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The Journal of Eukaryotic Microbiology Sep 2022Ciliates are defined by the presence of dimorphic nuclei as they have both a somatic macronucleus and germline micronucleus within each individual cell. The size and... (Review)
Review
Ciliates are defined by the presence of dimorphic nuclei as they have both a somatic macronucleus and germline micronucleus within each individual cell. The size and structure of both germline micronuclei and somatic macronuclei vary tremendously among ciliates. Except just after conjugation (i.e. the nuclear exchange in their life cycle), the germline micronucleus is transcriptionally inactive and contains canonical chromosomes that will be inherited between generations. In contrast, the transcriptionally active macronucleus contains chromosomes that vary in size in different classes of ciliates, with some lineages having extensively fragmented gene-sized somatic chromosomes while others contain longer multigene chromosomes. Here, we describe the variation in somatic macronuclear architecture in lineages sampled across the ciliate tree of life, specifically focusing on lineages with extensively fragmented chromosomes (e.g. the classes Phyllopharyngea and Spirotrichea). Further, we synthesize information from the literature on the development of ciliate macronuclei, focusing on changes in nuclear architecture throughout life cycles. These data highlight the tremendous diversity among ciliate nuclear cycles, extend our understanding of patterns of genome evolution, and provide insight into different germline and somatic nuclear features (e.g. nuclear structure and development) among eukaryotes.
Topics: Animals; Cell Nucleus; Ciliophora; Life Cycle Stages; Macronucleus
PubMed: 35178799
DOI: 10.1111/jeu.12898 -
European Journal of Protistology Oct 2017Epigenetics, a term with many meanings, can be broadly defined as the study of dynamic states of the genome. Ciliates, a clade of unicellular eukaryotes, can teach us... (Review)
Review
Epigenetics, a term with many meanings, can be broadly defined as the study of dynamic states of the genome. Ciliates, a clade of unicellular eukaryotes, can teach us about the intersection of epigenetics and evolution due to the advantages of working with cultivable ciliate lineages, plus their tendency to express extreme phenotypes such as heritable doublet morphology. Moreover, ciliates provide a powerful model for studying epigenetics given the presence of dimorphic nuclei - a somatic macronucleus and germline micronucleus - within each cell. Here, we exemplify the power of studying ciliates to learn about epigenetic phenomena. We highlight "classical" examples from morphology and physiology including cortical inheritance, mating type determination, and serotype expression. In addition, we detail molecular studies of epigenetic phenomena, including: DNA elimination; alternative processing and unscrambling; and copy number determination. Based on the implications of these studies, we discuss epigenetics as a possible functional mechanism for rapid speciation in ciliates.
Topics: Ciliophora; Epigenesis, Genetic; Genetic Speciation
PubMed: 28689743
DOI: 10.1016/j.ejop.2017.05.004 -
Microbiological Reviews Jun 1994Ciliates contain two types of nuclei: a micronucleus and a macronucleus. The micronucleus serves as the germ line nucleus but does not express its genes. The... (Comparative Study)
Comparative Study Review
Ciliates contain two types of nuclei: a micronucleus and a macronucleus. The micronucleus serves as the germ line nucleus but does not express its genes. The macronucleus provides the nuclear RNA for vegetative growth. Mating cells exchange haploid micronuclei, and a new macronucleus develops from a new diploid micronucleus. The old macronucleus is destroyed. This conversion consists of amplification, elimination, fragmentation, and splicing of DNA sequences on a massive scale. Fragmentation produces subchromosomal molecules in Tetrahymena and Paramecium cells and much smaller, gene-sized molecules in hypotrichous ciliates to which telomere sequences are added. These molecules are then amplified, some to higher copy numbers than others. rDNA is differentially amplified to thousands of copies per macronucleus. Eliminated sequences include transposonlike elements and sequences called internal eliminated sequences that interrupt gene coding regions in the micronuclear genome. Some, perhaps all, of these are excised as circular molecules and destroyed. In at least some hypotrichs, segments of some micronuclear genes are scrambled in a nonfunctional order and are recorded during macronuclear development. Vegetatively growing ciliates appear to possess a mechanism for adjusting copy numbers of individual genes, which corrects gene imbalances resulting from random distribution of DNA molecules during amitosis of the macronucleus. Other distinctive features of ciliate DNA include an altered use of the conventional stop codons.
Topics: Animals; Base Composition; Base Sequence; Cell Nucleus; Chromatin; Chromosomes; Ciliophora; Codon; DNA Replication; DNA Transposable Elements; DNA, Protozoan; Genes, Protozoan; Genetic Code; Molecular Sequence Data; Phylogeny; Tetrahymena
PubMed: 8078435
DOI: 10.1128/mr.58.2.233-267.1994 -
Essays in Biochemistry Sep 2010Ciliated protozoa undergo extensive DNA rearrangements, including DNA elimination, chromosome breakage and DNA unscrambling, when the germline micronucleus produces the... (Review)
Review
Ciliated protozoa undergo extensive DNA rearrangements, including DNA elimination, chromosome breakage and DNA unscrambling, when the germline micronucleus produces the new macronucleus during sexual reproduction. It has long been known that many of these events are epigenetically controlled by DNA sequences of the parental macronuclear genome. Recent studies in some model ciliates have revealed that these epigenetic regulations are mediated by non-coding RNAs. DNA elimination in Paramecium and Tetrahymena is regulated by small RNAs that are produced and operated by an RNAi (RNA interference)-related mechanism. It has been proposed that the small RNAs from the micronuclear genome can be used to identify eliminated DNAs by whole-genome comparison of the parental macronucleus and the micronucleus. In contrast, DNA unscrambling in Oxytricha is guided by long non-coding RNAs that are produced from the somatic parental macronuclear genome. These RNAs are proposed to act as templates for the direct unscrambling events that occur in the developing macronucleus. The possible evolutionary benefits of these RNA-directed epigenetic regulations of DNA rearrangement in ciliates are discussed in the present chapter.
Topics: Animals; DNA; Epigenesis, Genetic; Evolution, Molecular; Genome, Protozoan; RNA
PubMed: 20822488
DOI: 10.1042/bse0480089 -
Microbiology Spectrum Dec 2014Programmed genome rearrangements in the ciliate Paramecium provide a nice illustration of the impact of transposons on genome evolution and plasticity. During the sexual... (Review)
Review
Programmed genome rearrangements in the ciliate Paramecium provide a nice illustration of the impact of transposons on genome evolution and plasticity. During the sexual cycle, development of the somatic macronucleus involves elimination of ∼30% of the germline genome, including repeated DNA (e.g., transposons) and ∼45,000 single-copy internal eliminated sequences (IES). IES excision is a precise cut-and-close process, in which double-stranded DNA cleavage at IES ends depends on PiggyMac, a domesticated piggyBac transposase. Genome-wide analysis has revealed that at least a fraction of IESs originate from Tc/mariner transposons unrelated to piggyBac. Moreover, genomic sequences with no transposon origin, such as gene promoters, can be excised reproducibly as IESs, indicating that genome rearrangements contribute to the control of gene expression. How the system has evolved to allow elimination of DNA sequences with no recognizable conserved motif has been the subject of extensive research during the past two decades. Increasing evidence has accumulated for the participation of noncoding RNAs in epigenetic control of elimination for a subset of IESs, and in trans-generational inheritance of alternative rearrangement patterns. This chapter summarizes our current knowledge of the structure of the germline and somatic genomes for the model species Paramecium tetraurelia, and describes the DNA cleavage and repair factors that constitute the IES excision machinery. We present an overview of the role of specialized RNA interference machineries and their associated noncoding RNAs in the control of DNA elimination. Finally, we discuss how RNA-dependent modification and/or remodeling of chromatin may guide PiggyMac to its cognate cleavage sites.
Topics: DNA, Protozoan; Gene Rearrangement; Paramecium tetraurelia; RNA, Untranslated; Recombination, Genetic; Transposases
PubMed: 26104450
DOI: 10.1128/microbiolspec.MDNA3-0035-2014 -
The International Journal of... Feb 1996In the course of macronuclear development of the hypotrichous ciliates all genetic information not required for normal growth of the cell is removed from the new... (Review)
Review
In the course of macronuclear development of the hypotrichous ciliates all genetic information not required for normal growth of the cell is removed from the new macronucleus. This differentiation process involves DNA-splicing, excision of transposons, DNA-fragmentation, selective gene amplification and telomere addition. Since many of the processes observed during macronuclear development, such as DNA-transposition, DNA-rearrangement or selective DNA-amplification, may occur in differentiating cells of higher organisms, this biological system provides an unusual opportunity to study the ways in which DNA-sequences can be manipulated in a differentiating cell.
Topics: Animals; Cell Nucleus; Ciliophora; DNA Fragmentation; DNA Transposable Elements; DNA, Protozoan
PubMed: 8735923
DOI: No ID Found -
The Journal of Eukaryotic Microbiology Sep 2022This review addresses nine areas of knowledge revealed by micromanipulations performed with Paramecium. Microinjection has shown that sexual maturation and senescence of... (Review)
Review
This review addresses nine areas of knowledge revealed by micromanipulations performed with Paramecium. Microinjection has shown that sexual maturation and senescence of Paramecium caudatum is a programmed process conducted by a specific gene and its product protein. In Paramecium tetraurelia, autogamy was revealed to depend on the number of DNA syntheses rather than the number of cell divisions in clonal aging. The cytoplasmic complementarity test established that microinjection of wild-type cytoplasm can correct genetic defects of mutants. The concept of complementarity together with protein chemistry revealed compounds that control membrane excitability. In non-Mendelian inheritance, noncoding small RNAs made from the parental micronucleus regulate the rearrangement of the progeny's macronuclear DNA. The macronucleus has the potential to be used as a factory for genetic engineering. The development and differentiation of progeny's nuclei in mating pairs are controlled by the parental macronucleus. The chemical reaction processes associated with exocytosis have been revealed by microinjection of various enzymes and antibodies. Using the fusion gene of histone H2B and yellow-fluorescence protein, it was revealed that the fusion gene-mRNA is transferred between cells during mating. Experiments with endosymbiotic bacteria and the host shed light on the conditions needed to establish sustainable symbiotic relationships.
Topics: Cytoplasm; Macronucleus; Micromanipulation; Paramecium; Paramecium tetraurelia
PubMed: 35318763
DOI: 10.1111/jeu.12909 -
European Journal of Protistology Oct 2017Genome structure and nuclear organization have been intensely studied in model ciliates such as Tetrahymena and Paramecium, yet few studies have focused on nuclear... (Review)
Review
Genome structure and nuclear organization have been intensely studied in model ciliates such as Tetrahymena and Paramecium, yet few studies have focused on nuclear features of other ciliate clades including the class Karyorelictea. In most ciliates, both the somatic macronuclei and germline micronuclei divide during cell division and macronuclear development only occurs after conjugation. However, the macronuclei of Karyorelictea are non-dividing (i.e. division minus (Div-)) and develop anew from micronuclei during each asexual division. As macronuclei age within Karyorelictea, they undergo changes in morphology and DNA content until they are eventually degraded and replaced by newly developed macronuclei. No less than two macronuclei and one micronucleus are present in karyorelictid species, which suggests that a mature macronucleus 1) might be needed to sustain the cell while a new macronucleus is developing and 2) likely plays a role in guiding the development of the new macronucleus. Here we use a phylogenetic framework to compile information on the morphology and development of nuclei in Karyorelictea, largely relying on the work of Dr. Igor Raikov (1932-1998). We synthesize data to speculate on the functional implications of key features of Karyorelictea including the presence of at least two macronuclei in each cell and the inability for macronuclei to divide.
Topics: Cell Nucleus Division; Ciliophora; Macronucleus
PubMed: 28673471
DOI: 10.1016/j.ejop.2017.05.002 -
Biochimica Et Biophysica Acta Nov 2008The single-celled ciliate Tetrahymena thermophila possesses two versions of its genome, one germline, one somatic, contained within functionally distinct nuclei (called... (Review)
Review
The single-celled ciliate Tetrahymena thermophila possesses two versions of its genome, one germline, one somatic, contained within functionally distinct nuclei (called the micronucleus and macronucleus, respectively). These two genomes differentiate from identical zygotic copies. The development of the somatic nucleus involves large-scale DNA rearrangements that eliminate 15 to 20 Mbp of their germline-derived DNA. The genomic regions excised are dispersed throughout the genome and are largely composed of repetitive sequences. These germline-limited sequences are targeted for removal from the genome by a RNA interference (RNAi)-related machinery that directs histone H3 lysine 9 and 27 methylation to their associated chromatin. The targeting small RNAs are generated in the micronucleus during meiosis and then compared against the parental macronucleus to further enrich for germline-limited sequences and ensure that only non-genic DNA segments are eliminated. Once the small RNAs direct these chromatin modifications, the DNA rearrangement machinery, including the chromodomain proteins Pdd1p and Pdd3p, assembles on these dispersed chromosomal sequences, which are then partitioned into nuclear foci where the excision events occur. This DNA rearrangement mechanism is Tetrahymena's equivalent to the silencing of repetitive sequences by the formation of heterochromatin. The dynamic nuclear reorganization that occurs offers an intriguing glimpse into mechanisms that shape nuclear architecture during eukaryotic development.
Topics: Animals; Cell Nucleus; Genome, Protozoan; Heterochromatin; RNA Interference; Tetrahymena thermophila
PubMed: 18706458
DOI: 10.1016/j.bbamcr.2008.07.012 -
Current Biology : CB Jan 2021The replication band in the macronucleus of ciliated protozoa has fascinated microscopists since the 19 Century. It migrates through the nucleus, corresponding to a...
The replication band in the macronucleus of ciliated protozoa has fascinated microscopists since the 19 Century. It migrates through the nucleus, corresponding to a region of DNA replication and nascent chromatin assembly. A new study shows that calcium and actin filaments may participate in the formation and migration of the replication band.
Topics: Cell Nucleus; Chromatin Assembly and Disassembly; Ciliophora; DNA Replication
PubMed: 33434478
DOI: 10.1016/j.cub.2020.10.058