Electron microscopy of the chromosomes of dinoflagellates in situ: confirmation of Bouligand's liquid crystal hypothesis

Gautier, A; Michel-Salamin, L.; Tosi-Couture, E.; McDowall, Alasdair W.; Dubochet, Jacques

doi:10.1016/s0889-1605(86)80003-9

Cited by 58 publications

(51 citation statements)

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“…By observing ultrathin sections of dinoflagellate chromosomes using high-resolution transmission electron microscopy (TEM), plectonemic structures with nested series of arches and bands were seen (8,12,39). This architecture resembles the molecular architecture of thin-section TEM in vitro cholesteric liquid crystals (12,39,43).Knowledge of the condensation process would not only be of interest in terms of eukaryotic genome packaging, but would also provide new insights for the use of DNA as building blocks for nanotechnology applications. Self-assembly is increasingly understood to be of great significance in the regulation of various macromolecules in the crowded environment of living cells (7,15,16,35,36).…”

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confidence: 92%

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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“…9 представлен вид сечения хромосомы Amphidinium elegans под углом к оси спиральной структуры. Впоследствии интен-сивные работы в этом направлении проведены и проанализированы в работах авторов [47][48][49][50][51], использовавших разные приемы фиксации хромосом.…”

Section: компьютерное моделированиеunclassified

“…Более того, на рис. 11 представлена теоретическая модель хромосомы этих микроорганизмов, предложенная в работе [53], и виды ее сечений, тщательно проанали-зированные в работах [54,55]. Исходя из этой модели, можно утверждать, что только при организации хромосомы в виде слоев из фрагментов молекулы ДНК, поворачивающихся в пространстве на определенный угол, можно наблюдать на определенных срезах этих хромосом дугообразные структуры [56].…”

Section: рис 9 электронная микрофотография сечения хромосомы динофлunclassified

“…Однако вопрос о реальности «квази-нематических слоев» и их роли при образовании холестерической структуры полимеров, в том числе и ДНК, остается предметом дискуссий [8,20,21,[36][37][38][39][40]. При этом конкретный ответ на  вопрос о том, какова природа упаковки молекул ДНК в холестерической фазе, по сравнению с закрученной нематической фазой коротких молекул, практически отсутствует [41].…”

Section: Introductionunclassified

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About Spatial Organization of Double-Stranded DNA Molecules in Cholesteric Liquid-Crystalline Phase

Yevdokimov¹,

Skuridin²,

Salyanov³

et al. 2016

Liq. Cryst. and their Appl.

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“…Being a helix itself, DNA, when condensed, forms a range of distinct liquid crystalline phases [15]. The DNA of dinoflagellates, which is much longer than a human chromosome, organizes into a cholesteric liquid crystal [16,17]. Human mitotic chromosomes also appear to have liquid crystalline features when viewed under the microscope [18].…”

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Shape Transitions and Chiral Symmetry Breaking in the Energy Landscape of the Mitotic Chromosome

Zhang

Wolynes

2015

Preprint

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We derive an unbiased information theoretic energy landscape for chromosomes at metaphase using a maximum entropy approach that accurately reproduces the details of the experimentally measured pair-wise contact probabilities between genomic loci. Dynamical simulations using this landscape lead to cylindrical, helically twisted structures reflecting liquid crystalline order. These structures are similar to those arising from a generic ideal homogenized chromosome energy landscape. The helical twist can be either right or left handed so chiral symmetry is broken spontaneously. The ideal chromosome landscape when augmented by interactions like those leading to topologically associating domain (TAD) formation in the interphase chromosome reproduces these behaviors. The phase diagram of this landscape shows the helical fiber order and the cylindrical shape persist at temperatures above the onset of chiral symmetry breaking which is limited by the TAD interaction strength.When cells divide, their chromosomes dramatically condense before forming a pair of sister chromatids that exhibits the famous X shape of the mitotic phase [1]. Microscopy reveals the overall morphology of the mitotic chromatin, but its internal structure remains controversial [2][3][4]. A complete understanding of chromosomal organization is challenging since the condensation of the chromosome into its dense mitotic form permits many different orderings and phase transitions. Owing to the large scale of the chromosome, we also can expect interesting non-equilibrium glassy dynamics and possible kinetic control of structure formation [5][6][7][8][9][10][11][12][13].Structural models of the mitotic chromosome have been proposed, including the radial loop model [4], the chromatin network model [14] and the hierarchical folding model [3]. These models often highlight the biologically specific role of protein molecules but the intrinsic properties of the DNA as a long highly helical molecule must also be at work. Being a helix itself, DNA, when condensed, forms a range of distinct liquid crystalline phases [15]. The DNA of dinoflagellates, which is much longer than a human chromosome, organizes into a cholesteric liquid crystal [16,17]. Human mitotic chromosomes also appear to have liquid crystalline features when viewed under the microscope [18]. Chiral symmetry appears to be broken: the daughter chromatids formed on cell division seem to be of opposite handedness in microscope images. In this letter, we use inverse statistical mechanics to infer from high resolution chromosome conformation capture data two energy landscapes that yield ensembles of three-dimensional (3D) structures for the mitotic chromosome. One of these energy landscapes is constructed to be agnostic as to the origin of the fluctuating order, while the other is based on a model constructed by adding to an ideal homogenized chromosome landscape that leads to helical order, sequence dependent interactions that give rise to topologically associating domains (TADs) in the interphase chromo...

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Electron microscopy of the chromosomes of dinoflagellates in situ: confirmation of Bouligand's liquid crystal hypothesis

Cited by 58 publications

References 29 publications

Birefringence and DNA Condensation of Liquid Crystalline Chromosomes

Birefringence and DNA Condensation of Liquid Crystalline Chromosomes

About Spatial Organization of Double-Stranded DNA Molecules in Cholesteric Liquid-Crystalline Phase

Shape Transitions and Chiral Symmetry Breaking in the Energy Landscape of the Mitotic Chromosome

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