Organization of the genome and gene expression in a nuclear environment lacking histones and nucleosomes: the amazing dinoflagellates

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

doi:10.1016/j.ejcb.2005.01.002

Cited by 74 publications

(57 citation statements)

References 97 publications

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“…For example, does the mode of prokaryotic genome evolution apply to planktomycetes that house their nucleoid within the membranous compartment (2)? Dinoflagellates, the eukaryotic protists that, like prokaryotes, maintain condensed chromosomes throughout the interphase and lack histone-based nucleosome packaging of DNA (172), could be predicted to have prokaryote-like fast DNA replication and progressive chromosome segregation (whatever its mechanisms turn out to be). Spectacular pictures of mitosis in dinoflagellates (the so-called "dinomitosis") are indeed highly suggestive (173).…”

Section: Resultsmentioning

confidence: 99%

The Precarious Prokaryotic Chromosome

Kuzminov

2014

J Bacteriol

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Evolutionary selection for optimal genome preservation, replication, and expression should yield similar chromosome organizations in any type of cells. And yet, the chromosome organization is surprisingly different between eukaryotes and prokaryotes. The nuclear versus cytoplasmic accommodation of genetic material accounts for the distinct eukaryotic and prokaryotic modes of genome evolution, but it falls short of explaining the differences in the chromosome organization. I propose that the two distinct ways to organize chromosomes are driven by the differences between the global-consecutive chromosome cycle of eukaryotes and the local-concurrent chromosome cycle of prokaryotes. Specifically, progressive chromosome segregation in prokaryotes demands a single duplicon per chromosome, while other "precarious" features of the prokaryotic chromosomes can be viewed as compensations for this severe restriction.

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Section: Resultsmentioning

confidence: 99%

The Precarious Prokaryotic Chromosome

Kuzminov

2014

J Bacteriol

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“…Linker histones in the protein configuration of Metazoans, appear first in late protists [84]. Dinoflagellates have secondarily lost their histones and do not form nucleosomes [115]. Their major ChAP, HCC, is most closely related to bacterial HU proteins [188].…”

Section: The Architecture Of Chromatinmentioning

confidence: 99%

Innovation in gene regulation: The case of chromatin computation

Prohaska

Stadler

Krakauer

2010

Journal of Theoretical Biology

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Chromatin regulation is understood to be one of the fundamental modes of gene regulation in eukaryotic cells. We argue that the basic proteins that determine the chromatin architecture constitute an evolutionary ancient layer of transcriptional regulation common to all three domains of life. We explore phylogenetically, sources of innovation in chromatin regulation, focusing on protein domains related to chromatin structure and function, demonstrating a step-wise increase of complexity in chromatin regulation. Building upon the highly conserved use of variants of chromosomal architectural proteins to distinguish chromosomal states, Eukarya secondarily acquired mechanisms for "writing" chemical modifications onto chromatin that constitute persistent signals. The acquisition of reader domains enabled decoding of these complex, signal combinations and a decoupling of the signal from immediate biochemical effects. We show how the coupling of reading and writing, which is most prevalent in crown-group Eukarya, could have converted chromatin into a powerful computational device capable of storing and processing more information than pure cis-regulatory networks.Key words: Chromatin, gene regulation, evolution Summary of Findings and Evolutionary HypothesisGene regulation in extant organisms is a complex adaptive system making use of a diversity of mechanisms to ensure that proteins and complementary macromolecular components are produced and maintained at functional levels in variable environments.In this contribution we focus on one key regulatory subsystem of the cell: chromatin regulation. We argue that chromatin functioned as general regulator of transcription in the primordial nucleus, and that a series of key molecular innovations has significantly expanded the regulatory scope of the cell. In this section we summarize the key empirical results of the paper. Sections 2 through 6 provide the empirical support for these claims. In section 7, we formulate an evolutionary Email addresses: sonja@bioinf.uni-leipzig.de (Sonja J. Prohaska), studla@bioinf.uni-leipzig.de (Peter F. Stadler), krakauer@santafe.edu (David C. Krakauer) hypothesis that seeks to explain our findings in terms of the evolution of proto-genetic regulation. We then interpret this evolutionary sequence in terms of increasing computational power by locating key stages of the evolutionary sequence within a formal model of computation. Since sections 2-6 are primarily concerned with presenting evidence, those interested in the conceptual development of the argument can focus on sections 7 and 8.Two variants of Chromosomal Architectural Proteins (ChAPs) are sufficient to define binary genomic, and potentially phenotypic, states. We show how extensions to this binary system lead to potential distinctions among an increasing number of genomic states, culminating in forms of control localized to specific sites in the genome, as illustrated for example by extant mammalian histone variants capable of differential expression and/or localization to r...

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“…Relatively large amount of DNA Spector, 1984 Unusual sterols Withers, 1983 Hypermethylated DNA Ten Lohuis and Miller, 1998 Hydroxymethyluracil substituted for thymine Rae, 1976 Most are uninucleates, but some binucleates exist Rizzo, 2003 Permanently condensed chromosomes Rizzo, 2003 Lack histones and nucleosomes Moreno Diaz et al, 2005 Possess a vegetative haploid nuclear phase Santos and Coffroth, 2003 Typical eukaryotic nuclear envelope, but it remains intact during mitosis Bhaud et al, 2000 Typical eukaryotic 9 + 2 axoneme flagella Maruyama, 1985 Membrane-bound organelles (endoplasmic reticula, Golgi apparatus, mitochondria, and chloroplasts) Spector, 1984 Percentages of repetitive DNA (50-60%) consistent with higher eukaryotic genomes Moreno Diaz et al, 2005 Typical eukaryotic cell cycle Moreno Diaz et al, 2005 Heavy (28S) and light (17S) rRNA that is structurally similar to higher eukaryotes Herzog and Maroteaux, 1986 Lack the TATA-box (typical eukaryotic promoter) Guillebault et al, 2002 …”

Section: Table Imentioning

confidence: 99%