Pathogen-Responsive Expression of a Putative ATP-Binding Cassette Transporter Gene Conferring Resistance to the Diterpenoid Sclareol Is Regulated by Multiple Defense Signaling Pathways in Arabidopsis

Plant Physiology

Volumn 133, Issue 3, 2003, Pages 1272-1284

  Campbell, Emma J ^a   Schenk, Peer M ^a   Kazan, Kemal ^a   Penninckx, Iris A M A ^b   Anderson, Jonathan P ^a   Maclean, Don J ^a   Cammue, Bruno P A ^b   Ebert, Paul R ^a   Manners, John M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GENES; PLANTS (BOTANY); PROTEINS; SEED;

ARABIDPOSIS GENE;

ADENOSINETRIPHOSPHATE;

ARABIDOPSIS; INSERTION SEQUENCES;

EID: 0344099015     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.103.024182     Document Type: Article

References (55)

1. Aubourg S, Lecharny A, Bohlman J (2002) Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol Genet Genome 267: 730-745
2. Bailey JA, Vincent GG, Burden RS (1974) Diterpenes from Nicotiana glutinosa and their effect on fungal growth. J Gen Microbiol 85: 57-64
3. Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9: 1573-1584
4. Brown RL, Kazan K, McGrath K, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol 132: 1020-1032
5. Charrier B, Champion A, Henry I, Martin K (2002) Expression profiling of the whole Arabidopsis shaggy-like kinase multigene family by real-time reverse transcriptase-polymerase chain reaction. Plant Physiol 130: 577-590
6. Chen F, Tholl D, D'Auria JC, Farooq A, Pichersky E (2003) Biosynthesis and emission of terpenoids volatiles from Arabidopsis flowers. Plant Cell 15: 481-494
7. Clarke JD, Volko SM, Ledford H, Ausubel F, Dong X (2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12: 2175-2190
8. Coleman JOD, Blake-Kaiff MMA, Davies TGE (1997) Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentation. Trends Plant Sci 2: 144-151
9. Cutler HG, Reid W, Deletang J (1977) Plant growth inhibiting properties of diterpenes from tobacco. Plant Cell Physiol 18: 711-714
10. Davies TGE, Coleman JOD (2000) The Arabidopsis thaliana ATP-binding cassette proteins: an emerging superfamily. Plant Cell Environ 23: 431-443
11. Desikan RA-H, Mackerness S, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127: 159-172
12. Devadas SK, Enyedi A, Raina R (2002) The Arabidopsis hrl1 mutation reveals novel overlapping roles for salicylic acid, jasmonic acid and ethylene signalling in cell death and defence against pathogens. Plant J 30: 467-480
13. Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1: 316-323
14. Du L, Chen Z (2000) Identification of genes encoding receptor-like protein kinases as possible targets of pathogen-and salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. Plant J 24: 837-847
15. Eggermont K, Goderis IJ, Broekaert WF (1996) High-throughput RNA extraction from plant samples based on homogenisation by reciprocal shaking in the presence of a mixture of sand and glass beads. Plant Mol Biol Rep 14: 273-279
16. Feys BJ, Parker JE (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet 16: 449-455
17. Fleißner A, Sopalla C, Weldring K-M (2002) An ATP-binding cassette multidrug-resistance transporter is necessary for tolerance of Gibberela pulicaris to phytoalexins and virulence on potato tubers. Mol Plant-Microbe Interact 15: 102-108
18. Gaedeke N, Klein M, Kolukisaoglu U, Forestier C, Muller A, Ansorge M, Becker D, Mamnun Y, Kuchler K, Schulz B et al. (2001) The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J 20: 1875-1887
19. Grec S, Vanham D, de Ribaucourt JC, Purnelle B, Boutry M (2003) Identification of regulatory sequence elements within the transcription promoter region of NpABC1, a gene encoding a plant ABC transporter induced by diterpenes. Plant J 35: 237-250
20. Hayashi K, Schoonbeek HJ, Waard MA (2002) Bcmfs1, a novel major facilitator superfamily transporter from Botrytis cinerea, provides tolerance towards the natural toxic compounds camptothecin and cercosporin and towards fungicides. Appl Environ Microbiol 68: 4996-5004
21. Jasinski M, Ducos E, Martinoia E, Boutry M (2003) The ATP-binding cassette transporters: structure, function and gene family comparison between rice and Arabidopsis. Plant Physiol 131: 1169-1177
22. Jasinski M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert, Boutry M (2001) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13: 1095-1107
23. Klinedinst S, Pascuzzi P, Redman J, Desai M, Arias JR (2000) A xenobiotic-stress-activated transcription factor and its cognate target genes are preferentially expressed in root tip meristems. Plant Mol Biol 42: 679-688
24. Kunkel BN, Brooks DM (2002) Crosstalk between signalling pathways in pathogen defence. Current Opin Plant Biol 5: 325-331
25. Li L, He Z, Pandey GK, Tsuchiya T, Luan S (2002) Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J Biol Chem 277: 5360-5368
26. Logemann E, Hahlbrock K (2002) Crosstalk among stress responses in plants: pathogen defense overrides UV protection through an inversely regulated ACE/ACE type of light-responsive gene promoter unit. Proc Natl Acad Sci USA 99: 2428-2432
27. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis during systemic acquired resistance. Nat Genet 26: 403-410
28. Mladek C, Guger K, Hauser M-T (2003) Identification and characterization of the ARIADNE gene family in Arabidopsis. A group of putative E3 ligases. Plant Physiol 131: 27-40
29. Mohr PG, Cahill DM (2003) Abscisic acid influence the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct Plant Biol 30: 461-469
30. Murray SL, Thomson C, Chini A, Read ND, Loake GJ (2002) Characterization of a novel, defense-related Arabidopsis mutant, cir1, isolated by luciferase imaging. Mol Plant-Microbe Interact 15: 557-566
31. Nakaune R, Adachi K, Nawata O, Tomiyama M, Akutsu K, Hibi T (1998) A novel ATP-binding cassette transporter involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum. Appl Environ Microbiol 64: 3983-3988
32. Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13: 2441-2454
33. Orsel M, Krapp A, Daniel-Vedele F (2002) Analysis of the NRT2 nitrate transporter family in Arabidopsis: structure and gene expression. Plant Physiol 129: 886-896
34. Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE et al. (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103: 1111-1120
35. Rairdan GJ, Delaney TP (2002) Role of salicylic acid and NIM1/NPR1 in race-specific resistance in Arabidopsis. Genetics 161: 803-811
36. Rate DN, Cuenca JV, Bowman G, Guttman DS, Greenberg JT (1999) The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signalling pathway in controlling cell death, defenses and cell growth. Plant Cell 11: 1695-1708
37. Rate DN, Greenberg JT (2001) The Arabidopsis aberrant growth and death 2 mutant shows resistance to Pseudomonas syringae and reveals a role for NPR1 in suppressing hypersensitive cell death. Plant J 27: 203-211
38. Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defence gene expression. Curr Opin Plant Biol 1: 401-411
39. Richmond T, Somerville S (2000) Chasing the dream: plant EST microarrays. Curr Opin Plant Biol 3: 108-116
40. Sasabe M, Toyoda K, Shiraishi T, Inagaki Y, Ichinose Y (2002) cDNA cloning and characterization of tobacco ABC transporter: NtPDR1 is a novel elicitor-responsive gene. FEBS Lett 518: 164-168
41. Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E (2001) Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13: 113-123
42. Schenk PM, Kazan K, Manners JM, Anderson JP, Simpson B, Wilson I, Somerville SC, Maclean DJ (2003) Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. Plant Physiol 132: 999-1010
43. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by cDNA microarray analysis. Proc Natl Acad Sci USA 97: 11655-11660
44. Schoonbeek H, Del Sorbo G, De Waard MA (2001) The ABC transporter BcatrB affects the sensitivity of Botrytis cinerea to the phytoalexin resveratrol and the fungicide fenpiclonil. Mol Plant-Microbe Interact 14: 562-571
45. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Microarray monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA. Plant Cell 13: 61-72
46. Seo S, Seto H, Koshino H, Yoshida S, Ohashi Y (2003) A diterpene as an endogenous signal for the activation of defense responses to infection with tobacco mosaic virus and wounding in tobacco. Plant Cell 15: 863-873
47. Shah J, Kachroo P, Nandi A, Klessig DF (2001) A recessive mutation in the Arabidopsis SSI2 gene confers SA-and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens. Plant J 25: 563-574
48. Shimada Y, Goda H, Nakamura A, Takatsuto S, Fujioka S, Yoshida S (2003) Organ-specific expression of Brassinosteroid-biosynthetic genes and distribution of endogenous Brassinosteroids in Arabidopsis. Plant Physiol 131: 287-297
49. Siebert PD, Chenchik A, Kellogg DE, Lukyanov KA, Lukyanov SA (1995) An improved PCR method for walking in uncloned genomic DNA. Nucleic Acids Res 23: 1087-1088
50. Sidler M, Hassa P, Hasan S, Ringli C, Dudler R (1998) Involvement of an ABC transporter in a developmental pathway regulating hypocotyl cell elongation in the light. Plant Cell 10: 1623-1636
51. Thomma BP, Penninckx IA, Broekaert WF, Cammue BP (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13: 63-68
52. Urban M, Bhargava T, Hamer JE (1999) An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO J 18: 512-521
53. van den Brûle S, Müller A, Fleming AJ, Smart CC (2002) The ABC transporter SpTUR2 confers resistance to the antifungal diterpene sclareol. Plant J 30: 649-662
54. van den Brûle S, Smart CC (2002) The Plant PDR family of ABC transporters. Planta 216: 95-106
55. Yu D, Chen C, Chen Z (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13: 1527-1540