Ultrastructural and Biochemical Nuclear Aspects of Eukaryote Classification: Independent Evolution of the Dinoflagellates as a Sister Group of the Actual Eukaryotes?

Herzog, Michel; Boletzky, Sigurd von; Soyer, Marie-Odile

doi:10.1007/978-94-009-6398-6_5

Cited by 9 publications

(14 citation statements)

References 43 publications

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“…The dinoflagellates, counterintuitively, have the largest known genomes among all living organisms, with a DNA content per genome ranging from 1.5 pg to 200 pg per haploid cell (19,25,43). An extraordinarily high level of DNA condensation must be attained in order to sequester these genomes within the bounds of the nucleus, and this is achieved through the form of LCCs.…”

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confidence: 99%

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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Birefringence and DNA Condensation of Liquid Crystalline Chromosomes

et al. 2010

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“…Geological records and molecular phylogenies suggest that: (1) Cyanobacteria probably appeared on Earth about 2500 million years ago; (2)Dinophyceae and ancient Prasinophyceae, about 1500 million years ago; and (3) the filamentous Conjugatophyceae and pennate Bacillariophyceae, about 500000 years ago (Margulis & Schwartz, 1982;Dodge, 1983;Herzog et al, 1984;Gunderson et al, 1987;Baroin et al, 1988;Lee, 1989;Lenaers et al, 1989;Knoll, 1992;van den Hoek, 1993). Assuming an average increase in a day's duration of 1 h every 200 million years (see "Introduction"), a day may have lasted 11.5, 16.5, or 21.5 h at the first appearance of groups (1), (2), or (3).…”

Section: Discussionmentioning

confidence: 99%

The influence of the slowing of Earth's rotation: A hypothesis to explain cell division synchrony under different day duration in earlier and later evolved unicellular algae

Costas

González-Gil

López‐Rodas

et al. 1996

Helgolander Meeresunters

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Every year the Earth's rotation period is reduced, mainly due to the tidal drag of the moon. The length of day increases continuously by about 1 h every 200 million years. The period of rotation around the Sun remains constant; hence, the length of the year remains constant, so years acquire progressively fewer days. Many unicellular algae show rhythmicity in their cell division cycle. If primitive algae evolved under a shorter day duration, then it is possible that the earlyevolved algae had to synchronize their cell division cycle to shorter lengths of day than did laterevolved algae. We tested this hypothesis by growing Cyanobacteria, Dinophyceae, Prasinophyceae, Baciltariophyceae and Conjugatophyceae (evolutionary appearance probably in this order)

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“…This behavior could be attributed to the very low DNA/protein ratio, to the absence of certain proteins and nucleosomes and the substitution of more than 60 % of its thymine by 5-hydroxy-methyluracil (Herzog et al, 1984), but mainly to the very peculiar spatial organization of dinoflagellate chromatin and its permanent condensation.…”

Section: Specific Nuclear Featuresmentioning

confidence: 99%

“…Dodge (1965Dodge ( , 1966 and Loeblich (1976) proposed that dinoflagellates could be intermediate between prokaryotes and eukaryotes, and that dinoflagellates should be described as mesokaryotes. Herzog et al (1984), after a detailed analysis of both structural and functional features of the dinoflagellate nucleus and exhaustive comparison to those commonly found in prokaryotes and eukaryotes, suggested that dinoflagellate protists while showing ancestral characters also found in prokaryotes are above prokaryotes but below other eukaryotes. They proposed an independent evolution of dinoflagellates as a sister group of actual eukaryotes.…”

Section: Insight Into Evolutionary Hypothesismentioning

confidence: 99%

Architecture and evolution of dinoflagellate chromosomes: an enigmatic origin

Costas

Goyanes²

2005

Cytogenet Genome Res

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Dinoflagellates are a highly diversified group of unicellular protists that present fascinating nuclear features which have intrigued researchers for many years. As examples, a dense nuclear matrix accommodates permanently condensed chromosomes that are composed of fibers organized without histones and nucleosomes in stacked rows of parallel nested arches. The macromolecular chromosome structure corresponds to cholesteric liquid crystals with a constant left-handed twist. RNA acts to maintain the chromosome structure. Whole mounted chromosomes have a left-handed screw-like configuration with coils which progressively increase their pitch. This helical arrangement seems to be the result of a couple of narrow strands coiling together. Chromosomes do not show Q, G and C banding patterns. However, a roughly spherical differentiated upper end (primitive kinetochore?) and two differentiated coiling regions, the upper one composed of two to three coils where a couple of sister strands run together and parallel to each other, and the lower one where sister strands run out of phase by 180° angular difference along the immediate next turns, can be distinguished. The chromosome segregation into two daughter chromatids begins at the telomere that attaches to the nuclear envelope, follows along the chromosome axis constituting first a Y-shaped and afterwards a V-shaped chromosome, which packs the newly synthesized DNA inside the “old” chromosome. Dividing chromosomes remain highly condensed, and the diameters of the new chromatids and the undivided chromosome are similar, but the number of arches is twice as large in G1 as in G2. The nuclear envelope remains through the cell cycle and shows spindle fibers, which penetrate intranuclear cytoplasmic channels during mitosis constituting an extra nuclear spindle. These and other cytogenetic features suggest that dinoflagellates are a group of enigmatic protists, unique and different from the usual eukaryotes. In contrast, DNA sequence studies propose that dinoflagellates are true eukaryotes, closely related to Apicomplexa, and ciliates (Alveolata), suggesting that the unusual features of chromosome and nuclear organization are not primitive but derived characters. Nevertheless, dinoflagellates have reached enigmatic specific nuclear and chromosome solutions, extremely far from those of other living beings.

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Ultrastructural and Biochemical Nuclear Aspects of Eukaryote Classification: Independent Evolution of the Dinoflagellates as a Sister Group of the Actual Eukaryotes?

Cited by 9 publications

References 43 publications

Birefringence and DNA Condensation of Liquid Crystalline Chromosomes

Birefringence and DNA Condensation of Liquid Crystalline Chromosomes

The influence of the slowing of Earth's rotation: A hypothesis to explain cell division synchrony under different day duration in earlier and later evolved unicellular algae

Architecture and evolution of dinoflagellate chromosomes: an enigmatic origin

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