Two fatty acid desaturases, STEAROYL-ACYL CARRIER PROTEIN Δ9-DESATURASE6 and FATTY ACID DESATURASE3, are involved in drought and hypoxia stress signaling in Arabidopsis crown galls

Plant Physiology

Volumn 164, Issue 2, 2014, Pages 570-583

  Klinkenberg, Joern ^a,d   Faist, Hanna ^a   Saupe, Stefanie ^a   Lambertz, Sophie ^a   Krischke, Markus ^a   Stingl, Nadja ^a   Fekete, Agnes ^a   Mueller, Martin J ^a   Feussner, Ivo ^c   Hedrich, Rainer ^a,b   Deeken, Rosalia ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DESATURASE; ARABIDOPSIS PROTEIN; FAD3 PROTEIN, ARABIDOPSIS; FATTY ACID; PHOSPHOLIPID; SAD6 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; CELL HYPOXIA; CHLOROPLAST; DROUGHT; ENDOPLASMIC RETICULUM; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMIDITY; INFLORESCENCE; METABOLISM; MUTATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; PLANT TUMOR; SIGNAL TRANSDUCTION; UPREGULATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL HYPOXIA; CHLOROPLASTS; DROUGHTS; ENDOPLASMIC RETICULUM; FATTY ACID DESATURASES; FATTY ACIDS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HUMIDITY; INFLORESCENCE; MUTATION; PHOSPHOLIPIDS; PLANT LEAVES; PLANT TUMORS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; UP-REGULATION;

EID: 84893515011     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.230326     Document Type: Article

References (70)

1. Ahmann K, Heilmann M, Feussner I (2011) Identification of a D4-desaturase from the microalga Ostreococcus lucimarinus. Eur J Lipid Sci Technol 113: 832-840
2. An YQ, McDowell JM, Huang S, McKinney EC, Chambliss S, Meagher RB (1996) Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J 10: 107-121
3. Bayer MH (1991) Fatty acid composition of galactolipids and phospholipids in neoplasmatic plant tissues (cecidia) and normal leaf tissue. Physiol Plant 81: 313-318
4. Berberich T, Harada M, Sugawara K, Kodama H, Iba K, Kusano T (1998) Two maize genes encoding omega-3 fatty acid desaturase and their differential expression to temperature. Plant Mol Biol 36: 297-306
5. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917
6. Blokhina O, Fagerstedt KV (2010) Oxidative metabolism, ROS and NO under oxygen deprivation. Plant Physiol Biochem 48: 359-373
7. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot (Lond) 91: 179-194
8. Brown DJ, Beevers H (1987) Fatty acids of rice coleoptiles in air and anoxia. Plant Physiol 84: 555-559
9. Browse J, McConn M, James D Jr, Miquel M (1993) Mutants of Arabidopsis deficient in the synthesis of alpha-linolenate: biochemical and genetic characterization of the endoplasmic reticulum linoleoyl desaturase. J Biol Chem 268: 16345-16351
10. Cahoon EB, Mills LA, Shanklin J (1996) Modification of the fatty acid composition of Escherichia coli by coexpression of a plant acyl-acyl carrier protein desaturase and ferredoxin. J Bacteriol 178: 936-939
11. Cahoon EB, Shah S, Shanklin J, Browse J (1998) A determinant of substrate specificity predicted from the acyl-acyl carrier protein desaturase of developing cat's claw seed. Plant Physiol 117: 593-598
12. Cao Y, Xian M, Yang J, Xu X, Liu W, Li L (2010) Heterologous expression of stearoyl-acyl carrier protein desaturase (S-ACP-DES) from Arabidopsis thaliana in Escherichia coli. Protein Expr Purif 69: 209-214
13. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
14. Collados R, Andreu V, Picorel R, Alfonso M (2006) A light-sensitive mechanism differently regulates transcription and transcript stability of omega3 fatty-acid desaturases (FAD3, FAD7 and FAD8) in soybean photosynthetic cell suspensions. FEBS Lett 580: 4934-4940
15. Crawford R (1992) Oxygen availability as an ecological limit to plant distribution. Adv Ecol Res 23: 93-185
16. Curtis MD, Grossniklaus U (2003) A Gateway cloning vector set for highthroughput functional analysis of genes in planta. Plant Physiol 133: 462-469
17. Dakhma WS, Zarrouk M, Cherif A (1995) Effects of drought-stress on lipids in rape leaves. Phytochemistry 40: 1383-1386
18. Deeken R, Engelmann JC, Efetova M, Czirjak T, Müller T, Kaiser WM, Tietz O, Krischke M, Mueller MJ, Palme K, et al (2006) An integrated view of gene expression and solute profiles of Arabidopsis tumors: a genome-wide approach. Plant Cell 18: 3617-3634
19. Efetova M, Zeier J, Riederer M, Lee CW, Stingl N, Mueller M, Hartung W, Hedrich R, Deeken R (2007) A central role of abscisic acid in drought stress protection of Agrobacterium-induced tumors on Arabidopsis. Plant Physiol 145: 853-862
20. Gao J, Ajjawi I, Manoli A, Sawin A, Xu C, Froehlich JE, Last RL, Benning C (2009) FATTY ACID DESATURASE4 of Arabidopsis encodes a protein distinct from characterized fatty acid desaturases. Plant J 60: 832-839
21. Gee MM, Sun CN, Dwyer JD (1967) An electron microscope study of sunflower crown gall tumor. Protoplasma 64: 195-200
22. Gibson S, Arondel V, Iba K, Somerville C (1994) Cloning of a temperature-regulated gene encoding a chloroplast omega-3 desaturase from Arabidopsis thaliana. Plant Physiol 106: 1615-1621
23. Gigon A, Matos AR, Laffray D, Zuily-Fodil Y, Pham-Thi AT (2004) Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype Columbia). Ann Bot (Lond) 94: 345-351
24. Grantz DA (1990) Plant response to atmospheric humidity. Plant Cell Environ 13: 667-679
25. Holsters M, Silva B, Van Vliet F, Genetello C, De Block M, Dhaese P, Depicker A, Inzé D, Engler G, Villarroel R, et al (1980) The functional organization of the nopaline A. tumefaciens plasmid pTiC58. Plasmid 3: 212-230
26. James DW, Dooner HK (1990) Isolation of EMS-induced mutants in Arabidopsis altered in seed fatty acid composition. Theor Appl Genet 80: 241-245
27. Jia SR, Kumar PP, Kush A (1996) Oxidative stress in Agrobacteriuminduced tumors on Kalanchoe plants. Plant J 10: 545-551
28. Jiang CJ, Shimono M, Maeda S, Inoue H, Mori M, Hasegawa M, Sugano S, Takatsuji H (2009) Suppression of the rice fatty-acid desaturase gene OsSSI2 enhances resistance to blast and leaf blight diseases in rice. Mol Plant Microbe Interact 22: 820-829
29. Kachroo A, Shanklin J, Whittle E, Lapchyk L, Hildebrand D, Kachroo P (2007) The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis. Plant Mol Biol 63: 257-271
30. Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig DF (2001) A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc Natl Acad Sci USA 98: 9448-9453
31. Kim SI, Veena, Gelvin SB (2007) Genome-wide analysis of Agrobacterium T-DNA integration sites in the Arabidopsis genome generated under non-selective conditions. Plant J 51: 779-791
32. Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204: 383-396
33. Kwast KE, Burke PV, Poyton RO (1998) Oxygen sensing and the transcriptional regulation of oxygen-responsive genes in yeast. J Exp Biol 201: 1177-1195
34. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics. 23: 2947-2948
35. Latz A, Ivashikina N, Fischer S, Ache P, Sano T, Becker D, Deeken R, Hedrich R (2007) In planta AKT2 subunits constitute a pH-and Ca2+-sensitive inward rectifying K+ channel. Planta 225: 1179-1191
36. Lee CW, Efetova M, Engelmann JC, Kramell R, Wasternack C, Ludwig-Müller J, Hedrich R, Deeken R (2009) Agrobacterium tumefaciens promotes tumor induction by modulating pathogen defense in Arabidopsis thaliana. Plant Cell 21: 2948-2962
37. Lightner J, Wu J, Browse J (1994) A mutant of Arabidopsis with increased levels of stearic acid. Plant Physiol 106: 1443-1451
38. Liu F, Vantoai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137: 1115-1129
39. Loreti E, Poggi A, Novi G, Alpi A, Perata P (2005) A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiol 137: 1130-1138
40. Los DA, Murata N (1998) Structure and expression of fatty acid desaturases. Biochim Biophys Acta 1394: 3-15
41. McConn M, Hugly S, Browse J, Somerville C (1994) A mutation at the fad8 locus of Arabidopsis identifies a second chloroplast [omega]-3 desaturase. Plant Physiol 106: 1609-1614
42. Mène-Saffrané L, Dubugnon L, Chételat A, Stolz S, Gouhier-Darimont C, Farmer EE (2009) Nonenzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis. J Biol Chem 284: 1702-1708
43. Mikami K, Murata N (2003) Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. Prog Lipid Res 42: 527-543
44. Monteiro de Paula F, Pham-Thi A, Zuily-Fodil Y, Ferrari-Iliou R, Vieira da Silva J, Mazliak P (1993) Effect of water stress on the biosynthesis and degradation of polyunsaturated lipid molecular species in leaves of Vigna unguiculata. Plant Physiol Biochem 31: 707-715
45. Mustroph A, Zanetti ME, Jang CJ, Holtan HE, Repetti PP, Galbraith DW, Girke T, Bailey-Serres J (2009) Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc Natl Acad Sci USA 106: 18843-18848
46. Nakagawa Y, Sugioka S, Kaneko Y, Harashima S (2001) O2R, a novel regulatory element mediating Rox1p-independent O2 and unsaturated fatty acid repression of OLE1 in Saccharomyces cerevisiae. J Bacteriol 183: 745-751
47. Nour-Eldin HH, Hansen BG, Nørholm MH, Jensen JK, Halkier BA (2006) Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res 34: e122
48. Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7: 957-970
49. Okamoto M, Tanaka Y, Abrams SR, Kamiya Y, Seki M, Nambara E (2009) High humidity induces abscisic acid 89-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis. Plant Physiol 149: 825-834
50. Okuley J, Lightner J, Feldmann K, Yadav N, Lark E, Browse J (1994) Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid synthesis. Plant Cell 6: 147-158
51. Pineda M, Sajnani C, Barón M (2010) Changes induced by the Pepper mild mottle tobamovirus on the chloroplast proteome of Nicotiana benthamiana. Photosynth Res 103: 31-45
52. Pitzschke A, Hirt H (2010) New insights into an old story: Agrobacteriuminduced tumour formation in plants by plant transformation. EMBO J 29: 1021-1032
53. Schultz DJ, Suh MC, Ohlrogge JB (2000) Stearoyl-acyl carrier protein and unusual acyl-acyl carrier protein desaturase activities are differentially influenced by ferredoxin. Plant Physiol 124: 681-692
54. Schurr U, Schuberth B, Aloni R, Pradel KS, Schmundt D, Jaehne B, Ullrich CI (1996) Structural and functional evidence for xylem-mediated water transport and high transpiration in Agrobacterium tumefaciensinduced tumors of Ricinus communis. Bot Acta 109: 405-411
55. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18: 1121-1133
56. Shanklin J, Somerville C (1991) Stearoyl-acyl-carrier-protein desaturase from higher plants is structurally unrelated to the animal and fungal homologs. Proc Natl Acad Sci USA 88: 2510-2514
57. Somerville C, Browse J (1991) Plant lipids: metabolism, mutants, and membranes. Science 252: 80-87
58. Szyroki A, Ivashikina N, Dietrich P, Roelfsema MR, Ache P, Reintanz B, Deeken R, Godde M, Felle H, Steinmeyer R, et al (2001) KAT1 is not essential for stomatal opening. Proc Natl Acad Sci USA 98: 2917-2921
59. Thomashow MF, Nutter R, Montoya AL, Gordon MP, Nester EW (1980) Integration and organization of Ti plasmid sequences in crown gall tumors. Cell 19: 729-739
60. Thompson GA, Scherer DE, Foxall-Van Aken S, Kenny JW, Young HL, Shintani DK, Kridl JC, Knauf VC (1991) Primary structures of the precursor and mature forms of stearoyl-acyl carrier protein desaturase from safflower embryos and requirement of ferredoxin for enzyme activity. Proc Natl Acad Sci USA 88: 2578-2582
61. Tooker JF, De Moraes CM (2009) A gall-inducing caterpillar species increases essential fatty acid content of its host plant without concomitant increases in phytohormone levels. Mol Plant Microbe Interact 22: 551-559
62. Torres-Franklin ML, Repellin A, Huynh VB, d'Arcy-Lameta A, Zuily-Fodil Y, Pham-Thi AT (2009) Omega-3 fatty acid desaturase (FAD3, FAD7, FAD8) gene expression and linolenic acid content in cowpea leaves submitted to drought and after rehydration. Environ Exp Bot 65: 162-169
63. Triantaphylidès C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, Van Breusegem F, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148: 960-968
64. Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 30: 967-977
65. Vasconcelles MJ, Jiang Y, McDaid K, Gilooly L, Wretzel S, Porter DL, Martin CE, Goldberg MA (2001) Identification and characterization of a low oxygen response element involved in the hypoxic induction of a family of Saccharomyces cerevisiae genes: implications for the conservation of oxygen sensing in eukaryotes. J Biol Chem 276: 14374-14384
66. Vergunst AC, Schrammeijer B, den Dulk-Ras A, de Vlaam CM, Regensburg-Tuïnk TJ, Hooykaas PJ (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290: 979-982
67. Vergunst AC, van Lier MC, den Dulk-Ras A, Hooykaas PJ (2003) Recognition of the Agrobacterium tumefaciens VirE2 translocation signal by the VirB/D4 transport system does not require VirE1. Plant Physiol 133: 978-988
68. Veselov D, Langhans M, Hartung W, Aloni R, Feussner I, Götz C, Veselova S, Schlomski S, Dickler C, Bächmann K, et al (2003) Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid. Planta 216: 512-522
69. Whittle E, Cahoon EB, Subrahmanyam S, Shanklin J (2005) A multifunctional acyl-acyl carrier protein desaturase from Hedera helix L. (English ivy) can synthesize 16-and 18-carbon monoene and diene products. J Biol Chem 280: 28169-28176
70. Zhang M, Barg R, Yin M, Gueta-Dahan Y, Leikin-Frenkel A, Salts Y, Shabtai S, Ben-Hayyim G (2005) Modulated fatty acid desaturation via overexpression of two distinct omega-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants. Plant J 44: 361-371