Concentration-dependent organization of DNA by the dinoflagellate histone-like protein HCc3

Chan, Yat‐Sun; Wong, Joseph T.Y.

doi:10.1093/nar/gkm165

Cited by 49 publications

(39 citation statements)

References 85 publications

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“…In the absence of nucleosomes, the ability of peripheral transcriptional loops to be maintained in such a crowded environment is made possible only because the bulk of the remaining DNA is maintained as a highly dense liquid crystalline chromosome. The ability to straighten DNA by using the recombinant dinoflagellate histone-like protein HCc3 (6) and the presence at the chromosomal periphery of the native HCc protein (13,42) are both consistent with its role in VOL. 9,2010 LIQUID CRYSTALLINE CHROMOSOMES 1583 maintaining these "extrachromosomal" loops.…”

Section: Discussionmentioning

confidence: 55%

Birefringence and DNA Condensation of Liquid Crystalline Chromosomes

et al. 2010

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DNA can self-assemble in vitro into several liquid crystalline phases at high concentrations. The largest known genomes are encoded by the cholesteric liquid crystalline chromosomes (LCCs) of the dinoflagellates, a diverse group of protists related to the malarial parasites. Very little is known about how the liquid crystalline packaging strategy is employed to organize these genomes, the largest among living eukaryotes-up to 80 times the size of the human genome. Comparative measurements using a semiautomatic polarizing microscope demonstrated that there is a large variation in the birefringence, an optical property of anisotropic materials, of the chromosomes from different dinoflagellate species, despite their apparently similar ultrastructural patterns of bands and arches. There is a large variation in the chromosomal arrangements in the nuclei and individual karyotypes. Our data suggest that both macroscopic and ultrastructural arrangements affect the apparent birefringence of the liquid crystalline chromosomes. Positive correlations are demonstrated for the first time between the level of absolute retardance and both the DNA content and the observed helical pitch measured from transmission electron microscopy (TEM) photomicrographs. Experiments that induced disassembly of the chromosomes revealed multiple orders of organization in the dinoflagellate chromosomes. With the low protein-to-DNA ratio, we propose that a highly regulated use of entropy-driven force must be involved in the assembly of these LCCs. Knowledge of the mechanism of packaging and arranging these largest known DNAs into different shapes and different formats in the nuclei would be of great value in the use of DNA as nanostructural material.DNA molecules are the indispensable genetic material of every organism. Apart from having the encoding power of a 4-base double-stranded polymer, DNA also has an enormous capacity to be condensed. It is probably this ability that allowed the evolution of increasing genome sizes in the eukaryotes. Histone-mediated nucleosome-based chromatin is the prevailing method for DNA packaging, but it is not the only way that DNA is condensed in the eukaryotes. Highly compact liquid crystalline DNA has been reported in several animal sperm nuclei (11, 28) and was also found in the nucleosomeless liquid crystalline chromosomes (LCCs) of dinoflagellates. Neither animal sperm nuclei nor dinoflagellate nuclei employ histones. In fact, the histone core octamer may hinder the attainment of ultrahigh levels of condensation due to its restrictive volume. In the sperm model, protamine is a sperm-specific DNA-binding protein (ϳ7 kDa) that is an order of magnitude smaller than the histone core octamer, and it adopts a structural role in the organization of the male gametic genome (1, 3). It is this very reduction in the protein-to-DNA ratio that may well enable the high DNA compaction into a liquid crystalline state. The dinoflagellate chromosomes are known to have a proteinto-DNA ratio even smaller than those of the prokaryo...

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Section: Discussionmentioning

confidence: 55%

Birefringence and DNA Condensation of Liquid Crystalline Chromosomes

et al. 2010

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“…In eukaryotes, histone proteins are involved in chromatin modulation, whereas in prokaryotes, histone-like proteins play a role in chromatin modulation. Although it was previously thought that dinoflagellates lacked histone proteins [40] and used histone-like proteins for DNA organization [41], recent studies have revealed the presence of genes that encode four core nucleosomal histones, H2A, H2B, H3, and H4 [42][43][44]. Histone deacetylase [45], nucleosome assembly protein [45], and an H1-type linker histonelike protein [46] have also been found in dinoflagellates.…”

Section: Molecular Basis Of Permanently Condensed Chromatinmentioning

confidence: 99%

Draft Assembly of the Symbiodinium minutum Nuclear Genome Reveals Dinoflagellate Gene Structure

et al. 2013

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“…Dinoflagellate/viral nucleoproteins (DVNPs) are similar to uncharacterized proteins from phycodnaviruses, are distributed in all dinoflagellates yet examined, and represent a family of basic proteins with high DNA-binding affinity (4). In contrast, dinoflagellate histone-like proteins (HLPs) are of bacterial origin and have been found only in certain core dinoflagellate species; they are primarily detected at the chromosome periphery, where they are predicted to organize extended DNA loops during transcription (68). We identified DVNPs in all transcriptomes in our dataset, confirming their ubiquitous distribution among dinoflagellates.…”

Section: Cyanobacteria (N=17)mentioning

confidence: 99%

Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics

Janouškovec

Gavelis

Burki

et al. 2016

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

237

211

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Dinoflagellates are key species in marine environments, but they remain poorly understood in part because of their large, complex genomes, unique molecular biology, and unresolved in-group relationships. We created a taxonomically representative dataset of dinoflagellate transcriptomes and used this to infer a strongly supported phylogeny to map major morphological and molecular transitions in dinoflagellate evolution. Our results show an earlybranching position of Noctiluca, monophyly of thecate (plate-bearing) dinoflagellates, and paraphyly of athecate ones. This represents unambiguous phylogenetic evidence for a single origin of the group's cellulosic theca, which we show coincided with a radiation of cellulases implicated in cell division. By integrating dinoflagellate molecular, fossil, and biogeochemical evidence, we propose a revised model for the evolution of thecal tabulations and suggest that the late acquisition of dinosterol in the group is inconsistent with dinoflagellates being the source of this biomarker in pre-Mesozoic strata. Three distantly related, fundamentally nonphotosynthetic dinoflagellates, Noctiluca, Oxyrrhis, and Dinophysis, contain cryptic plastidial metabolisms and lack alternative cytosolic pathways, suggesting that all free-living dinoflagellates are metabolically dependent on plastids. This finding led us to propose general mechanisms of dependency on plastid organelles in eukaryotes that have lost photosynthesis; it also suggests that the evolutionary origin of bioluminescence in nonphotosynthetic dinoflagellates may be linked to plastidic tetrapyrrole biosynthesis. Finally, we use our phylogenetic framework to show that dinoflagellate nuclei have recruited DNA-binding proteins in three distinct evolutionary waves, which included two independent acquisitions of bacterial histone-like proteins.dinoflagellates | phylogeny | theca | plastids | dinosterol D inoflagellates comprise approximately 2,400 named extant species, of which approximately half are photosynthetic (1). However, this represents a fraction of their estimated diversity: in surface marine waters, dinoflagellates are some of the most abundant and diverse eukaryotes known (2). Dinoflagellates' ecological significance befits their abundance: photosynthetic species are dominant marine primary producers, and phagotrophic species play an important role in the microbial loop through predation and nutrient recycling. Approximately 75-80% of the toxic eukaryotic phytoplankton species are dinoflagellates, and they cause shellfish poisoning and harmful algal blooms of global importance. Symbiotic genera like Symbiodinium participate in interactions with metazoans and are essential for the formation of reef ecosystems, and parasitic forms play a central role in the collapse of harmful algal blooms, including those caused by dinoflagellates themselves (3). Dinoflagellates synthesize important secondary metabolites including sterols, polyketides, toxins, and dimethylsulfide, and several of them have evolved bioluminescence. They ...

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Concentration-dependent organization of DNA by the dinoflagellate histone-like protein HCc3

Cited by 49 publications

References 85 publications

Birefringence and DNA Condensation of Liquid Crystalline Chromosomes

Birefringence and DNA Condensation of Liquid Crystalline Chromosomes

Draft Assembly of the Symbiodinium minutum Nuclear Genome Reveals Dinoflagellate Gene Structure

Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics

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