Abstract

BackgroundDivision of double-membraned plastids (primary plastids) is performed by constriction of a ring-like division complex consisting of multiple plastid division proteins. Consistent with the endosymbiotic origin of primary plastids, some of the plastid division proteins are descended from cyanobacterial cell division machinery, and the others are of host origin. In several algal lineages, complex plastids, the “secondary plastids”, have been acquired by the endosymbiotic uptake of primary plastid-bearing algae, and are surrounded by three or four membranes. Although homologous genes for primary plastid division proteins have been found in genome sequences of secondary plastid-bearing organisms, little is known about the function of these proteins or the mechanism of secondary plastid division.ResultsTo gain insight into the mechanism of secondary plastid division, we characterized two plastid division proteins, FtsZD-1 and FtsZD-2, in chlorarachniophyte algae. FtsZ homologs were encoded by the nuclear genomes and carried an N-terminal plastid targeting signal. Immunoelectron microscopy revealed that both FtsZD-1 and FtsZD-2 formed a ring-like structure at the midpoint of bilobate plastids with a projecting pyrenoid in Bigelowiella natans. The ring was always associated with a shallow plate-like invagination of the two innermost plastid membranes. Furthermore, gene expression analysis confirmed that transcripts of ftsZD genes were periodically increased soon after cell division during the B. natans cell cycle, which is not consistent with the timing of plastid division.ConclusionsOur findings suggest that chlorarachniophyte FtsZD proteins are involved in partial constriction of the inner pair of plastid membranes, but not in the whole process of plastid division. It is uncertain how the outer pair of plastid membranes is constricted, and as-yet-unknown mechanism is required for the secondary plastid division in chlorarachniophytes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0662-7) contains supplementary material, which is available to authorized users.

Highlights

  • Division of double-membraned plastids is performed by constriction of a ring-like division complex consisting of multiple plastid division proteins

  • Sequences of plastid division protein FtsZD in chlorarachniophytes To identify homologous genes of primary plastid division proteins in chlorarachniophytes, we surveyed B. natans genomes by reciprocal BLAST with corresponding known sequences of Arabidopsis thaliana, Chlamydomonas reinhardtii, and Cyanidioschyzon merolae [12, 13]

  • The C-terminal regions of FtsZD proteins were divergent in sequence and length, whereas their C-terminal ends were mostly conserved among FtsZD-1 and FtsZD-2 proteins; the C-terminal conserved motif of FtsZD-1 is ‘T-L-R/G-G-K-A-K-R-x-A

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Summary

Introduction

Division of double-membraned plastids (primary plastids) is performed by constriction of a ring-like division complex consisting of multiple plastid division proteins. The outermost membrane is connected to the endoplasmic reticulum (ER) in some secondary plastids of red algal origin, and the recent ER-enclosure model has proposed that the outer pair of membranes are derived from the host ER [8]. These additional membranes should be a barrier for transport of nucleus-encoded plastid proteins as well as for metabolite exchange. In terms of plastid division, new mechanisms would be necessary for constriction of the additional membranes in secondary plastids

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