• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Oct 29, 1996; 93(22): 12094–12097.

Programmed cell death: a way of life for plants.


Cell death in higher plants has been widely observed in predictable patterns throughout development and in response to pathogenic infection. Genetic, biochemical, and morphological evidence suggests that these cell deaths occur as active processes and can be defined formally as examples of programmed cell death (PCD). Intriguingly, plants have at least two types of PCD, an observation that is also true of PCD in animals [Schwartz, L. M., Smith, W.W., Jones, M. E. E. & Osborne, B. A. (1993) Proc. Natl. Acad. Sci. USA 90, 980-984]. Thus, in plants, PCD resembles either a common form of PCD seen in animals called apoptosis or it resembles a morphologically distinct form of cell death. The ubiquitous occurrence and necessity of PCD for plant development and defense suggest that the underlying mechanisms of regulation and execution of these processes merit further examination.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (885K), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ellis RE, Yuan JY, Horvitz HR. Mechanisms and functions of cell death. Annu Rev Cell Biol. 1991;7:663–698. [PubMed]
  • Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972 Aug;26(4):239–257. [PMC free article] [PubMed]
  • Wyllie AH, Kerr JF, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol. 1980;68:251–306. [PubMed]
  • Williams GT. Programmed cell death: a fundamental protective response to pathogens. Trends Microbiol. 1994 Dec;2(12):463–464. [PubMed]
  • Khelef N, Zychlinsky A, Guiso N. Bordetella pertussis induces apoptosis in macrophages: role of adenylate cyclase-hemolysin. Infect Immun. 1993 Oct;61(10):4064–4071. [PMC free article] [PubMed]
  • Levine A, Pennell RI, Alvarez ME, Palmer R, Lamb C. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol. 1996 Apr 1;6(4):427–437. [PubMed]
  • Wang H, Li J, Bostock RM, Gilchrist DG. 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. [PMC free article] [PubMed]
  • 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. 1995 Jan;7(1):29–42. [PMC free article] [PubMed]
  • Ryerson DE, Heath MC. 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. [PMC free article] [PubMed]
  • Nakashima T, Sekiguchi T, Kuraoka A, Fukushima K, Shibata Y, Komiyama S, Nishimoto T. Molecular cloning of a human cDNA encoding a novel protein, DAD1, whose defect causes apoptotic cell death in hamster BHK21 cells. Mol Cell Biol. 1993 Oct;13(10):6367–6374. [PMC free article] [PubMed]
  • Sugimoto A, Hozak RR, Nakashima T, Nishimoto T, Rothman JH. dad-1, an endogenous programmed cell death suppressor in Caenorhabditis elegans and vertebrates. EMBO J. 1995 Sep 15;14(18):4434–4441. [PMC free article] [PubMed]
  • Apte SS, Mattei MG, Seldin MF, Olsen BR. The highly conserved defender against the death 1 (DAD1) gene maps to human chromosome 14q11-q12 and mouse chromosome 14 and has plant and nematode homologs. FEBS Lett. 1995 Apr 24;363(3):304–306. [PubMed]
  • Demura T, Fukuda H. Novel vascular cell-specific genes whose expression is regulated temporally and spatially during vascular system development. Plant Cell. 1994 Jul;6(7):967–981. [PMC free article] [PubMed]
  • Rao PV, Krishna CM, Zigler JS., Jr Identification and characterization of the enzymatic activity of zeta-crystallin from guinea pig lens. A novel NADPH:quinone oxidoreductase. J Biol Chem. 1992 Jan 5;267(1):96–102. [PubMed]
  • Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, Korsmeyer SJ. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 1993 Oct 22;75(2):241–251. [PubMed]
  • Schindler T, Bergfeld R, Schopfer P. Arabinogalactan proteins in maize coleoptiles: developmental relationship to cell death during xylem differentiation but not to extension growth. Plant J. 1995 Jan;7(1):25–36. [PubMed]
  • Raff MC. Social controls on cell survival and cell death. Nature. 1992 Apr 2;356(6368):397–400. [PubMed]
  • DeLong A, Calderon-Urrea A, Dellaporta SL. 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. [PubMed]
  • Wang H, Wu HM, Cheung AY. Pollination induces mRNA poly(A) tail-shortening and cell deterioration in flower transmitting tissue. Plant J. 1996 May;9(5):715–727. [PubMed]
  • Theologis A. One rotten apple spoils the whole bushel: the role of ethylene in fruit ripening. Cell. 1992 Jul 24;70(2):181–184. [PubMed]
  • Hensel LL, Grbić V, Baumgarten DA, Bleecker AB. Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in arabidopsis. Plant Cell. 1993 May;5(5):553–564. [PMC free article] [PubMed]
  • Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell. 1993 Nov 19;75(4):641–652. [PubMed]
  • Blank A, McKeon TA. Expression of Three RNase Activities during Natural and Dark-Induced Senescence of Wheat Leaves. Plant Physiol. 1991 Dec;97(4):1409–1413. [PMC free article] [PubMed]
  • Rouet-Mayer MA, Bureau JM, Laurière C. Identification and characterization of lipoxygenase isoforms in senescing carnation petals. Plant Physiol. 1992 Mar;98(3):971–978. [PMC free article] [PubMed]
  • Lincoln JE, Cordes S, Read E, Fischer RL. Regulation of gene expression by ethylene during Lycopersicon esculentum (tomato) fruit development. Proc Natl Acad Sci U S A. 1987 May;84(9):2793–2797. [PMC free article] [PubMed]
  • Oeller PW, Lu MW, Taylor LP, Pike DA, Theologis A. Reversible inhibition of tomato fruit senescence by antisense RNA. Science. 1991 Oct 18;254(5030):437–439. [PubMed]
  • He SY, Huang HC, Collmer A. 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):1255–1266. [PubMed]
  • Mehdy MC. Active Oxygen Species in Plant Defense against Pathogens. Plant Physiol. 1994 Jun;105(2):467–472. [PMC free article] [PubMed]
  • Levine A, Tenhaken R, Dixon R, Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994 Nov 18;79(4):583–593. [PubMed]
  • Glazener JA, Orlandi EW, Baker CJ. The Active Oxygen Response of Cell Suspensions to Incompatible Bacteria Is Not Sufficient to Cause Hypersensitive Cell Death. Plant Physiol. 1996 Mar;110(3):759–763. [PMC free article] [PubMed]
  • Atkinson MM, Huang JS, Knopp JA. The Hypersensitive Reaction of Tobacco to Pseudomonas syringae pv. pisi: Activation of a Plasmalemma K/H Exchange Mechanism. Plant Physiol. 1985 Nov;79(3):843–847. [PMC free article] [PubMed]
  • Greenberg JT, Guo A, Klessig DF, Ausubel FM. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell. 1994 May 20;77(4):551–563. [PubMed]
  • Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, Dangl JL. Arabidopsis mutants simulating disease resistance response. Cell. 1994 May 20;77(4):565–577. [PubMed]
  • Bestwick CS, Bennett MH, Mansfield JW. Hrp Mutant of Pseudomonas syringae pv phaseolicola Induces Cell Wall Alterations but Not Membrane Damage Leading to the Hypersensitive Reaction in Lettuce. Plant Physiol. 1995 Jun;108(2):503–516. [PMC free article] [PubMed]
  • Walbot V. Maize Mutants for the 21st Century. Plant Cell. 1991 Sep;3(9):851–856. [PMC free article]
  • Wang W, Jones C, Ciacci-Zanella J, Holt T, Gilchrist DG, Dickman MB. Fumonisins and Alternaria alternata lycopersici toxins: sphinganine analog mycotoxins induce apoptosis in monkey kidney cells. Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3461–3465. [PMC free article] [PubMed]
  • Goldberg RB, Beals TP, Sanders PM. Anther development: basic principles and practical applications. Plant Cell. 1993 Oct;5(10):1217–1229. [PMC free article] [PubMed]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


  • MedGen
    Related information in MedGen
  • PubMed
    PubMed citations for these articles
  • Substance
    PubChem Substance links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...