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

Hirakawa, Yoshihisa; Ishida, Koichi

doi:10.1186/s12870-015-0662-7

Cited by 10 publications

(14 citation statements)

References 75 publications

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“…We previously showed that some, but not all, nucleus-encoded chloroplast-division genes/proteins are specifically expressed in the S phase in a variety of algal lineages that possess chloroplasts of primary cyanobacterial endosymbiotic origin (11). In addition, cellcycle stage-specific expression of FtsZ mRNA was also reported in a diatom, which possesses chloroplasts of a secondary red algal endosymbiotic origin (32), and in a chlorarachniophyte alga, which possesses chloroplasts of a green algal secondary endosymbiotic origin (33). These studies suggest that the host cell restricts the onset of chloroplast division at a specific stage of the host cell cycle by the regulation of gene/protein expression.…”

Section: Discussionmentioning

confidence: 94%

Chloroplast division checkpoint in eukaryotic algae

Sumiya

Fujiwara

Era

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Chloroplasts evolved from a cyanobacterial endosymbiont. It is believed that the synchronization of endosymbiotic and host cell division, as is commonly seen in existing algae, was a critical step in establishing the permanent organelle. Algal cells typically contain one or only a small number of chloroplasts that divide once per host cell cycle. This division is based partly on the S-phase-specific expression of nucleus-encoded proteins that constitute the chloroplast-division machinery. In this study, using the red alga Cyanidioschyzon merolae, we show that cell-cycle progression is arrested at the prophase when chloroplast division is blocked before the formation of the chloroplastdivision machinery by the overexpression of Filamenting temperaturesensitive (Fts) Z2-1 (Fts72-1), but the cell cycle progresses when chloroplast division is blocked during division-site constriction by the overexpression of either FtsZ2-1 or a dominant-negative form of dynamin-related protein 5B (DRP5B). In the cells arrested in the prophase, the increase in the cyclin B level and the migration of cyclin-dependent kinase B (CDKB) were blocked. These results suggest that chloroplast division restricts host cell-cycle progression so that the cell cycle progresses to the metaphase only when chloroplast division has commenced. Thus, chloroplast division and host cell-cycle progression are synchronized by an interactive restriction that takes place between the nucleus and the chloroplast. In addition, we observed a similar pattern of cell-cycle arrest upon the blockage of chloroplast division in the glaucophyte alga Cyanophora paradoxa, raising the possibility that the chloroplast division checkpoint contributed to the establishment of the permanent organelle.chloroplast division | algal cell cycle | Cyanidioschyzon merolae | Cyanophora paradoxa C hloroplasts trace their origin to a primary endosymbiotic event that took place more than a billion years ago, a process in which an ancestral cyanobacterium became integrated into a previously nonphotosynthetic eukaryote. The ancient alga that resulted from this primary endosymbiotic event evolved into the Glaucophyta (glaucophyte algae), Rhodophyta (red algae), and Viridiplantae (green algae, streptophyte algae, and land plants), which together are grouped as the Plantae (sensu stricto) or Archaeplastida. After these primitive green and red algae had become established, chloroplasts then spread into other eukaryote lineages through secondary endosymbiotic events in which a red or green alga became integrated into previously nonphotosynthetic eukaryotes (1).The continuity of chloroplasts has been maintained for more than a billion years. The majority of algae (both unicellular and multicellular, with both possessing chloroplasts of primary and secondary endosymbiotic origin) have one or at most only a few chloroplasts per cell. Thus, chloroplast division is synchronized with the host cell cycle so that the chloroplast divides before cytokinesis and is thus transmitted into each daughter cell ...

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Section: Discussionmentioning

confidence: 94%

Chloroplast division checkpoint in eukaryotic algae

Sumiya

Fujiwara

Era

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Our previous studies have shown that a couple of nuclear genes for plastid- and nucleomorph-targeted proteins of B. natans were transcriptionally regulated under a diurnal cycle ( Hirakawa et al 2011 , Hirakawa and Ishida 2015 ). To obtain a comprehensive overview, we performed genome-wide transcript profiling using RNA-seq data along the B. natans cell cycles temporally synchronized by diurnal light and dark cycles.…”

Section: Introductionmentioning

confidence: 99%

Diurnal Transcriptional Regulation of Endosymbiotically Derived Genes in the ChlorarachniophyteBigelowiella natans

2016

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Chlorarachniophyte algae possess complex plastids acquired by the secondary endosymbiosis of a green alga, and the plastids harbor a relict nucleus of the endosymbiont, the so-called nucleomorph. Due to massive gene transfer from the endosymbiont to the host, many proteins involved in plastid and nucleomorph are encoded by the nuclear genome. Genome sequences have provided a blueprint for the fate of endosymbiotically derived genes; however, transcriptional regulation of these genes remains poorly understood. To gain insight into the evolution of endosymbiotic genes, we performed genome-wide transcript profiling along the cell cycle of the chlorarachniophyte Bigelowiella natans, synchronized by light and dark cycles. Our comparative analyses demonstrated that transcript levels of 7,751 nuclear genes (35.7% of 21,706 genes) significantly oscillated along the diurnal/cell cycles, and those included 780 and 147 genes for putative plastid and nucleomorph-targeted proteins, respectively. Clustering analysis of those genes revealed the existence of transcriptional networks related to specific biological processes such as photosynthesis, carbon metabolism, translation, and DNA replication. Interestingly, transcripts of many plastid-targeted proteins in B. natans were induced before dawn, unlike other photosynthetic organisms. In contrast to nuclear genes, 99% nucleomorph genes were found to be constitutively expressed during the cycles. We also found that the nucleomorph DNA replication would be controlled by a nucleus-encoded viral-like DNA polymerase. The results of this study suggest that nucleomorph genes have lost transcriptional regulation along the diurnal cycles, and nuclear genes exert control over the complex plastid including the nucleomorph.

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“…Through a poorly understood mechanism, FtsZ, along with components on the cytoplasmic 3 face of the chloroplast, then generates the contractile force required for membrane 3 constriction, and eventually, fission (Osawa et al, 2008). Recent work by Hirakawa et al 3 demonstrated the function of FtsZ proteins in the secondary plastid of chlorarachniophytes, 3 and in Bigelowiella natans, both FtsZD-1 and FtsZD-2 formed a ring-like structure that 3 bisected the midpoint of a bilobate pyrenoid found in the secondary chloroplast of this 3 species (Hirakawa & Ishida, 2015). This ring was constitutively present at this region and…”

mentioning

confidence: 96%

The algal pyrenoid: key unanswered questions

Meyer

Whittaker

Griffiths

2017

Journal of Experimental Botany

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The confinement of Rubisco in a chloroplast microcompartment, or pyrenoid, is a distinctive feature of most microalgae, and contributes to perhaps ~30 Pg of carbon fixed each year, yet our understanding of pyrenoid composition, regulation, and function remains fragmentary. Recently, significant progress in understanding the pyrenoid has arisen from studies using mutant lines, mass spectrometric analysis of isolated pyrenoids, and advanced ultrastructural imaging of the microcompartment in the model alga Chlamydomonas. The emergence of molecular details in other lineages provides a comparative framework for this review, and evidence that most pyrenoids function similarly, even in the absence of a common ancestry. The objective of this review is to explore pyrenoid diversity throughout key algal lineages and discuss whether common ultrastructural and cellular features are indicative of common functional processes. By characterizing pyrenoid origins in terms of mechanistic and structural parallels, we hope to provide key unanswered questions which will inform future research directions.

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

Cited by 10 publications

References 75 publications

Chloroplast division checkpoint in eukaryotic algae

Chloroplast division checkpoint in eukaryotic algae

Diurnal Transcriptional Regulation of Endosymbiotically Derived Genes in the ChlorarachniophyteBigelowiella natans

The algal pyrenoid: key unanswered questions

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