Viral proteins as a potential driver of histone depletion in dinoflagellates

Irwin, Nicholas A. T.; Martin, Bernice M.; Young, Barry P.; Browne, Martin J. G.; Flaus, Andrew; Loewen, Christopher; Keeling, Patrick J.; Howe, LeAnn

doi:10.1038/s41467-018-03993-4

Cited by 46 publications

(45 citation statements)

References 69 publications

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“…Histones have been replaced by specialized positively-charged proteins at early stages of dinoflagellate evolution. Two groups of these proteins were characterized: (1) DVNPs (Dinoflagellate/Viral NucleoProteins) that show a strong homology with proteins of algae viruses from Phycodnaviridae family (Gornik et al, 2012;Irwin et al, 2018) and (2) HLPs (Histone-Like Proteins) that were identified in some dinoflagellate species (Sala-Rovira et al, 1991;Taroncher-Oldenburg and Anderson, 2000;Chudnovsky et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Ultrastructural organization of the chromatin elements in chromosomes of the dinoflagellate Prorocentrum minimum

Golyshev¹,

Berdieva²,

Musinova³

et al. 2018

Protistology

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DNA of the majority of present-day eukaryotes is folded with the aid of highly conserved histone proteins to form nucleosome fibers, which further condense via interactions with histones and non-histone chromatin proteins. Dinoflagellate chromatin is unique among eukaryotes, as their chromosomes lack the histones and remain condensed throughout the cell cycle. Here, we report the results of electron microscopy study of chromatin elements inside the chromosomes of potentially toxic planktonic dinoflagellate Prorocentrum minimum. We found that chromatin fibers inside the condensed chromosomes of P. minimum form not only arch-like structures, that were repeatedly described for various dinoflagellate species, but also rosette-like complexes with chromatin fibers radiating from its electron-dense center. The effects of histone loss in the evolution of dinoflagellates are discussed within the frames of the hierarchical chromatin folding paradigm.

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Section: Introductionmentioning

confidence: 99%

Ultrastructural organization of the chromatin elements in chromosomes of the dinoflagellate Prorocentrum minimum

Golyshev¹,

Berdieva²,

Musinova³

et al. 2018

Protistology

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“…Histones are replaced by other basic proteins, e.g. histone-like proteins derived from bacteria and dinoflagellates/viral nucleoproteins (DVNPs) derived from viruses 20,61,63 .…”

Section: Mammalian Genomes Also Display Domainal Features (Topologicamentioning

confidence: 99%

Chromosome-scale assembly of the coral endosymbiontSymbiodinium microadriaticumgenome provides insight into the unique biology of dinoflagellate chromosomes

Nand

Salazar

et al. 2020

Preprint

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AbstractDinoflagellates are major primary producers in the world’s oceans, the cause of harmful algal blooms, and endosymbionts of marine invertebrates. Much remains to be understood about their biology including their peculiar crystalline chromosomes. Here we used Hi-C to order short read-based sub-scaffolds into 94 chromosome-scale scaffolds of the genome of the coral endosymbiont Symbiodinium microadriaticum. Hi-C data show that chromosomes are folded as linear rods within which loci separated by up to several Mb are highly packed. Each chromosome is composed of a series of structural domains separated by boundaries. Genes are enriched towards the ends of chromosomes and are arranged in unidirectional blocks that alternate between top and bottom strands. Strikingly, the boundaries of chromosomal domains are positioned at sites where transcription of two gene blocks converges, indicating a correlation between gene orientation, transcription and chromosome folding. Some chromosomes are enriched for genes involved in specific biological processes (e.g., photosynthesis, and nitrogen-cycling), and functionally related genes tend to co-occur at adjacent sites in the genome. All chromosomes contain several repeated segments that are enriched in mobile elements. The assembly of the S. microadriaticum genome and initial description of its genetic and spatial organization provide a foundation for deeper exploration of the extraordinary biology of dinoflagellates and their chromosomes.

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“…As widely distributed primary producers, essential coral endosymbionts, and the greatest contributors of harmful algal blooms and biotoxins in the ocean, dinoflagellates are a diverse group of unicellular protists with great ecological significance, evolutionary uniqueness, and numerous cytological and genomic peculiarities. While early diverging lineages share more similarities to typical eukaryotes, later diverging (namely "core") dinoflagellates have immense and permanently condensed genomes with many chromosomes [1][2][3]; their genomes have a low protein-DNA ratio and histones are functionally replaced with dinoflagellate viral nuclear proteins (DVNPs) [4,5]; there are high numbers of repetitive non-coding regions and gene copies-in some species, up to~5000 copies-organized in tandem arrays [6,7]; only 5-30% of their genes are transcriptionally regulated [7][8][9], with microRNAs appearing to be the major gene regulating mechanism [10]; and they have undergone extreme plastid evolution, transferring a massive quantity of plastid genes to the nucleus in most of the photoautotrophic species [11][12][13]. However, the molecular underpinnings of these unusual features remain elusive.…”

Section: Introductionmentioning

confidence: 99%

Nuclear Gene Transformation in the Dinoflagellate Oxyrrhis marina

2020

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The lack of a robust gene transformation tool that allows proper expression of foreign genes and functional testing for the vast number of nuclear genes in dinoflagellates has greatly hampered our understanding of the fundamental biology in this ecologically important and evolutionarily unique lineage of microeukaryotes. Here, we report the development of a dinoflagellate expression vector containing various DNA elements from phylogenetically separate dinoflagellate lineages, an electroporation protocol, and successful expression of introduced genes in an early branching dinoflagellate, Oxyrrhis marina. This protocol, involving the use of Lonza’s Nucleofector and a codon-optimized antibiotic resistance gene, has been successfully used to produce consistent results in several independent experiments for O. marina. It is anticipated that this protocol will be adaptable for other dinoflagellates and will allow characterization of many novel dinoflagellate genes.

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Viral proteins as a potential driver of histone depletion in dinoflagellates

Cited by 46 publications

References 69 publications

Ultrastructural organization of the chromatin elements in chromosomes of the dinoflagellate Prorocentrum minimum

Ultrastructural organization of the chromatin elements in chromosomes of the dinoflagellate Prorocentrum minimum

Chromosome-scale assembly of the coral endosymbiontSymbiodinium microadriaticumgenome provides insight into the unique biology of dinoflagellate chromosomes

Nuclear Gene Transformation in the Dinoflagellate Oxyrrhis marina

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