Disruption of glycosylphosphatidylinositol-anchored lipid transfer protein gene altered cuticular lipid composition, increased plastoglobules, and enhanced susceptibility to infection by the fungal pathogen alternaria brassicicola

Plant Physiology

Volumn 150, Issue 1, 2009, Pages 42-54

  Lee, Saet Buyl ^a   Go, Young Sam ^a   Bae, Hyun Jong ^b   Park, Jong Ho ^c,d   Cho, Sung Ho ^c,d   Cho, Hong Joo ^e   Lee, Dong Sook ^e   Park, Ohkmae K ^e   Hwang, Inhwan ^f   Suh, Mi Chung ^a  

^a Department of Plant Biotechnology   (South Korea)

^b Department of Wood Science and Technology ^*

^c Chonnam National University   (South Korea)

^d Inha University   (South Korea)

^e Korea University   (South Korea)

^f Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNARIA; ALTERNARIA BRASSICICOLA; ARABIDOPSIS; ARABIDOPSIS THALIANA; FUNGI; TRACHEOPHYTA;

EID: 66149095028     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.109.137745     Document Type: Article

References (69)

1. Aarts MGM, Keijzer CJ, Stiekema WJ, Pereira A (1995) Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7: 2115-2127
2. Abel S, Theologis A (1998) Transient gene expression in protoplasts of Arabidopsis thaliana. Methods Mol Biol 82: 209-217
3. An G (1987) Binary Ti vector for plant transformation and promoter analysis. Methods Enzymol 153: 292-305
4. Austin JR II, Frost E, Vidi PA, Kessler F, Staehelin LA (2006) Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18: 1693-1703
5. Baker CJ, McCormick SL, Bateman DF (1982) Effects of purified cutin esterase upon the permeability and mechanical strength of cutin membranes. Phytopathology 72: 420-423
6. Bechtold N, Ellis J, Pelletier G (1993) In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C R Acad Sci Paris Life Sci 316: 1194-1199
7. Beisson F, Koo AJ, Ruuska S, Schwender J, PollardM, Thelen JJ, Paddock T, Salas JJ, Savage L, Milcamps A, et al (2003) Arabidopsis gene 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 Physiol 132: 681-697
8. Bessire M, Chassot C, Jacquat AC, Humphry M, Borel S, Petétot JMC, Métraux JP, Nawrath C (2007) A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J 26: 2158-2168
9. Bevan MW (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res 12: 8711-8721
10. Bird D, Beisson F, Brigham A, Shin J, Greer S, Jetter R, Kunst L, Wu X, Yephremov A, Samuels L (2007) Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J 52: 485-498
11. Bonaventure G, Beisson F, Ohlrogge J, Pollard M (2004) Analysis of the aliphatic monomer composition of polyesters associated with Arabidopsis epidermis: occurrence of octadeca-cis-6,cis-9-diene-1,18-dioate as the major component. Plant J 40: 920-930
12. Borner GHH, Lilley KS, Stevens TJ, Dupree P (2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis: a proteomic and genomic analysis. Plant Physiol 132: 568-577
13. Bréhélin C, Kessler F, van Wijk KJ (2007) Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12: 260-266
14. Cameron KD, Teece MA, Smart LB (2006) Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiol 140: 176-183
15. Choi AM, Lee SB, Cho SH, Hwang I, Hur CG, Suh MC (2008) Isolation and characterization of multiple abundant lipid transfer protein isoforms in developing sesame (Sesamum indicum L.) seeds. Plant Physiol Biochem 46: 127-139
16. Clemens S, Kunst L, inventors. January 2, 2001. Plant long chain fatty acid biosynthetic enzyme. European Patent Application WO 0107586
17. Dietrich CR, Perera MA, D Yandeau-Nelson M, Meeley RB, Nikolau BJ, Schnable PS (2005) Characterization of two GL8 paralogs reveals that the 3-ketoacyl reductase component of fatty acid elongase is essential for maize (Zea mays L.) development. Plant J 42: 844-861
18. Elortza F,Mohammed S, Bunkenborg J, Foster LJ, Nühse TS, Brodbeck U, Peck SC, Jensen ON (2006) Modification-specific proteomics of plasma membrane proteins: identification and characterization of glycosylphosphatidylinositol- anchored proteins released upon phospho-lipase D treatment. J Proteome Res 5: 935-943
19. Fan CY, Köller W (1998) Diversity of cutinases from plant pathogenic fungi: differential and sequential expression of cutinolytic esterases by Alternaria brassicicola. FEMS Microbiol Lett 158: 33-38
20. Fiebig A, Mayfield JA, Miley NL, Chau S, Fischer RL, Preuss D (2000) Alterations in CER6, a gene identical to CUT1, differentially affect longchain lipid content on the surface of pollen and stems. Plant Cell 12: 2001-2008
21. Heredia A (2003) Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer. Biochim Biophys Acta 1620: 1-7
22. Hoffmann-Benning S, Kende H (1994) Cuticle biosynthesis in rapidly growing internodes of deepwater rice. Plant Physiol 104: 719-723
23. Holloway PJ (1982) Structure and histochemistry of plant cuticular membranes: an overview. In The Plant Cuticle. Academic Press, London, pp 1-32
24. Hooker TS,Millar AA, Kunst L (2002) Significance of the expression of the CER6 condensing enzyme for cuticular wax production in Arabidopsis. Plant Physiol 129: 1568-1580
25. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907
26. Jeffree CE (1996) Structure and ontogeny of plant cuticles. In G Kerstiens, ed, Plant Cuticles: An Integrated Functional Approach. BIOS Scientific Publishers, Oxford, pp 33-82
27. Jenks MA, Eigenbrode S, Lemieux B (2002) Cuticular waxes of Arabidopsis. In CR Somerville, EM Meyerowitz, eds, The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD, doi/10.1199/ tab.0016, http://www.aspb.org/publications/arabidopsis/
28. Jeroen N, Feron R, Huisman BAH, Fasolino A, Hilbers CW, Derksen J, Mariani C (2005) Lipid transfer proteins enhance cell wall extension in tobacco. Plant Cell 17: 2009-2019
29. Kader JC (1996) Lipid-transfer proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 627-654
30. Koch E, Slusarenko AJ (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2: 437-445
31. Kolattukudy PE (2001) Polyesters in higher plants. Adv Biochem Eng Biotechnol 71: 1-49
32. Kumar A, Tripathi K, Rana M, Purwar S, Garg GK(2004) Dibutyryl c-AMP as an inducer of sporidia formation: biochemical and antigenic changes during morphological differentiation of Karnal bunt (Tilletia indica) pathogen in axenic culture. J Biosci 29: 23-31
33. Kunst L, Samuels AL (2003) Biosynthesis and secretion of plant cuticular wax. Prog Lipid Res 42: 51-80
34. Kunst L, Samuels AL, Jetter R (2005) The plant cuticle: formation and structure of epidermal surfaces. In D Murphy, ed, Plant Lipids: Biology, Utilisation and Manipulation. Blackwell Scientific, Oxford, pp 270-302
35. Li Y, Beisson F, Koo AJ, Molina I, Pollard M, Ohlrogge J (2007) Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci USA 104: 18339-18344
36. Lolle SJ, Hsu W, Pruitt RE (1998) Genetic analysis of organ fusion in Arabidopsis thaliana. Genetics 149: 607-619
37. Luo B, Xue XY, Hu WL,Wang LJ, Chen XY (2007) An ABC transporter gene of Arabidopsis thaliana, AtWBC11, is involved in cuticle development and prevention of organ fusion. Plant Cell Physiol 48: 1790-1802
38. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signaling in Arabidopsis. Nature 419: 399-403
39. Mayor S, Riezman H (2004) Sorting GPI-anchored proteins. Nat Rev Mol Cell Biol 5: 110-120
40. McRoberts N, Lennard JH (1996) Pathogen behaviour and plant cell reactions in interactions between Alternaria species and leaves of host and nonhost plants. Plant Pathol 45: 742-752
41. Millar AA, Clemens S, Zachgo S, Giblin EM, Taylor DC, Kunst L (1999) CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatty acid condensing enzyme. Plant Cell 11: 825-838
42. Millar AA, Kunst L (1997) Very-long-chain fatty acid biosynthesis is controlled through the expression and specificity of the condensing enzyme. Plant J 12: 121-131
43. MinMK, Kim SJ, Miao Y, Shin JY, Jiang L, Hwang I (2007) Overexpression of Arabidopsis AGD7 causes relocation of Golgi-localized proteins to the endoplasmic reticulum and inhibits protein trafficking in plant cells. Plant Physiol 143: 1601-1614
44. Molina A, García-Olmedo F (1997) Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2. Plant J 12: 669-675
45. Moran P, Raab H, Kohr WJ, Caras IW (1991) Glycophospholipid membrane anchor attachment: molecular analysis of the cleavage/attachment site. J Biol Chem 266: 1250-1257
46. Motose H, Sugiyama M, Fukuda H (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429: 873-878
47. Nawrath C (2002) The biopolymers cutin and suberin. In CR Somerville, EM Meyerowitz, eds, The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD, doi/10.1199/tab.0021, http://www.aspb.org/ publications/arabidopsis/
48. Nawrath C (2006) Unraveling the complex network of cuticular structure and function. Curr Opin Plant Biol 9: 281-287
49. Nuoffer C, Horvath A, Riezman H (1993) Analysis of the sequence requirements for glycosylphosphatidylinositol anchoring of Saccharomyces cerevisiae Gas1 protein. J Biol Chem 268: 10558-10563
50. Pighin JA, Zheng H, Balakshin LJ, Goodman LP, Western TL, Jetter R, Kunst L, Samuels AL (2004) Plant cuticular lipid export requires an ABC transporter. Science 306: 702-704
51. Pyee J, Kolattukudy PE (1995) The gene for the major cuticular waxassociated protein and three homologous genes from broccoli (Brassica oleracea) and their expression patterns. Plant J 7: 49-59
52. Riederer M, Schreiber L (2001) Protecting against water loss: analysis of the barrier properties of plant cuticles. J Exp Bot 52: 2023-2032
53. Rowland O, Zheng H, Hepworth SR, Lam P, Jetter R, Kunst L (2006) CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol 142: 866-877
54. Roy-Barman S, Sautter C, Chattoo BB (2006) Expression of the lipid transfer protein Ace-AMP1 in transgenic wheat enhances antifungal activity and defense responses. Transgenic Res 15: 435-446
55. Schulz B, Frommer WB (2004) A plant ABC transporter takes the lotus seat. Science 306: 622-625
56. Schweizer P, Felix G, Buchala A, Muller C, Metraux JP (1996) Perception of free cutin monomers by plant cells. Plant J 10: 331-341
57. Shin DH, Lee JY, Hwang KY, Kim KK, Suh SW (1995) High-resolution crystal structure of the non-specific lipid-transfer protein from maize seedlings. Structure 3: 189-199
58. Sieber P, Schorderet M, Ryser U, Buchala A, Kolattukudy P, Metraux JP, Nawrath C (2000) Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12: 721-737
59. Somerville C, Browse J, Jaworski JG, Ohlrogge JB (2000) Lipids. In BB Buchanan, W Gruissem, RL Jones, eds, Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD, pp 456-527
60. Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protocols 1: 2019-2025
61. Stark RE, Tian S (2006) The cutin biopolymer matrix. In M Riederer, C Mü ller, eds, Biology of the Plant Cuticle. Blackwell Publishing, Oxford, pp 126-144
62. SuhMC, Samuels AL, Jetter R, Kunst L, Pollard M, Ohlrogge J, Beisson F (2005) Cuticular lipid composition, surface structure, and gene expression in Arabidopsis stem epidermis. Plant Physiol 139: 1649-1665
63. TianGW,Mohanty A, Chary SN, Li S, Paap B, Drakakaki G, Kopec CD, Li J, Ehrhardt D, Jackson D, et al (2004) High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol 135: 25-38
64. Todd J, Post-Beittenmiller D, Jaworski JG (1999) KCS1 encodes a fatty acid elongase 3-ketoacyl-CoA synthase affecting wax biosynthesis in Arabidopsis thaliana. Plant J 17: 119-130
65. Udenfriend S, Kodukula K (1995) How glycosylphosphatidylinositolanchored membrane proteins are made. Annu Rev Biochem 64: 563-591
66. Weigel D, Glazebrook J (2002) Arabidopsis: A Laboratory Manual, Ed 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 165-170
67. Yao K, Paliyath G, Humphrey RW, Hallet FR, Thompson JE (1991) Identification and characterization of nonsedimentable lipid-protein microvesicles. Proc Natl Acad Sci USA 88: 2269-2273
68. Yephremov A, Wisman E, Huijser P, Huijser C, Wellesen K, Saedler H (1999) Characterization of the FIDDLEHEAD gene of Arabidopsis reveals a link between adhesion response and cell differentiation in the epidermis. Plant Cell 11: 2187-2201
69. Zheng H, Rowland O, Kunst L (2005) Disruptions of the Arabidopsis enoyl-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis. Plant Cell 17: 1467-1481