Nicotiana plumbaginifolia plants silenced for the ATP-binding cassette transporter gene NpPDR1 show increased susceptibility to a group of fungal and oomycete pathogens

Molecular Plant Pathology

Volumn 10, Issue 5, 2009, Pages 651-663

  Bultreys, Alain ^a   Trombik, Tomasz ^b   Drozak, Anna ^b   Boutry, Marc ^b  

^a WALLOON AGRICULTURAL RESEARCH CENTRE   (Belgium)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BETA GLUCURONIDASE; VEGETABLE PROTEIN;

ARTICLE; BOTRYTIS; FLOWER; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; MICROBIOLOGY; OOMYCETES; PHYSIOLOGY; PLANT GENE; PLANT LEAF; PLANT ROOT; TOBACCO;

ATP-BINDING CASSETTE TRANSPORTERS; BOTRYTIS; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENES, PLANT; GLUCURONIDASE; OOMYCETES; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; TOBACCO;

BOTRYOTINIA FUCKELIANA; FUNGI; FUSARIUM OXYSPORUM; HYPHOMYCETES; NICOTIANA PLUMBAGINIFOLIA; NICOTIANA TABACUM; PHYTOPHTHORA; PHYTOPHTHORA NICOTIANAE; THANATEPHORUS CUCUMERIS;

EID: 68449104863     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2009.00562.x     Document Type: Article

References (50)

1. Alves-Santos, F.M., Martínez-Bermejoa, D., Rodríguez- Molinab, M.C. Dieza, J.J. (2007) Cultural characteristics, pathogenicity and genetic diversity of Fusarium oxysporum isolates from tobacco fields in Spain. Physiol. Mol. Plant Pathol. 71, 26 32.
2. Apple, J.L. (1962) Physiological specialization within Phytophthora parasitica var. nicotianae. Phytopathology, 52, 351 354.
3. Armstrong, G.M. Armstrong, J.K. (1958) The Fusarium wilt complex as related to the sweet potato. Plant Dis. Rep. 42, 1319 1329.
4. Bradford, M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248 254.
5. Braun, P.G. Sutton, J.C. (1988) Infection cycle and population dynamics of Botrytis cinerea in strawberry leaves. Can. J. Plant Pathol. 10, 133 141.
6. van den Brûle, S. Smart, C.C. (2002) The plant PDR family of ABC transporters. Planta, 216, 95 106.
7. van den Brûle, S., Muller, A., Fleming, A.J. Smart, C.C. (2002) The ABC transporter SpTUR2 confers resistance to the antifungal diterpene sclareol. Plant J. 30, 649 662.
8. Campbell, E.J., Schenk, P.M., Kazan, K., Penninckx, I.A., Anderson, J.P., Maclean, D.J., Cammue, B.P., Ebert, P.R. Manners, J.M. (2003) 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 Physiol. 133, 1272 1284.
9. Carlson, S.R., Wolff, M.F., Shew, H.D. Wernsman, E.A. (1997) Inheritance of resistance to race 0 of Phytophthora parasitica var. nicotianae from the flue-cured tobacco cultivar Coker 371-Gold. Plant Dis. 81, 1269 1274.
10. Ceresini, P.C., Shew, H.D., Vilgalys, R.J. Cubeta, M.A. (2002) Genetic diversity of Rhizoctonia solani AG-3 from potato and tobacco in North Carolina. Mycologia, 94, 437 449.
11. Cessna, S.G., Sears, V.E., Dickman, M.B. Low, P.S. (2000) Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell, 12, 2191 2199.
12. Clark, C.A., Hyun, J.-W. Hoy, M.W. (1998) Relationships among wilt-inducing isolates of Fusarium oxysporum from sweet potato and tobacco. Plant Dis. 82, 530 536.
13. Crouzet, J., Trombik, T., Fraysse, A.S. Boutry, M. (2006) Organization and function of the plant pleiotropic drug resistance ABC transporter family. FEBS Lett. 580, 1123 1130.
14. Csinos, A.S. (1999) Stem and root resistance to tobacco black shank. Plant Dis. 83, 777 780.
15. Csinos, A.S. (2005) Relationship of isolate origin to pathogenicity of race 0 and 1 of Phytophthora parasitica var. nicotianae on tobacco cultivars. Plant Dis. 89, 332 337.
16. Deighton, N., Muckenschnabel, I., Colmenares, A.J., Collado, I.G. Williamson, B. (2001) Botrydial is produced in plant tissues infected by Botrytis cinerea. Phytochemistry, 57, 689 692.
17. Derckel, J.-P., Baillieul, F., Manteau, S., Audran, J.-C., Haye, B., Lambert, B. Legendre, L. (1999) Differential induction of grapevine defenses by two strains of Botrytis cinerea. Phytopathology, 89, 197 203.
18. Eichhorn, H., Klinghammer, M., Becht, P. Tenhaken, R. (2006) Isolation of a novel ABC-transporter gene from soybean induced by salicylic acid. J. Exp. Bot. 57, 2193 2201.
19. Glombitza, S., Dubuis, P.H., Thulke, O., Welzl, G., Bovet, L., Gotz, M., Affenzeller, M., Geist, B., Hehn, A., Asnaghi, C., Ernst, D., Seidlitz, H.K., Gundlach, H., Mayer, K.F., Martinoia, E., Werck-Reichhart, D., Mauch, F. Schaffner, A.R. (2004) Crosstalk and differential response to abiotic and biotic stressors reflected at the transcriptional level of effector genes from secondary metabolism. Plant Mol. Biol. 54, 817 835.
20. Grec, S., Vanham, D., de Ribaucourt, J.C., 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.
21. Gutierrez, W.A., Shew, H.D. Melton, T.A. (1997) Sources of inoculum and management for Rhizoctonia solani damping-off on tobacco transplants under greenhouse conditions. Plant Dis. 81, 604 606.
22. Holland, I.B. Blight, A.M. (1999) ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. J. Mol. Biol. 293, 381 399.
23. Holz, G., Gütschow, M., Coertze, S. Calitz, F.J. (2003) Occurrence of Botrytis cinerea and subsequent disease expression at different positions on leaves and bunches of grape. Plant Dis. 87, 351 358.
24. Jasinski, M., Stukkens, Y., Degand, H., Purnelle, B., Marchand-Brynaert, J. Boutry, M. (2001) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell, 13, 1095 1107.
25. 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.
26. Johnson, E.S., Wolff, M.F., Wernsman, E.A., Atchley, W.R. Shew, H.D. (2002) Origin of the black shank resistance gene, Ph, in tobacco cultivar Coker 371-Gold. Plant Dis. 86, 1080 1084.
27. Keller, M., Viret, O. Cole, F.M. (2003) Botrytis cinerea infection in grape flowers: defense reaction, latency, and disease expression. Phytopathology, 93, 316 322.
28. Kobae, Y., Sekino, T., Yoshioka, H., Nakagawa, T., Martinoia, E. Maeshima, M. (2006) Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant Cell Physiol. 47, 309 318.
29. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680 685.
30. Lee, M., Lee, K., Lee, J., Noh, E.W. Lee, Y. (2005) AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiol. 138, 827 836.
31. Locher, K.P. (2004) Structure and mechanism of ABC transporters. Curr. Opin. Struct. Biol. 14, 426 431.
32. Maliga, P., Sz-Breznovits, A. Marton, L. (1973) Streptomycin-resistant plants from callus culture of haploid tobacco. Nat. New Biol. 244, 29 30.
33. Masuda, D., Ishida, M., Yamaguchi, K., Yamaguchi, I., Kimura, M. Nishiuchi, T. (2007) Phytotoxic effects of trichothecenes on the growth and morphology of Arabidopsis thaliana. J. Exp. Bot. 58, 1617 1626.
34. +-ATPase activate the enzyme and modify the structure of the C-terminal region. J. Biol. Chem. 273, 34 837 34 842.
35. Pape, H. (1921) Beobachtungen bei Erkrankungen durch Botrytis. Gartenflora, 70, 48 50.
36. Peters, L. (1912) Krankheiten und Beschädigungen des Tabaks. Erster Teil. Krankheiten des Tabaks. Mitt. K. Biol. Anst. Land u. Forstw. 13, 7 76.
37. Powelson, R.L. (1960) Initiation of strawberry fruit rot caused by Botrytis cinerea. Phytopathology, 50, 491 494.
38. Rea, P.A. (2007) Plant ATP-binding cassette transporters. Annu. Rev. Plant Biol. 58, 347 375.
39. Rowe, H.C. Kliebenstein, D.J. (2008) Complex genetics control natural variation in Arabidopsis thaliana resistance to Botrytis cinerea. Genetics, 180, 2237 2250.
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. Smith, T.E. Shaw, K.J. (1943) Pathogenicity studies with Fusaria isolated from tobacco, sweet potato and cotton. Phytopathology, 33, 469 483.
42. Stein, M., Dittgen, J., Sanchez-Rodriguez, C., Hou, B.H., Molina, A., Schulze-Lefert, P., Lipka, V. Somerville, S. (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell, 18, 731 746.
43. Stukkens, Y., Bultreys, A., Grec, S., Trombik, T., Vanham, D. Boutry, M. (2005) NpPDR1, a pleiotropic drug resistance-type ATP-binding cassette transporter from Nicotiana plumbaginifolia, plays a major role in plant pathogen defense. Plant Physiol. 139, 341 352.
44. Sugiyama, A., Shitan, N., Sato, S., Nakamura, Y., Tabata, S. Yazaki, K. (2006) Genome-wide analysis of ATP-binding cassette (ABC) proteins in a model legume plant, Lotus japonicus: comparison with Arabidopsis ABC protein family. DNA Res. 13, 205 228.
45. Sullivan, M.J., Melton, T.A. Shew, H.D. (2005a) Fitness of races 0 and 1 of Phytophthora parasitica var. nicotianae. Plant Dis. 89, 1220 1228.
46. Sullivan, M.J., Melton, T.A. Shew, H.D. (2005b) Managing the race structure of Phytophthora parasitica var. nicotianae with cultivar rotation. Plant Dis. 89, 1285 1294.
47. Van Jaarsveld, E., Wingfield, M.J. Drenth, A. (2002) Evaluation of tobacco cultivars for resistance to races of Phytophthora nicotianae in South Africa. J. Phytopathol. 150, 456 462.
48. Van Jaarsveld, E., Wingfield, M.J. Drenth, A. (2003) Rapid seedling based screening technique to assay tobacco for resistance to Phytophthora nicotianae. J. Phytopathol. 151, 389 394.
49. Verrier, P.J., Bird, D., Burla, B., Dassa, E., Forestier, C., Geisler, M., Klein, M., Kolukisaoglu, U., Lee, Y., Martinoia, E., Murphy, A., Rea, P.A., Samuels, L., Schulz, B., Spalding, E.J., Yazaki, K. Theodoulou, F.L. (2008) Plant ABC proteins - a unified nomenclature and updated inventory. Trends Plant Sci. 13, 151 159.
50. Wolf, F.A. (1931) Gray mold of tobacco. J. Agric. Res. 43, 165 175.