Visualization of a Cytoskeleton-like Ftsz Network in Chloroplasts

It has been a long-standing dogma in life sciences that only eukaryotic organisms possess a cytoskeleton. Recently, this belief was questioned by the finding that the bacterial cell division protein FtsZ resembles tubulin in sequence and structure and, thus, may be the progenitor of this major eukaryotic cytoskeletal element. Here, we report two nuclear-encoded plant ftsZ genes which are highly conserved in coding sequence and intron structure. Both their encoded proteins are imported into plastids and there, like in bacteria, they act on the division process in a dose-dependent manner. Whereas in bacteria FtsZ only transiently polymerizes to a ring-like structure, in chloroplasts we identified persistent, highly organized filamentous scaffolds that are most likely involved in the maintenance of plastid integrity and in plastid division. As these networks resemble the eukaryotic cytoskeleton in form and function, we suggest the term “plastoskeleton” for this newly described subcellular structure.

[1]  W. Wooster,et al.  Crystal structure of , 2005 .

[2]  K. Pyke,et al.  A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus , 2000, Current Biology.

[3]  H. Erickson Dynamin and Ftsz , 2000, The Journal of cell biology.

[4]  G. McFadden,et al.  Mitochondrial FtsZ in a chromophyte alga. , 2000, Science.

[5]  W. Margolin,et al.  Genetic and Functional Analyses of the Conserved C-Terminal Core Domain of Escherichia coli FtsZ , 1999, Journal of bacteriology.

[6]  J. Löwe,et al.  Crystal structure of the N-terminal domain of MukB: a protein involved in chromosome partitioning. , 1999, Structure.

[7]  L. Amos,et al.  Tubulin‐like protofilaments in Ca2+‐induced FtsZ sheets , 1999, The EMBO journal.

[8]  K. Harter,et al.  Nuclear Import of the Parsley bZIP Transcription Factor CPRF2 Is Regulated by Phytochrome Photoreceptors , 1999, The Journal of cell biology.

[9]  K. Osteryoung,et al.  Chloroplast Division in Higher Plants Requires Members of Two Functionally Divergent Gene Families with Homology to Bacterial ftsZ , 1998, Plant Cell.

[10]  K. Pyke,et al.  Plastid division: evidence for a prokaryotically derived mechanism. , 1998, Current opinion in plant biology.

[11]  R. Herrmann,et al.  Gene transfer from organelles to the nucleus: how much, what happens, and Why? , 1998, Plant physiology.

[12]  J. Lutkenhaus Organelle division: From coli to chloroplasts , 1998, Current Biology.

[13]  W. Doolittle,et al.  Cytoskeletal proteins: The evolution of cell division , 1998, Current Biology.

[14]  Tibor Vellai,et al.  A New Aspect to the Origin and Evolution of Eukaryotes , 1998, Journal of Molecular Evolution.

[15]  R. Reski,et al.  Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[16]  R. Reski,et al.  Moss (Physcomitrella patens) Expressed Sequence Tags Include Several Sequences which are Novel for Plants , 1998 .

[17]  L. Amos,et al.  Crystal structure of the bacterial cell-division protein FtsZ , 1998, Nature.

[18]  H. Erickson,et al.  FtsZ, a tubulin homologue in prokaryote cell division. , 1997, Trends in cell biology.

[19]  D. Ehrhardt,et al.  Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[20]  E. Vierling,et al.  Conserved cell and organelle division , 1995, Nature.

[21]  R. J. Thomas,et al.  Pasture soils as carbon sink , 1995, Nature.

[22]  H. Erickson,et al.  FtsZ, a prokaryotic homolog of tubulin? , 1995, Cell.

[23]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[24]  J. Lutkenhaus,et al.  Guanine nucleotide-dependent assembly of FtsZ into filaments , 1994, Journal of bacteriology.

[25]  J. Lutkenhaus FtsZ ring in bacterial cytokinesis , 1993, Molecular microbiology.

[26]  Yves Van de Peer,et al.  TREECON: a software package for the construction and drawing of evolutionary trees , 1993, Comput. Appl. Biosci..

[27]  D. Raychaudhuri,et al.  Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein , 1992, Nature.

[28]  L. Rothfield,et al.  The essential bacterial cell-division protein FtsZ is a GTPase , 1992, Nature.

[29]  P Bork,et al.  An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[30]  E. Bi,et al.  FtsZ ring structure associated with division in Escherichia coli , 1991, Nature.

[31]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[32]  J. Lutkenhaus,et al.  Overproduction of FtsZ induces minicell formation in E. coli , 1985, Cell.

[33]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[34]  B. Lang,et al.  Mitochondrial evolution. , 1999, Science.

[35]  D. Bramhill,et al.  Bacterial cell division. , 1997, Annual review of cell and developmental biology.

[36]  J. Lutkenhaus,et al.  Bacterial cell division and the Z ring. , 1997, Annual review of biochemistry.

[37]  R. Reski,et al.  Fate of a Mutant Macrochloroplast in Somatic Hybrids , 1994 .

[38]  M W Gray,et al.  The endosymbiont hypothesis revisited. , 1992, International review of cytology.

[39]  N. Saito The neighbor-joining method : A new method for reconstructing phylogenetic trees , 1987 .

[40]  J. Possingham,et al.  Observations of microtubule-like structures within spinach plastids , 1984 .