Telomeric DNA localization on dinoflagellate chromosomes: structural and evolutionary implications

Alverca, Elsa; Cuadrado, Ángeles; Jouve, N.; França, Susana; Espina, Susana Moreno Dı́az de la

doi:10.1159/000098191

Cited by 21 publications

(20 citation statements)

References 97 publications

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“…nd nondigested DNA, M DNA size marker (low-range PFG Marker, NEB) chromatin does not contradict their eukaryotic character. Moreover, the presence of telomeres and telomerase points to the linear character of dinoflagellate chromosomes, in accordance with previous evidence showing telomere-like signals in FISH experiments using the Arabidopsis-type telomeric probe (Alverca et al 2007). In addition to Fig.…”

Section: Discussionsupporting

confidence: 91%

“…The two species also represent very different mode of lives: K. papilionacea is an athecate autotrophic species, whereas C. cohnii is a thecat heterotrophic dinoflagellate. The Arabidopsis-type telomere repeat seems to be a common feature even among evolutionarily distant dinoflagellate genera as it is present in Prorocentrum micans and Amphidinium arterae (Alverca et al 2007) as well as in K. papilionacea and C. cohnii (this study).…”

Section: Discussionmentioning

confidence: 63%

“…These observations suggest that ends of dinoflagellate chromosomes have novel properties and additional functions in chromosome segregation. Although in situ hybridisation has confirmed the presence of eukaryotic telomeric sequences on dinoflagellate chromosomes (Alverca et al 2007), a detailed characterisation of canonical telomere structures has not yet been performed, and evidence of active telomerase is still lacking. In this paper, we demonstrate the presence of plant-type telomeric tracts at the ends of dinoflagellate chromosomes which are tens of kilobases long.…”

Section: Introductionmentioning

confidence: 99%

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Telomere maintenance in liquid crystalline chromosomes of dinoflagellates

et al. 2010

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The organisation of dinoflagellate chromosomes is exceptional among eukaryotes. Their genomes are the largest in the Eukarya domain, chromosomes lack histones and may exist in liquid crystalline state. Therefore, the study of the structural and functional properties of dinoflagellate chromosomes is of high interest. In this work, we have analysed the telomeres and telomerase in two Dinoflagellata species, Karenia papilionacea and Crypthecodinium cohnii. Active telomerase, synthesising exclusively Arabidopsis-type telomere sequences, was detected in cell extracts. The terminal position of TTTAGGG repeats was determined by in situ hybridisation and BAL31 digestion methods and provides evidence for the linear characteristic of dinoflagellate chromosomes. The length of telomeric tracts, 25-80 kb, is the largest among unicellular eukaryotic organisms to date. Both the presence of long arrays of perfect telomeric repeats at the ends of dinoflagellate chromosomes and the existence of active telomerase as the primary tool for their high-fidelity maintenance demonstrate the general importance of these structures throughout eukaryotes. We conclude that whilst chromosomes of dinoflagellates are unique in many aspects of their structure and composition, their telomere maintenance follows the most common scenario.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 63%

Section: Introductionmentioning

confidence: 99%

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Telomere maintenance in liquid crystalline chromosomes of dinoflagellates

et al. 2010

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“…Another group that often has giant nuclei and a proteinaceous lamina are the dinoflagellates. This coupled with the evolution of an extranuclear spindle with kinetochores embedded in the nuclear envelope probably allowed peridinean dinoflagellates to dispense entirely with heterochromatin as a nuclear skeleton and even largely also with histones, which are absent from the majority of their DNA [296] which is neutralized by divalent cations instead [297] and sparse bacterial-type DNA-binding proteins [298,299]; only one standard histone is known, perhaps involved in double-strand break repair [300]; the loss of histones entailed radically altered transcription factors that bind to TTTT instead of TATA boxes, but dinoflagellates retain standard telomeres associated with the nuclear envelope [301] and relatively normal spliceosomal intron splicing [302]. …”

Section: Results: the Origin Of Mitosis And The Nucleusmentioning

confidence: 99%

Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution

2010

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BackgroundThe transition from prokaryotes to eukaryotes was the most radical change in cell organisation since life began, with the largest ever burst of gene duplication and novelty. According to the coevolutionary theory of eukaryote origins, the fundamental innovations were the concerted origins of the endomembrane system and cytoskeleton, subsequently recruited to form the cell nucleus and coevolving mitotic apparatus, with numerous genetic eukaryotic novelties inevitable consequences of this compartmentation and novel DNA segregation mechanism. Physical and mutational mechanisms of origin of the nucleus are seldom considered beyond the long-standing assumption that it involved wrapping pre-existing endomembranes around chromatin. Discussions on the origin of sex typically overlook its association with protozoan entry into dormant walled cysts and the likely simultaneous coevolutionary, not sequential, origin of mitosis and meiosis.ResultsI elucidate nuclear and mitotic coevolution, explaining the origins of dicer and small centromeric RNAs for positionally controlling centromeric heterochromatin, and how 27 major features of the cell nucleus evolved in four logical stages, making both mechanisms and selective advantages explicit: two initial stages (origin of 30 nm chromatin fibres, enabling DNA compaction; and firmer attachment of endomembranes to heterochromatin) protected DNA and nascent RNA from shearing by novel molecular motors mediating vesicle transport, division, and cytoplasmic motility. Then octagonal nuclear pore complexes (NPCs) arguably evolved from COPII coated vesicle proteins trapped in clumps by Ran GTPase-mediated cisternal fusion that generated the fenestrated nuclear envelope, preventing lethal complete cisternal fusion, and allowing passive protein and RNA exchange. Finally, plugging NPC lumens by an FG-nucleoporin meshwork and adopting karyopherins for nucleocytoplasmic exchange conferred compartmentation advantages. These successive changes took place in naked growing cells, probably as indirect consequences of the origin of phagotrophy. The first eukaryote had 1-2 cilia and also walled resting cysts; I outline how encystation may have promoted the origin of meiotic sex. I also explain why many alternative ideas are inadequate.ConclusionNuclear pore complexes are evolutionary chimaeras of endomembrane- and mitosis-related chromatin-associated proteins. The keys to understanding eukaryogenesis are a proper phylogenetic context and understanding organelle coevolution: how innovations in one cell component caused repercussions on others.ReviewersThis article was reviewed by Anthony Poole, Gáspár Jékely and Eugene Koonin.

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“…Apicomplexa species use three different motifs [4][5][6], and ciliates use two [4,7]. Dinoflagellates use T 3 AG 3 [8], similar to plants and green algae, while diatoms use T 2 AG 3 [9], similar to unikonts. Photosynthetic species in the Chromalveolates are derived from the engulfment of a red alga.…”

Section: Chromalveolatamentioning

confidence: 99%