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Plant Cell, Vol. 10, 1991-2004, December 1998, Copyright © 1998, American Society of Plant Physiologists
Chloroplast Division in Higher Plants Requires Members of Two Functionally Divergent Gene Families with Homology to Bacterial f tsZ
Katherine W. Osteryounga,
Kevin D. Stokesa,
Stephen M. Rutherforda,
Ann L. Percivala, and
Won Y. Leea
a Department of Biology/314, University of Nevada, Reno, Nevada 89557-0015
Correspondence to:
Katherine W. Osteryoung, oster_k{at}med.unr.edu (E-mail), 702-784-1650 (fax).
The division of plastids is critical for viability in photosynthetic eukaryotes, but the mechanisms associated with this process are still poorly understood. We previously identified a nuclear gene from Arabidopsis encoding a chloroplast-localized homolog of the bacterial cell division protein FtsZ, an essential cytoskeletal component of the prokaryotic cell division apparatus. Here, we report the identification of a second nuclear-encoded FtsZ-type protein from Arabidopsis that does not contain a chloroplast targeting sequence or other obvious sorting signals and is not imported into isolated chloroplasts, which strongly suggests that it is localized in the cytosol. We further demonstrate using antisense technology that inhibiting expression of either Arabidopsis FtsZ gene (AtFtsZ1-1 or AtFtsZ2-1) in transgenic plants reduces the number of chloroplasts in mature leaf cells from 100 to one, indicating that both genes are essential for division of higher plant chloroplasts but that each plays a distinct role in the process. Analysis of currently available plant FtsZ sequences further suggests that two functionally divergent FtsZ gene families encoding differentially localized products participate in chloroplast division. Our results provide evidence that both chloroplastic and cytosolic forms of FtsZ are involved in chloroplast division in higher plants and imply that important differences exist between chloroplasts and prokaryotes with regard to the roles played by FtsZ proteins in the division process.
Related articles in Plant Cell:
- Plastid Division: The Origin of Replication
- Kevin Pyke
Plant Cell 1998 10: 1971-1972.
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|
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|
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|
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|
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|
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|
 |
|

|
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|
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|
 |
|

|
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|
 |
 
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[Full Text]
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|
 |
|

|
 |

|
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[Abstract]
[Full Text]
|
 |
|

|
 |

|
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|
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13(3):
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[Abstract]
[Full Text]
|
 |
|

|
 |

|
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114(19):
3565 - 3574.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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J. Cell Biol.,
December 18, 2000;
151(7):
1423 - 1434.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Plant Physiology,
December 1, 2000;
124(4):
1668 - 1677.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
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J. Cell Biol.,
November 13, 2000;
151(4):
945 - 950.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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J. Cell Biol.,
November 13, 2000;
151(4):
F19 - F22.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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The Dynamin-related GTPase, Mgm1p, Is an Intermembrane Space Protein Required for Maintenance of Fusion Competent Mitochondria
J. Cell Biol.,
October 18, 2000;
151(2):
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[Abstract]
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|
 |
|

|
 |

|
 |
 
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J. Cell Biol.,
October 18, 2000;
151(2):
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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J. Cell Biol.,
October 18, 2000;
151(2):
367 - 380.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Plant Cell Physiol.,
October 1, 2000;
41(10):
1119 - 1128.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Organelle Fission. Crossing the Evolutionary Divide
Plant Physiology,
August 1, 2000;
123(4):
1213 - 1216.
[Full Text]
|
 |
|

|
 |

|
 |
 
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J. Cell Biol.,
March 20, 2000;
148(6):
1103 - 1106.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Mitochondrial FtsZ in a Chromophyte Alga
Science,
February 18, 2000;
287(5456):
1276 - 1279.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
R. Kohler, P Schwille, W. Webb, and M. Hanson
Active protein transport through plastid tubules: velocity quantified by fluorescence correlation spectroscopy
J. Cell Sci.,
January 11, 2000;
113(22):
3921 - 3930.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
K. A. Pyke
Plastid Division and Development
PLANT CELL,
April 1, 1999;
11(4):
549 - 556.
[Full Text]
|
 |
|

|
 |

|
 |
 
X. Yu, W Margolin, M. Gonzalez-Garay, and F Cabral
Vinblastine induces an interaction between FtsZ and tubulin in mammalian cells
J. Cell Sci.,
January 7, 1999;
112(14):
2301 - 2311.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Pyke
Plastid Division: The Origin of Replication
PLANT CELL,
December 1, 1998;
10(12):
1971 - 1972.
[Full Text]
|
 |
|
|
|