ARC3 is a stromal Z‐ring accessory protein essential for plastid division

Abstract

In plants, chloroplast division is an integral part of development, and these vital organelles arise by binary fission from pre-existing cytosolic plastids. Chloroplasts arose by endosymbiosis and although they have retained elements of the bacterial cell division machinery to execute plastid division, they have evolved to require two functionally distinct forms of the FtsZ protein and have lost elements of the Min machinery required for Z-ring placement. Here, we analyse the plastid division component accumulation and replication of chloroplasts 3 (ARC3) and show that ARC3 forms part of the stromal plastid division machinery. ARC3 interacts specifically with AtFtsZ1, acting as a Z-ring accessory protein and defining a unique function for this family of FtsZ proteins. ARC3 is involved in division site placement, suggesting that it might functionally replace MinC, representing an important advance in our understanding of the mechanism of chloroplast division and the evolution of the chloroplast division machinery.

CDP1, a novel component of chloroplast division site positioning system in Arabidopsis

“…Yeast two-hybrid and BiFC analyses suggested that AtCDP1 may participate in chloroplast division by interacting with ARC3, which is reported to be a stroma protein and localized to a ring at the midpoint of chloroplasts when the chloroplast division initiates [5,22,25]. In addition, ARC3 has an important role in chloroplast division because it interacts with AtFtsZ1 [25,32], AtMinD and AtMinE [25] at different locations of chloroplasts as shown by BiFC assay.…”

“…The E. coli cell division site positioning system does not include such a protein. Furthermore, oscillation of MinD and MinE in higher plants has not been reported [12,13] and the genuine homolog of MinC has not been found in higher plants, despite that ARC3 is regarded as a MinC-like protein but its function is still not very clear [25]. Now, we show that AtCDP1, as a new component of the Min system, is involved in chloroplast division through the interaction with ARC3 at the early stage of chloroplast division process to ensure the constriction of the ring structure at the midpoint of chloroplasts.…”

“…In addition, ARC3 has an important role in chloroplast division because it interacts with AtFtsZ1 [25,32], AtMinD and AtMinE [25] at different locations of chloroplasts as shown by BiFC assay. These data indicate that CDP1 is a new component of the chloroplast division site positioning system.…”

“…Mutation of ARC3 causes a phenotype of misplacement of chloroplast division site, similar to that of minD mutant or MinE-overexpressing transgenic plants [22,[25][26][27]. So far, the homolog of MinC is still missing in higher plants.…”

GTP-dependent Heteropolymer Formation and Bundling of Chloroplast FtsZ1 and FtsZ2

“…This would further imply that chloroplast Z ring dynamics should be regulated in part by factors that inhibit protofilament bundling. One candidate for such a factor is the chloroplast division protein ARC3, a proposed functional replacement for bacterial MinC (46,54), which was recently shown to inhibit lateral interactions between EcFtsZ protofilaments assembled in vitro (55).…”