PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis

Abstract

SUMMARYChloroplast division in plant cells is accomplished through the coordinated action of the tubulin-like FtsZ ring inside the organelle and the dynamin-like ARC5 ring outside the organelle. This coordination is facilitated by ARC6, an inner envelope protein required for both assembly of FtsZ and recruitment of ARC5. Recently, we showed that ARC6 specifies the mid-plastid positioning of the outer envelope proteins PDV1 and PDV2, which have parallel functions in dynamin recruitment. PDV2 positioning involves direct ARC6-PDV2 interaction, but PDV1 and ARC6 do not interact indicating that an additional factor functions downstream of ARC6 to position PDV1. Here, we show that PARC6 (paralog of ARC6), an ARC6-like protein unique to vascular plants, fulfills this role. Like ARC6, PARC6 is an inner envelope protein with its N-terminus exposed to the stroma and Arabidopsis parc6 mutants exhibit defects of chloroplast and FtsZ filament morphology. However, whereas ARC6 promotes FtsZ assembly, PARC6 appears to inhibit FtsZ assembly, suggesting that ARC6 and PARC6 function as antagonistic regulators of FtsZ dynamics. The FtsZ inhibitory activity of PARC6 may involve its interaction with the FtsZ-positioning factor ARC3. A PARC6-GFP fusion protein localizes both to the mid-plastid and to a single spot at one pole, reminiscent of the localization of ARC3, PDV1 and ARC5. Although PARC6 localizes PDV1, it is not required for PDV2 localization or ARC5 recruitment. Our findings indicate that PARC6, like ARC6, plays a role in coordinating the internal and external components of the chloroplast division complex, but that PARC6 has evolved distinct functions in the division process.

Emerging facets of plastid division regulation

“…Indeed, PARC6, a paralogue of ARC6, has been shown to localize to the inner chloroplast envelope where it destabilizes the Z-ring but not through a direct interaction with FtsZ ). PARC6 does, however, interact with ARC3, which also has the ability to interact with FtsZ1 Glynn et al 2009), suggesting that Z-ring destabilization may be mediated through ARC3. ARC3 has two main domains, a non-catalytic N-terminal FtsZ-like domain and a C-terminal Membrane Occupation and Recognition Nexus domain (MORN).…”

“…This leads to a model suggesting that during constriction ARC5 is recruited from the cytosol to the division site by PDV1 and PDV2 to form a ring structure during late stage division. Further work demonstrated that PDV1 constriction site localization is dependent on PARC6 whilst PDV2 localization is dependent on ARC6 (Miyagishima et al 2006;Glynn et al 2009). ARC6 can indeed interact with PDV2 within the intermembrane space where loss of interaction results in PDV2 mislocalization followed by loss of ARC5 recruitment (Miyagishima et al 2006).…”

Genetic Dissection of Chloroplast Biogenesis and Development: An Overview

“…Chloroplast division is mediated by tubulin-like proteins known as FtsZ and dynaminlike proteins, such as ARC5 (accumulation and replication of chloroplasts) that form concentric rings within and outside the chloroplast envelope, respectively (Yang et al, 2008). Recent findings include a role for chaperones, cpn60, and PARC60 in coordinating and regulating division (Glynn et al, 2009;Suzuki et al, 2009). Affected chloroplast division, though, does not have any substantive effect on chloroplast development.…”

The evolution of the regulatory mechanism of chloroplast division

“…6,15 In addition, a recent study showed that the recruitment of PDV1 is mediated by PARC6 (a paralog of ARC6 unique to vascular plants). 16 Finally, the dynamin-related protein DRP5B is recruited by PDV1 and PDV2, and the entire division complex is involved in the fission of the chloroplast at the division site 6 (Fig. 1).…”

“…However, mosses have PDV2 and ARC6, but not PDV1 and PARC6, which are conserved in vascular plants. 13,16 Therefore, the modulation of the chloroplast division rate by PDV proteins, and the evolution of the PDV and ARC6…”