Trends in Plant Science
Volume 8, Issue 9, September 2003, Pages 432-438
Journal home page for Trends in Plant Science

An evolutionary puzzle: chloroplast and mitochondrial division rings

https://doi.org/10.1016/S1360-1385(03)00193-6Get rights and content

Abstract

Consistent with their bacterial origin, chloroplasts and primitive mitochondria retain a FtsZ ring for division. However, chloroplasts and mitochondria have lost most of the proteins required for bacterial division other than FtsZ and certain homologues of the Min proteins, but they do contain plastid and mitochondrion dividing rings, which were recently shown to be distinct from the FtsZ ring. Moreover, recent studies have revealed that rings of the eukaryote-specific dynamin-related family of GTPases regulate the division of chloroplasts and mitochondria, and these proteins emerged early in eukaryotic evolution. These findings suggest that the division of chloroplasts and primitive mitochondria involve very similar systems, consisting of an amalgamation of rings from bacteria and eukaryotes.

Section snippets

The FtsZ ring descended from ancestral bacteria

The first protein that was shown to play a role in organelle division was a plant homolog of the key bacterial division protein FtsZ, which is involved in the division of chloroplasts 5, 6. Filamentous temperature-sensitive (fts) genes were identified from Escherichia coli mutants collected in the late 1960 s. The fts mutants have a defect in cytokinesis and, as a result, elongate to form filaments [10]. FtsZ is a GTPase that is structurally similar to tubulin and self-assembles into a ring

Assembling the four pieces of the evolutionary puzzle

Insights into the origin of and relationships between the ring structures given by recent studies enable us to arrange the four pieces of the evolutionary puzzle (Fig. 4). The most striking suggestion is that a very similar event occurred in both chloroplasts and mitochondria during their establishment. Although the structural and behavioral similarity of the PD and MD rings is one element of this proposal, the identification of the respective components will provide more exact information. One

Acknowledgements

Our apologies to those whose work could not be cited because of space constraints. Our work was supported by the JSPS Research Fellowship for Young Scientists (no. 7498 to SM) and by grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan (nos 12446222 and 12874111 to TK) and from the Program for the Promotion of Basic Research Activities for Innovative Biosciences (to TK).

References (75)

  • A.M. van der Bliek

    Functional diversity in the dynamin family

    Trends Cell Biol.

    (1999)
  • A.M. Labrousse

    C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane

    Mol. Cell

    (1999)
  • W. Margolin

    Organelle division: self-assembling GTPase caught in the middle

    Curr. Biol.

    (2000)
  • A. Koch

    Dynamin-like protein 1 is involved in peroxisomal fission

    J. Biol. Chem.

    (2003)
  • G.I. McFadden

    Primary and secondary endosymbiosis and the origin of plastids

    J. Phycol.

    (2001)
  • K.W. Osteryoung et al.

    The plastid division machine

    Annu. Rev. Plant Physiol. Plant Mol. Biol.

    (2001)
  • P.L. Beech

    Mitochondrial FtsZ in a chromophyte alga

    Science

    (2000)
  • S. Miyagishima

    A plant-specific dynamin-related protein forms a ring at the chloroplast division site

    Plant Cell

    (2003)
  • H. Gao

    ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery

    Proc. Natl. Acad. Sci. U. S. A.

    (2003)
  • J. Errington

    Cytokinesis in bacteria

    Microbiol. Mol. Biol. Rev.

    (2003)
  • K.W. Osteryoung et al.

    Conserved cell and organelle division

    Nature

    (1995)
  • R. Strepp

    Plant molecular gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin

    Proc. Natl. Acad. Sci. U. S. A.

    (1998)
  • K.W. Osteryoung

    Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ

    Plant Cell

    (1998)
  • S. Vitha

    FtsZ ring formation at the chloroplast division site in plants

    J. Cell Biol.

    (2001)
  • T. Mori

    Visualization of an FtsZ ring in chloroplasts of Lilium longiflorum leaves

    Plant Cell Physiol.

    (2001)
  • R.S. McAndrew

    Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZ1 and FtsZ2 in higher plants

    Plant Physiol.

    (2001)
  • D. Wang

    Isolation of two plastid division ftsZ genes from Chlamydomonas reinhardtii and its evolutionary implication for the role of FtsZ in plastid division

    J. Exp. Bot.

    (2003)
  • X. Ma et al.

    Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ

    J. Bacteriol.

    (1999)
  • M. Takahara

    A putative mitochondrial ftsZ gene is encoded in the unicellular primitive red alga Cyanidioschyzon merolae

    Mol. Gen. Genet.

    (2000)
  • M. Takahara

    Localization of the mitochondrial FtsZ protein in a dividing mitochondrion

    Cytologia

    (2001)
  • K. Nishida

    Dynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga

    Proc. Natl. Acad. Sci. U. S. A.

    (2003)
  • T. Wakasugi

    Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division

    Proc. Natl. Acad. Sci. U. S. A.

    (1997)
  • K. Kanamaru

    Chloroplast targeting, distribution and transcriptional fluctuation of AtMinD1, a Eubacteria-type factor critical for chloroplast division

    Plant Cell Physiol.

    (2000)
  • R. Itoh

    A chloroplast protein homologous to the eubacterial topological specificity factor minE plays a role in chloroplast division

    Plant Physiol.

    (2001)
  • M.S. Reddy

    Overexpression of the Arabidopsis thaliana MinE1 bacterial division inhibitor homologue gene alters chloroplast size and morphology in transgenic Arabidopsis and tobacco plants

    Planta

    (2002)
  • J. Maple

    The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis

    Plant J.

    (2002)
  • T. Mita

    A ring structure around the dividing plane of the Cyanidium caldarium chloroplast

    Protoplasma

    (1986)
  • Cited by (58)

    • Chloroplasts around the plant cell cycle

      2016, Current Opinion in Plant Biology
    • The Bacterial ZapA-like Protein ZED Is Required for Mitochondrial Division

      2009, Current Biology
      Citation Excerpt :

      These comprise a chimera of inner rings of proteins, such as FtsZ from bacteria (localized in the matrix or stroma); outer rings of proteins, such as the MD/PD ring, which is detected as an electron-dense specialized structure; and dynamin-related protein from eukaryotes (in the cytoplasm) [6–10]. The presence and function of these proteins in the oligomeric complex comprising the outer rings are thought to be universal [7–11]. In the MD and PD machineries, the inner rings are formed before the outer rings [12, 13]; therefore, the inner rings are important for initiation of endosymbiotic organelle division.

    • Chapter 3 Vesicle, Mitochondrial, and Plastid Division Machineries with Emphasis on Dynamin and Electron-Dense Rings

      2008, International Review of Cell and Molecular Biology
      Citation Excerpt :

      2) The dynamin rings in MDF and PDF machineries in C. merolae were ∼20 or 100 times larger in diameter and more than 1000 times greater in volume than that of VD machinery (Miyagishima and Kuroiwa, 2006; Miyagishima et al., 2003b; Nishida et al., 2003). However, even when the dynamin rings were observed clearly by immunoelectron and immunofluorescence microscopy, they were never observed directly using electron microscopy (Miyagishima et al., 2003b; Nishida et al., 2003). ( 3) Although fine filamentous linear structures and rings of FtsZ proteins were constructed in in vitro experiments (Erickson et al., 1996), they have never been seen as electron‐dense filaments in vivo in prokaryotes (Bi and Lutkenhaus, 1991), C. merolae (Takahara et al., 2000) or P. zonale (Kuroiwa et al., 2002).

    View all citing articles on Scopus
    View full text