Plastid division: evolution, mechanism and complexity

Abstract

Background: The continuity of chloroplasts is maintained by division of pre-existing chloroplasts. Chloroplasts originated as bacterial endosymbionts; however, the majority of bacterial division factors are absent from chloroplasts and the eukaryotic host has added several new components. For example, the ftsZ gene has been duplicated and modified, and the Min system has retained MinE and MinD but lost MinC, acquiring at least one new component ARC3. Further, the mechanism has evolved to include two members of the dynamin protein family, ARC5 and FZL, and plastid-dividing (PD) rings were most probably added by the eukaryotic host.

Scope: Deciphering how the division of plastids is coordinated and controlled by nuclear-encoded factors is key to our understanding of this important biological process. Through a number of molecular-genetic and biochemical approaches, it is evident that FtsZ initiates plastid division where the coordinated action of MinD and MinE ensures correct FtsZ (Z)-ring placement. Although the classical FtsZ antagonist MinC does not exist in plants, ARC3 may fulfil this role. Together with other prokaryotic-derived proteins such as ARC6 and GC1 and key eukaryotic-derived proteins such as ARC5 and FZL, these proteins make up a sophisticated division machinery. The regulation of plastid division in a cellular context is largely unknown; however, recent microarray data shed light on this. Here the current understanding of the mechanism of chloroplast division in higher plants is reviewed with an emphasis on how recent findings are beginning to shape our understanding of the function and evolution of the components.

Conclusions: Extrapolation from the mechanism of bacterial cell division provides valuable clues as to how the chloroplast division process is achieved in plant cells. However, it is becoming increasingly clear that the highly regulated mechanism of plastid division within the host cell has led to the evolution of features unique to the plastid division process.

Fig. 1.

Model of protein–protein interactions within the plastid division machinery. (A) Bimolecular fluorescence complementation assays have been successfully used to confirm protein interactions between stromal plastid division components in planta: assays were performed by co-expressing stromal plastid division components fused to the N-terminal (NY) or C-terminal (CY) half of YFP, and reconstituted YFP fluorophore, indicative of a positive interaction, was detected by epifluorescence microscopy. E, AtMinE1; D, AtMinD1; F1, AtFtsZ1-1; F2, AtFtsZ2-1. (B) Working model for plastid division showing the identified protein components to date, their localization patterns and protein–protein interaction properties. AtMinE1 and AtMinD1 localize to discrete spots close to the chloroplast membrane and interact to form a complex. MSL2 and MSL3 (MSL) are predicted transmembrane proteins and co-localize with AtMinE1 to the poles of the chloroplast. GC1 localizes to the stromal side of the inner envelope membrane and forms dimers, but is unable to interact with other plastid division components. AtFtsZ1-1 (F1) and AtFtsZ2-1 (F2) form a ring-like structure at the chloroplast mid point and can form homodimers and heterodimers. AtFtsZ1-1 interacts with ARC3 (3) and AtFtsZ2-1 interacts with ARC6 (6). ARC3 and ARC6 both localize to ring-like structures and both can dimerize. ARC5 localizes to a ring-like structure on the cytosolic surface of the outer envelope membrane. Modified with the permission of Blackwell Publishing Ltd from Maple et al. (2005).

Fig. 2.

Models for Min protein movement in Arabidopsis. AtMinD1 and AtMinE1 (red/yellow circle) may oscillate within chloroplasts analogous to the E. coli model in the wild type (the arrow represents side to side oscillations along a spiral pathway) (A) or spherical rodA mutant (B) cells. Equivalent to the B. subtilis model, AtMinD1 and AtMinE1 may remain associated with each pole of the chloroplast (C). Alternatively, a plant-specific solution may involve AtMinD1 and AtMinE1 relocating along a different pathway to circumvent the thylakoid membranes (D).

Fig. 3.

The effect of plastid division inhibition on nuclear gene expression. (A) Categorization of Arabidopsis genes up- and downregulated ≥ 3-fold in plants where plastid division has been inhibited by constitutive overexpression of AtMinD1, based on their annotations to terms used in the GO cellular component (Berardini et al., 2004). (B) Effect of constitutive overexpression of AtMinD1 on the transcript levels of other characterized plastid division components.