The Plant Cell, Vol. 13, 1803-1818,
August 2001, Copyright © 2001,
American Society of Plant Biologists
The PET1-CMS Mitochondrial Mutation in Sunflower Is Associated with Premature Programmed Cell Death and Cytochrome c Release
Janneke Balk1 and
Christopher J. Leaver
University of Oxford, Department of Plant Sciences, South Parks Road, Oxford OX1 3RB, United Kingdom
1 To whom correspondence should be addressed. E-mail janneke.balk{at}plant-sciences.ox.ac.uk; fax 44-1865-275144
In mammals, mitochondria have been shown to play a key intermediary role in apoptosis, a morphologically distinct form of programmed cell death (PCD), for example, through the release of cytochrome c, which activates a proteolytic enzyme cascade, resulting in specific nuclear DNA degradation and cell death. In plants, PCD is a feature of normal development, including the penultimate stage of anther development, leading to dehiscence and pollen release. However, there is little evidence that plant mitochondria are involved in PCD. In a wide range of plant species, anther and/or pollen development is disrupted in a class of mutants termed CMS (for cytoplasmic male sterility), which is associated with mutations in the mitochondrial genome. On the basis of the manifestation of a number of morphological and biochemical markers of apoptosis, we have shown that the PET1-CMS cytoplasm in sunflower causes premature PCD of the tapetal cells, which then extends to other anther tissues. These features included cell condensation, oligonucleosomal cleavage of nuclear DNA, separation of chromatin into delineated masses, and initial persistence of mitochondria. In addition, immunocytochemical analysis revealed that cytochrome c was released partially from the mitochondria into the cytosol of tapetal cells before the gross morphological changes associated with PCD. The decrease in cytochrome c content in mitochondria isolated from male sterile florets preceded a decrease in the integrity of the outer mitochondrial membrane and respiratory control ratio. Our data suggest that plant mitochondria, like mammalian mitochondria, play a key role in the induction of PCD. The tissue-specific nature of the CMS phenotype is discussed with regard to cellular respiratory demand and PCD during normal anther development.
This article has been cited by other articles:

|
 |

|
 |
 
Y. Zhu, T. Saraike, Y. Yamamoto, H. Hagita, S. Takumi, and K. Murai
orf260cra, a Novel Mitochondrial Gene, is Associated with the Homeotic Transformation of Stamens into Pistil-Like Structures (Pistillody) in Alloplasmic Wheat
Plant Cell Physiol.,
November 1, 2008;
49(11):
1723 - 1733.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Yang, T. Terachi, and H. Yamagishi
Inhibition of chalcone synthase Expression in Anthers of Raphanus sativus with Ogura Male Sterile Cytoplasm
Ann. Bot.,
October 1, 2008;
102(4):
483 - 489.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Fujii and K. Toriyama
Genome Barriers between Nuclei and Mitochondria Exemplified by Cytoplasmic Male Sterility
Plant Cell Physiol.,
October 1, 2008;
49(10):
1484 - 1494.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
U. Mabalirajan, A. K. Dinda, S. Kumar, R. Roshan, P. Gupta, S. K. Sharma, and B. Ghosh
Mitochondrial Structural Changes and Dysfunction Are Associated with Experimental Allergic Asthma
J. Immunol.,
September 1, 2008;
181(5):
3540 - 3548.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. K. Azad, T. Ishikawa, T. Ishikawa, Y. Sawa, and H. Shibata
Intracellular energy depletion triggers programmed cell death during petal senescence in tulip
J. Exp. Bot.,
May 31, 2008;
(2008)
ern066v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Xu, Y. Yang, Z. Zhang, W. Chen, C. Zhang, L. Zhang, S. Zou, and Z. Ma
Expression of the nuclear gene TaFAd is under mitochondrial retrograde regulation in anthers of male sterile wheat plants with timopheevii cytoplasm
J. Exp. Bot.,
April 4, 2008;
(2008)
ern068v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Gonzalez-Melendi, M. Uyttewaal, C. N. Morcillo, J. R. Hernandez Mora, S. Fajardo, F. Budar, and M. M. Lucas
A light and electron microscopy analysis of the events leading to male sterility in Ogu-INRA CMS of rapeseed (Brassica napus)
J. Exp. Bot.,
March 1, 2008;
59(4):
827 - 838.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. R. Phillips, A. Suttangkakul, and R. D. Vierstra
The ATG12-Conjugating Enzyme ATG10 Is Essential for Autophagic Vesicle Formation in Arabidopsis thaliana
Genetics,
March 1, 2008;
178(3):
1339 - 1353.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. J. Reape, E. M. Molony, and P. F. McCabe
Programmed cell death in plants: distinguishing between different modes
J. Exp. Bot.,
February 5, 2008;
(2008)
erm258v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. A. Eckardt
Programmed Cell Death in Plants: A Role for Mitochondrial-Associated Hexokinases
PLANT CELL,
September 1, 2006;
18(9):
2097 - 2099.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Vizcay-Barrena and Z. A. Wilson
Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant.
J. Exp. Bot.,
August 1, 2006;
57(11):
2709 - 2717.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Kawanabe, T. Ariizumi, M. Kawai-Yamada, H. Uchimiya, and K. Toriyama
Abolition of the Tapetum Suicide Program Ruins Microsporogenesis
Plant Cell Physiol.,
June 1, 2006;
47(6):
784 - 787.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. A. Vacca, D. Valenti, A. Bobba, R. S. Merafina, S. Passarella, and E. Marra
Cytochrome c Is Released in a Reactive Oxygen Species-Dependent Manner and Is Degraded via Caspase-Like Proteases in Tobacco Bright-Yellow 2 Cells en Route to Heat Shock-Induced Cell Death
Plant Physiology,
May 1, 2006;
141(1):
208 - 219.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. J. ROGERS
Programmed Cell Death in Floral Organs: How and Why do Flowers Die?
Ann. Bot.,
March 1, 2006;
97(3):
309 - 315.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. L. Taylor, J. L. Heazlewood, D. A. Day, and A. H. Millar
Differential Impact of Environmental Stresses on the Pea Mitochondrial Proteome
Mol. Cell. Proteomics,
August 1, 2005;
4(8):
1122 - 1133.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Casolo, E. Petrussa, J. Krajnakova, F. Macri, and A. Vianello
Involvement of the mitochondrial KATP+ channel in H2O2- or NO-induced programmed death of soybean suspension cell cultures
J. Exp. Bot.,
March 1, 2005;
56(413):
997 - 1006.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. C. Pagnussat, H.-J. Yu, Q. A. Ngo, S. Rajani, S. Mayalagu, C. S. Johnson, A. Capron, L.-F. Xie, D. Ye, and V. Sundaresan
Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis
Development,
February 1, 2005;
132(3):
603 - 614.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. W. Yang, S. K. Kim, and W. T. Kim
Perturbation of NgTRF1 Expression Induces Apoptosis-Like Cell Death in Tobacco BY-2 Cells and Implicates NgTRF1 in the Control of Telomere Length and Stability
PLANT CELL,
December 1, 2004;
16(12):
3370 - 3385.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. R. Hanson and S. Bentolila
Interactions of Mitochondrial and Nuclear Genes That Affect Male Gametophyte Development
PLANT CELL,
June 1, 2004;
16(suppl_1):
S154 - S169.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. V. Chichkova, S. H. Kim, E. S. Titova, M. Kalkum, V. S. Morozov, Y. P. Rubtsov, N. O. Kalinina, M. E. Taliansky, and A. B. Vartapetian
A Plant Caspase-Like Protease Activated during the Hypersensitive Response
PLANT CELL,
January 1, 2004;
16(1):
157 - 171.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. L. Heazlewood, J. S. Tonti-Filippini, A. M. Gout, D. A. Day, J. Whelan, and A. H. Millar
Experimental Analysis of the Arabidopsis Mitochondrial Proteome Highlights Signaling and Regulatory Components, Provides Assessment of Targeting Prediction Programs, and Indicates Plant-Specific Mitochondrial Proteins
PLANT CELL,
January 1, 2004;
16(1):
241 - 256.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Giege, J. L. Heazlewood, U. Roessner-Tunali, A. H. Millar, A. R. Fernie, C. J. Leaver, and L. J. Sweetlove
Enzymes of Glycolysis Are Functionally Associated with the Mitochondrion in Arabidopsis Cells
PLANT CELL,
September 1, 2003;
15(9):
2140 - 2151.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Zheng, Q. Xia, M. Dauk, W. Shen, G. Selvaraj, and J. Zou
Arabidopsis AtGPAT1, a Member of the Membrane-Bound Glycerol-3-Phosphate Acyltransferase Gene Family, Is Essential for Tapetum Differentiation and Male Fertility
PLANT CELL,
August 1, 2003;
15(8):
1872 - 1887.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X. Yang, C. A. Makaroff, and H. Ma
The Arabidopsis MALE MEIOCYTE DEATH1 Gene Encodes a PHD-Finger Protein That Is Required for Male Meiosis
PLANT CELL,
June 1, 2003;
15(6):
1281 - 1295.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
H. Thomas, H. J. Ougham, C. Wagstaff, and A. D. Stead
Defining senescence and death
J. Exp. Bot.,
April 1, 2003;
54(385):
1127 - 1132.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. Frank and C. M. Barr
Programmed Cell Death and Hybrid Incompatibility
J. Hered.,
March 1, 2003;
94(2):
181 - 183.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Liu and P. S. Schnable
Functional Specialization of Maize Mitochondrial Aldehyde Dehydrogenases
Plant Physiology,
December 1, 2002;
130(4):
1657 - 1674.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. VIROLAINEN, O. BLOKHINA, and K. FAGERSTEDT
Ca2+-induced High Amplitude Swelling and Cytochrome c Release From Wheat (Triticum aestivum L.) Mitochondria Under Anoxic Stress
Ann. Bot.,
October 1, 2002;
90(4):
509 - 516.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Christensen, S. W. Gorsich, R. H. Brown, L. G. Jones, J. Brown, J. M. Shaw, and G. N. Drews
Mitochondrial GFA2 Is Required for Synergid Cell Death in Arabidopsis
PLANT CELL,
September 1, 2002;
14(9):
2215 - 2232.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Robson and G. C. Vanlerberghe
Transgenic Plant Cells Lacking Mitochondrial Alternative Oxidase Have Increased Susceptibility to Mitochondria-Dependent and -Independent Pathways of Programmed Cell Death
Plant Physiology,
August 1, 2002;
129(4):
1908 - 1920.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. C. Vanlerberghe, C. A. Robson, and J. Y.H. Yip
Induction of Mitochondrial Alternative Oxidase in Response to a Cell Signal Pathway Down-Regulating the Cytochrome Pathway Prevents Programmed Cell Death
Plant Physiology,
August 1, 2002;
129(4):
1829 - 1842.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Arpagaus, A. Rawyler, and R. Braendle
Occurrence and Characteristics of the Mitochondrial Permeability Transition in Plants
J. Biol. Chem.,
January 11, 2002;
277(3):
1780 - 1787.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|