Home LiteratureArticle Details
PMID: 14688291 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Programmed cell death remodels lace plant leaf shape during development.

The Plant cell ·Vol. 16 ·No. 1 ·2004-01-00 ·Pages 60-73

Gunawardena AH, Greenwood JS, Dengler NG

Abstract

Programmed cell death (PCD) functions in the developmental remodeling of leaf shape in higher plants, a process analogous to digit formation in the vertebrate limb. In this study, we provide a cytological characterization of the time course of events as PCD remodels young expanding leaves of the lace plant. Tonoplast rupture is the first PCD event in this system, indicated by alterations in cytoplasmic streaming, loss of anthocyanin color, and ultrastructural appearance. Nuclei become terminal deoxynucleotidyl transferase-mediated dUTP nick end labeling positive soon afterward but do not become morphologically altered until late stages of PCD. Genomic DNA is fragmented, but not into internucleosomal units. Other cytoplasmic changes, such as shrinkage and degradation of organelles, occur later. This form of PCD resembles tracheary element differentiation in cytological execution but requires unique developmental regulation so that discrete panels of tissue located equidistantly between veins undergo PCD while surrounding cells do not.

MeSH Terms
Anthocyanins/metabolism Apoptosis Cell Differentiation Cell Nucleus/metabolism Cell Wall/metabolism Cytoplasmic Streaming/genetics,physiology DNA Fragmentation Magnoliopsida/genetics,growth & development,ultrastructure Microscopy, Electron Plant Leaves/genetics,growth & development,ultrastructure Vacuoles/metabolism
Chemicals
Anthocyanins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Gunawardena Arunika H L A N
Department of Botany, University of Toronto, Toronto, Ontario, Canada M5S 1A1.
Greenwood John S
Dengler Nancy G
References (43)
43 references, click to expand
  1. Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia.
    Plant Physiol. 2001 Feb;125(2):615-26 PMID: 11161019
  2. Cell death: the significance of apoptosis.
    Int Rev Cytol. 1980;68:251-306 PMID: 7014501
  3. Ethylene-Mediated Programmed Cell Death during Maize Endosperm Development of Wild-Type and shrunken2 Genotypes.
    Plant Physiol. 1997 Oct;115(2):737-751 PMID: 12223841
  4. Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells.
    Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15794-9 PMID: 12438691
  5. Leaf Vascular Pattern Formation.
    Plant Cell. 1997 Jul;9(7):1121-1135 PMID: 12237378
  6. Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.).
    Planta. 2001 Jan;212(2):205-14 PMID: 11216841
  7. How plants make tubes.
    Trends Plant Sci. 2003 Apr;8(4):159-64 PMID: 12711227
  8. Pathogen-induced programmed cell death in tobacco.
    J Cell Sci. 1997 Jun;110 ( Pt 11):1333-44 PMID: 9202394
  9. Apoptosis in developing anthers and the role of ABA in this process during androgenesis in Hordeum vulgare L.
    Plant Mol Biol. 1999 Feb;39(3):489-501 PMID: 10092177
  10. 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
  11. Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators.
    Bioessays. 2003 Jan;25(1):47-57 PMID: 12508282
  12. The nucellus degenerates by a process of programmed cell death during the early stages of wheat grain development.
    Planta. 2001 Jul;213(3):352-60 PMID: 11506357
  13. Developmental programmed cell death in plants.
    Curr Opin Plant Biol. 2002 Dec;5(6):568-73 PMID: 12393021
  14. 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
  15. The Wnt antagonist Dickkopf-1 is regulated by Bmp signaling and c-Jun and modulates programmed cell death.
    EMBO J. 2002 Mar 1;21(5):966-75 PMID: 11867524
  16. Cell death and cell protection genes determine the fate of pistils in maize.
    Development. 1999 Feb;126(3):435-41 PMID: 9876173
  17. Defining senescence and death.
    J Exp Bot. 2003 Apr;54(385):1127-32 PMID: 12654863
  18. Loss of Tonoplast Integrity Programmed in Tracheary Element Differentiation.
    Plant Physiol. 1999 Nov;121(3):763-774 PMID: 10557224
  19. Barley aleurone cell death is not apoptotic: characterization of nuclease activities and DNA degradation
    Plant J. 1999 Nov;20(3):305-15 PMID: 10571891
  20. Programmed cell death during embryogenesis in maize.
    Ann Bot. 2002 Aug;90(2):287-92 PMID: 12197527
  21. Induction of Enzymes Associated with Lysigenous Aerenchyma Formation in Roots of Zea mays during Hypoxia or Nitrogen Starvation.
    Plant Physiol. 1994 Jul;105(3):861-865 PMID: 12232249
  22. Endonucleases.
    Plant Mol Biol. 2000 Oct;44(3):387-97 PMID: 11199396
  23. Characterization of nuclease activities and DNA fragmentation induced upon hypersensitive response cell death and mechanical stress.
    Plant Mol Biol. 1997 May;34(2):209-21 PMID: 9207837
  24. Programmed cell death during plant growth and development.
    Cell Death Differ. 1997 Dec;4(8):649-61 PMID: 16465277
  25. Electron microscopy of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to oxygen shortage.
    Planta. 1983 Jul;157(4):350-7 PMID: 24264269
  26. 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
  27. Programmed cell death of tracheary elements as a paradigm in plants.
    Plant Mol Biol. 2000 Oct;44(3):245-53 PMID: 11199386
  28. Okadaic acid, a protein phosphatase inhibitor, blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells.
    Plant Cell. 1996 Feb;8(2):259-69 PMID: 8742711
  29. ZEN1 is a key enzyme in the degradation of nuclear DNA during programmed cell death of tracheary elements.
    Plant Cell. 2002 Dec;14(12):3201-11 PMID: 12468737
  30. Does the plant mitochondrion integrate cellular stress and regulate programmed cell death?
    Trends Plant Sci. 2000 May;5(5):225-30 PMID: 10785669
  31. Programmed cell death in development and defense.
    Plant Physiol. 2001 Jan;125(1):94-7 PMID: 11154305
  32. Hydrogen peroxide induces programmed cell death features in cultured tobacco BY-2 cells, in a dose-dependent manner.
    J Exp Bot. 2001 Aug;52(361):1721-30 PMID: 11479338
  33. Apoptosis in barley aleurone during germination and its inhibition by abscisic acid.
    Plant Mol Biol. 1996 Dec;32(6):1125-34 PMID: 9002611
  34. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response.
    Curr Biol. 1996 Apr 1;6(4):427-37 PMID: 8723347
  35. Autolysis during in vitro tracheary element differentiation: formation and location of the perforation.
    Plant Cell Physiol. 2000 Nov;41(11):1267-71 PMID: 11092912
  36. Early gene expression associated with the commitment and differentiation of a plant tracheary element is revealed by cDNA-amplified fragment length polymorphism analysis.
    Plant Cell. 2002 Nov;14(11):2813-24 PMID: 12417703
  37. Nuclease activities and DNA fragmentation during programmed cell death of megagametophyte cells of white spruce (Picea glauca) seeds.
    Plant Mol Biol. 2003 Mar;51(4):509-21 PMID: 12650617
  38. Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation.
    EMBO J. 1993 Sep;12(9):3679-84 PMID: 8253089
  39. LEAF DEVELOPMENT IN ANGIOSPERMS.
    Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:419-446 PMID: 15012215
  40. Hypersensitive response-related death.
    Plant Mol Biol. 2000 Oct;44(3):321-34 PMID: 11199391
  41. Programmed cell death in animal development.
    Cell. 1997 Feb 7;88(3):347-54 PMID: 9039261
  42. The sex determination process in maize.
    Science. 1994 Dec 2;266(5190):1501-5 PMID: 7985019
  43. Programmed Cell Death in Plants.
    Plant Cell. 1997 Jul;9(7):1157-1168 PMID: 12237381
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2004-01-00
Epub
2003-00-19
Pages
60-73
Language
English
Region
England
NLM ID
9208688
PMCID
PMC301395
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