Transcribed germline-limited coding sequences in<i>Oxytricha trifallax</i>

Miller, Richard V; Neme, Rafik; Clay, Derek M.; Pathmanathan, Jananan S.; Lu, Michael W; Yerlici, V. Talya; Khurana, Jaspreet S.; Landweber, Laura F.

doi:10.1093/g3journal/jkab092

Cited by 6 publications

(4 citation statements)

References 53 publications

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“…Oxytricha displays the greatest proportion of repetitive elements (telomere-bearing elements [TBE], other repeats, and tandem repeats) relative to the other species. Oxytricha MIC-specific genes were annotated in Chen et al, 2014 ; Miller et al, 2021 . ( D–F ) Phylogenetic analysis of the three TBE open reading frames (ORFs) in Oxytricha and Tetmemena : ( D ) 42 kD, ( E ) 22 kD, and ( F ) 57 kD, suggest that TBE3 (green) is the ancestral transposon family in Oxytricha .…”

Section: Resultsmentioning

confidence: 99%

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

Feng

Neme

Beh

et al. 2022

eLife

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Ciliates are microbial eukaryotes that undergo extensive programmed genome rearrangement, a natural genome editing process that converts long germline chromosomes into smaller gene-rich somatic chromosomes. Three well-studied ciliates include Oxytricha trifallax, Tetrahymena thermophila and Paramecium tetraurelia, but only the Oxytricha lineage has a massively scrambled genome, whose assembly during development requires hundreds of thousands of precise programmed DNA joining events, representing the most complex genome dynamics of any known organism. Here we study the emergence of such complex genomes by examining the origin and evolution of discontinuous and scrambled genes in the Oxytricha lineage. This study compares six genomes from three species, the germline and somatic genomes for Euplotes woodruffi, Tetmemena sp., and the model ciliate Oxytricha trifallax. To complement existing data, we sequenced, assembled and annotated the germline and somatic genomes of Euplotes woodruffi, which provides an outgroup, and the germline genome of Tetmemena sp.. We find that the germline genome of Tetmemena is as massively scrambled and interrupted as Oxytricha's : 13.6% of its gene loci require programmed translocations and/or inversions, with some genes requiring hundreds of precise gene editing events during development. This study revealed that the earlier-diverged spirotrich, E. woodruffi, also has a scrambled genome, but only roughly half as many loci (7.3%) are scrambled. Furthermore, its scrambled genes are less complex, together supporting the position of Euplotes as a possible evolutionary intermediate in this lineage, in the process of accumulating complex evolutionary genome rearrangements, all of which require extensive repair to assemble functional coding regions. Comparative analysis also reveals that scrambled loci are often associated with local duplications, supporting a gradual model for the origin of complex, scrambled genomes via many small events of DNA duplication and decay.

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Section: Resultsmentioning

confidence: 99%

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

Feng

Neme

Beh

et al. 2022

eLife

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“…Older IESs are much shorter, compatible with the “fade” step of the model. Moreover, some conserved IESs encode MIC-limited genes [ 3 , 12 ] or provide a “switch” to regulate gene expression.…”

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confidence: 99%

Transposon debris in ciliate genomes

Feng

Landweber

2021

PLoS Biol

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“…In ciliates, after mating, DNA deletion (including sequences with homology to transposable elements) is an extreme example both of ‘turning off’ genes and of the potential for transposable elements to define special contexts or behaviours in genomes. DNA of the chromosomes of the unicellular ciliate Oxytricha nova is fragmented into thousands of pieces; a subset then is assembled in an ‘unscrambled’ order in the somatic macronucleus (Miller et al., 2021), astounding us by the genome's self‐organization. Protection and assembly of ‘unscrambled’ somatic ciliate genome DNA involves non‐protein‐coding RNAs.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary feedback from the environment shapes mechanisms that generate genome variation

Caporale

2024

The Journal of Physiology

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Darwin recognized that ‘a grand and almost untrodden field of inquiry will be opened, on the causes and laws of variation.’ However, because the Modern Synthesis assumes that the intrinsic probability of any individual mutation is unrelated to that mutation's potential adaptive value, attention has been focused on selection rather than on the intrinsic generation of variation. Yet many examples illustrate that the term ‘random’ mutation, as widely understood, is inaccurate. The probabilities of distinct classes of variation are neither evenly distributed across a genome nor invariant over time, nor unrelated to their potential adaptive value. Because selection acts upon variation, multiple biochemical mechanisms can and have evolved that increase the relative probability of adaptive mutations. In effect, the generation of heritable variation is in a feedback loop with selection, such that those mechanisms that tend to generate variants that survive recurring challenges in the environment would be captured by this survival and thus inherited and accumulated within lineages of genomes. Moreover, because genome variation is affected by a wide range of biochemical processes, genome variation can be regulated. Biochemical mechanisms that sense stress, from lack of nutrients to DNA damage, can increase the probability of specific classes of variation. A deeper understanding of evolution involves attention to the evolution of, and environmental influences upon, the intrinsic variation generated in gametes, in other words upon the biochemical mechanisms that generate variation across generations. These concepts have profound implications for the types of questions that can and should be asked, as omics databases become more comprehensive, detection methods more sensitive, and computation and experimental analyses even more high throughput and thus capable of revealing the intrinsic generation of variation in individual gametes. These concepts also have profound implications for evolutionary theory, which, upon reflection it will be argued, predicts that selection would increase the probability of generating adaptive mutations, in other words, predicts that the ability to evolve itself evolves. image

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Transcribed germline-limited coding sequences inOxytricha trifallax

Cited by 6 publications

References 53 publications

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

Transposon debris in ciliate genomes

Evolutionary feedback from the environment shapes mechanisms that generate genome variation

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