Salt-induced expression of peroxisome-associated genes requires components of the ethylene, jasmonate and abscisic acid signalling pathways

Plant, Cell and Environment

Volumn 28, Issue 4, 2005, Pages 513-524

  Charlton, Wayne L ^a   Matsui, Kyoko ^c   Johnson, Barbara ^a   Graham, Ian A ^b   Ohme Takagi, Masaru ^c   Baker, Alison ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

Abscisic acid; Ethylene; Jasmonate; Peroxisome; Quantitative polymerase chain reaction; Salt stress

Indexed keywords

BOTANY; ENVIRONMENTAL STRESS; GENE EXPRESSION; SALINITY;

EID: 15944411822     PISSN: 01407791     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2004.01293.x     Document Type: Article

References (63)

1. Arenas-Huertero F., Arroyo A., Zhou L., Sheen J. & Leon P. (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes and Development 14, 2085-2096.
2. Bechtold N., Ellis J. & Pelletier G. (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C Royal Academy of Science Paris, Life Sciences 316, 1194-1199.
3. Becker D. (1990) Binary vectors which allow the exchange of plant selectable markers and reporter genes. Nucleic Acids Research 18, 203.
4. Bleecker A.B., Estelle M.A., Sommerville C. & Kende H. (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241, 1086-1089.
5. Brown R.L., Kazan K., McGrath K.C., Maclean D.J. & Manners J.M. (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiology 132, 1020-1032.
6. Castillo M.C., Martinez C., Buchala A., Metraux J.-P. & Leon J. (2004) Gene-specific involvement of {beta}-oxidation in wound-activated responses in Arabidopsis. Plant Physiology 135, 85-94.
7. Chen W., Provart N.J., Glazebrook J., et al. (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14, 559-574.
8. Cheong Y.H., Chang H.-S., Gupta R., Wang X., Zhu T. & Luan S. (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiology 129, 661-677.
9. Choi H.-I., Hong J.-H., Ha J.-O., Kang J.-Y. & Kim S.Y. (2000) ABFs, a family of ABA-responsive element binding factors. Journal of Biological Chemistry 275, 1723-1730.
10. Collins C.S., Kalish J.E., Morrell J.C., McCaffery J.M. & Gould S.J. (2000) The peroxisome biogenesis factors Pex4p, Pex22p, Pex1p, and Pex6p act in the terminal steps of peroxisomal matrix protein import. Molecular and Cellular Biology 20, 7516-7526.
11. Cornah J.E. & Smith S.M. (2002) Synthesis and function of glyoxylate cycle enzymes. In Peroxisomes: Biochemistry, Cell Biology and Biotechnological Applications (eds A. Baker & I.A. Graham), pp. 57-101. Kluwer Academic Publishers, Dordrecht, The Netherlands.
12. Corpas F.J., Gomez M., Hernandez J.A. & del Rio L.A. (1993) Metabolism of activated oxygen in peroxisomes from two Pisum sativum L. cultivars with different sensitivity to sodium chloride. Journal of Plant Physiology 141, 160-165.
13. Dammann C., Ichida A., Hong B., Romanowsky S.M., Hrabak E.M., Harmon A.C., Pickard B.G. & Harper J.F. (2003) Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiology 132, 1840-1848.
14. Finkelstein R.R. & Lynch T.J. (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12, 599-610.
15. Finkelstein R.R., Wang M.L., Lynch T.J., Rao S. & Goodman H.M. (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10, 1043-1054.
16. Fujimoto S.Y., Ohta M., Usui A., Shinshi H. & Ohme-Takagi M. (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12, 393-404.
17. Gazzarrini S. & McCourt P. (2001) Genetic interactions between ABA, ethylene and sugar signaling pathways. Current Opinion in Plant Biology 4, 387-391.
18. Germain V., Rylott E.L., Larson T.R., Sherson S.M., Bechtold N., Carde J.-P., Bryce J.H., Graham I.A. & Smith S.M. (2001) Requirement for 3-ketoacyl-CoA thiolase-2 in peroxisome development, fatty acid β-oxidation and breakdown of triacylglycerol in lipid bodies of Arabidopsis seedlings. Plant Journal 28, 1-12.
19. Giraudat J., Hauge B.M., Valon C., Smalle J., Parcy F. & Goodman H.M. (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4, 1251-1261.
20. Guzman P. & Ecker J.R. (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2, 513-523.
21. Hayashi M., Toriyama K., Kondo M. & Nishimura M. (1998) 2,4-Dichlorophenoxybutyric acid-resistant mutants of Arabidopsis have defects in glyoxysomal fatty acid β-oxidation. Plant Cell 10, 183-196.
22. Hiratsu K., Matsui K., Koyama T. & Ohme-Takagi M. (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant Journal 34, 733-739.
23. Hooks M.A. (2002) Molecular biology, enzymology and physiology of β-oxidation. In Plant Peroxisomes: Biochemistry, Cell Biology and Biotechnological Applications (eds A. Baker & I.A. Graham), pp. 19-55. Kluwer Academic Publishers, Dordrecht, The Netherlands.
24. Hooks M.A., Kellas F. & Graham I.A. (1999) Long-chain acyl-CoA oxidases of Arabidopsis. Plant Journal 20, 1-13.
25. Hoth S., Morgante M., Sanchez J.-P., Hanafey M.K., Tingey S.V. & Chua N.-H. (2002) Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. Journal of Cell Science 115, 4891-4900.
26. Jaglo-Ottosen K.R., Gilmour S.J., Zarka D.G., Schabenberger O. & Thomashow M.F. (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280, 104-106.
27. Kasuga M., Liu Q., Miura S., Yamaguchi-Shinozaki K. & Shinozaki K. (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnology 17, 287-291.
28. Kishitani S., Takanami T., Suzuki M., Oikawa M., Yokoi S., Ishitani M., Alvarez-Nakase A.M. & Takabe T. (2000) Compatibility of glycinebetaine in rice plants: evaluation using transgenic rice plants with a gene for peroxisomal betaine aldehyde dehydrogenase from barley. Plant, Cell and Environment 23, 107-114.
29. Knight H. & Knight M.R. (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends in Plant Science 6, 262-267.
30. Laby R.J., Kincaid M.S., Kim D. & Gibson S.I. (2000) The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant Journal 23, 587-596.
31. Lescot M., Dehais P., Thijs G., Marchal K., Moreau Y., Van de Peer Y., Rouze P. & Rombauts S. (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30, 325-327.
32. Leung J., Merlot S. & Giraudat J. (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9, 759-771.
33. Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K. & Shinozaki K. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391-1406.
34. Lopez-Huertas E., Charlton W.L., Johnson B., Graham I.A. & Baker A. (2000) Stress induces peroxisome biogenesis genes. EMBO Journal 19, 6770-6777.
35. Lopez-Huertas E., Sandalio L.M. & del Rio L.A. (1995) Integral membrane polypeptides of pea leaf peroxisomes: characterization and response to plant stress. Plant Physiology and Biochemistry 33, 295-302.
36. Lorenzo O., Piqueras R., Sanchez-Serrano J.J. & Solano R. (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15, 165-178.
37. 2+ channels in guard cells requires cytosolic NAD (P) H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13, 2513-2523.
38. Nakamura T., Yokota S., Muramoto Y., Tsutsui K., Oguri Y., Fukui K. & Takabe T. (1997) Expression of a betaine aldehyde dehydrogenase gene in rice, a glycinebetaine nonaccumulator, and possible localization of its protein in peroxisomes. Plant Journal 11, 1115-1120.
39. Nambara E., Naito S. & McCourt P. (1992) A mutant of Arabidopsis which is defective in seed development and storage protein accumulation is a new abi3 allele. Plant Journal 2, 435-441.
40. Narusaka Y., Nakashima K., Shinwari Z.K., Sakuma Y., Furihata T., Abe H., Narusaka M., Shinozaki K. & Yamaguchi-Shinozaki K. (2003) Intercation between two cis-acting elements ABRE and DRE in ABA-dependent expression at Arabidopsis rd29A gene in response to dehydration and high salinity stresses. Plant Journal 34, 137-148.
41. Ohme-Takagi M. & Shinshi H. (1995) Ethylene inducible DNA binding proteins that interact with an ethylene responsive element. Plant Cell 7, 173-182.
42. Okumoto K., Itoh R., Shimozawa N., Suzuki Y., Tamura S., Kondo N. & Fujiki Y. (1998) Mutations in PEX10 is the cause of Zellweger peroxisome deficiency syndrome of complementation group B. Human Molecular Genetics 7, 1399-1405.
43. Pastori G.M. & del Rio L.A. (1997) Natural senescence of pea leaves (an activated oxygen-mediated function for peroxisomes). Plant Physiology 113, 411-418.
44. Quesada V., Ponce M.R. & Micol J.L. (2000) Genetic analysis of salt-tolerant mutants in Arabidopsis thaliana. Genetics 154, 421-436.
45. Sanders D., Pelloux J., Brownlee C. & Harper J.F. (2002) Calcium at the crossroads of signaling. Plant Cell 14, S401-S417.
46. Schumann U., Wanner G., Veenhuis M., Schmid M. & Gietl C. (2003) AthPEX10, a nuclear gene essential for peroxisome and storage organelle formation during Arabidopsis embryogenesis. Proceedings of the National Academy of Sciences of the USA 100, 9626-9631.
47. Seki M., Kamei A., Yamaguchi-Shinozaki K. & Shinozaki K. (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Current Opinion in Biotechnology 14, 194-199.
48. Seki M., Narusaka M., Ishida J., et al. (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought cold and high-salinity stresses using a full- length cDNA, microarray. Plant Journal 31, 279-292.
49. Snedecor G.W. & Cochran W.G. (1989) Statistical Methods 8th edn. Iowa State University Press, Ames, IA, USA.
50. Sparkes I.A. & Baker A. (2002) Peroxisome biogenesis and protein import in plants, animals and yeasts: enigma and variations? (Review). Molecular Membrane Biology 19, 171-185.
51. Sparkes I.A., Brandizzi F., Slocombe S.P., El-Shami M., Hawes C. & Baker A. (2003) An Arabidopsis pex10 null mutant is embryo lethal, implicating peroxisomes in an essential role during plant embryogenesis. Plant Physiology pp. 103.031252.
52. Staswick P., Su W. & Howell S. (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proceedings of the National Academy of Sciences of the USA 89, 6837-6840.
53. 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. Plant Cell 14, 1405-1415.
54. Stintzi A. & Browse J. (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proceedings of the National Academy of Sciences of the USA 97, 10625-10630.
55. Titorenko V.I. & Rachubinski R.A. (2000) Peroxisomal membrane fusion requires two AAA family ATPases, Pex1p and Pex6p. Journal of Cell Biology 150, 881-886.
56. Turner J.G., Ellis C. & Devoto A. (2002) The jasmonate signal pathway. Plant Cell 14, S153-S164.
57. Uno Y., Furihata T., Abe H., Yoshida R., Shinozaki K. & Yamaguchi-Shinozaki K. (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proceedings of the National Academy of Sciences of the USA 97, 11632-11637.
58. Wang K.L.-C., Li H. & Ecker J.R. (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14, S131-S151.
59. Wang K.L.-C., Yoshida H., Lurin C. & Ecker J.R. (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428, 945-950.
60. Werner J.E. & Finkelstein R.R. (1995) Arabidopsis mutants with reduced response to NaCI and osmotic stress. Physiologia Plantarum 93, 659-666.
61. Xiong L.M., Schumaker K.S. & Zhu J.K. (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14, S165-S183.
62. Yamaguchi-Shinozaki K. & Shinozaki K. (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6, 251-264.
63. Zhu J.K. (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247-273.