GER1, a GDSL Motif-Encoding Gene from Rice is a Novel Early Light- and Jasmonate-Induced Gene

M. Riemann; C. Gutjahr; A. Korte; B. Danger; T. Muramatsu; U. Bayer; F. Waller; M. Furuya; P. Nick

doi:10.1055/s-2006-924561

Plant Biology, Table of Contents

Plant Biol (Stuttg) 2007; 9(1): 32-40
DOI: 10.1055/s-2006-924561

Research Paper

Georg Thieme Verlag Stuttgart KG · New York

GER1, a GDSL Motif-Encoding Gene from Rice is a Novel Early Light- and Jasmonate-Induced Gene

M. Riemann¹ ^, ² , C. Gutjahr³ , A. Korte³ , M. Riemann³ , B. Danger³ , T. Muramatsu⁴ , U. Bayer³ , F. Waller⁵ , M. Furuya⁴ , P. Nick¹

¹Botanisches Institut 1, Technische Universität Karlsruhe, Kaiserstraße 2, 76128 Karlsruhe, Germany
²Department of Plant Physiology, National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan
³Biologisches Institut II, Albert-Ludwigs-Universität Freiburg, Schänzlestraße 1, 79104 Freiburg, Germany
⁴Hitachi Advanced Research Laboratory, Hatoyama, Saitama 350-0395, Japan
⁵Institute of Phytopathology and Applied Zoology, Justus-Liebig-Universität Gießen, Heinrich-Buff-Ring 26 - 32, 35392 Gießen, Germany

Abstract

The reaction of the rice mutant hebiba differs from that of wild-type rice in that the mutant responds inversely to red light and is defective in the light-triggered biosynthesis of jasmonic acid (JA). Using the wild type and the hebiba mutant of rice in a differential display screen, we attempted to identify genes that act in or near the convergence point of light and JA signalling. We isolated specifically regulated DNA fragments from approximately 10 000 displayed bands, and identified a new early light- and JA-induced gene. This gene encodes an enzyme containing a GDSL motif, showing 38 % identity at the amino acid level to lipase Arab-1 in Arabidopsis thaliana. The GDSL CONTAINING ENZYME RICE 1 gene (GER1) is rapidly induced by both red (R) and far-red (FR) light and by JA. The results are discussed with respect to a possible role for GER1 as a negative regulator of coleoptile elongation in the context of recent findings on the impact of JA on light signalling.

Key words

Jasmonate - GDSL motif - phytochrome - rice (Oryza sativa L. japonica).

Full Text

References

1 Abel S., Nguyen M. D., Theologis A.. The ps-iaa4/5-like family of early auxin-inducible messenger-RNAs in Arabidopsis thaliana. . Journal of Molecular Biology. (1995); 251 533-549
2 Akoh C. C., Lee G. C., Liaw Y. C., Huang T. H., Shaw J. F.. GDSL family of serine esterases/lipases. Progress in Lipid Research. (2004); 43 534-552
3 Beisson F., Koo A. J., Ruuska S., Schwender J., Pollard M., Thelen J. J., Paddock T., Salas J. J., Savage L., Milcamps A., Mhaske V. B., Cho Y., Ohlrogge J. B.. Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiology. (2003); 132 681-697
4 Brick D. J., Brumlik M. J., Buckley J. T., Cao J. X., Davies P. C., Misra S., Tranbarger T. J., Upton C.. A new family of lipolytic plant enzymes with members in rice, Arabidopsis and maize. FEBS Letters. (1995); 377 475-480
5 Briggs W. R., Christie J. M.. Phototropins 1 and 2: versatile plant blue-light receptors. Trends in Plant Science. (2002); 7 204-210
6 Chaban C., Waller F., Furuya M., Nick P.. Auxin responsiveness of a novel cytochrome P450 in rice coleoptiles. Plant Physiology. (2003); 133 2000-2009
8 Devoto A., Turner J. G.. Regulation of jasmonate-mediated plant responses in Arabidopsis. . Annals of Botany. (2003); 92 329-337
9 Devoto A., Turner J. G.. Jasmonate-regulated Arabidopsis stress signalling network. Physiologia Plantarum. (2005); 123 161-172
10 Dickstein R., Prusty R., Peng T., Ngo W., Smith M. E.. ENOD8, a novel early nodule-specific gene, is expressed in empty alfalfa nodules. Molecular Plant and Microbe Interaction. (1993); 6 715-721
11 Emanuelsson O., Nielsen H., Brunak S., von Heijne G.. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology. (2000); 300 1005-1016
12 Flieger A., Neumeister B., Cianciotto N. P.. Characterization of the gene encoding the major secreted lysophospholipase A of Legionella pneumophila and its role in detoxification of lysophosphatidylcholine. Infection and Immunity. (2002); 70 6094-6106
14 Furuya M., Pjon C. J., Fujii T., Ito M.. Phytochrome action in Oryza sativa L. III. The separation of photoperceptive site and growing zone in coleoptiles, and auxin transport as effector system. Development, Growth and Differentiation. (1969); 11 62-76
15 Gil P., Green P. J.. Regulatory activity exerted by the SAUR‐AC1 promoter region in transgenic plants. Plant Molecular Biology. (1997); 34 803-808
16 Guilfoyle T. J.. Auxin-regulated genes and promoters. Hooykaas, P. J. J., Hall, M. A., and Libbenga, K. R., eds. Biochemistry and Molecular Biology of Plant Hormones. Amsterdam, The Netherlands; Elsevier (1999)
17 Gutjahr C., Riemann M., Mueller A., Duechting P., Weiler E. W., Nick P.. Cholodny-Went revisited a role for jasmonate in gravitropism of rice coleoptiles. Planta. (2005); 222 575-585
18 Haga K., Iino M.. Phytochrome-mediated transcriptional up-regulation of ALLENE OXIDE SYNTHASE in rice seedlings. Plant and Cell Physiology. (2004); 45 119-128
19 Halliday K. J., Fankhauser C.. Phytochrome-hormonal signalling networks. New Phytologist. (2003); 157 449-463
20 Hara-Nishimura I., Matsushima R.. A wound-inducible organelle derived from endoplasmic reticulum: a plant strategy against environmental stresses?. Current Opinion in Plant Biology. (2003); 6 583-588
21 He G., Tarui Y., Iino M.. A novel receptor kinase involved in jasmonate-mediated wound and phytochrome signalling in maize. Plant and Cell Physiology. (2005); 46 870-883
22 Holweg C., Süßlin C., Nick P.. Capturing in vivo dynamics of the actin cytoskeleton. Plant and Cell Physiology. (2004); 45 855-863
23 Hsieh H. L., Okamoto H., Wang M., Ang L. H., Matsui M., Goodman H., Deng X. W.. 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. (2000); 14 1958-1970
24 Imaizumi T., Tran H. G., Swartz T. E., Briggs W. R., and Kay S. A.. FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature. (2003); 426 302-306
25 Ishiguro S., Kawai-Oda A., Ueda J., Nishida I., Okada K.. The DEFECTIVE IN ANTHER DEHISCENCE 1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell. (2001); 13 2191-2209
26 Kircher S., Wellmer F., Nick P., Rugner A., Schafer E., Harter K.. Nuclear import of the parsley bZIP transcription factor CPRF2 is regulated by phytochrome photoreceptors. Journal of Cell Biology. (1999); 144 201-211
27 Kuno N., Muramatsu T., Hamazato F., Furuya M.. Identification by large-scale screening of phytochrome regulated genes in etiolated seedlings of Arabidopsis using a fluorescent differential display technique. Plant Physiology. (2000 a); 122 15-24
28 Kuno N., Furuya M.. Phytochrome regulation of nuclear gene expression in plants. Seminars in Cell and Developmental Biology. (2000 b); 11 485-493
29 Lee K. A., Cho T. J.. Characterization of a salicylic acid- and pathogen-induced lipase-like gene in Chinese cabbage. Journal of Biochemistry and Molecular Biology. (2003); 36 433-441
30 Lin C., Shailitin D.. Cryptochrome structure and signal transduction. Annual Review of Plant Biology. (2003); 54 469-496
31 Mathur J., Mathur N., Hülskamp M.. Simultaneous visualization of peroxisomes and cytoskeletal elements reveals actin and not microtubule-based peroxisome motility in plants. Plant Physiology. (2002); 128 1031-1045
32 Mohr H., Meyer U., Hartmann K.. Die Beeinflussung der Farnsporenkeimung (Osmunda cinnamomea [L.] und O. claytoniana [L.]) über das Phytochromsystem und die Photosynthese. Planta. (1964); 60 483-496
33 Munnik T., Irvine R. F., Musgrave A.. Phospolipid signaling in plants. Biochimica et Biophysica Acta. (1998); 1389 222-272
34 Nagy F., Schäfer E.. Phytochromes control photomorphogenesis by differentially regulated, interacting signalling pathways in higher plants. Annual Review of Plant Biology. (2003); 53 329-355
35 Nakai K., Kanehisa M.. Expert system for predicting protein localization sites in gram-negative bacteria. Proteins. (1991); 11 95-110
36 Nick P., Yatou O., Furuya M., Lambert A.-M.. Auxin-dependent microtubule responses and seedling development are affected in a rice mutant resistant to EPC. The Plant Journal. (1994); 6 651-663
37 Quail P. H.. Phytochrome photosensory signalling networks. Nature Reviews Molecular Cell Biology. (2002); 3 85-93
38 Reed J. W., Nagpal P., Poole D. S., Furuya M., Chory J.. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell. (1993); 5 147-157
39 Riemann M., Müller A., Korte A., Furuya M., Weiler E. W., and Nick P.. Impaired induction of the jasmonate pathway in the rice mutant hebiba. Plant Physiology. (2003); 133 1820-1830
40 Sambrook L., Fitsch E., Maniatis T.. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor, NY; Spring Harbor Laboratory (1989)
41 Schwechheimer C., Serino G., Deng X. W.. Multiple ubiquitin ligase mediated processes require COP9 signalosome and AXR1 function. Plant Cell. (2002); 14 2553-2563
43 Sobajima H., Takeda M., Sugimori M., Kobashi N., Kiribuchi K., Cho E.-M., Akimoto C., Yamaguchi T., Minami E., Shibuya N., Schaller F., Weiler E. W., Yoshihara T., Nishida H., Nojiri H., Omori T., Nishiyama M., Yamane H.. Cloning and characterization of a jasmonic acid-responsive gene encoding 12-oxophytodienoic acid reductase in suspension-cultured rice cells. Planta. (2003); 216 692-698
44 Staswick P. E., Tiryaki I., Rowe M. L.. 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. (2002); 14 1405-1415
45 Takano M., Kanegae H., Shinomura T., Miyao A., Hirochika H., Furuya M.. Isolation and characterization of rice phytochrome A mutants. Plant Cell. (2001); 13 521-534
46 Takano M., Inagaki N., Xie X., Yuzurihara N., Hihara F., Ishizuka T., Yano M., Nishimura M., Miyao A., Hirochika H., Shinomura T.. Distinct and cooperative functions of Phytochromes A, B, and C in the control of deetiolation and flowering in rice. Plant Cell. (2005); 17 3311-3325
47 Tanaka S., Mochizuki N., Nagatani A.. Expression of the AtGH3a gene, an Arabidopsis homologue of the soybean GH3 gene, is regulated by phytochrome B. Plant and Cell Physiology. (2002); 43 281-289
48 Turner J. G., Ellis C., Devoto A.. The jasmonate signal pathway. Plant Cell. (2002); S153-S164
49 Upton C., Buckley J. T.. A new family of lipolytic enzymes?. Trends in Biochemical Science. (1995); 20 178-179
50 Waller F., Furuya M., Nick P.. OsARF1, an auxin response factor from rice, is auxin-regulated and classifies as a primary auxin responsive gene. Plant Molecular Biology. (2002); 50 415-425
52 Whitelam G. C., Johnson E., Peng J., Carol P., Anderson M. L., Cowl J. S., Harberd N. P.. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell. (1993); 5 757-768
53 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
54 Yadav V., Mallappa C., Gangappa S. N., Bhatia S., Chattopadhyay S.. A basic helix-loop-helix transcription factor in Arabidopsis, MYC2, acts as a repressor of blue-light mediated photomorphogenic growth. Plant Cell. (2005); 17 1953-1966

M. Riemann

Botanisches Institut 1
Technische Universität Karlsruhe

Kaiserstraße 2

76128 Karlsruhe

Germany

Email: michael.riemann@bio.uni-karlsruhe.de

Editor: B. Demmig-Adams