Plastid division

AoB PLANTS http://aobplants.oxfordjournals.org/ Open access – Invited mini-review Plastid division Kevin Andrew Pyke* Received: 7 July 2010; Returned for revision: 19 August 2010; Accepted: 28 September 2010; Published: 5 October 2010 Citation details: Pyke KA. 2010. Plastid division. AoB PLANTS 2010: plq016, doi:10.1093/aobpla/plq016 Abstract Background and aims Plastids undergo a process of binary fission in order to replicate. Plastid replication is required at two distinct stages of plant growth: during cell division to ensure correct plastid segregation, and during cell expansion and development to generate large populations of functional plastids, as in leaf mesophyll cells. This review considers some of the recent advances in the understanding of how plastids undergo binary fission, a process which uses several different proteins, both internal and external to the plastid, which have been derived from the original endosymbiont’s genome as well as new proteins that have been recruited from the host genome. Key points Several of the proteins currently used in this process in higher plants have homologues in modern-day bacteria. An alternative mode of replication by a budding-type mechanism also appears to be used in some circumstances. The review also highlights how most of our knowledge of plastid division is centred on the chloroplast developing in leaf mesophyll cells and a role for plastid division during the development of other plastid types is poorly understood. Whilst models for a protein-based mechanism have been devised, exactly how the division process is controlled at the plastid level and at the plastid population level is poorly understood. Introduction Plastids form a group of organelles found in the cells of higher and lower plants, which originally evolved from prokaryotic ancestors around 2 billion years ago, when an endosymbiotic event took place, namely the uptake of a free-living photosynthetic prokaryote into a eukaryotic protozoan (McFadden, 1999, 2001). Through the course of subsequent evolution, plastids have become a defining feature of plants and contribute a very significant number of properties to plant function (Pyke, 2009). Foremost among these is the process of photosynthesis, enabling plants to increase in biomass and synthesize complex organic molecules and polymers from simple building molecules of carbon dioxide and water. In order for a functional endosymbiotic relationship to evolve, as is seen today in extant green plants, the original prokaryote had to adapt to the internal cellular environment of the eukaryote. Since the eukaryotic cell will have undergone cell divisions, the endosymbiotic prokaryote will have been required to divide as well, in order to remain resident within the cell. The result of this requirement in modern-day plants is that plastids have the ability to divide inside their host plant cells, giving rise to, in cell types such as leaf mesophyll cells, large populations of plastids within individual cells (Pyke, 1997). Another plastid trait which has evolved as higher and lower plants became multicellular organisms with defined cell types, was for the Plant and Crop Sciences Division, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK * Corresponding author’s e-mail address: AoB PLANTS Vol. 2010, plq016, doi:10.1093/aobpla/plq016, available online at www.aobplants.oxfordjournals.org & The Authors 2010. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5/uk/) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited. AoB PLANTS Vol. 2010, plq016, doi:10.1093/aobpla/plq016 & The Authors 2010 1 Pyke — Plastid division 2 chloroplasts could be observed with central constrictions, which result eventually in the production of two equally sized daughter plastids. These daughter plastids then need to grow in size before division can occur again. Extensive analysis of constricted chloroplasts in the context of cell expansion and an increase in the number of plastids per cell showed how this dynamic division process, termed binary fission, leads to an increase in chloroplast number (Leech et al., 1981; Ellis and Leech, 1983; Pyke and Leech, 1992; Robertson et al., 1996; Pyke, 1997). Proplastids are thought to divide in the same basic way, although they are much more difficult to observe, residing in small meristematic cells. Electron micrographs, however, do show centrally constricted proplastids in these cells, which are considered to be undergoing plastid division (Chaley and Possingham, 1981; Robertson et al., 1995, 1996). Their morphology, however, is much more heterogeneous than that seen in chloroplast division, with the constriction often extending to produce a long thin isthmus, joining the two plastid bodies. The challenge of the last 20 years has been to elucidate the molecular machinery that drives this chloroplast division process, to understand how it works and how it is powered, and to work out how such a division apparatus is controlled in its activity, i.e. what tells chloroplasts to start to divide and what tells them to stop dividing. Much progress has been made in defining the molecules that participate in the division process in chloroplasts, primarily through the characterization of genes encoding proteins involved in the process, which are revealed as conveying mutant chloroplast phenotypes when mutants of Arabidopsis thaliana are systematically screened. The original mutant screen that produced arc mutants of A. thaliana (Pyke and Leech, 1992, 1994) and other screens since (Miyagishima et al. 2006) have been highly productive in revealing plastid division genes. An alternative approach has been to search for genes involved in prokaryotic cell division in genomes of higher plants (Osteryoung and Vierling, 1995; Colletti et al., 2000). Interestingly, these approaches have revealed that proteins involved in the constriction process have originated by two different routes. One group of proteins were originally involved in the division of the free-living prokaryote, which invaded the eukaryotic cell and are prokaryotic in nature, whereas another group have been recruited from the eukaryotic genome or have been hijacked from other genes during the course of evolution. Thus, what is known currently of the plastid division machinery reveals a complex mechanism with a variety of different functional proteins. AoB PLANTS Vol. 2010, plq016, doi:10.1093/aobpla/plq016 & The Authors 2010 plastid to become differentiated into different plastid types in different types of plant cell. This trait arose for the purpose of storing different types of molecules or for the benefit of performing different types of bio (...truncated)