Plastid division

The fact that plastids can divide as distinct organelles within the cytoplasm of the eukaryotic plant cell was confirmed by several studies in the late 1960s in which populations of plastids were counted and changes in their population size were established in correlation with cell expansion in developing leaves (see Pyke 1997). These studies clearly showed that there were two different points in plastid development where division takes place. Firstly in dividing cells in the meristem, pro-plastids are required to divide in order to maintain their lineage in newly divided cells. Without such a division, proplastids would likely be lost and aplastidic cells would be generated. Secondly, during the expansion phase of leaves, mesophyll cells increase in volume and the young chloroplasts divide during this period in order to maintain a population in an ever-enlarging cell. The final outcome of this process is mature mesophyll cells containing large populations of individual chloroplasts. The actual number of chloroplasts present is mainly related to the size of the cell, a relationship that extends across different species. In mature leaves in most species, the mesophyll cells contain between 50 and 200 chloro-plasts. It is normally assumed that the basic mechanism by which plastids divide is the same for proplastids and for young chloroplasts although the control factors for these two processes are likely to differ. Cells in other green tissues in plants also accumulate chloroplasts in a similar manner although the end point of plastid population size and the size of individual plastids in different tissues and cell types varies greatly.

The plastid division process involves the constriction of the plastid centrally, which eventually leads to a pinching of the envelope membrane and fusion producing two separate daughter plastids, a process termed binary fission.

Progress in understanding the molecular basis of the plastid division machinery has been significant in the last 15 years due to approaches on two fronts. Firstly mutants of Arabidopsis were identified in which chloroplast numbers in leaf cells were altered significantly and secondly, genes involved in prokaryotic cell division were discovered in plant genomes and shown to function in plastid division (Pyke and Leech 1994; Pyke 1999). These two approaches have revealed many nuclear genes and their associated proteins and have enabled working models to be developed of how plastids divide (Aldridge et al. 2005). Central to the division process is the formation of a constriction ring composed primarily of FtsZ proteins that resides on the inside of the plastid envelope in the stroma (Osteryoung and Vierling 1995; Osteryoung et al. 1998; Vitha et al. 2001; McAndrew et al. 2001;

Kuroiwa et al. 2002). FtsZ proteins have characteristics of the cytoskeletal protein tubulin, and plant FtsZ proteins are homologues of those present in prokaryotic bacteria, which function in bacterial cell division. The FtsZ ring is stabilized by the protein ARC6, originally identified from an Arabidopsis mutant with few giant chloroplasts (Pyke et al. 1994; Vitha et al. 2003). FtsZ proteins assemble in the ring structure at the onset of plastid division and constriction of the ring and force generation appears to be controlled by the protein ARC5, which is a dynamin-like protein (Gao et al. 2003; Miyagishima et al. 2003) which functions on the outer surface of the plastid envelope. Evidence that ARC5 generates force and constricts the FtsZ ring complex comes from viewing isolated FtsZ rings and inducing constriction by adding ARC5 protein to them (Yoshida et al. 2006). Coordination of events on either side of the plastid envelope as the division process progresses appears to be controlled by PDV1 proteins, which form foci in the outer plastid envelope overlying the stromal FtsZ ring (Miyagishima et al. 2006). Undoubtedly, the complete plastid division machinery is a complex structure and probably contains other unknown proteins which function in a combinatorial fashion to facilitate the division process (Maple et al. 2005) especially since imaging of isolated plastid division rings containing FtsZ show distinct rings on the outer and inner surfaces of the plastid envelope (Kuroiwa et al. 2002; Miyagishima et al. 2001, 2003). Figure 3 shows a tentative model of how these proteins and the plastid division rings could be arranged. Plastid division normally occurs at the midpoint of the plastid such that the two daughter plastids, which result from the division process, are equally sized. The mechanism that ensures this equality is based on the system of Min genes, which function for a similar purpose in bacterial cell division. MinD (Colletti et al. 2000) and MinE (Itoh et al. 2001) both dictate that the FtsZ ring is allowed to form only in the middle of the plastid's long axis and is prevented from forming at either pole (Fujiwara et al. 2004). Interestingly these genes define the fact that plastids have distinct poles and are not unpolarised organelles as has been generally believed. Although the third member of the bacterial family of Min genes, MinC, appears to be absent from plant genomes, expression of the prokaryotic MinC gene in Arabidopsis interferes with the plastid division machinery and results in abnormally large chloroplasts (Tavva et al. 2006). Whether this is a direct interaction between the Min proteins or an effect of MinC directly on FtsZ functionality is unclear.

A clear theme which has arisen from the recent knowledge about the molecular basis of plastid division is that the division machinery currently used by chloro-plasts involves proteins originally involved in prokaryotic cell division, reflecting the plastid's ancestry, and new genes which have been hijacked from the plant's genome. In addition to the genes already mentioned, ARTEMIS (Fulgosi et al. 2002) and GIANT CHLOROPLAST 1 (Maple et al. 2004) are both related to pro-karyotic proteins and both function in plastid division, since perturbation of them results in abnormal plastids. Conversely, ARC5 has no prokaryotic relations and ARC3 is a chimera of an FtsZ gene and a eukaryotic gene, phosphatidylinositol-4-phosphate 5-kinase (Shimada et al. 2004). It is clear that during the evolution of the plastid replication process, plant nuclear genes were recruited to interact with

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Fig. 3. A tentative model for the arrangement of proteins and the plastid dividing rings at the midpoint of a plastid about to commence division. ARC5 is associated with the outer plastid division ring and the proteins PDV1 and PDV2 link the outer plastid division ring to the plastid envelope membrane. An unknown protein spans the lumen of the envelope membrane and provides attachment points for ARC6, which links the inner envelope membrane to the inner plastid division ring and the FtsZ ring, composed of FtsZ1 and FtsZ2 proteins. Adapted from Glynn et al. (2007).

Fig. 3. A tentative model for the arrangement of proteins and the plastid dividing rings at the midpoint of a plastid about to commence division. ARC5 is associated with the outer plastid division ring and the proteins PDV1 and PDV2 link the outer plastid division ring to the plastid envelope membrane. An unknown protein spans the lumen of the envelope membrane and provides attachment points for ARC6, which links the inner envelope membrane to the inner plastid division ring and the FtsZ ring, composed of FtsZ1 and FtsZ2 proteins. Adapted from Glynn et al. (2007).

the solely prokaryotic process in order to enable control of the process in the en-dosymbiotic organelles by the plant nucleus. There are many questions still to be answered concerning the control of the plastid division machinery including how it is activated and stopped and how is the division of large populations of organelles during leaf cell expansion coordinated? Another often overlooked question is what suppresses the division machinery in cells where plastid replication rarely occurs and where plastid populations are relatively sparse, as in leaf epidermal cells. In addition, it is normally assumed that the binary fission type of plastid division as discussed here is the sole type of mechanism by which plastids divide. However, replication by a budding type of mechanism, which could be regarded as an extreme asymmetric type of binary division, does occur occasionally in plants (Kulandaielu and Gnanam 1985) and has been shown clearly in giant plas-tids of the suffulta mutant in tomato (Forth and Pyke 2006) where small budding vesicles bud off from the large plastid body as the chloroplasts differentiate into chromoplasts. Highly asymmetric chloroplast division has been observed in plants of arc11 (Marrison et al. 1999), which contain a mutation in the MinD gene (Fiji-

wara et al. 2004), so it is conceivable that a budding type mechanism could result from a breakdown in the Min centralizing system. To date, plastid division mechanisms and cell biology have only been studied in relatively few plants species and it will be interesting to ascertain the degree of variation in division mechanisms that might exist in all higher plants.

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  • Tesfay
    How plastids are individual?
    2 years ago

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