Abstract

Programmed genome rearrangements in ciliates provide fascinating examples of flexible epigenetic genome regulations and important insights into the interaction between transposable elements (TEs) and host genomes. DNA elimination in Tetrahymena thermophila removes approximately 12 000 internal eliminated sequences (IESs), which correspond to one-third of the genome, when the somatic macronucleus (MAC) differentiates from the germline micronucleus (MIC). More than half of the IESs, many of which show high similarity to TEs, are targeted for elimination in cis by the small RNA-mediated genome comparison of the MIC to the MAC. Other IESs are targeted for elimination in trans by the same small RNAs through repetitive sequences. Furthermore, the small RNA–heterochromatin feedback loop ensures robust DNA elimination. Here, we review an updated picture of the DNA elimination mechanism, discuss the physiological and evolutionary roles of DNA elimination, and outline the key questions that remain unanswered.

Highlights

  • Ciliated protozoa undergo extensive programmed genome rearrangements when the germline micronucleus (MIC) produces the new macronucleus (MAC) during sexual reproduction

  • Active transposable elements (TEs)-containing internal eliminated sequences (IESs) may be constrained by natural selection to localize at the gene-poor A-regions, where the production of Early-scnRNAs ensures that their DNA is eliminated from the new MAC

  • We discuss a fundamental question: why do Tetrahymena perform DNA elimination? Because a large fraction of IESs are related to TEs, and RNAi-related mechanisms repress TEs in many eukaryotes, DNA elimination has probably evolved from an ancestral mechanism of transposon silencing

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Summary

Introduction

Ciliated protozoa undergo extensive programmed genome rearrangements when the germline micronucleus (MIC) produces the new macronucleus (MAC) during sexual reproduction. In this process, many transposon-related sequences are removed from the MAC [1,2]. It has long been known that programmed genome rearrangements occur genome-wide and eliminate many sequences related to transposable elements (TEs), a global landscape concerning ‘what’ is eliminated—their numbers, chromosomal distributions and relationship with TEs—became available only after the recent establishment of the assemblies of nearly full-length MIC chromosomes [1].

The life of Tetrahymena
The eliminated sequences
Kinship between transposable elements and IESs
Systems point of view of small RNA-directed DNA elimination
Mechanistic point of view of small RNA-directed
What mechanism drives the small RNA – heterochromatin positive feedback loop?
How is the positive feedback loop downregulated at the ends of IESs?
What are the roles of the two late-scnRNA-loaded Argonaute proteins?
Why does the MIC maintain IESs?
Why do Tetrahymena perform DNA elimination?
Concluding remarks
Findings
Methods
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