Kleptochloroplast Enlargement, Karyoklepty and the Distribution of the Cryptomonad Nucleus in Nusuttodinium (= Gymnodinium) aeruginosum (Dinophyceae)

Onuma, Ryo; Horiguchi, Takeo

doi:10.1016/j.protis.2015.01.004

Cited by 28 publications

(35 citation statements)

References 40 publications

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“…While sequestration of nuclei and chloroplasts along with other prey organelles is well known for a few dinoflagellates species (Dodge, 1971; Farmer and Roberts, 1990; Horiguchi and Pienaar, 1992; Okamoto and Inouye, 2005; Gast et al, 2007; Yamaguchi et al, 2011; Onuma and Horiguchi, 2013, 2015; Kim et al, 2014), enlargement of the sequestered prey nucleus has not been reported in any of studies.…”

Section: Discussionmentioning

confidence: 96%

“…The sequestered prey nucleus has been inferred to allow the host cell to exploit photosynthetic performance of its sequestered prey chloroplasts; e.g., the dinoflagellates Amylax triacantha , Nusuttodinium aeruginosum , and N. myriopyrenoides and the ciliate M. rubrum (Johnson and Stoecker, 2005; Johnson et al, 2007; Kim et al, 2014, 2016; Onuma and Horiguchi, 2015). A few molecular and transcriptome studies focusing on the photosynthetic ability of M. rubrum in association with the sequestered prey nucleus (Johnson et al, 2007; Lasek-Nesselquist et al, 2015; Kim et al, 2016) have shown expression of nuclear-encoded plastid-targeted algal genes.…”

Section: Discussionmentioning

confidence: 99%

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Dynamics of Sequestered Cryptophyte Nuclei in Mesodinium rubrum during Starvation and Refeeding

et al. 2017

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The marine mixotrophic ciliate Mesodinium rubrum is known to acquire chloroplasts, mitochondria, nucleomorphs, and nucleus from its cryptophyte prey, particularly from species in the genera, Geminigera and Teleaulax. The sequestered prey nucleus and chloroplasts are considered to support photosynthesis of M. rubrum. In addition, recent studies have shown enlargement of the retained prey nucleus in starved M. rubrum and have inferred that enlargement results from the fusion of ingested prey nuclei. Thus far, however, little is known about the mechanism underlying the enlargement of the prey nucleus in M. rubrum. Here, we conducted starvation and refeeding studies to monitor the fate of prey nuclei acquired by M. rubrum when feeding on Teleaulax amphioxeia and to explore the influence of the retained prey nucleus on photosynthesis of M. rubrum. Results indicate that enlargement of the prey nucleus does not result from fusion of nuclei. Furthermore, the enlarged prey nucleus does not appear to divide during cell division of M. rubrum. The presence of a prey nucleus significantly affected photosynthetic performance of M. rubrum, while the number of retained chloroplasts had little influence on rate of carbon fixation. We interpret results within the context of a model that considers the dynamics of ingested prey nuclei during division of M. rubrum.

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Section: Discussionmentioning

confidence: 96%

Section: Discussionmentioning

confidence: 99%

Dynamics of Sequestered Cryptophyte Nuclei in Mesodinium rubrum during Starvation and Refeeding

et al. 2017

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“…For example, they may have sequestered the engulfed plastids and nuclei from the central phagosome into special vesicles in which these organelles were protected from digestion, as found in the dinoflagellate Amylax triacantha (Kim et al., ). Further, these hosts may have modified the engulfed plastids, such as by their enlargement, as observed in the dinoflagellate Nusuttodinium (= Gymnodinium ) aeruginosum (Onuma & Horiguchi, ).…”

Section: New Hypotheses For the Acquisition Of Red Multimembrane Plasmentioning

confidence: 99%

“…Moreover, their host cells possess highly advanced mechanisms for ingestion and maintenance of these algal cells or their organelles (e.g. Johnson et al, 2007;Kim et al, 2012;Onuma & Horiguchi, 2015).…”

Section: Kleptoplastid Systems In Ciliates and Dinoflagellates: A mentioning

confidence: 99%

Did some red alga‐derived plastids evolve via kleptoplastidy? A hypothesis

Bodył

2017

Biological Reviews

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The evolution of plastids has a complex and still unresolved history. These organelles originated from a cyanobacterium via primary endosymbiosis, resulting in three eukaryotic lineages: glaucophytes, red algae, and green plants. The red and green algal plastids then spread via eukaryote-eukaryote endosymbioses, known as secondary and tertiary symbioses, to numerous heterotrophic protist lineages. The number of these horizontal plastid transfers, especially in the case of red alga-derived plastids, remains controversial. Some authors argue that the number of plastid origins should be minimal due to perceived difficulties in the transformation of a eukaryotic algal endosymbiont into a multimembrane plastid, but increasingly the available data contradict this argument. I suggest that obstacles in solving this dilemma result from the acceptance of a single evolutionary scenario for the endosymbiont-to-plastid transformation formulated by Cavalier-Smith & Lee (1985). Herein I discuss data that challenge this evolutionary scenario. Moreover, I propose a new model for the origin of multimembrane plastids belonging to the red lineage and apply it to the dinoflagellate peridinin plastid. The new model has several general and practical implications, such as the requirement for a new definition of cell organelles and in the construction of chimeric organisms.

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“…Certain species of heterotrophic dinoflagellates engulf eukaryotic algae and use them as temporary chloroplasts (called "kleptoplasts") for a period of days to weeks before digesting them. In certain cases, the kleptoplast divides in accord with dinoflagellate cell division and is inherited for a number of generations (6). A few dinoflagellate species maintain a eukaryotic algal unicell (i.e., containing a nucleus, mitochondria, Golgi apparatus, and so forth) as a permanent endosymbiont by synchronizing the endosymbiont cell division to the host cell cycle (7,8).…”

mentioning

confidence: 99%

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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Kleptochloroplast Enlargement, Karyoklepty and the Distribution of the Cryptomonad Nucleus in Nusuttodinium (= Gymnodinium) aeruginosum (Dinophyceae)

Cited by 28 publications

References 40 publications

Dynamics of Sequestered Cryptophyte Nuclei in Mesodinium rubrum during Starvation and Refeeding

Dynamics of Sequestered Cryptophyte Nuclei in Mesodinium rubrum during Starvation and Refeeding

Did some red alga‐derived plastids evolve via kleptoplastidy? A hypothesis

Chloroplast division checkpoint in eukaryotic algae

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