Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1996 Apr;8(4):629–643. doi: 10.1105/tpc.8.4.629

Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat.

J Görlach 1, S Volrath 1, G Knauf-Beiter 1, G Hengy 1, U Beckhove 1, K H Kogel 1, M Oostendorp 1, T Staub 1, E Ward 1, H Kessmann 1, J Ryals 1
PMCID: PMC161125  PMID: 8624439

Abstract

Systemic acquired resistance is an important component of the disease resistance repertoire of plants. In this study, a novel synthetic chemical, benzo(1,2,3)thiadiazole-7-carbothioic acid S-methyl ester (BTH), was shown to induce acquired resistance in wheat. BTH protected wheat systemically against powdery mildew infection by affecting multiple steps in the life cycle of the pathogen. The onset of resistance was accompanied by the induction of a number of newly described wheat chemically induced (WCI) genes, including genes encoding a lipoxygenase and a sulfur-rich protein. With respect to both timing and effectiveness, a tight correlation existed between the onset of resistance and the induction of the WCI genes. Compared with other plant activators, such as 2,6-dichloroisonicotinic acid and salicylic acid, BTH was the most potent inducer of both resistance and gene induction. BTH is being developed commercially as a novel type of plant protection compound that works by inducing the plant's inherent disease resistance mechanisms.

Full Text

The Full Text of this article is available as a PDF (3.8 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abel P. P., Nelson R. S., De B., Hoffmann N., Rogers S. G., Fraley R. T., Beachy R. N. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science. 1986 May 9;232(4751):738–743. doi: 10.1126/science.3457472. [DOI] [PubMed] [Google Scholar]
  2. Alexander D., Goodman R. M., Gut-Rella M., Glascock C., Weymann K., Friedrich L., Maddox D., Ahl-Goy P., Luntz T., Ward E. Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7327–7331. doi: 10.1073/pnas.90.15.7327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bi Y. M., Kenton P., Mur L., Darby R., Draper J. Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J. 1995 Aug;8(2):235–245. doi: 10.1046/j.1365-313x.1995.08020235.x. [DOI] [PubMed] [Google Scholar]
  4. Brogue K., Chet I., Holliday M., Cressman R., Biddle P., Knowlton S., Mauvais C. J., Broglie R. Transgenic Plants with Enhanced Resistance to the Fungal Pathogen Rhizoctonia solani. Science. 1991 Nov 22;254(5035):1194–1197. doi: 10.1126/science.254.5035.1194. [DOI] [PubMed] [Google Scholar]
  5. Cejudo F. J., Murphy G., Chinoy C., Baulcombe D. C. A gibberellin-regulated gene from wheat with sequence homology to cathepsin B of mammalian cells. Plant J. 1992 Nov;2(6):937–948. [PubMed] [Google Scholar]
  6. Chen Z., Silva H., Klessig D. F. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science. 1993 Dec 17;262(5141):1883–1886. doi: 10.1126/science.8266079. [DOI] [PubMed] [Google Scholar]
  7. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Claes B., Dekeyser R., Villarroel R., Van den Bulcke M., Bauw G., Van Montagu M., Caplan A. Characterization of a rice gene showing organ-specific expression in response to salt stress and drought. Plant Cell. 1990 Jan;2(1):19–27. doi: 10.1105/tpc.2.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Conrath U., Chen Z., Ricigliano J. R., Klessig D. F. Two inducers of plant defense responses, 2,6-dichloroisonicotinec acid and salicylic acid, inhibit catalase activity in tobacco. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7143–7147. doi: 10.1073/pnas.92.16.7143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Delaney T. P., Friedrich L., Ryals J. A. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6602–6606. doi: 10.1073/pnas.92.14.6602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dufour E. Sequence homologies, hydrophobic profiles and secondary structures of cathepsins B, H and L: comparison with papain and actinidin. Biochimie. 1988 Oct;70(10):1335–1342. doi: 10.1016/0300-9084(88)90004-1. [DOI] [PubMed] [Google Scholar]
  12. Farmer E. E. Fatty acid signalling in plants and their associated microorganisms. Plant Mol Biol. 1994 Dec;26(5):1423–1437. doi: 10.1007/BF00016483. [DOI] [PubMed] [Google Scholar]
  13. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  14. Gaffney T., Friedrich L., Vernooij B., Negrotto D., Nye G., Uknes S., Ward E., Kessmann H., Ryals J. Requirement of salicylic Acid for the induction of systemic acquired resistance. Science. 1993 Aug 6;261(5122):754–756. doi: 10.1126/science.261.5122.754. [DOI] [PubMed] [Google Scholar]
  15. Görlach J., Schmid J., Amrhein N. Abundance of transcripts specific for genes encoding enzymes of the prechorismate pathway in different organs of tomato (Lycopersicon esculentum L.) plants. Planta. 1994;193(2):216–223. doi: 10.1007/BF00192533. [DOI] [PubMed] [Google Scholar]
  16. Holwerda B. C., Galvin N. J., Baranski T. J., Rogers J. C. In Vitro Processing of Aleurain, a Barley Vacuolar Thiol Protease. Plant Cell. 1990 Nov;2(11):1091–1106. doi: 10.1105/tpc.2.11.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Karunanandaa B., Singh A., Kao T. H. Characterization of a predominantly pistil-expressed gene encoding a gamma-thionin-like protein of Petunia inflata. Plant Mol Biol. 1994 Oct;26(1):459–464. doi: 10.1007/BF00039555. [DOI] [PubMed] [Google Scholar]
  18. Kogel K. H., Beckhove U., Dreschers J., Munch S., Romme Y. Acquired Resistance in Barley (The Resistance Mechanism Induced by 2,6-Dichloroisonicotinic Acid Is a Phenocopy of a Genetically Based Mechanism Governing Race-Specific Powdery Mildew Resistance). Plant Physiol. 1994 Dec;106(4):1269–1277. doi: 10.1104/pp.106.4.1269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lagrimini L. M., Burkhart W., Moyer M., Rothstein S. Molecular cloning of complementary DNA encoding the lignin-forming peroxidase from tobacco: Molecular analysis and tissue-specific expression. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7542–7546. doi: 10.1073/pnas.84.21.7542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lawton K., Weymann K., Friedrich L., Vernooij B., Uknes S., Ryals J. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact. 1995 Nov-Dec;8(6):863–870. doi: 10.1094/mpmi-8-0863. [DOI] [PubMed] [Google Scholar]
  21. Liu D., Raghothama K. G., Hasegawa P. M., Bressan R. A. Osmotin overexpression in potato delays development of disease symptoms. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1888–1892. doi: 10.1073/pnas.91.5.1888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lütcke H. A., Chow K. C., Mickel F. S., Moss K. A., Kern H. F., Scheele G. A. Selection of AUG initiation codons differs in plants and animals. EMBO J. 1987 Jan;6(1):43–48. doi: 10.1002/j.1460-2075.1987.tb04716.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Malamy J., Carr J. P., Klessig D. F., Raskin I. Salicylic Acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science. 1990 Nov 16;250(4983):1002–1004. doi: 10.1126/science.250.4983.1002. [DOI] [PubMed] [Google Scholar]
  24. Meier B. M., Shaw N., Slusarenko A. J. Spatial and temporal accumulation of defense gene transcripts in bean (Phaseolus vulgaris) leaves in relation to bacteria-induced hypersensitive cell death. Mol Plant Microbe Interact. 1993 Jul-Aug;6(4):453–466. doi: 10.1094/mpmi-6-453. [DOI] [PubMed] [Google Scholar]
  25. Mouradov A., Mouradova E., Scott K. J. Gene family encoding basic pathogenesis-related 1 proteins in barley. Plant Mol Biol. 1994 Oct;26(1):503–507. doi: 10.1007/BF00039561. [DOI] [PubMed] [Google Scholar]
  26. Métraux J. P., Signer H., Ryals J., Ward E., Wyss-Benz M., Gaudin J., Raschdorf K., Schmid E., Blum W., Inverardi B. Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber. Science. 1990 Nov 16;250(4983):1004–1006. doi: 10.1126/science.250.4983.1004. [DOI] [PubMed] [Google Scholar]
  27. Ohta H., Shirano Y., Tanaka K., Morita Y., Shibata D. cDNA cloning of rice lipoxygenase L-2 and characterization using an active enzyme expressed from the cDNA in Escherichia coli. Eur J Biochem. 1992 Jun 1;206(2):331–336. doi: 10.1111/j.1432-1033.1992.tb16931.x. [DOI] [PubMed] [Google Scholar]
  28. ROSS A. F. Localized acquired resistance to plant virus infection in hypersensitive hosts. Virology. 1961 Jul;14:329–339. doi: 10.1016/0042-6822(61)90318-x. [DOI] [PubMed] [Google Scholar]
  29. ROSS A. F. Systemic acquired resistance induced by localized virus infections in plants. Virology. 1961 Jul;14:340–358. doi: 10.1016/0042-6822(61)90319-1. [DOI] [PubMed] [Google Scholar]
  30. Ryals J., Uknes S., Ward E. Systemic Acquired Resistance. Plant Physiol. 1994 Apr;104(4):1109–1112. doi: 10.1104/pp.104.4.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. St John T. P., Davis R. W. Isolation of galactose-inducible DNA sequences from Saccharomyces cerevisiae by differential plaque filter hybridization. Cell. 1979 Feb;16(2):443–452. doi: 10.1016/0092-8674(79)90020-5. [DOI] [PubMed] [Google Scholar]
  32. Summermatter K., Sticher L., Metraux J. P. Systemic Responses in Arabidopsis thaliana Infected and Challenged with Pseudomonas syringae pv syringae. Plant Physiol. 1995 Aug;108(4):1379–1385. doi: 10.1104/pp.108.4.1379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Uknes S., Mauch-Mani B., Moyer M., Potter S., Williams S., Dincher S., Chandler D., Slusarenko A., Ward E., Ryals J. Acquired resistance in Arabidopsis. Plant Cell. 1992 Jun;4(6):645–656. doi: 10.1105/tpc.4.6.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Vernooij B., Friedrich L., Morse A., Reist R., Kolditz-Jawhar R., Ward E., Uknes S., Kessmann H., Ryals J. Salicylic Acid Is Not the Translocated Signal Responsible for Inducing Systemic Acquired Resistance but Is Required in Signal Transduction. Plant Cell. 1994 Jul;6(7):959–965. doi: 10.1105/tpc.6.7.959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ward E. R., Uknes S. J., Williams S. C., Dincher S. S., Wiederhold D. L., Alexander D. C., Ahl-Goy P., Metraux J. P., Ryals J. A. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance. Plant Cell. 1991 Oct;3(10):1085–1094. doi: 10.1105/tpc.3.10.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wilson T. M. Strategies to protect crop plants against viruses: pathogen-derived resistance blossoms. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3134–3141. doi: 10.1073/pnas.90.8.3134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. de Pater B. S., Schilperoort R. A. Structure and expression of a root-specific rice gene. Plant Mol Biol. 1992 Jan;18(1):161–164. doi: 10.1007/BF00018473. [DOI] [PubMed] [Google Scholar]
  38. van Mechelen J. R., Smits M., Douma A. C., Rouster J., Cameron-Mills V., Heidekamp F., Valk B. E. Primary structure of a lipoxygenase from barley grain as deduced from its cDNA sequence. Biochim Biophys Acta. 1995 Jan 20;1254(2):221–225. doi: 10.1016/0005-2760(94)00231-m. [DOI] [PubMed] [Google Scholar]
  39. von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. von Heijne G. Signal sequences. The limits of variation. J Mol Biol. 1985 Jul 5;184(1):99–105. doi: 10.1016/0022-2836(85)90046-4. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES