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PMID: 18515833 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Intracellular energy depletion triggers programmed cell death during petal senescence in tulip.

Journal of experimental botany ·Vol. 59 ·No. 8 ·2008-00-00 ·Pages 2085-95

Azad AK, Ishikawa T, Ishikawa T, Sawa Y, Shibata H

Abstract

Programmed cell death (PCD) in petals provides a model system to study the molecular aspects of organ senescence. In this study, the very early triggering signal for PCD during the senescence process from young green buds to 14-d-old petals of Tulipa gesneriana was determined. The opening and closing movement of petals of intact plants increased for the first 3 d and then gradually decreased. DNA degradation and cytochrome c (Cyt c) release were clearly observed in 6-d-old flowers. Oxidative stress or ethylene production can be excluded as the early signal for petal PCD. In contrast, ATP was dramatically depleted after the first day of flower opening. Sucrose supplementation to cut flowers maintained their ATP levels and the movement ability for a longer time than in those kept in water. The onset of DNA degradation, Cyt c release, and petal senescence was also delayed by sucrose supplementation to cut flowers. These results suggest that intracellular energy depletion, rather than oxidative stress or ethylene production, may be the very early signal to trigger PCD in tulip petals.

MeSH Terms
Adenosine Triphosphate/metabolism Aging Apoptosis Cytochromes c/metabolism DNA Fragmentation DNA, Plant/genetics,metabolism Deoxyribonucleases/metabolism Ethylenes/metabolism Flowers/genetics,growth & development,physiology Oxidative Stress Peptide Hydrolases/metabolism Sucrose/metabolism Time Factors Tulipa/genetics,growth & development,physiology
Chemicals
DNA, Plant Ethylenes Sucrose Adenosine Triphosphate Cytochromes c ethylene Deoxyribonucleases Peptide Hydrolases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Azad A K
Department of Life Science and Biotechnology, Shimane University, Shimane 690-8504, Japan.
Ishikawa Takayuki
Ishikawa Takahiro
Sawa Y
Shibata H
References (51)
51 references, click to expand
  1. Programmed cell death, mitochondria and the plant hypersensitive response.
    Nature. 2001 Jun 14;411(6839):848-53 PMID: 11459068
  2. Is petal senescence due to sugar starvation?
    Plant Physiol. 2004 Jan;134(1):35-42 PMID: 14730063
  3. Is a cysteine proteinase inhibitor involved in the regulation of petal wilting in senescing carnation (Dianthus caryophyllus L.) flowers?
    J Exp Bot. 2002 Mar;53(368):407-13 PMID: 11847238
  4. Programmed cell death remodels lace plant leaf shape during development.
    Plant Cell. 2004 Jan;16(1):60-73 PMID: 14688291
  5. Apoptosis is induced by decline of mitochondrial ATP synthesis in erythroleukemia cells.
    Free Radic Biol Med. 2003 May 1;34(9):1190-9 PMID: 12706499
  6. Programmed Cell Death in Plants.
    Plant Cell. 1997 Jul;9(7):1157-1168 PMID: 12237381
  7. Overexpression of catalase or Bcl-2 alters glucose and energy metabolism concomitant with dexamethasone resistance.
    Biochim Biophys Acta. 2004 Jul 23;1693(1):57-72 PMID: 15276325
  8. Regulation of cell death in flower petals.
    Plant Mol Biol. 2000 Oct;44(3):303-18 PMID: 11199390
  9. Characterization of protein phosphatase 2A acting on phosphorylated plasma membrane aquaporin of tulip petals.
    Biosci Biotechnol Biochem. 2004 May;68(5):1170-4 PMID: 15170131
  10. Increases in DNA fragmentation and induction of a senescence-specific nuclease are delayed during corolla senescence in ethylene-insensitive (etr1-1) transgenic petunias.
    J Exp Bot. 2005 Jan;56(409):15-23 PMID: 15475372
  11. Expression of a nitric oxide degrading enzyme induces a senescence programme in Arabidopsis.
    Plant Cell Environ. 2007 Jan;30(1):39-52 PMID: 17177875
  12. Repressed ethylene production in the gynoecium of long-lasting flowers of the carnation 'White Candle': role of the gynoecium in carnation flower senescence.
    J Exp Bot. 2004 Mar;55(397):641-50 PMID: 14966220
  13. Apoptotic pathways: the roads to ruin.
    Cell. 1998 Sep 18;94(6):695-8 PMID: 9753316
  14. Up-regulation of a cysteine protease accompanies the ethylene-insensitive senescence of daylily (Hemerocallis) flowers.
    Plant Mol Biol. 1995 Jun;28(3):575-82 PMID: 7632925
  15. Receptor-mediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD).
    J Physiol. 2001 Apr 1;532(Pt 1):3-16 PMID: 11283221
  16. 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
  17. Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death.
    Plant J. 2006 Dec;48(5):784-95 PMID: 17092315
  18. Characterization of an ascorbate peroxidase in plastids of tobacco BY-2 cells.
    Physiol Plant. 2003 Apr;117(4):550-557 PMID: 12675745
  19. The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release.
    Plant Cell. 2001 Aug;13(8):1803-18 PMID: 11487694
  20. 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
  21. Properties of DNA fragmentation activity generated by ATP depletion.
    Cell Death Differ. 2000 May;7(5):477-84 PMID: 10800081
  22. Regulation of senescence-related gene expression in carnation flower petals by ethylene.
    Plant Physiol. 1990 Aug;93(4):1370-5 PMID: 16667627
  23. The plant homologue of the defender against apoptotic death gene is down-regulated during senescence of flower petals.
    FEBS Lett. 1997 Mar 10;404(2-3):275-8 PMID: 9119078
  24. Cysteine protease gene expression and proteolytic activity during senescence of Alstroemeria petals.
    J Exp Bot. 2002 Feb;53(367):233-40 PMID: 11807127
  25. Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death.
    Plant Physiol. 2002 Apr;128(4):1271-81 PMID: 11950976
  26. A proteomic analysis of plant programmed cell death.
    Phytochemistry. 2004 Jun;65(12):1829-38 PMID: 15276441
  27. The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers.
    Biochemistry. 1968 Nov;7(11):4030-4 PMID: 4972613
  28. DNA degradation and nuclear degeneration during programmed cell death in petals of Antirrhinum, Argyranthemum, and Petunia.
    J Exp Bot. 2006;57(14):3543-52 PMID: 16957019
  29. Cell death and organ development in plants.
    Curr Top Dev Biol. 2005;71:225-61 PMID: 16344107
  30. Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response.
    Plant J. 2000 Apr;22(2):87-95 PMID: 10792824
  31. Programmed cell death induces male sterility in Actinidia deliciosa female flowers.
    Plant Physiol Biochem. 2004 Jun;42(6):537-41 PMID: 15246067
  32. AMP-activated protein kinase: the energy charge hypothesis revisited.
    Bioessays. 2001 Dec;23(12):1112-9 PMID: 11746230
  33. Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants.
    FEBS Lett. 1999 Dec 10;463(1-2):151-4 PMID: 10601657
  34. Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco Bright-Yellow 2 cells.
    Plant Physiol. 2004 Mar;134(3):1100-12 PMID: 15020761
  35. Defining senescence and death.
    J Exp Bot. 2003 Apr;54(385):1127-32 PMID: 12654863
  36. Flower opening and closure: a review.
    J Exp Bot. 2003 Aug;54(389):1801-12 PMID: 12869518
  37. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked.
    Science. 1997 Feb 21;275(5303):1129-32 PMID: 9027314
  38. Ethylene and flower longevity in Alstroemeria: relationship between tepal senescence, abscission and ethylene biosynthesis.
    J Exp Bot. 2005 Mar;56(413):1007-16 PMID: 15689338
  39. Programmed cell death in floral organs: how and why do flowers die?
    Ann Bot. 2006 Mar;97(3):309-15 PMID: 16394024
  40. Phosphorylation of plasma membrane aquaporin regulates temperature-dependent opening of tulip petals.
    Plant Cell Physiol. 2004 May;45(5):608-17 PMID: 15169943
  41. Molecular analysis of programmed cell death during senescence in Arabidopsis thaliana and Brassica oleracea: cloning broccoli LSD1, Bax inhibitor and serine palmitoyltransferase homologues.
    J Exp Bot. 2004 Jan;55(394):59-68 PMID: 14645391
  42. Mannose induces an endonuclease responsible for DNA laddering in plant cells.
    Plant Physiol. 1999 Sep;121(1):71-80 PMID: 10482662
  43. The roles of glutathione and antioxidant enzymes in menadione-induced oxidative stress.
    Toxicology. 2000 Nov 23;154(1-3):75-84 PMID: 11118672
  44. Activation of the programmed cell death pathway by inhibition of proteasome function in plants.
    J Biol Chem. 2003 May 23;278(21):19406-15 PMID: 12637532
  45. Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: potential signalling crosstalk?
    New Phytol. 2006;172(2):221-8 PMID: 16995910
  46. The pathophysiology of mitochondrial cell death.
    Science. 2004 Jul 30;305(5684):626-9 PMID: 15286356
  47. Analysis of changes in energy and redox states in HepG2 hepatoma and C6 glioma cells upon exposure to cadmium.
    Toxicology. 2004 Sep 1;201(1-3):105-13 PMID: 15297025
  48. Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and -independent pathways of programmed cell death.
    Plant Physiol. 2002 Aug;129(4):1908-20 PMID: 12177505
  49. Glucose deprivation induces mitochondrial dysfunction and oxidative stress in PC12 cell line.
    J Cell Mol Med. 2003 Jan-Mar;7(1):49-56 PMID: 12767261
  50. Transglutaminase activity during senescence and programmed cell death in the corolla of tobacco (Nicotiana tabacum) flowers.
    Cell Death Differ. 2002 Mar;9(3):309-21 PMID: 11859413
  51. Programmed cell death during pollination-induced petal senescence in petunia.
    Plant Physiol. 2000 Apr;122(4):1323-33 PMID: 10759529
Article Info
Journal
Journal of experimental botany
Abbr.
J Exp Bot
ISSN
1460-2431
Published
2008-00-00
Epub
2008-00-31
Pages
2085-95
Language
English
Region
England
NLM ID
9882906
PMCID
PMC2413268
Subset
IM
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