Cell death upon H2O2 induction in the unicellular green alga Micrasterias

Plant Biology

Volumn 10, Issue 6, 2008, Pages 732-745

  Darehshouri, A ^a   Affenzeller, M ^a   Lutz Meindl U ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

Author keywords

Caspase 3 activity; Green algae; H2O2; Micrasterias; Photosynthesis; Programmed cell death; Ultrastructure

Indexed keywords

APOPTOSIS; CONCENTRATION (COMPOSITION); ENVIRONMENTAL CONDITIONS; ENZYME ACTIVITY; EXPERIMENTAL STUDY; GREEN ALGA; HYDROGEN PEROXIDE; PHOTOSYNTHESIS; POND; REDUCTION; SURVIVAL; ULTRASTRUCTURE;

ALGAE; CHLOROPHYTA; EMBRYOPHYTA; MICRASTERIAS; MICRASTERIAS DENTICULATA;

ALGAL DNA; CASPASE 3; HYDROGEN PEROXIDE; PIGMENT;

APOPTOSIS; ARTICLE; CELL CYCLE; DNA FRAGMENTATION; DRUG EFFECT; GREEN ALGA; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; NICK END LABELING; PHOTOSYNTHESIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ALGAE, GREEN; APOPTOSIS; CASPASE 3; CELL CYCLE; DNA FRAGMENTATION; DNA, ALGAL; HYDROGEN PEROXIDE; IN SITU NICK-END LABELING; MICROSCOPY, ELECTRON, TRANSMISSION; PHOTOSYNTHESIS; PIGMENTS, BIOLOGICAL;

EID: 53549084873     PISSN: 14358603     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1438-8677.2008.00078.x     Document Type: Article

References (84)

1. Aichinger N., Lütz-Meindl U. (2005) Organelle interactions and possible degradation pathways visualized in high-pressure frozen algal cells. Journal of Microscopy, 219, 86 94.
2. Ameisen J.C. (1996) The origin of programmed cell death. Science, 272, 1278 1279.
3. Aranha M.M., Matos A.R., Mendes A.T., Pinto V.V., Rodrigues C.M.P., Arrabaça J.D. (2007) Dinitro-o-cresol induces apoptosis-like cell death but not alternative oxidase expression in soybean cells. Journal of Plant Physiology, 164, 675 684.
4. Berges J.A., Falkowski P.G. (1998) Physiological stress and cell death in marine phytoplankton: Induction of proteases in response to nitrogen or light limitation. Limnology and Oceanography, 43, 129 135.
5. Berman-Frank I., Bidle K.D., Haramaty L., Falkowski P.G. (2004) The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnology and Oceanography, 49, 997 1005.
6. Bidle K.D., Falkowski P.G. (2004) Cell death in planktonic, photosynthetic microorganisms. Nature Reviews Microbiology, 2, 643 655.
7. Casotti R., Mazza S., Brunet C., Vantrepotte V., Ianora A., Miralto A. (2005) Growth inhibition and toxicity of the diatom aldehyde 2-trans, 4-trans-decadienal on Thalassiosira weissflogii (Bacillariophyceae). Journal of Phycology, 41, 7 20.
8. Chen H., Yan C., Jiang X., Dai Y.-R. (1999) Hyperthermia-induced apoptosis and the inhibition of DNA laddering by zinc supplementation and withdrawal of calcium and magnesium in suspension culture of tobacco cells. Cellular and Molecular Life Sciences, 55, 303 309.
9. Collins R.J., Harmon B.V., Gobé G.C., Kerr J.F. (1992) Internucleosomal DNA cleavage should not be the sole criterion for identifying apoptosis. International Journal of Radiation Biology, 61, 451 453.
10. Danon A., Gallois P. (1998) UV-C radiation induces apoptotic-like changes in Arabidopsis thaliana. FEBS Letters, 437, 131 136.
11. Danon A., Delorme V., Mailhac N., Gallois P. (2000) Plant programmed cell death: a common way to die. Plant Physiology and Biochemistry, 38, 647 655.
12. Debrabant A., Lee N., Bertholet S., Duncan R., Nakhasi H.L. (2003) Programmed cell death in trypanosomatids and other unicellular organisms. International Journal for Parasitology, 33, 257 267.
13. van Doorn W.G., Woltering E.J. (2005) Many ways to exit? Cell death categories in plants. Trends in Plant Science, 10, 117 122.
14. Evans D.E. (2004) Programmed cell death in response to abiotic stress. In: Gray J. Ed Progammed Cell Death in Plants. CRC Press, Blackwell Publishing, Ohio, USA: 194 pp.
15. Fan T., Xing T. (2004) Heat shock induces programmed cell death in wheat leaves. Biologia Plantarum, 48, 389 394.
16. Franklin D.J., Berges J.A. (2004) Mortality in cultures of the dinoflagellate Amphidinium carterae during culture senescence and darkness. Proceedings of the Royal Society of London Series B-Biological Sciences, 271, 2099 2107.
17. Fukuda H. (2000) Programmed cell death of tracheary elements as a paradigm in plants. Plant Molecular Biology, 44, 245 253.
18. Gechev T.S., Hille J. (2005) Hydrogen peroxide as a signal controlling plant programmed cell death. Journal of Cell Biology, 168, 17 20.
19. Gechev T.S., Van Breusegem F., Stone J.M., Denev I., Laloi C. (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssay, 28, 1091 1101.
20. Geitmann A., Franklin-Tong V.E., Emons A.C. (2004) The self-incompatibility response in Papaver rhoeas pollen causes early and striking alterations to organelles. Cell Death and Differentiation, 11, 812 822.
21. Golstein P., Aubry L., Levraud J.P. (2003) Cell-death alternative model organisms: why and which? Nature Reviews Molecular Cell Biology, 4, 798 807.
22. Gordeeva A.V., Labas Y.A., Zvyagilskaya R.A. (2004) Apoptosis in unicellular organisms: mechanisms and evolution. Biochemistry (Moscow), 69, 1055 1066.
23. Grasl-Kraupp B., Ruttkay-Nedecky B., Koudelka H., Bukowska K., Bursch W., Schulte-Hermann R. (1995) In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology, 21, 1465 1468.
24. Gray J. (2004) Paradigms of the evolution of programmed cell death. In: Gray J. Ed Programmed Cell Death in Plants. CRC Press, Blackwell Publishing, Ohio, USA: 1 25.
25. Gunawardena A.H.L.A.N., Pearce D.M., Jackson M.B., Hawes C.R., Evans D.E. (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta, 212, 205 214.
26. Häcki J., Egger L., Monney L., Conus S., Rosse T., Fellay I., Borner C. (2000) Apoptotic crosstalk between the endoplasmic reticulum and mitochondria controlled by Bcl-2. Oncogene, 19, 2286 2295.
27. 2 in Arabidopsis. The Journal of Biological Chemistry, 283, 774 783.
28. Höftberger M., Url T., Meindl U. (1995) Disturbance of the secretory pathway in Micrasterias denticulata by tunicamycin and cyclopiazonic acid. Protoplasma, 189, 173 179.
29. Holzinger A., Lütz-Meindl U. (2001) Chondramides, novel cyclodepsipeptides from myxobacteria, influence cell development and induce actin filament polymerization in the green alga Micrasterias. Cell Motility and the Cytoskeleton, 48, 87 95.
30. Houot V., Etienne P., Petitot A.-S., Barbier S., Blein J.-P., Suty L. (2001) Hydrogen peroxide induces programmed cell death features in cultured tobacco BY-2 cells, in a dose-dependent manner. Journal of Experimental Botany, 52, 1721 1730.
31. Kerr J.F.R., Wylie A.H., Currie A.R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. British Journal of Cancer, 26, 239 257.
32. Kiermayer O. (1981) Cytoplasmic basis of morphogenesis in Micrasterias. In: Kiermayer O. (Ed Cytomorphogenesis in Plants. Springer, Vienna, New York, Cell Biology Monographs 8: 147 pp.
33. Kolb R.M., Dolder H., Cortelazzo A.L. (2004) Effects of anoxia on root ultrastructure of four neotropical trees. Protoplasma, 224, 99 105.
34. Korthout H.A.A.J., Berecki G., Bruin W., van Duijin B., Wang M. (2000) The presence and subcellular localization of caspase 3-like proteinases in plant cells. FEBS Letters, 475, 139 144.
35. Lam E., Kato N., Lawton M. (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature, 411, 848 853.
36. Lee N., Bertholet S., Debrabant A., Muller J., Duncan R., Nakhasi H.L. (2002) Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death and Differentiation, 9, 53 64.
37. Leu K.-L., Hsu B.-D. (2005) A programmed cell disintegration of Chlorella after heat stress. Plant Science, 168, 145 152.
38. Levine A., Pennell R.I., Alvarez M.E., Palmer R., Lamb C. (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Current Biology, 6, 427 437.
39. Lewis K. (2000) Programmed death in bacteria. Microbiology and Molecular Biology Reviews, 64, 503 514.
40. Li W., Dickman M.B. (2004) Abiotic stress induces apoptotic-like features in tobacco that is inhibited by expression of human Bcl-2. Biotechnology Letters, 26, 87 95.
41. Logan D.C. (2006) The mitochondrial compartment. Journal of Experimental Botany, 57, 1225 1243.
42. LoSchiavo F., Baldan B., Compagnin D., Ganz R., Mariani P., Terzi M. (2000) Spontaneous and induced apoptosis in embryogenic cell cultures of carrot (Daucus carota L.) in different physiological states. European Journal of Cell Biology, 79, 294 298.
43. Lütz C., Seidlitz H.K., Meindl U. (1997) Physiological and structural changes in the chloroplast of the green alga Micrasterias denticulata induced by UV-B simulation. Plant Ecology, 128, 54 64.
44. Madeo F., Fröhlich E., Fröhlich K.U. (1997) A yeast mutant showing diagnostic markers of early and late apoptosis. The Journal of Cell Biology, 139, 729 734.
45. McManus M.T., Thompson D.S., Merriman C., Lyne L., Osborne J. (1998) Transdifferentiation of mature cortical cells to functional abscission cells in bean. Plant Physiology, 116, 891 899.
46. Meindl U. (1990) Effects of temperature on cytomorphogenesis and ultrastructure of Micrasterias denticulata Bréb. Protoplasma, 157, 3 18.
47. Meindl U. (1993) Micrasterias cells as a model system for research on morphogenesis. Microbiological Reviews, 57, 415 433.
48. Meindl U., Wittmann-Pinegger D., Kiermayer O. (1989) Cell multiplication and ultrastructure of Micrasterias denticulata (Desmidiaceae) grown under salt stress. Plant Systematics and Evolution, 164, 197 208.
49. Meindl U., Lancelle S.A., Hepler P.K. (1992) Vesicle production and fusion during lobe formation in Micrasterias visualized by high-pressure freeze fixation. Protoplasma, 170, 104 114.
50. Mittler R., Cheung A.Y. (2004) Biological role of cell death in development and homeostasis. Cell death in plant development and defense. In: Lockshine R.A., Zaken A. (Eds When Cells Die II. John Wiley & Sons, Inc, Hoboken, New Jersey: 99 pp.
51. Mittler R., Simon L., Lam E. (1997) Pathogen-induced programmed cell death in tobacco. Journal of Cell Science, 110, 1333 1344.
52. Moharikar S., D'Souza J.S., Kulkarni A.B., Rao B.J. (2006) Apoptotic-like cell death pathway is induced in unicellular chlorophyte Chlamydomonas reinhardtii (Chlorophyceae) cells following UV irradiation: detection and functional analyses. Journal of Phycology, 42, 423 433.
53. Murray M.G., Thompson W.F. (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research, 8, 4321 4325.
54. Nooden L.D. (2004) Plant Cell Death Processes. Elsevier Academic Press, California, USA.
55. Oberhammer F., Wilson J.W., Dive C., Morris I.D., Hickman J.A., Wakeling A.E., Walker P.R., Sikorska M. (1993) Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. The EMBO Journal, 12, 3679 3684.
56. Oertel A., Aichinger N., Hochreiter R., Thalhamer J., Lütz-Meindl U. (2004) Analysis of mucilage secretion and excretion in Micrasterias (Chlorophyta) by means of immunoelectron microscopy and digital time lapse video microscopy. Journal of Phycology, 40, 711 720.
57. Overmyer K., Brosche M., Pellinen R., Kuittinen T., Tuominen H., Ahlfors R., Keinänen M., Saarma M., Scheel D., Kangasjärvi J. (2005) Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant. Plant Physiology, 137, 1092 1104.
58. de Pinto M.C., Paradiso A., Leonetti P., De Gara L. (2006) Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death. The Plant Journal, 48, 784 795.
59. Polverari A., Buonaurio R., Guiderdone S., Pezzotti M., Marte M. (2000) Ultrastructural observations and DNA degradation analysis of pepper leaves undergoing a hypersensitive reaction to Xanthomonas campestris pv. vesicatoria. European Journal of Plant Pathology, 106, 423 431.
60. Pommerville J.C., Kochert G.D. (1982) Effects of senescence on somatic cell physiology in the green alga Volvox carteri. Experimental Cell Research, 140, 39 45.
61. Salomon S., Meindl U. (1996) Brefeldin A induces reversible dissociation of the Golgi apparatus in the green alga Micrasterias. Protoplasma, 194, 231 242.
62. Schlösser U.G. (1982) List of strains. Berichte der Deutschen Botanischen Gesellschaft, 95, 181 206.
63. Segovia M., Berges J.A. (2005) Effect of inhibitors of protein synthesis and DNA replication on the induction of proteolytic activities, caspase-like activities and cell death in the unicellular chlorophyte Dunaliella tertiolecta. European Journal of Phycology, 40, 21 30.
64. Segovia M., Haramaty L., Berges J.A., Falkowski P.G. (2003) Cell death in the unicellular chlorophyte Dunaliella tertiolecta. A hypothesis on the evolution of apoptosis in higher plants and metazoans. Plant Physiology, 132, 99 105.
65. Selga T., Selga M., Pavila V. (2005) Death of mitochondria during programmed cell death of leaf mesophyll cells. Cell Biology International, 29, 1050 1056.
66. Sen N., Das B.B., Ganguly A., Mukherjee T., Tripathi G., Bandyopadhyay S., Rakshit S., Sen T., Majumder H.K. (2004) Camptothecin induced mitochondrial dysfunction leading to programmed cell death in unicellular hemoflagellate Leishmania donovani. Cell Death and Differentiation, 11, 924 936.
67. Sloop G.D., Roa J.C., Delgado A.G., Balart J.T., Hines M.O., Hill J.M. (1999) Histologic sectioning produces TUNEL reactivity. A potential cause of false-positive staining. Archives of Pathology and Laboratory Medicine, 123, 529 532.
68. Srivastava A., Strasser R.J., Govindjee (1999) Greening of peas: parallel measurements of 77 K emission spectra, OJIP chlorophyll a fluorescence transient, period four oscillation of the initial fluorescence level, delayed light emission, and P700. Photosynthetica, 37, 365 392.
69. Stein J.C., Hansen G. (1999) Mannose induces an endonuclease responsible for DNA laddering in plant cells. Plant Physiology, 121, 71 80.
70. Strasser R.J., Srivastava A., Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochemistry and Photobiology, 61, 32 42.
71. Tian R.-H., Zhang G.-Y., Yan C.-H., Dai Y.-R. (2000) Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells. FEBS Letters, 474, 11 15.
72. Tiwari B.S., Belenghi B., Levine A. (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiology, 128, 1271 1281.
73. 2 limitation and oxidative stress. Current Biology, 9, 1061 1064.
74. Vardi A., Schatz D., Beeri K., Motro U., Sukenik A., Levine A., Kaplan A. (2002) Dinoflagellate-cyanobacterium communication may determine the composition of phytoplankton assemblages in a mesotrophic lake. Current Biology, 12, 1767 1772.
75. Veldhuis M.J.W., Kraay G.W., Timmermans K.R. (2001) Cell death in phytoplankton: correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth. European Journal of Phycology, 36, 167 177.
76. 2+-induced high amplitude swelling and cytochrome c release from wheat (Triticum aestivum L.) mitochondria under anoxic stress. Annals of Botany, 90, 509 516.
77. Weiss D., Lütz C., Lütz-Meindl U. (1999) Photosynthesis and heat response of the green alga Micrasterias denticulata (Desmidiaceae). Zeitschrift für Naturforschung, 54c, 508 516.
78. Welburn S.C., Barcinski M.A., Williams G.T. (1997) Programmed cell death in trypanosomatids. Parasitology Today, 13, 22 26.
79. Wyllie A.H. (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature, 284, 555 556.
80. Yamori W., Kogami H., Masuzawa T. (2005) Freezing tolerance in alpine plants as assessed by the FDA-staining method. Polar Bioscience, 18, 73 81.
81. Yao N., Tada Y., Park P., Nakayashiki H., Tosa Y., Mayama S. (2001) Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats. The Plant Journal, 28, 13 26.
82. Yu X.-H., Perdue T.D., Heimer Y.M., Jones A.M. (2002) Mitochondrial involvement in tracheary element programmed cell death. Cell Death and Differentiation, 9, 189 198.
83. Zuppini A., Navazio L., Mariani P. (2004) Endoplasmic reticulum stress-induced programmed cell death in soybean cells. Journal of Cell Science, 117, 2591 2598.
84. Zuppini A., Andreoli C., Baldan B. (2007) Heat stress: an inducer of programmed cell death in Chlorella saccharophila. Plant and Cell Physiology, 48, 1000 1009.