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. 1994 Nov;6(11):1543–1552. doi: 10.1105/tpc.6.11.1543

A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death.

G B Martin 1, A Frary 1, T Wu 1, S Brommonschenkel 1, J Chunwongse 1, E D Earle 1, S D Tanksley 1
PMCID: PMC160542  PMID: 7827490

Abstract

Leaves of tomato cultivars that contain the Pto bacterial resistance locus develop small necrotic lesions within 24 hr after exposure to fenthion, an organophosphorous insecticide. Recently, the Pto gene was isolated and shown to be a putative serine/threonine protein kinase. Pto is one member of a multigene family that is clustered within a 400-kb region on chromosome 5. Here, we report that another member of this gene family, termed Fen, is responsible for the sensitivity to fenthion. Fen was isolated by map-based cloning using closely linked DNA markers to identify a yeast artificial chromosome clone that spanned the Pto region. After transformation with the Fen gene under control of the cauliflower mosaic virus (CaMV) 35S promoter, tomato plants that are normally insensitive to fenthion rapidly developed extensive necrotic lesions upon exposure to fenthion. Two related insecticides, fensulfothion and fenitrothion, also elicited necrotic lesions specifically on Fen-transformed plants. Transgenic tomato plants harboring integrated copies of the Pto gene under control of the CaMV 35S promoter displayed sensitivity to fenthion but to a lesser extent than did wild-type fenthion-sensitive plants. The Fen protein shares 80% identity (87% similarity) with Pto but does not confer resistance to Pseudomonas syringae pv tomato. These results suggest that Pto and Fen participate in the same signal transduction pathway.

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Selected References

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  1. Baker C. J., Orlandi E. W., Mock N. M. Harpin, An Elicitor of the Hypersensitive Response in Tobacco Caused by Erwinia amylovora, Elicits Active Oxygen Production in Suspension Cells. Plant Physiol. 1993 Aug;102(4):1341–1344. doi: 10.1104/pp.102.4.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Boyes D. C., Nasrallah J. B. Physical linkage of the SLG and SRK genes at the self-incompatibility locus of Brassica oleracea. Mol Gen Genet. 1993 Jan;236(2-3):369–373. doi: 10.1007/BF00277135. [DOI] [PubMed] [Google Scholar]
  3. Buss J. E., Kamps M. P., Gould K., Sefton B. M. The absence of myristic acid decreases membrane binding of p60src but does not affect tyrosine protein kinase activity. J Virol. 1986 May;58(2):468–474. doi: 10.1128/jvi.58.2.468-474.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carland F. M., Staskawicz B. J. Genetic characterization of the Pto locus of tomato: semi-dominance and cosegregation of resistance to Pseudomonas syringae pathovar tomato and sensitivity to the insecticide Fenthion. Mol Gen Genet. 1993 May;239(1-2):17–27. doi: 10.1007/BF00281596. [DOI] [PubMed] [Google Scholar]
  5. Chang C., Schaller G. E., Patterson S. E., Kwok S. F., Meyerowitz E. M., Bleecker A. B. The TMK1 gene from Arabidopsis codes for a protein with structural and biochemical characteristics of a receptor protein kinase. Plant Cell. 1992 Oct;4(10):1263–1271. doi: 10.1105/tpc.4.10.1263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Ganal M. W., Bonierbale M. W., Roeder M. S., Park W. D., Tanksley S. D. Genetic and physical mapping of the patatin genes in potato and tomato. Mol Gen Genet. 1991 Mar;225(3):501–509. doi: 10.1007/BF00261693. [DOI] [PubMed] [Google Scholar]
  8. Hulbert S. H., Bennetzen J. L. Recombination at the Rp1 locus of maize. Mol Gen Genet. 1991 May;226(3):377–382. doi: 10.1007/BF00260649. [DOI] [PubMed] [Google Scholar]
  9. Keen N. T. Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet. 1990;24:447–463. doi: 10.1146/annurev.ge.24.120190.002311. [DOI] [PubMed] [Google Scholar]
  10. Lamb C. J., Lawton M. A., Dron M., Dixon R. A. Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell. 1989 Jan 27;56(2):215–224. doi: 10.1016/0092-8674(89)90894-5. [DOI] [PubMed] [Google Scholar]
  11. Liang P., Pardee A. B. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science. 1992 Aug 14;257(5072):967–971. doi: 10.1126/science.1354393. [DOI] [PubMed] [Google Scholar]
  12. Maeda N., Smithies O. The evolution of multigene families: human haptoglobin genes. Annu Rev Genet. 1986;20:81–108. doi: 10.1146/annurev.ge.20.120186.000501. [DOI] [PubMed] [Google Scholar]
  13. Martin G. B., Brommonschenkel S. H., Chunwongse J., Frary A., Ganal M. W., Spivey R., Wu T., Earle E. D., Tanksley S. D. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science. 1993 Nov 26;262(5138):1432–1436. doi: 10.1126/science.7902614. [DOI] [PubMed] [Google Scholar]
  14. Martin G. B., Ganal M. W., Tanksley S. D. Construction of a yeast artificial chromosome library of tomato and identification of cloned segments linked to two disease resistance loci. Mol Gen Genet. 1992 May;233(1-2):25–32. doi: 10.1007/BF00587557. [DOI] [PubMed] [Google Scholar]
  15. Newman S. M., Eannetta N. T., Yu H., Prince J. P., de Vicente M. C., Tanksley S. D., Steffens J. C. Organisation of the tomato polyphenol oxidase gene family. Plant Mol Biol. 1993 Mar;21(6):1035–1051. doi: 10.1007/BF00023601. [DOI] [PubMed] [Google Scholar]
  16. Pichersky E., Bernatzky R., Tanksley S. D., Breidenbach R. B., Kausch A. P., Cashmore A. R. Molecular characterization and genetic mapping of two clusters of genes encoding chlorophyll a/b-binding proteins in Lycopersicon esculentum (tomato). Gene. 1985;40(2-3):247–258. doi: 10.1016/0378-1119(85)90047-2. [DOI] [PubMed] [Google Scholar]
  17. Pichersky E., Bernatzky R., Tanksley S. D., Cashmore A. R. Evidence for selection as a mechanism in the concerted evolution of Lycopersicon esculentum (tomato) genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3880–3884. doi: 10.1073/pnas.83.11.3880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rick C. M., Tanksley S. D., Fobes J. F. A pseudoduplication in Lycopersicon pimpinellifolium. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3435–3439. doi: 10.1073/pnas.76.7.3435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ronald P. C., Salmeron J. M., Carland F. M., Staskawicz B. J. The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. J Bacteriol. 1992 Mar;174(5):1604–1611. doi: 10.1128/jb.174.5.1604-1611.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Salmeron J. M., Barker S. J., Carland F. M., Mehta A. Y., Staskawicz B. J. Tomato mutants altered in bacterial disease resistance provide evidence for a new locus controlling pathogen recognition. Plant Cell. 1994 Apr;6(4):511–520. doi: 10.1105/tpc.6.4.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Stein J. C., Howlett B., Boyes D. C., Nasrallah M. E., Nasrallah J. B. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8816–8820. doi: 10.1073/pnas.88.19.8816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Stein J. C., Nasrallah J. B. A plant receptor-like gene, the S-locus receptor kinase of Brassica oleracea L., encodes a functional serine/threonine kinase. Plant Physiol. 1993 Mar;101(3):1103–1106. doi: 10.1104/pp.101.3.1103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Van Aelst L., Barr M., Marcus S., Polverino A., Wigler M. Complex formation between RAS and RAF and other protein kinases. Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6213–6217. doi: 10.1073/pnas.90.13.6213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Vojtek A. B., Hollenberg S. M., Cooper J. A. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell. 1993 Jul 16;74(1):205–214. doi: 10.1016/0092-8674(93)90307-c. [DOI] [PubMed] [Google Scholar]
  26. Walker J. C., Zhang R. Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature. 1990 Jun 21;345(6277):743–746. doi: 10.1038/345743a0. [DOI] [PubMed] [Google Scholar]
  27. 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]

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