Journal of Experimental Botany, Vol. 54, No. 384, pp. 1115-1116,
March 1, 2003
© 2003 Oxford University Press
Isolation of two plastid division ftsZ genes from Chlamydomonas reinhardtii and its evolutionary implication for the role of FtsZ in plastid division
Received 6 September 2002; Accepted 16 December 2002
1 College of Life Sciences, Beijing Normal University, Beijing 100875, China
2 Department of Biology, Capital Normal University, Beijing 100037, China
3 Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
4 Co-first authors.
5 To whom correspondence should be addressed: (until September 2003) DCMB, Department of Biology, LSRC Building, Research Drive. Box 91000, Duke University, Durham, NC 27708-1000, USA. E-mail: yhe{at}duke.edu; (after September 2003) Department of Biology, Capital Normal University, Beijing 100037, China. E-mail: yhe{at}email.cnu.edu.cn
Abbreviations: fts, filament temperature sensitive; RT-PCR, reverse transcription PCR.
 |
Abstract |
|---|
 Top Abstract IntroductionReferences |
|---|
In order to elucidate the origin of the plastid division gene ftsZ in green plant lineage, and to understand the significance of this divergence for the function of FtsZ proteins in plants, two full-length cDNAs (accession numbers AF449446 and AB084236) were isolated from Chlamydomonas reinhardtii, a base species of green plant lineage. A phylogenetic analysis based on amino acid sequences of eukaryotic FtsZs reveals that an ancient duplication of the ftsZ gene occurred after the endosymbiotic event. The ancient duplication implies that two ftsZ families might play an indispensable role at the early endosymbiotic stage.
Key words: Ancient gene duplication, Chlamydomonas reinhardtii, ftsZ, plastid division.
|
Introduction |
|---|
|
TopAbstractIntroductionReferences |
|---|
As a primitive cytoskeleton protein existing in nearly all prokaryotes, FtsZ had also been found in eukaryotic lineage. In addition to a few FtsZ proteins related to mitochondria division in non-green algae, all FtsZ proteins in green plants are plastid related (Osteryoung and McAndrew, 2001; Reski, 2002). By contrast, although only one ftsZ gene existed in almost all eubacteria, several FtsZ proteins encoded by two small gene families had been identified in plants (Osteryoung et al., 1998). A model has been proposed to illustrate the functional relationship between the two FtsZ protein groups, with the two ftsZ families being thought to have different functions in plastid division (Osteryoung et al., 1998; Osteryoung, 2000; Osteryoung and McAndrew, 2001), recent researches indicate that this model is incomplete, and whether there is a distinct functional difference between two FtsZ groups is a matter of debate (Fujiwara and Yoshida, 2001; McAndrew et al., 2001; Miyagishima et al., 2001; Kuroiwa et al., 2002; Wang et al., 2002).
To gain a new insight into the role of FtsZ proteins in plastid division in green plants’ lineage, the isolation of two ftsZ genes from Chlamydomonas reinhardtii and the phylogenetic analysis of eukaryotic FtsZ proteins is reported in this study. An evolutionary view has been proposed to understand the role of two FtsZ groups in plastid division.
A 572 bp fragment obtained from C. reinhadtii total RNA by degenerated primers RT-PCR (forward 5'-CTTGAATTCAA(T/C)GCNGTNAA(T/C)CGNATG-3'; reverse 5'-CTTGAATTCAC (A/G)TC(A/T/G) GC(A/G)AA(A/G)TCNAC(A/G)TT-3') was used as a probe to search ChlamyDB (http://www.biology.duke.edu/chlamy_genome/blast). Several EST clones in the database have been identified. Two full-length cDNAs have been assembled from these EST clones. To verify the results of assembly, two pairs of gene-specific primers were designed according to the assembled sequences and the end-to-end PCR reactions were performed (primers for CrFtsZ2: forward 5'-ACACC TACGATGGCCACTT TGT-3', reverse 5'-CACACAAGGCCACACTTG-3'; for CrFtsZ3: forward 5'-AAGCTCTGAGCGCCACTGAGTCTAC-3', reverse 5'-CACGTGTCCAATCCTTCCCACA-3'). These verified and sequenced cDNAs were designated as CrFtsZ2 and CrFtsZ3, and deposited into public database under the accession numbers AF449446 and AB084236, respectively. The deduced amino acid sequences of CrFtsZ2 and CrFtsZ3 exhibit high sequence similarity with those of known FtsZ proteins. They contain the typical motifs that exist in all FtsZ proteins. Furthermore, a common GTP binding motif (GGGTGT/SG) found both in FtsZ and tubulin also existed in the second motif (data not shown). Therefore, the two CrFtsZ proteins are used in phylogenetic analysis with other eukaryotic and prokaryotic FtsZ proteins.
Consistent with previous studies (Osteryoung et al., 1998; Gilson and Beech, 2001), the plant FtsZ proteins form two distinct and separate groups. When CrFtsZ2 and CrFtsZ3 were included in this analysis, they fell respectively into the FtsZ1 and FtsZ2 clusters and so cannot unite the two plant FtsZ groups into a monophyletic clade (Fig. 1). Thus, it is obvious that the formation of two ftsZ gene families is prior to the divergence of green algae from the green plants lineage. Furthermore, when the FtsZ sequences from red and brown algae were used in this analysis, the topology of the phylogenetic tree changed little, suggesting that the origin of two plant ftsZ families probably results from an ancient duplication just after the first endosymbiotic event or even that the duplication occurred in the first endosymbiotic cyanobacterium as suggested by Gilson and Beech (2001).
|
What can be learnt from this ancient origin of ftsZ genes? Although the existence of two distinct ftsZ families in higher plants strongly suggests the possible functional difference between different proteins in plastid division (Osteryoung et al., 1998; Osteryoung, 2000; Stokes et al., 2000), recent studies cannot draw that conclusion (McAndrew et al., 2001; Kuroiwa et al., 2002; Wang et al., 2002; D Kong and Y He, unpublished data). In fact, all the available experimental evidence supports the view that the members from the two different ftsZ families are involved in plastid division. Therefore, given the important role that both types of FtsZ proteins played in plastid division and the early origin of these two gene families revealed in this study, the ancient duplication of the ftsZ gene might play an indispensable role in the establishment of a stable endosymbiotic relationship between the eukaryotic host cell and its endosymbiont at the early evolutionary stage.
|
Acknowledgements |
|---|
This work was partly supported by the Chinese National Natural Science Foundation Grant No. 39970356, Beijing Natural Science Foundation Grant No. 5992003 to YH and the Chinese Postdoctoral Science Foundation to DW.
|
References |
|---|
|
TopAbstractIntroductionReferences |
|---|
Fujiwara M, Yoshida S. 2001. Chloroplast targeting of chloroplast division FtsZ2 proteins in Arabidopsis. Biochemical and Biophysical Research Communications 287, 462–467.[CrossRef][Web of Science][Medline]
Gilson PR, Beech PL. 2001. Cell division protein FtsZ: running rings around bacteria, chloroplasts and mitochondria. Research in Microbiology 152, 3–10.[Medline]
Kuroiwa H, Mori T, Takahara M, Miyagishima S, Kuroiwa T. 2002. Chloroplast division machinery as revealed by immunofluorescence and electron microscopy. Planta 215, 185–190.[CrossRef][Web of Science][Medline]
McAndrew RS, Froehlich JE, Vitha S, Stokes KD, Osteryoung KW. 2001.Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZ1 and FtsZ2 in higher plants. Plant Physiology 127, 1656–1666.
Miyagishima S, Takahara M, Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T. 2001. Plastid division is driven by a complex mechanism that involves differential transition of the bacterial and eukaryotic division rings. The Plant Cell 13, 2257–2268.
Osteryoung KW. 2000. Organelle fission: crossing the evolutionary divide. Plant Physiology 123, 1213–1216.
Osteryoung KW, McAndrew RS. 2001. The plastid division machine. Annual Review of Plant Physiology and Plant Molecular Biology 52, 315–333.[CrossRef][Web of Science][Medline]
Osteryoung KW, Stokes KD, Rutherford SM, Percival AL, Lee WY. 1998. Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacteria ftsZ. The Plant Cell 10, 1991–2004.
Reski R. 2002. Rings and networks: the amazing complexity of FtsZ in chloroplasts. Trends in plant science 7, 103–105.[CrossRef][Web of Science][Medline]
Stokes KD, McAndrew RS, Figueroa R, Vitha S, Osteryoung KW. 2000. Chloroplast division and morphology are differentially affected by overexpression of FtsZ1 and FtsZ2 genes in Arabidopsis. Plant Physiology 124, 1668–1677.
Saitou N, Nei M. 1987. The Neighbor–Joining methods: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 306–425.
Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
van de Peer Y, de Wachter R. 1993. TREECON: A software package for the construction and drawing of evolutionary trees. Computer Applications in Biosciences 9, 177–182.
Wang D, Kong DD, Ju CL, Hu Y, He YK, Sun JS. 2002. Effects of tobacco plastid division genes NtFtsZ1-1 and NtFtsZ1-2 on the division and morphology of chloroplasts. Acta Botanica Sinica 44, 838–844.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  M. Vitova, J. Hendrychova, M. Cizkova, V. Cepak, J. G. Umen, V. Zachleder, and K. Bisova Accumulation, Activity and Localization of Cell Cycle Regulatory Proteins and the Chloroplast Division Protein FtsZ in the Alga Scenedesmus quadricauda under Inhibition of Nuclear DNA Replication Plant Cell Physiol., December 1, 2008; 49(12): 1805 - 1817. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. W. Yoder, D. Kadirjan-Kalbach, B. J. S. C. Olson, S.-y. Miyagishima, S. L. DeBlasio, R. P. Hangarter, and K. W. Osteryoung Effects of Mutations in Arabidopsis FtsZ1 on Plastid Division, FtsZ Ring Formation and Positioning, and FtsZ Filament Morphology in Vivo Plant Cell Physiol., June 1, 2007; 48(6): 775 - 791. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Lohse, B. Hause, G. Hause, and T. Fester FtsZ Characterization and Immunolocalization in the Two Phases of Plastid Reorganization in Arbuscular Mycorrhizal Roots of Medicago truncatula Plant Cell Physiol., August 1, 2006; 47(8): 1124 - 1134. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Vitha, J. E. Froehlich, O. Koksharova, K. A. Pyke, H. van Erp, and K. W. Osteryoung ARC6 Is a J-Domain Plastid Division Protein and an Evolutionary Descendant of the Cyanobacterial Cell Division Protein Ftn2 PLANT CELL, August 1, 2003; 15(8): 1918 - 1933. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||