Home LiteratureArticle Details
PMID: 9207837 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Characterization of nuclease activities and DNA fragmentation induced upon hypersensitive response cell death and mechanical stress.

Plant molecular biology ·Vol. 34 ·No. 2 ·1997-05-00 ·Pages 209-21

Mittler R, Lam E

Abstract

Programmed cell death (PCD) is activated during the response of multicellular organisms to some invading pathogens. One of the key aspects of this process is the degradation of nuclear DNA which is thought to facilitate the recycling of DNA from dead cells. The PCD of tobacco plants (genotype NN) infected with tobacco mosaic virus (TMV) is accompanied by the induction of nuclease activities and the cleavage of nuclear DNA to fragments of about 50 kb. We examined the correlation between the increase in nuclease activities and the fragmentation of nuclear DNA during TMV- and bacteria-induced PCD in tobacco. We found that the increase in nuclease activities did not always correlate with fragmentation of nuclear DNA. Thus, in addition to pathogens that induce PCD, mechanical injury and infiltration of leaves with 1 M sucrose or bacteria that did not induce PCD also resulted in an increase in nuclease activities. Analysis of nuclease activities in total leaf extracts, nuclear extracts, and intercellular fluid (i.e., apoplast) revealed that at least four different nuclease activities are induced during PCD in tobacco; of these at least three appear to be secreted into the intercellular fluid. Although the latter were also induced in response to treatments that did not result in DNA fragmentation, they may function in the recycling of plant DNA during late stages of PCD when the integrity of the plasma membrane is compromised. This suggestion is supported by the finding that DNA degradation occurred late during TMV-induced PCD in tobacco. In addition, the finding of induced nuclease activities in the intercellular fluid raises the possibility that they may serve a protective function by degrading the DNA of invading pathogens.

MeSH Terms
Apoptosis DNA Fragmentation Endodeoxyribonucleases/biosynthesis,genetics,metabolism Enzyme Induction/genetics Plant Leaves/enzymology,genetics,virology Plant Proteins/biosynthesis,genetics,metabolism Plants, Toxic Stress, Mechanical Tobacco/enzymology,genetics,virology Tobacco Mosaic Virus/genetics
Chemicals
Plant Proteins Endodeoxyribonucleases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Mittler R
Center for Agricultural Molecular Biology, Rutgers, The State University of New Jersey, Cook College, New Brunswick 08903-0231, USA.
Lam E
References (39)
39 references, click to expand
  1. Detection of the initial stages of DNA fragmentation in apoptosis.
    Biotechniques. 1993 Dec;15(6):1032-40 PMID: 8292335
  2. Pseudomonas syringae pv. syringae harpinPss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants.
    Cell. 1993 Jul 2;73(7):1255-66 PMID: 8324821
  3. XYLOGENESIS: INITIATION, PROGRESSION, AND CELL DEATH.
    Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:299-325 PMID: 15012291
  4. Barley aleurone layers secrete a nuclease in response to gibberellic Acid : purification and partial characterization of the associated ribonuclease, deoxyribonuclease, and 3'-nucleotidase activities.
    Plant Physiol. 1986 Nov;82(3):801-6 PMID: 16665113
  5. DNA fragmentation during apoptosis is caused by frequent single-strand cuts.
    Nucleic Acids Res. 1993 Sep 11;21(18):4206-9 PMID: 8414975
  6. Inhibition of Programmed Cell Death in Tobacco Plants during a Pathogen-Induced Hypersensitive Response at Low Oxygen Pressure.
    Plant Cell. 1996 Nov;8(11):1991-2001 PMID: 12239372
  7. Coordinated Activation of Programmed Cell Death and Defense Mechanisms in Transgenic Tobacco Plants Expressing a Bacterial Proton Pump.
    Plant Cell. 1995 Jan;7(1):29-42 PMID: 12242350
  8. Dicing with death: dissecting the components of the apoptosis machinery.
    Trends Biochem Sci. 1994 Jan;19(1):26-30 PMID: 8140617
  9. Sacrifice in the face of foes: pathogen-induced programmed cell death in plants.
    Trends Microbiol. 1996 Jan;4(1):10-15 PMID: 8824789
  10. Improvement and simplification of low-background silver staining of proteins by using sodium dithionite.
    Electrophoresis. 1988 Jun;9(6):288-91 PMID: 2466660
  11. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins.
    Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7742-6 PMID: 1457005
  12. Cleavage of Nuclear DNA into Oligonucleosomal Fragments during Cell Death Induced by Fungal Infection or by Abiotic Treatments.
    Plant Cell. 1996 Mar;8(3):393-402 PMID: 12239388
  13. Arabidopsis mutants simulating disease resistance response.
    Cell. 1994 May 20;77(4):565-77 PMID: 8187176
  14. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response.
    Cell. 1992 Jul 10;70(1):21-30 PMID: 1623521
  15. The role of DNA fragmentation in apoptosis.
    Trends Cell Biol. 1995 Jan;5(1):21-6 PMID: 14731429
  16. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics.
    Br J Cancer. 1972 Aug;26(4):239-57 PMID: 4561027
  17. The mode of death of pig kidney cells infected with cowpox virus is governed by the expression of the crmA gene.
    Virology. 1996 Mar 1;217(1):384-91 PMID: 8599227
  18. In Situ Detection of nDNA Fragmentation during the Differentiation of Tracheary Elements in Higher Plants.
    Plant Physiol. 1995 Jun;108(2):489-493 PMID: 12228486
  19. Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death.
    Plant Cell. 1995 Nov;7(11):1951-62 PMID: 8535145
  20. Identification and purification of a nuclease from Zinnia elegans L.: a potential molecular marker for xylogenesis.
    Planta. 1989 Sep;179(2):181-95 PMID: 24201517
  21. High sequence similarity between a ribonuclease from ginseng calluses and fungus-elicited proteins from parsley indicates that intracellular pathogenesis-related proteins are ribonucleases.
    Planta. 1994;193(3):470-2 PMID: 7764876
  22. Apoptosis: A Functional Paradigm for Programmed Plant Cell Death Induced by a Host-Selective Phytotoxin and Invoked during Development.
    Plant Cell. 1996 Mar;8(3):375-391 PMID: 12239387
  23. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions.
    Cell. 1994 May 20;77(4):551-63 PMID: 8187175
  24. Programmed cell death: a way of life for plants.
    Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12094-7 PMID: 8901538
  25. Evidence for a Mechanically Induced Oxidative Burst.
    Plant Physiol. 1995 Dec;109(4):1259-1266 PMID: 12228667
  26. Nuclease I from suspension-cultured Nicotiana tabacum: purification and properties of the extracellular enzyme.
    Arch Biochem Biophys. 1982 Jun;216(1):223-33 PMID: 6285829
  27. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.
    Cell. 1994 Nov 18;79(4):583-93 PMID: 7954825
  28. Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants.
    J Bacteriol. 1986 Nov;168(2):512-22 PMID: 3023280
  29. Defense-related proteins in higher plants.
    Annu Rev Biochem. 1990;59:873-907 PMID: 2197993
  30. FINE STRUCTURE OF LESION PERIPHERY PRODUCED BY TOBACCO MOSAIC VIRUS.
    Phytopathology. 1965 Apr;55:387-92 PMID: 14288717
  31. Shigella flexneri induces apoptosis in infected macrophages.
    Nature. 1992 Jul 9;358(6382):167-9 PMID: 1614548
  32. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response.
    Curr Biol. 1996 Apr 1;6(4):427-37 PMID: 8723347
  33. Biochemical properties and hormonal regulation of barley nuclease.
    Eur J Biochem. 1987 Oct 15;168(2):357-64 PMID: 2822411
  34. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  35. Apoptosis: the biochemistry and molecular biology of programmed cell death.
    Endocr Rev. 1993 Apr;14(2):133-51 PMID: 8325248
  36. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death.
    Cell. 1991 Jun 28;65(7):1107-15 PMID: 1648447
  37. Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis.
    J Pathol. 1984 Jan;142(1):67-77 PMID: 6422024
  38. The apoptosis endonucleases: cleaning up after cell death?
    Trends Cell Biol. 1994 Feb;4(2):37-41 PMID: 14731864
  39. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor.
    Cell. 1994 Sep 23;78(6):1101-15 PMID: 7923359
Article Info
Journal
Plant molecular biology
Abbr.
Plant Mol Biol
ISSN
0167-4412
Published
1997-05-00
Pages
209-21
Language
English
Region
Netherlands
NLM ID
9106343
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com