-386. Humana Press, Totowa, NJ.
33. Sheard L.B., Tan X., Mao H., etal. (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468, 400-405.
34. Shimizu T., Miyamoto K., Miyamoto K., Minami E., Nishizawa Y., Iino M., Nojiri H., Yamane H. & Okada K. (2013) OsJAR1 contributes mainly to biosynthesis of the stress-induced jasmonoyl-isoleucine involved in defense responses in rice. Bioscience, Biotechnology and Biochemistry 77, 1556-1564.
35. Staswick P.E. & Tiryaki I. (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. The Plant Cell 16, 2117-2127.
36. Staswick P.E., Tiryaki I. & Rowe M.L. (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. The Plant Cell 14, 1405-1415.
37. Staswick P.E., Serban B., Rowe M., Tiryaki I., Maldonado M.T., Maldonado M.C. & Suza W. (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. The Plant Cell 17, 616-627.
38. Svyatyna K. & Riemann M. (2012) Light-dependent regulation of the jasmonate pathway. Protoplasma 249, S137-S145.
39. Terol J., Domingo C. & Talon M. (2006) The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371, 279-290.
40. Thines B., Katsir L., Melotto M., Niu Y., Mandaokar A., Liu G., Nomura K., He S.Y., Howe G.A. & Browse J. (2007) JAZ repressor proteins are targets of the SCFCO11 complex during jasmonate signalling. Nature 448, 661-665.
41. Wakuta S., Suzuki E., Saburi W., Matsuura H., Nabeta K., Imai R. & Matsui H. (2011) OsJAR1 and OsJAR2 are jasmonyl-L-isoleucine synthases involved in wound- and pathogen-induced jasmonic acid signalling. Biochemical and Biophysical Research Communications 409, 634-639.
42. Wang L., Halitschke R., Kang J.H., Berg A., Harnisch F. & Baldwin I.T. (2007) Independently silencing two JAR family members impairs levels of trypsin proteinase inhibitors but not nicotine. Planta 226, 159-167.
43. Wasternack C. & Hause B. (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany 111, 1021-1058.
44. Wasternack C. & Kombrink E. (2010) Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chemical Biology 5, 63-77.
45. Westfall C.S., Zubieta C., Herrmann J., Kapp U., Nanao M.H. & Jez J.M. (2012) Structural basis for prereceptor modulation of plant hormones by GH3 proteins. Science 336, 1708-1711.
46. Yamada S., Kano A., Tamaoki D., Miyamoto A., Shishido H., Miyoshi S., Taniguchi S., Akimitsu K. & Gomi K. (2012) Involvement of OsJAZ8 in jasmonate-induced resistance to bacterial blight in rice. Plant and Cell Physiology 53, 2060-2072.
47. Yan J., Zhang C., Gu M., etal. (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. The Plant Cell 21, 2220-2236.
48. Ye H., Du H., Tang N., Li X. & Xiong L. (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Molecular Biology 71, 291-305.
49. Ye J., Coulouris G., Zaretskaya I., Cutcutache I., Rozen S. & Madden T. (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13, 134.
50. Yoshimoto K., Jikumaru Y., Kamiya Y., Kusano M., Consonni C., Panstruga R., Ohsumi Y. & Shirasu K. (2009) Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. The Plant Cell 21, 2914-2927.