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. 1995 Jan;7(1):29–42. doi: 10.1105/tpc.7.1.29

Coordinated Activation of Programmed Cell Death and Defense Mechanisms in Transgenic Tobacco Plants Expressing a Bacterial Proton Pump.

R Mittler 1, V Shulaev 1, E Lam 1
PMCID: PMC160762  PMID: 12242350

Abstract

In plants, programmed cell death is thought to be activated during the hypersensitive response to certain avirulent pathogens and in the course of several differentiation processes. We describe a transgenic model system that mimics the activation of programmed cell death in higher plants. In this system, expression of a bacterial proton pump in transgenic tobacco plants activates a cell death pathway that may be similar to that triggered by recognition of an incompatible pathogen. Thus, spontaneous lesions that resemble hypersensitive response lesions are formed, multiple defense mechanisms are apparently activated, and systemic resistance is induced in the absence of a pathogen. Interestingly, mutation of a single amino acid in the putative channel of this proton pump renders it inactive with respect to lesion formation and induction of resistance to pathogen challenge. This transgenic model system may provide insights into the mechanisms involved in mediating cell death in higher plants. In addition, it may also be used as a general agronomic tool to enhance disease protection.

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Selected References

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  1. Atkinson M. M., Baker C. J. Role of the Plasmalemma H-ATPase in Pseudomonas syringae-Induced K/H Exchange in Suspension-Cultured Tobacco Cells. Plant Physiol. 1989 Sep;91(1):298–303. doi: 10.1104/pp.91.1.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bachmair A., Becker F., Masterson R. V., Schell J. Perturbation of the ubiquitin system causes leaf curling, vascular tissue alterations and necrotic lesions in a higher plant. EMBO J. 1990 Dec;9(13):4543–4549. doi: 10.1002/j.1460-2075.1990.tb07906.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bissonnette R. P., Echeverri F., Mahboubi A., Green D. R. Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature. 1992 Oct 8;359(6395):552–554. doi: 10.1038/359552a0. [DOI] [PubMed] [Google Scholar]
  4. Bowles D. J. Defense-related proteins in higher plants. Annu Rev Biochem. 1990;59:873–907. doi: 10.1146/annurev.bi.59.070190.004301. [DOI] [PubMed] [Google Scholar]
  5. DeLong A., Calderon-Urrea A., Dellaporta S. L. Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell. 1993 Aug 27;74(4):757–768. doi: 10.1016/0092-8674(93)90522-r. [DOI] [PubMed] [Google Scholar]
  6. Dietrich R. A., Delaney T. P., Uknes S. J., Ward E. R., Ryals J. A., Dangl J. L. Arabidopsis mutants simulating disease resistance response. Cell. 1994 May 20;77(4):565–577. doi: 10.1016/0092-8674(94)90218-6. [DOI] [PubMed] [Google Scholar]
  7. Driscoll M., Chalfie M. The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration. Nature. 1991 Feb 14;349(6310):588–593. doi: 10.1038/349588a0. [DOI] [PubMed] [Google Scholar]
  8. Elkind Y., Edwards R., Mavandad M., Hedrick S. A., Ribak O., Dixon R. A., Lamb C. J. Abnormal plant development and down-regulation of phenylpropanoid biosynthesis in transgenic tobacco containing a heterologous phenylalanine ammonia-lyase gene. Proc Natl Acad Sci U S A. 1990 Nov;87(22):9057–9061. doi: 10.1073/pnas.87.22.9057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Enyedi A. J., Yalpani N., Silverman P., Raskin I. Signal molecules in systemic plant resistance to pathogens and pests. Cell. 1992 Sep 18;70(6):879–886. doi: 10.1016/0092-8674(92)90239-9. [DOI] [PubMed] [Google Scholar]
  10. Felix G., Grosskopf D. G., Regenass M., Boller T. Rapid changes of protein phosphorylation are involved in transduction of the elicitor signal in plant cells. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8831–8834. doi: 10.1073/pnas.88.19.8831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gavrieli Y., Sherman Y., Ben-Sasson S. A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol. 1992 Nov;119(3):493–501. doi: 10.1083/jcb.119.3.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Greenberg J. T., Ausubel F. M. Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J. 1993 Aug;4(2):327–341. doi: 10.1046/j.1365-313x.1993.04020327.x. [DOI] [PubMed] [Google Scholar]
  13. Hoffmann A., Hildebrandt V., Heberle J., Büldt G. Photoactive mitochondria: in vivo transfer of a light-driven proton pump into the inner mitochondrial membrane of Schizosaccharomyces pombe. Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9367–9371. doi: 10.1073/pnas.91.20.9367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hoisington D. A., Neuffer M. G., Walbot V. Disease lesion mimics in maize. I. Effect of genetic background, temperature, developmental age, and wounding on necrotic spot formation with Les1. Dev Biol. 1982 Oct;93(2):381–388. doi: 10.1016/0012-1606(82)90125-7. [DOI] [PubMed] [Google Scholar]
  15. Krebs M. P., Khorana H. G. Mechanism of light-dependent proton translocation by bacteriorhodopsin. J Bacteriol. 1993 Mar;175(6):1555–1560. doi: 10.1128/jb.175.6.1555-1560.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lamb C. J. Plant disease resistance genes in signal perception and transduction. Cell. 1994 Feb 11;76(3):419–422. doi: 10.1016/0092-8674(94)90106-6. [DOI] [PubMed] [Google Scholar]
  17. Mailhos C., Howard M. K., Latchman D. S. Heat shock protects neuronal cells from programmed cell death by apoptosis. Neuroscience. 1993 Aug;55(3):621–627. doi: 10.1016/0306-4522(93)90428-i. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Nagy F., Boutry M., Hsu M. Y., Wong M., Chua N. H. The 5'-proximal region of the wheat Cab-1 gene contains a 268-bp enhancer-like sequence for phytochrome response. EMBO J. 1987 Sep;6(9):2537–2542. doi: 10.1002/j.1460-2075.1987.tb02541.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nürnberger T., Nennstiel D., Jabs T., Sacks W. R., Hahlbrock K., Scheel D. High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell. 1994 Aug 12;78(3):449–460. doi: 10.1016/0092-8674(94)90423-5. [DOI] [PubMed] [Google Scholar]
  22. Otto H., Marti T., Holz M., Mogi T., Stern L. J., Engel F., Khorana H. G., Heyn M. P. Substitution of amino acids Asp-85, Asp-212, and Arg-82 in bacteriorhodopsin affects the proton release phase of the pump and the pK of the Schiff base. Proc Natl Acad Sci U S A. 1990 Feb;87(3):1018–1022. doi: 10.1073/pnas.87.3.1018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Schwartzman R. A., Cidlowski J. A. Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr Rev. 1993 Apr;14(2):133–151. doi: 10.1210/edrv-14-2-133. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Wolter M., Hollricher K., Salamini F., Schulze-Lefert P. The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defence mimic phenotype. Mol Gen Genet. 1993 May;239(1-2):122–128. doi: 10.1007/BF00281610. [DOI] [PubMed] [Google Scholar]
  27. Wyllie A. H., Morris R. G., Smith A. L., Dunlop D. Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J Pathol. 1984 Jan;142(1):67–77. doi: 10.1002/path.1711420112. [DOI] [PubMed] [Google Scholar]

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