ESCRT Machinery Mediates Cytokinetic Abscission in the Unicellular Red Alga Cyanidioschyzon merolae

Yagisawa, Fumi; Fujiwara, Takayuki; Takemura, Tamiko; Kobayashi, Yuki; Sumiya, Nobuko; Miyagishima, Shin Ya; Nakamura, Soichi; Imoto, Yuuta; Misumi, Osami; Tanaka, Kan; Kuroiwa, Haruko; Kuroiwa, Tsuneyoshi

doi:10.3389/fcell.2020.00169

Cited by 15 publications

(11 citation statements)

References 83 publications

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“…Sulfolobus to almost every eukaryote, including Plantae, Amoebozoa, Fungi, and Animals (Yagisawa et al 2020). This suggests that the host organism was a Sulfolobuslike species.…”

Section: Discussionmentioning

confidence: 99%

“…It is thought that mitochondria and plastids arose about 1-2 billion years ago when autonomous α-proteobacteria and cyanobacteria lived together in the cytoplasm of a eukaryotic ancestor, which resembles a thermophile archaeon Sulforobus in a form of cell division (Yagisawa et al 2020) and had emerged from Asgard archaea (Zaremba-Niedzwiedzka et al 2017). The symbiotic α-proteobacteria lost autonomy and were integrated with the host organism via endosymbiotic gene transfer and converted to mitochondria.…”

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confidence: 99%

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Smooth Loop-Like Mitochondrial Nucleus in the Primitive Red Alga <i>Cyanidioschyzon merolae</i> Revealed by Drying Treatment

et al. 2021

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It is thought that mitochondria were generated by the symbiosis of autonomous α-proteobacteria and a eukaryote-like organism derived from an archaeon of the species Sulfolobus. Soon after the symbiosis, most of the genome of the α-proteobacterium, which was required for autonomy, was lost. Many genes were transferred into the host genome. However, a small amount of DNA the mitochondrial genome (mt-genome, mtDNA) remained in the symbiotic organelle. The primitive eukaryotic cells increased the mtDNA copy number and formed a mitochondrial nucleus (mt-nucleus). The primitive unicellular eukaryote evolved into organisms with one mitochondrion containing multiple mtDNA copies per cell, and organisms with multiple mitochondria with a small number of mtDNA copies in each cell. There have been many studies on the mitochondria and mt-genomes of amoeba, plants, and animals which contain many mitochondria per cell, but only a few studies have reported morphological characteristics of the mitochondria and their genomes in primitive unicellular organisms that have only a single mitochondrion per cell. Here, we show that centrally located mt-nuclei in the primitive red alga Cyanidioschyzon merolae form smooth rings following the application of a drying method that produces slight cell swelling. We discuss regulatory mechanisms for genome function in endosymbiotic organelles on the basis of the differences between the copy number of mtDNA in smooth-ring shaped mt-nuclei and plastid DNA in beadshaped plastid nuclei.

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“…Sulfolobus to almost every eukaryote, including Plantae, Amoebozoa, Fungi, and Animals (Yagisawa et al 2020). This suggests that the host organism was a Sulfolobuslike species.…”

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Smooth Loop-Like Mitochondrial Nucleus in the Primitive Red Alga <i>Cyanidioschyzon merolae</i> Revealed by Drying Treatment

et al. 2021

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“…During cytokinesis, an actin-based contractile ring is not formed, unlike in its relative Cyanidium caldarium . A recent study has shown that, as in animal cells and archaea, ESCRT proteins are involved in C. merolae cytokinesis ( Yagisawa et al 2020 ).…”

Section: Cellular Architecture and Proliferation Mode Of C Merolaementioning

confidence: 99%

The Unicellular Red AlgaCyanidioschyzon merolae—The Simplest Model of a Photosynthetic Eukaryote

Miyagishima

Tanaka

2021

Plant and Cell Physiology

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Several species of unicellular eukaryotic algae exhibit relatively simple genomic and cellular architecture. Laboratory cultures of these algae grow faster than plants and often provide homogeneous cellular populations exposed to an almost equal environment. These characteristics are ideal for conducting experiments at the cellular and subcellular levels. Many microalgal lineages have recently become genetically tractable, which have started to evoke new streams of studies. Among such algae, the unicellular red alga Cyanidioschyzon merolae is the simplest organism; it possessses the minimum number of membranous organelles, only 4,775 protein-coding genes in the nucleus, and its cell cycle progression can be highly synchronized with the diel cycle. These properties facilitate diverse omics analyses of cellular proliferation and structural analyses of the intracellular relationship among organelles. C. merolae cells lack a rigid cell wall and are thus relatively easily disrupted, facilitating biochemical analyses. Multiple chromosomal loci can be edited by highly efficient homologous recombination. The procedures for the inducible/repressive expression of a transgene or an endogenous gene in the nucleus and for chloroplast genome modification have also been developed. Here we summarize the features and experimental techniques of C. merolae and provide examples of studies using this alga. From these studies, it is clear that C. merolae – either alone or in comparative and combinatory studies with other photosynthetic organisms – can provide significant insights into the biology of photosynthetic eukaryotes.

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“…Cytokinesis in red algae typically occurs by a furrowing process [37,43] (Figure 3, panel a.3) that involves an actin ring (Figure 3b) and has intriguing similarities to the process in animals (e.g., [56,57,59]). While observation of furrowing cytokinesis in a plant might be surprising to researchers familiar with cell division in streptophyte green algae and land plants (where cytoplasmic partitioning is driven by a structure called the phragmoplast), a similar actin-ring-associated furrowing process divides the cytoplasm in most green algae including the familiar model organism Chlamydomonas (see [60] and Figure 16-11 in [1]).…”

Section: Cytokinesismentioning

confidence: 99%

Cytoskeletal diversification across 1 billion years: What red algae can teach us about the cytoskeleton, and vice versa

2021

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The cytoskeleton has a central role in eukaryotic biology, enabling cells to organize internally, polarize, and translocate. Studying cytoskeletal machinery across the tree of life can identify common elements, illuminate fundamental mechanisms, and provide insight into processes specific to less-characterized organisms. Red algae represent an ancient lineage that is diverse, ecologically significant, and biomedically relevant.Recent genomic analysis shows that red algae have a surprising paucity of cytoskeletal elements, particularly molecular motors. Here, we review the genomic and cell biological evidence and propose testable models of how red algal cells might perform processes including cell motility, cytokinesis, intracellular transport, and secretion, given their reduced cytoskeletons. In addition to enhancing understanding of red algae and lineages that evolved from red algal endosymbioses (e.g., apicomplexan parasites), these ideas may also provide insight into cytoskeletal processes in animal cells.

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ESCRT Machinery Mediates Cytokinetic Abscission in the Unicellular Red Alga Cyanidioschyzon merolae

Cited by 15 publications

References 83 publications

Smooth Loop-Like Mitochondrial Nucleus in the Primitive Red Alga <i>Cyanidioschyzon merolae</i> Revealed by Drying Treatment

Smooth Loop-Like Mitochondrial Nucleus in the Primitive Red Alga <i>Cyanidioschyzon merolae</i> Revealed by Drying Treatment

The Unicellular Red AlgaCyanidioschyzon merolae—The Simplest Model of a Photosynthetic Eukaryote

Cytoskeletal diversification across 1 billion years: What red algae can teach us about the cytoskeleton, and vice versa

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