Two Types of FtsZ Proteins in Mitochondria and Red-Lineage Chloroplasts: The Duplication of FtsZ Is Implicated in Endosymbiosis

Abstract

The ancestors of plastids and mitochondria were once free-living bacteria that became organelles as a result of endosymbiosis. According to this theory, a key bacterial division protein, FtsZ, plays a role in plastid division in algae and plants as well as in mitochondrial division in lower eukaryotes. Recent studies have shown that organelle division is a process that combines features derived from the bacterial division system with features contributed by host eukaryotic cells. Two nonredundant versions of FtsZ, FtsZ1 and FtsZ2, have been identified in green-lineage plastids, whereas most bacteria have a single ftsZ gene. To examine whether there is also more than one type of FtsZ in red-lineage chloroplasts (red algal chloroplasts and chloroplasts that originated from the secondary endosymbiosis of red algae) and in mitochondria, we obtained FtsZ sequences from the complete sequence of the primitive red alga Cyanidioschyzon merolae and the draft sequence of the stramenopile (heterokont) Thalassiosira pseudonana. Phylogenetic analyses that included known FtsZ proteins identified two types of chloroplast FtsZ in red algae (FtsZA and FtsZB) and stramenopiles (FtsZA and FtsZC). These analyses also showed that FtsZB emerged after the red and green lineages diverged, while FtsZC arose by the duplication of an ftsZA gene that in turn descended from a red alga engulfed by the ancestor of stramenopiles. A comparison of the predicted proteins showed that like bacterial FtsZ and green-lineage FtsZ2, FtsZA has a short conserved C-termmal sequence (the C-terminal core domain), whereas FtsZB and FtsZC, like the green-lineage FtsZ1, lack this sequence. In addition, the Cyanidioschyzon and Dictyostelium genomes encode two types of mitochondrial FtsZ proteins, one of which lacks the C-terminal variable domain. These results suggest that the acquisition of an additional FtsZ protein with a modified C terminus was common to the primary and secondary endosymbioses that produced plastids and that this also occurred during the establishment of mitochondria, presumably to regulate the multiplication of these organelles.

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Acknowledgements

We are deeply indebted to Dr. E. Virginia Armbrust, School of Oceanography, University of Washington, and the U.S. Department of Energy Joint Genome Institute for permission to use the Thalassiosira sequences before publication. This work was supported by a research fellowship from the Japanese Society for the Promotion of Science for Young Scientists (No. 7498 to S.M.) and by grants from the Ministry of Education, Culture, Sports, Science, and Technology, Japan (Nos. 12446222 and 12874111 to T.K.) and from the Program for the Promotion of Basic Research Activities for Innovative Biosciences (to T.K.).

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Correspondence to Shin-ya Miyagishima.

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Miyagishima, S., Nozaki, H., Nishida, K. et al. Two Types of FtsZ Proteins in Mitochondria and Red-Lineage Chloroplasts: The Duplication of FtsZ Is Implicated in Endosymbiosis . J Mol Evol 58, 291–303 (2004). https://doi.org/10.1007/s00239-003-2551-1

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Keywords

  • Chloroplast division
  • Endosymbiosis
  • FtsZ
  • Mitochondrial division
  • Red algae
  • Stramenopiles (Heterokonts)