Identification of natural diterpenes that inhibit bacterial wilt disease in Tobacco, Tomato and Arabidopsis

Plant and Cell Physiology

Volumn 53, Issue 8, 2012, Pages 1432-1444

  Seo, Shigemi ^a   Gomi, Kenji ^b   Kaku, Hisatoshi ^c   Abe, Hiroshi ^d   Seto, Hideharu ^e   Nakatsu, Shingo ^f   Neya, Masahiro ^f   Kobayashi, Michie ^a,i   Nakaho, Kazuhiro ^g   Ichinose, Yuki ^h   Mitsuhara, Ichiro ^a   Ohashi, Yuko ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b KAGAWA UNIVERSITY   (Japan)

^c Sakata Seed Ibérica SLU   (Japan)

^d RIKEN BIORESOURCE CENTER   (Japan)

^e RIKEN   (Japan)

^f KNC Laboratories Co Ltd   (Japan)

^g NATIONAL AGRICULTURAL RESEARCH CENTER   (Japan)

^h OKAYAMA UNIVERSITY   (Japan)

ⁱ NATIONAL INSTITUTE OF VEGETABLE AND TEA SCIENCE   (Japan)

Author keywords

ABC transporter; Diterpene; Ralstonia solanacearum; Wilt disease

Indexed keywords

ABC TRANSPORTER; ABIENOL; ABSCISIC ACID; ANTIINFECTIVE AGENT; ARABIDOPSIS PROTEIN; DITERPENE; ETHYLENE; ETHYLENE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE; NAPHTHOL DERIVATIVE; PDR12 PROTEIN, ARABIDOPSIS; SCLAREOL;

ARABIDOPSIS; ARTICLE; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROARRAY ANALYSIS; MICROBIOLOGY; MUTATION; PATHOGENICITY; PLANT DISEASE; PLANT ROOT; RALSTONIA SOLANACEARUM; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; TOBACCO; TOMATO;

ABSCISIC ACID; ANTI-BACTERIAL AGENTS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATP-BINDING CASSETTE TRANSPORTERS; DITERPENES; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; MICROARRAY ANALYSIS; MITOGEN-ACTIVATED PROTEIN KINASES; MUTATION; NAPHTHOLS; PLANT DISEASES; PLANT ROOTS; RALSTONIA SOLANACEARUM; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; TOBACCO;

EID: 84865216377     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs085     Document Type: Article

References (51)

1. Abe, H., Ohnishi, J., Narusaka, M., Seo, S., Narusaka, Y., Tsuda, S. et al. (2008) Function of jasmonate in response and tolerance of Arabidopsis to thrip feeding. Plant Cell Physiol. 49: 68-80.
2. Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H., Shinn, P. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. Bailey, J.A., Vincent, G.G. and Burden, R.S. (1974) Diterpenes from Nicotiana glutinosa and their effect on fungal growth. J. Gen. Microbiol. 85: 57-64.
4. Bailey, J.A., Carter, G.A., Burden, R.S. and Wain, R.L. (1975) Control of rust disease by diterpenes from Nicotiana glutinosa. Nature 255: 328-329.
5. Campbell, E.J., Schenk, P.M., Kazan, K., Penninckx, I.A.M.A., Anderson, J.P., Maclean, D.J. et al. (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: 1-13.
6. Chaturvedi, R., Venables, B., Petros2, R.A., Nalam, V., Li, M., Wang, X. et al. (2012) An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J. in press.
7. Chen, Y.Y., Lin, Y.M., Chao, T.C., Wang, J.F., Liu, A.C., Ho, F.I. et al. (2009) Virus-induced gene silencing reveals the involvement of ethylene-, salicylic acid-and mitogen-activated protein kinase-related defense pathways in the resistance of tomato to bacterial wilt. Physiol. Plant. 136: 324-335.
8. Cook, D., Barlow, E. and Sequeira, L. (1989) Genetic diversity of Pseudomonas solanacearum: detection of restriction fragment length polymorphisms with DNA probes that specify virulence and the hypersensitive response. Mol. Plant-Microbe Interact. 2: 113-121.
9. Cowan, M.M. (1999) Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12: 564-582.
10. Cutler, H.G., Reid, W.W. and Delétang, G. (1977) Plant growth inhibiting properties of diterpenes from tobacco. Plant Cell Physiol. 18: 711-714.
11. Deslandes, L., Pileur, F., Liaubet, L., Camut, S., Can, C., Williams, K. et al. (1998) Genetic characterization of RPS1, a recessive locus in Arabidopsis thaliana that confers resistance to the bacterial soil-borne pathogen Ralstonia solanacearum. Mol. Plant-Microbe Interact. 7: 659-667.
12. Deslandes, L., Olivier, J., Theulières, F., Hirsch, J., Feng, D.X., Bittner-Eddy, P. et al. (2002) Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R genes, a member of a novel family of resistance genes. Proc. Natl Acad. Sci. USA 99: 2404-2409.
13. Dong, X. (1998) SA, JA, ethylene, and disease resistance in plants. Curr. Opin. Plant Biol. 1: 316-323.
14. Eschen-Lippold, L., Altmann, S. and Rosahl, S. (2010) DL-b-Aminobutyric acid-induced resistance of potato against Phytophthora infestans requires salicylic acid but not oxylipins. Mol. Plant-Microbe Interact. 23: 585-592.
15. Friedrich, L., Lawton, K., Ruess, W., Masner, P., Specker, N., Gut Rella, M. et al. (1996) A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J. 10: 61-70.
16. Ghareeb, H., Bozsó, Z., Ott, P.G., Repennning, C., Stahl, F. and Wydra, K. (2011) Transcriptome of silicon resistance against Ralstonia solana-cearum in the silicon non-accumulation tomato implicates priming effect. Physiol. Mol. Plant Pathol. 75: 83-89.
17. Glazebrook, J. (2005) Contrasting mechanisms of defense against bio-trophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43: 205-227.
18. Grec, S., Vanham, D., de Ribaucourt, J.C., Purnelle, B. and 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.
19. Grimault, V. and Prior, P. (1994) Grafting tomato cultivars resistant or susceptible to bacterial wilt: analysis of resistance mechanisms. J. Phytopathol. 141: 330-344.
20. Guo, Z.H., Severson, R.F. and Wagner, G.J. (1994) Biosynthesis of the diterpene cis-abienol in cell-free extracts of tobacco trichomes. Arch. Biochem. Biophys. 308: 103-108.
21. Guo, Z.H. and Wagner, G.J. (1995) Biosynthesis of labdenediol and sclareol in cell-free extracts of trichomes of Nicotiana glutinosa. Planta 197: 627-632.
22. Hayward, A.C. (1991) Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 29: 65-87.
23. Hernández-Blanco, C., Feng, D.X., Hu, J., Sánchez-Vallet, A., Deslandes, L., Llorente, F. et al. (2007) Impairment of cellulose syn-thases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell 19: 890-903.
24. Hieda, T., Mikami, Y., Obi, Y. and Kisaki, T. (1982) Microbial transformation of cis-abienol. Agric. Biol. Chem. 46: 2249-2255.
25. Hirsch, J., Deslandes, L., Feng, D.X., Balagu, C. and Marco, Y. (2002) Delayed symptom development in ein2-1, and an Arabidopsis ethylene-insensitive mutant, in response to bacterial wilt disease caused by Ralstonia solanacearum. Phytopathology 92: 1142-1148.
26. Jackson, D.M. and Danehower, D.A. (1996) Integrated dace study: Nicotiana leaf-surface components and their effects on insect pests and diseases. In Plant Cuticles: An Integrated Functional Approach. Edited by Kerstines, G. pp. 231-254. BIOS Scientific Publishers, Oxford.
27. Jasiński, M., Stukkens, Y., Degand, H., Purnelle, B., Marchand-Brynaert, J. and Boutry, M. (2001) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpen-oid secretion. Plant Cell 13: 1095-1107.
28. Kang, J., Hwang, J.U., Lee, M., Kim, Y.Y., Assmann, S.M., Martinoia, E. et al. (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc. Natl Acad. Sci. USA 107: 2355-2360.
29. Kennedy, B.S., Nielsen, M.T., Severson, R.T., Sisson, V.A., Stephenson, M.K. and Jackson, D.M. (1992) Leaf surface chemicals from Nicotiana affecting germination of Peronospora tabacina (Adam) sporangia. J. Chem. Ecol. 18: 1467-1478.
30. Kobayashi, M., Seo, S., Hirai, K., Yamamoto-Katou, A., Katou, S., Seto, H. et al. (2010) Silencing of WIPK and SIPK mitogen-activated protein kinases reduces Tobacco mosaic virus accumulation but permits systemic viral movement in tobacco possessing the N resistance gene. Mol. Plant-Microbe Interact. 23: 1032-1041.
31. Leon-Reyes, A., Spoel, S.H., de Lange, E.S., Abe, H., Kobayashi, M., Tsuda, S. et al. (2009) Ethylene modulates the role of NONEXPRESSOR OF PARTHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol. 149: 1797-1809.
32. Liu, F., Wei, F., Wang, L., Liu, H., Zhu, X. and Liang, Y. (2010) Riboflavin activates defense responses in tobacco and induces resistance against Phytophthora parasitica and Ralstonia solanacearum. Physiol. Plant Mol. Pathol. 74: 330-336.
33. Maimbo, M., Ohnishi, K., Hikichi, Y., Yoshioka, H. and Kiba, A. (2007) Induction of a small heat shock protein and its functional roles in Nicotiana plants in the defense response against Ralstonia solana-cearum. Plant Physiol. 145: 1588-1599.
34. Nakaho, K., Inoue, H., Takayama, T. and Miyagawa, H. (2004) Distribution and multiplication of Ralstonia solanacearum in tomato plants with resistance derived from different origins. J. Gen. Plant Pathol. 70: 115-119.
35. Nakaho, K., Takaya, S. and Sumida, Y. (1996) Conditions that increase latent infection of grafted or non-grafted tomatoes with Pseudomonas solanacearum. Annu. Phytopathol. Soc. Jpn. 62: 234-239.
36. Nakashita, H., Yoshioka, K., Yasuda, M., Nitta, T., Arai, Y., Yoshida, S. et al. (2002) Probenazole induces systemic acquired resistance in tobacco through salicylic acid accumulation. Physiol. Mol. Plant Pathol. 61: 197-203.
37. Ohtsubo, N., Mitsuhara, I., Koga, M., Seo, S. and Ohashi, Y. (1999) Ethylene promotes the necrotic lesion formation and basic PR gene expression in TMV-infected tobacco. Plant Cell Physiol. 40: 808-817.
38. Raes, J., Rohde, A., Christensen, J.H., van de Peer, Y. and Boerjan, W. (2003) Genome-wide characterization of the lignifications toolbox in Arabidopsis. Plant Physiol. 133: 1051-1071.
39. Rea, P.A. (2007) Plant ATP-binding cassette transporters. Annu. Rev. Plant Biol. 58: 347-375.
40. Sasabe, M., Toyoda, K., Shiraishi, T., Inagaki, Y. and Ichinose, Y. (2002) cDNA cloning and characterization of tobacco ABC transporter: NtPDR1 is a novel elicitor-responsive gene. FEBS Lett. 518: 164-168.
41. Schell, M.A. (2000) Control of virulence and pathogenicity genes of Ralstonia solanacearum by an elaborate sensory network. Annu. Rev. Phytopathol. 38: 263-292.
42. Seo, S., Seto, H., Koshino, H., Yoshida, S. and 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.
43. Suzuki, S., Suzuki, Y., Yamamoto, N., Hattori, T., Sakamoto, M. and Umezawa, T. (2009) High-throughput determination of thioglycolic acid lignin from rice. Plant Biotechnol. 26: 337-340.
44. Takabatake, R., Seo, S., Mitsuhara, I., Tsuda, S. and Ohashi, Y. (2006) Accumulation of the two transcripts of the N gene, conferring resistance to Tobacco mosaic virus, is probably important for N gene-dependent hypersensitive cell death. Plant Cell Physiol. 47: 254-261.
45. Takahashi, F., Yoshida, R., Ichimura, K., Mizoguchi, T., Seo, S., Yonezawa, M. et al. (2007) The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell 19: 805-818.
46. Ton, J. and Mauchi-Mani, B. (2004) b-Amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J. 38: 119-130.
47. Vasse, J., Frey, P. and Trigalet, A. (1995) Microscopic studies of intercellular infection and protoxylem invasion of tomato roots by Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 8: 241-251.
48. Vernooij, B., Friedrich, L., Ahl Goy, P., Staub, T., Kessmann, H. and Ryals, J. (1995) 2, 6-Dichloroisonicotinic acid-induced resistance to pathogens without the accumulation of salicylic acid. Mol. Plant-Microbe Interact. 8: 228-234.
49. Watanabe, T., Igarashi, H., Matsumoto, K., Seki, S., Mase, S. and Sekizawa, Y. (1977) The characteristics of probenazole (Oryzemate) for the control of rice blast. J. Pesticide Sci. 2: 291-296.
50. Yoshioka, K., Nakashita, H., Klessig, D.F. and Yamaguchi, I. (2001) Probenazole induces systemic acquired resistance in Arabidopsis with a novel type of action. Plant J. 25: 149-157.
51. Zhang, H., Zhang, D., Chen, J., Yang, Y., Huang, Z., Huang, D. et al. (2004) Tomato stress-responsive factor TSRF1 interacts with ethyl-ene responsive element GCC box and regulates pathogen resistance to Ralstonia solanacearum. Plant Mol. Biol. 55: 825-834.