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Prospective function of FtsZ proteins in the secondary plastid of chlorarachniophyte algae

BACKGROUND: Division 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 c...

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Autores principales: Hirakawa, Yoshihisa, Ishida, Ken-ichiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4641359/
https://www.ncbi.nlm.nih.gov/pubmed/26556725
http://dx.doi.org/10.1186/s12870-015-0662-7
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author Hirakawa, Yoshihisa
Ishida, Ken-ichiro
author_facet Hirakawa, Yoshihisa
Ishida, Ken-ichiro
author_sort Hirakawa, Yoshihisa
collection PubMed
description BACKGROUND: Division 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. RESULTS: To 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. CONCLUSIONS: Our 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 MATERIAL: The online version of this article (doi:10.1186/s12870-015-0662-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-46413592015-11-12 Prospective function of FtsZ proteins in the secondary plastid of chlorarachniophyte algae Hirakawa, Yoshihisa Ishida, Ken-ichiro BMC Plant Biol Research Article BACKGROUND: Division 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. RESULTS: To 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. CONCLUSIONS: Our 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 MATERIAL: The online version of this article (doi:10.1186/s12870-015-0662-7) contains supplementary material, which is available to authorized users. BioMed Central 2015-11-10 /pmc/articles/PMC4641359/ /pubmed/26556725 http://dx.doi.org/10.1186/s12870-015-0662-7 Text en © Hirakawa and Ishida. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Hirakawa, Yoshihisa
Ishida, Ken-ichiro
Prospective function of FtsZ proteins in the secondary plastid of chlorarachniophyte algae
title Prospective function of FtsZ proteins in the secondary plastid of chlorarachniophyte algae
title_full Prospective function of FtsZ proteins in the secondary plastid of chlorarachniophyte algae
title_fullStr Prospective function of FtsZ proteins in the secondary plastid of chlorarachniophyte algae
title_full_unstemmed Prospective function of FtsZ proteins in the secondary plastid of chlorarachniophyte algae
title_short Prospective function of FtsZ proteins in the secondary plastid of chlorarachniophyte algae
title_sort prospective function of ftsz proteins in the secondary plastid of chlorarachniophyte algae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4641359/
https://www.ncbi.nlm.nih.gov/pubmed/26556725
http://dx.doi.org/10.1186/s12870-015-0662-7
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