Macronuclear gene-sized molecules of hypotrichs

Hoffman, David C.; Anderson, Richard C. E.; DuBois, Michelle L.; Prescott, David M.

doi:10.1093/nar/23.8.1279

Cited by 64 publications

(66 citation statements)

References 65 publications

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“…Such genes are expected to generate two separate hits to different regions of the same protein in BLASTx searches, with the two matching regions of the macronuclear DNA molecule encoding polypeptides in different reading frames. Such results can also be due to the presence of introns, which are rare in spirotrich genes (17), but an intron is also expected to result in a gap in the alignment of the conceptually translated DNA sequence with the protein homolog, while genes requiring a frameshift should not display such an alignment gap. In addition, based on the typical arrangement of ϩ1 frameshift genes in Euplotes, the initial open reading frame (reading frame 0) is expected to terminate with the sequence 5Ј-AAA-TA(A/g)-3Ј (22).…”

Section: Resultsmentioning

confidence: 99%

Sequencing of Random Euplotes crassus Macronuclear Genes Supports a High Frequency of +1 Translational Frameshifting

Klobutcher

2005

Eukaryot Cell

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Programmed translational frameshifts have been identified in genes from a broad range of organisms, but typically only a very few genes in a given organism require a frameshift for expression. In contrast, a recent analysis of gene sequences available in GenBank from ciliates in the genus Euplotes indicated that >5% required one or more ؉1 translational frameshifts to produce their predicted protein products. However, this sample of genes was nonrandom, biased, and derived from multiple Euplotes species. To test whether there truly is an abundance of frameshift genes in Euplotes, and to more accurately assess their frequency, we sequenced a random sample of 25 cloned genes/macronuclear DNA molecules from Euplotes crassus. Three new candidate ؉1 frameshift genes were identified in the sample that encode a membrane occupation and recognition nexus (MORN) repeat protein, a C 2 H 2 -type zinc finger protein, and a Ser/Thr protein kinase. Reverse transcription-PCR analyses indicate that all three genes are expressed in vegetatively proliferating cells and that the mRNAs retain the requirement of a frameshift. Although the sample of sequenced genes is relatively small, the results indicate that the frequency of genes requiring frameshifts in E. crassus is between 3.7% and 31.7% (at a 95% confidence interval). The current and past data also indicate that frameshift sites are found predominantly in genes that likely encode nonabundant proteins in the cell.During the translation of an mRNA, a shift in reading frame is usually a catastrophic event, often resulting in a truncated and/or nonfunctional protein. Translational frameshifting is infrequent during the translation of most mRNAs (Ͻ5 ϫ 10 Ϫ5 frameshifts per codon translated [25]), but a number of mRNAs require a frameshift to express a functional protein and appear to have evolved to stimulate frameshifting. Such programmed translational frameshifting (reviewed in references 13 and 32) is relatively rare but is phylogenetically widespread, as examples are known in prokaryotes, eukaryotes, and a number of mobile genetic elements. Sequence elements within the mRNA facilitate programmed frameshifting, and these typically reside at the site of the frameshift, but more distally located sequences can also be involved.A number of genes in ciliated protozoa of the genus Euplotes (class Spirotrichea) have been identified that appear to require a ϩ1 translational frameshift to produce their protein products. The putative ϩ1-frameshift genes encode the regulatory subunit of cyclic AMP-dependent protein kinase and a nuclear protein kinase of Euplotes octocarinatus (39, 40), a La motif protein (p43) in Euplotes aediculatus (1), the Euplotes crassus Tec2 transposon ORF2 protein (11,18), and the reverse transcriptase subunits of telomerase (TERT) in three euplotid species (20,29,42). Since the complete sequences of less than 100 Euplotes genes have been determined, it appears that frameshifting is unusually common in euplotids, with perhaps Ͼ5% of genes requiring a frameshift for ...

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Section: Resultsmentioning

confidence: 99%

Sequencing of Random Euplotes crassus Macronuclear Genes Supports a High Frequency of +1 Translational Frameshifting

Klobutcher

2005

Eukaryot Cell

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“…2d), indicating that the hydrogenase is encoded by gene-sized pieces of N. ovalis macronuclear DNA 10 (Fig. 2c).…”

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“…2c). The genomic fragment terminates in a G 3 T 4 G 3 (T 4 G 4 ) 5 repeat that is very similar to the telomere sequences of hypotrichous ciliates 10 . The cDNA start was about 180 base pairs downstream from the telomere.…”

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confidence: 99%

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A hydrogenosome with a genome

Akhmanova

Voncken

Alen

et al. 1998

Nature

254

158

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“…Because most of Oxytricha's more than 20,000 unique "nanochromosomes" in its somatic nucleus bear only a single gene (23,24) and copy number can vary independently (25), Oxytricha provides a unique opportunity to study copy number variation. The absence of physical linkage potentially releases most constraints on gene copy number, encouraging gene regulation at the level of DNA copy number, in addition to transcription.…”

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RNA-mediated epigenetic regulation of DNA copy number

Nowacki

Haye

Fang

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Increasing evidence suggests that parentally supplied RNA plays crucial roles during eukaryotic development. This epigenetic contribution may regulate gene expression from the earliest stages. Although present in a variety of eukaryotes, maternally inherited characters are especially prominent in ciliated protozoa, in which parental noncoding RNA molecules instruct whole-genome reorganization. This includes removal of nearly all noncoding DNA and sorting the remaining fragments, producing extremely gene-rich somatic genomes. Chromosome fragmentation and extensive replication produce variable DNA copy numbers in the somatic genome. Understanding the forces that drive and regulate copy number change is fundamental. We show that RNA molecules present in parental cells during sexual reproduction can regulate chromosome copy number in the developing nucleus of the ciliate Oxytricha . Experimentally induced changes in RNA abundance can both increase and decrease the levels of corresponding DNA molecules in progeny, demonstrating epigenetic inheritance of chromosome copy number. These results suggest that maternal RNA, in addition to controlling gene expression or DNA processing, can also program DNA amplification levels.

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Macronuclear gene-sized molecules of hypotrichs

Cited by 64 publications

References 65 publications

Sequencing of Random Euplotes crassus Macronuclear Genes Supports a High Frequency of +1 Translational Frameshifting

Sequencing of Random Euplotes crassus Macronuclear Genes Supports a High Frequency of +1 Translational Frameshifting

A hydrogenosome with a genome

RNA-mediated epigenetic regulation of DNA copy number

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