Copy number variations of 11 macronuclear chromosomes and their gene expression in Oxytricha trifallax

Xu, Ke; Doak, Thomas G.; Lipps, Hans J.; Wang, Jingmei; Swart, Estienne C.; Chang, Wei‐Jen

doi:10.1016/j.gene.2012.05.045

Cited by 31 publications

(39 citation statements)

References 73 publications

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“…Previously a survey of 11 orthologous nanochromosomes in S. lemnae and O. trifallax showed that the relative copy number of these nanochromosomes is similar (Xu et al 2012). Although we were examining alternative nanochromosome fragmentation, we noticed that the patterns of sequence coverage of the different nanochromosome isoforms from Stylonychia and Oxytricha are similar (fig.…”

Section: Resultsmentioning

confidence: 99%

The Draft Assembly of the Radically Organized Stylonychia lemnae Macronuclear Genome

Aeschlimann¹,

Jönsson²,

Postberg³

et al. 2014

Genome Biology and Evolution

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Stylonychia lemnae is a classical model single-celled eukaryote, and a quintessential ciliate typified by dimorphic nuclei: A small, germline micronucleus and a massive, vegetative macronucleus. The genome within Stylonychia’s macronucleus has a very unusual architecture, comprised variably and highly amplified “nanochromosomes,” each usually encoding a single gene with a minimal amount of surrounding noncoding DNA. As only a tiny fraction of the Stylonychia genes has been sequenced, and to promote research using this organism, we sequenced its macronuclear genome. We report the analysis of the 50.2-Mb draft S. lemnae macronuclear genome assembly, containing in excess of 16,000 complete nanochromosomes, assembled as less than 20,000 contigs. We found considerable conservation of fundamental genomic properties between S. lemnae and its close relative, Oxytricha trifallax, including nanochromosomal gene synteny, alternative fragmentation, and copy number. Protein domain searches in Stylonychia revealed two new telomere-binding protein homologs and the presence of linker histones. Among the diverse histone variants of S. lemnae and O. trifallax, we found divergent, coexpressed variants corresponding to four of the five core nucleosomal proteins (H1.2, H2A.6, H2B.4, and H3.7) suggesting that these ciliates may possess specialized nucleosomes involved in genome processing during nuclear differentiation. The assembly of the S. lemnae macronuclear genome demonstrates that largely complete, well-assembled highly fragmented genomes of similar size and complexity may be produced from one library and lane of Illumina HiSeq 2000 shotgun sequencing. The provision of the S. lemnae macronuclear genome sets the stage for future detailed experimental studies of chromatin-mediated, RNA-guided developmental genome rearrangements.

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Section: Resultsmentioning

confidence: 99%

The Draft Assembly of the Radically Organized Stylonychia lemnae Macronuclear Genome

Aeschlimann¹,

Jönsson²,

Postberg³

et al. 2014

Genome Biology and Evolution

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“…A positive correlation between copy number and gene expression for three pheromone genes exists in Euplotes raikovi (CI: Spirotrichea, La Terza et al 1995). In Oxytricha trifallax (CI: Spirotrichea), the copy numbers of 11 MAC chromosomes are moderately correlated to gene expression levels, though the pattern is not conserved in closely related species or even between two subpopulations of one strain (Xu et al 2012). In contrast, a recent study in Chilodonella uncinata revealed that members of the β-tubulin gene family that are abundant in the macronucleus tend to be expressed at low levels, while rarer gene family members are expressed at higher levels (Bellec and Katz 2012).…”

Section: Introductionmentioning

confidence: 99%

Nanochromosome Copy Number Does not Correlate with RNA Levels Though Patterns are Conserved between Strains of the Ciliate Morphospecies Chilodonella uncinata

Huang¹,

Katz²

2014

Protist

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In some ciliates, extensive genome fragmentation leads to a macronucleus (i.e. somatic nucleus) containing gene-sized chromosomes that vary in copy number. Yet the relationship between copy number and expression level is not well understood as previous work has shown a variety of patterns. For example, nanochromosome copy numbers are positively correlated to mRNA levels in spirotrichous ciliates, while one study of Chilodonella uncinata suggested that they were inversely correlated. To study further copy number and expression levels in C. uncinata, we analyzed 11 members in five gene families (SSU-rDNA, actin, alpha-tubulin, histidine acid phosphatase family protein and protein kinase domain containing protein) from one strain. We find that macronuclear copy numbers of these genes range from hundreds to thousands per cell, and that copy number does not correlate with expression level as measured by steady-state RNA in predominantly-vegetative cultures. We also compared six of these genes to their orthologs in a second genetically-isolated strain to reveal that patterns of nanochromosome and transcript copy numbers are conserved between strains. Our data suggest that nanochromosome copy number may be related to a feature like nuclear architecture.

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“…Copy number of chromosomes in the macronucleus is another epigenetically controlled phenomenon in ciliates with extensively processed, gene-sized macronuclear chromosomes (Bellec and Katz, 2012; Xu et al, 2012). Ciliates with multigene macronuclear chromosomes, such as Paramecium and Tetrahymena , have roughly even copy numbers of all chromosomes in their macronuclei (Xu et al, 2012).…”

Section: Part Ii: Molecular Studiesmentioning

confidence: 99%

“…Ciliates with multigene macronuclear chromosomes, such as Paramecium and Tetrahymena , have roughly even copy numbers of all chromosomes in their macronuclei (Xu et al, 2012). For example, each chromosome in Paramecium tetraurelia is amplified to ~800 copies (Duret et al, 2008).…”

Section: Part Ii: Molecular Studiesmentioning

confidence: 99%

“…Like unscrambling, copy number determination is thought to rely on long template RNAs from the old macronucleus (Heyse et al, 2010; Nowacki et al, 2011; Xu et al, 2012). In Stylonychia , the developing macronucleus begins with roughly the same copy number for each gene, like the zygotic nucleus from which it came (Heyse et al, 2010).…”

Section: Part Ii: Molecular Studiesmentioning

confidence: 99%

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Insights into transgenerational epigenetics from studies of ciliates

Pilling

Rogers

Gulla-Devaney

et al. 2017

European Journal of Protistology

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Epigenetics, a term with many meanings, is 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, and serotype. In addition, we detail molecular studies including DNA elimination; alternative processing and unscrambling; and copy number determination in model lineages. Based on the implications of such studies, we explore epigenetics as a possible functional mechanism for rapid speciation in ciliates.

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Copy number variations of 11 macronuclear chromosomes and their gene expression in Oxytricha trifallax

Cited by 31 publications

References 73 publications

The Draft Assembly of the Radically Organized Stylonychia lemnae Macronuclear Genome

The Draft Assembly of the Radically Organized Stylonychia lemnae Macronuclear Genome

Nanochromosome Copy Number Does not Correlate with RNA Levels Though Patterns are Conserved between Strains of the Ciliate Morphospecies Chilodonella uncinata

Insights into transgenerational epigenetics from studies of ciliates

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