Skip to main content
Log in

Markers for hypersensitive response and senescence show distinct patterns of expression

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Controlled cellular suicide is an important process that can be observed in various organs during plant development. From the generation of proper sexual organs in monoecious plants to the hypersensitive response (HR) that occurs during incompatible pathogen interactions, programmed cell death (PCD) can be readily observed. Although several biochemical and morphological parameters have been described for various types of cell death in plants, the relationships existing between those different types of PCD events remain unclear. In this work, we set out to examine if two early molecular markers of HR cell death (HIN1 and HSR203J) as well as a senescence marker (SAG12) are coordinately induced during these processes. Our result indicates that although there is evidence of some cross-talk between both cell death pathways, spatial and temporal characteristics of activation for these markers during hypersensitive response and senescence are distinct. These observations indicate that these markers are relatively specific for different cell death programs. Interestingly, they also revealed that a senescence-like process seems to be triggered at the periphery of the HR necrotic lesion. This suggests that cells committed to die during the HR might release a signal able to induce senescence in the neighboring cells. This phenomenon could correspond to the establishment of a second barrier against pathogens. Lastly, we used those cell death markers to better characterize cell death induced by copper and we showed that this abiotic induced cell death presents similarities with HR cell death.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Baudouin E, Charpenteau M, Roby D, Marco Y, Ranjeva R, Ranty B: Functional expression of a tobacco gene related to the serine hydrolase family. Esterase activity towards short chain dinitrophenyl acylesters. Eur J Biochem 248: 700–706 (1997).

    PubMed  Google Scholar 

  2. Beckman KB, Ingram DS: The inhibition of the hypersensitive response of potato tuber tissue by cytokinins: similarities between senescence and plant defence responses. Physiol Plant Path 45: 229–246 (1994).

    Google Scholar 

  3. Bergeron L, Perez GI, Macdonald G, Shi L, Sun Y, Jurisicova A, Varmuza S, Latham KE, Flaws JA, Salter JCM, Hara H, Moskowitz MA, Li E, Greenberg A, Tilly JL, Yuan J: Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev 12: 1304–1314 (1998).

    PubMed  Google Scholar 

  4. Buchanan-Wollaston V: The molecular biology of leaf senescence. J Exp Bot 48: 181–199 (1997).

    Google Scholar 

  5. Century KS, Holub EB, Staskawicz BJ: NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc Natl Acad Sci USA 92: 6597–6601 (1995).

    PubMed  Google Scholar 

  6. Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ: NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278: 1963–1965 (1997).

    Article  PubMed  Google Scholar 

  7. de Laat AMM, van Loon LC: The relationship between stimulated ethylene production and symptom expression in virus-infected tobacco leaves. Physiol Plant Path 22: 261–273 (1983).

    Google Scholar 

  8. Del Pozo O, Lam E: Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr Biol 8: 1129–1132. (1998).

    PubMed  Google Scholar 

  9. Gan S, Amasino RM: Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270: 1986–1988 (1995).

    PubMed  Google Scholar 

  10. Gan S, Amasino RM: Making sense of senescence. Plant Physiol 113: 313–319 (1997).

    PubMed  Google Scholar 

  11. Gopalan S, Wei W, He SY: hrp gene induction of HIN1, a plant gene activated rapidly by both harpins and the avrPto gene-mediated signal. Plant J 10: 591–600 (1996).

    Article  PubMed  Google Scholar 

  12. Gopalan S, He SY: Disease resistance: beyond the resistance genes. Trends Plant Sci 3: 207–208 (1998).

    Google Scholar 

  13. Gray J, Close PS, Briggs SP, Johal GS: A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89: 25–31 (1997).

    PubMed  Google Scholar 

  14. Greenberg JT: Programmed cell death: a way of life for plants. Proc Natl Acad Sci USA 93: 12094–12097 (1996).

    PubMed  Google Scholar 

  15. Haberlach GT, Budde AD, Sequeira L, Helgeson JP: Modification of disease resistance of tobacco callus tissues by cytokinins. Plant Physiol 62: 522–525 (1978).

    Google Scholar 

  16. Hanfrey C, Fife M, Buchanan-Wollaston V: Leaf senescence in Brassica napus: expression of genes encoding pathogenesis-related proteins. Plant Mol Biol 30: 597–609 (1996).

    PubMed  Google Scholar 

  17. Hengartner MO: Programmed cell death in invertebrates. Curr Opin Genet Dev 6: 34–38 (1996).

    PubMed  Google Scholar 

  18. Hewelt A, Prinsen E, Schell J, Van Onckelen H, Schmulling T: Promoter tagging with a promoterless ipt gene leads to cytokinin-induced phenotypic variability in transgenic tobacco plants: implications of gene dosage effects. Plant J 6: 879–891 (1994).

    Article  PubMed  Google Scholar 

  19. Holt CA, Hodgson RA, Coker FA, Beachy RN, Nelson RS: Characterization of the masked strain of tobacco mosaic virus: identification of the region responsible for symptom attenuation by analysis of an infectious cDNA clone. Mol Plant-Microbe Interact 3: 417–423 (1990).

    PubMed  Google Scholar 

  20. Jefferson RA, Kavanagh TA, Bevan MN: GUS gene fusions: β glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907 (1987).

    PubMed  Google Scholar 

  21. Kiraly Z, Szirmai J: The influence of kinetin on tobacco mosaic virus production in Nicotiana glutinosa leaf discs. Virology 23: 286–288 (1964).

    PubMed  Google Scholar 

  22. Lasserre E, Godard F, Bouquin T, Hernandez JA, Pech JC, Balague C: Differential activation of two ACC oxidase gene promoters from melon during plant development and in response to pathogen attack. Mol Gen Genet 256: 211–222 (1997).

    PubMed  Google Scholar 

  23. Li Y, Hagen G, Guilfoyle TJ: Altered morphology in transgenic tobacco plants that overproduce cytokinins in specific tissues and organs. Dev Biol 153: 386–395 (1992).

    Article  PubMed  Google Scholar 

  24. Lindgren PB, Peet RC, Panopoulos NJ: Gene cluster of Pseudomonas syringae pv. phaseolicola controls pathogenicity of bean plants and hypersensitivity on nonhost plants. J Bact 168: 512–522 (1986).

    PubMed  Google Scholar 

  25. Lohman KN, Gan S, John MC, Amasino RM: Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol Plant 92: 322–328 (1994).

    Article  Google Scholar 

  26. Luna CM, González CA, Trippi VS: Oxidative damage caused by an excess of copper in oat leaves. Plant Cell Physiol 35: 11–15 (1994).

    Google Scholar 

  27. McCall K, Steller H: Facing death in the fly: genetic analysis of apoptosis in Drosophila. Trends Genet 13: 222–226 (1997).

    PubMed  Google Scholar 

  28. Mackinney G: The absorption of light by chlorophyll solutions. J Biol Chem 140: 315–322 (1941).

    Google Scholar 

  29. Martineau B, Houck CM, Sheehy RE, Hiatt WR: Fruit-specific expression of the A. tumefaciens isopentenyl transferase gene in tomato: effects on fruit ripening and defence-related gene expression in leaves. Plant J 5: 11–19 (1994).

    Google Scholar 

  30. Meyer SLF, Heath MC: A comparison of the cell death induced by fungal invasion or toxic chemicals in cowpea epidermal cells. I. Cell death induced by heavy metal salts. Can J Bot 66: 613–623 (1988).

    Google Scholar 

  31. Meyer SLF, Heath MC: A comparison of the cell death induced by fungal invasion or toxic chemicals in cowpea epidermal cells. II. Reponses induced by Erysiphe cichoracearum. Can J Bot 66: 624–634 (1988).

    Google Scholar 

  32. Mhiri C, Morel JB, Vernhettes S, Casacuberta J, Lucas H, Grandbastien MA: The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. Plant Mol Biol 33: 257–266 (1997).

    PubMed  Google Scholar 

  33. Mittler R, Shulaev V, Lam E: Coordinated activation of programmed cell death and defense mechanisms in transgenic tobacco plants expressing a bacterial proton pump. Plant Cell 7: 29–42 (1995).

    PubMed  Google Scholar 

  34. Mittler R, Lam E: Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death. Plant Cell 7: 1951–1962 (1995).

    PubMed  Google Scholar 

  35. Mittler R, Lam E: Characterization of nuclease activities and DNA fragmentation induced upon hypersensitive response cell death and mechanical stress. Plant Mol Biol 34: 209–221 (1997).

    PubMed  Google Scholar 

  36. Morel JB, Dangl JL: The hypersensitive response and the induction of cell death in plants. Cell Death Diff 4: 671–683 (1997).

    Google Scholar 

  37. Nagy F, Boutry M, Hsu MY, Wong M, Chua NH: The 5′ proximal region of the wheat cab1 gene contains a 268 bp enhancer-like sequence for phytochrome response. EMBO J 6: 2537–2542 (1987).

    PubMed  Google Scholar 

  38. Nam HG: The molecular genetic analysis of leaf senescence. Curr Opin Biotechnol 8: 200–207 (1997).

    PubMed  Google Scholar 

  39. Novacky A: Suppression of the bacterially induced hypersensitive reaction by cytokinins. Physiol Plant Path 2: 101–104 (1972).

    Google Scholar 

  40. Pennell RI, Lamb C: Programmed cell death in plants. Plant Cell 9: 1157–1168 (1997).

    PubMed  Google Scholar 

  41. Pontier D, Godiard L, Marco Y, Roby D: HSR203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant-pathogen interactions. Plant J 5: 507–521 (1994).

    Article  PubMed  Google Scholar 

  42. Pontier D, Tronchet M, Rogowsky P, Roby D: Activation of HSR203J, a plant gene expressed during incompatible plantpathogen interactions, is correlated with programmed cell death. Mol Plant-Microbe Interact 11: 544–554 (1998).

    PubMed  Google Scholar 

  43. Roby D, Broglie K, Cressman R, Chet I, Broglie R: Activation of a bean chitinase promoter in transgenic plants by phytopathogenic fungi. Plant Cell 2: 999–1007 (1990).

    Article  PubMed  Google Scholar 

  44. Ryerson DE, Heath MC: Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell 8: 393–402 (1996).

    PubMed  Google Scholar 

  45. Shaham S, Shuman MA, Herskowitz I: Death-defying yeast identity novel apoptosis genes. Cell 92: 425–427 (1998).

    PubMed  Google Scholar 

  46. Smart CM: Gene expression during leaf senescence. New Phytol 126: 419–448 (1994).

    Google Scholar 

  47. Villa P, Kaufmann SH, Earnshaw WC: Caspases and caspase inhibitors. Trends Biol Sci 22: 388–393 (1997).

    Google Scholar 

  48. Weaver LM, Gan S, Quirino B, Amasino RM: A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37: 455–469 (1998).

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pontier, D., Gan, S., Amasino, R.M. et al. Markers for hypersensitive response and senescence show distinct patterns of expression. Plant Mol Biol 39, 1243–1255 (1999). https://doi.org/10.1023/A:1006133311402

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006133311402

Navigation