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  • Review Article
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Genome gymnastics: unique modes of dna evolution and processing in ciliates

Nature Reviews Genetics volume 1, pages 191–198 (2000)Cite this article

Key Points

  • During development of a somatic nucleus (macronucleus) from a germline nucleus (micronucleus) in hypotrichous ciliates, 95% or more of the DNA sequences are eliminated.

  • Elimination of DNA sequences converts very high molecular weight micronuclear DNA to very low molecular weight macronuclear DNA.

  • With rare exceptions, each of the thousands of different, short macronuclear DNA molecules (400 to 15,000 bp) encodes a single gene.

  • In the micronucleus, genes are interrupted by short, multiple, (A+T)-rich, non-coding sequences called internal eliminated segments or IESs. IESs are spliced out of genes during macronuclear development.

  • During evolution, IESs shift along DNA of micronuclear genes without changing the nucleotide sequences of the genes. IES shifting seems to occur by point mutations.

  • In some germline genes, gene segments created by the presence of IESs are in disorder (including inversions), creating scrambled genes. Scrambled genes are unscrambled during macronuclear development.

  • The elaborate DNA manipulations during macronuclear development are accompanied by activation of the silent micronuclear genes into actively transcribed macronuclear genes.

  • The spectacular contortions of germline DNA in hypotrichous ciliates may be important in the evolution of these organisms.

Abstract

In some ciliates, the DNA sequences of the germline genomes have been profoundly modified during evolution, providing unprecedented examples of germline DNA malleability. Although the significance of the modifications and malleability is unclear, they may reflect the evolution of mechanisms that facilitate evolution. Because of the modifications, these ciliates must perform remarkable feats of cutting, splicing, rearrangement and elimination of DNA sequences to convert the chromosomal DNA in the germline genome (micronuclear genome) into gene-sized DNA molecules in the somatic genome (macronuclear genome). How these manipulations of DNA are guided and carried out is largely unknown. However, the organization and manipulation of ciliate DNA sequences are new phenomena that expand a general appreciation for the flexibility of DNA in evolution and development.

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Figure 1: The behaviour of ciliate nuclei.
Figure 2: Ciliate genome organization.
Figure 3: Interruptions in micronuclear genes.
Figure 4: Scrambled genes.
Figure 5: A model for nonrandom scrambling.
Figure 6: An extremely scrambled gene.
Figure 7: A model for MDS–IES junction shifting.

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Acknowledgements

This work is supported by the NIGMS and the NSF.

Author information

Authors and Affiliations

  1. Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, 80309-0347, Colorado, USA

    David M. Prescott

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  1. David M. Prescott
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Related links

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DATABASE LINKS

Tetrahymena thermophila

Oxytricha trifallax

Oxytricha nova

Euplotes

Oxytricha

Stylonychia

Gastrostyla

Pleurotricha

Paraurostyla

Uroleptus

Stylonychia mytilus

Paramecium tetraurelia

Stylonychia lemnae

FURTHER INFORMATION

David Prescott's lab page

ENCYCLOPEDIA OF LIFE SCIENCES

Ciliophora

Euplotes

Tetrahymena

Developmentally programmed DNA rearrangements

Glossary

CILIATES

Single-celled organisms containing a micronucleus (germline nucleus), a macronucleus (somatic nucleus) and cilia for swimming and food capture.

RNA SELF-SPLICING

Removal of the intron sequence from precursor RNA and splicing of the mature RNA by catalytic action of the intron RNA, showing the enzyme-like activity of RNA.

POLYTENE CHROMOSOME

A giant chromosome formed by many replications of the DNA. The replicated DNA molecules tightly align side-by-side in parallel register, creating a non-mitotic chromosome visible by light microscopy.

SEQUENCE COMPLEXITY

The number of different DNA sequences in a genome, originally measured by the rate of reassociation of heat-denatured DNA.

PARITY RULE 2

This rule derives from parity rule 1. In the absence of strand bias for mutation or selection, A = T and C = G within a strand of the double helix.

PARITY RULE 1

In the absence of strand bias for mutation or selection, the 12 substitution rates between all four bases reduce to six rates, that is A→T = T→A, G→C = C→G, A→G = T→C, G→A = C→T, C→A = G→T and A→C = T→G.

TRANSITION

A mutation in which a purine is replaced by a purine, or a pyrimidine is replaced by a pyrimidine.

TRANSVERSION

A mutation in which a pyrimidine is replaced by a purine or vice versa.

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Prescott, D. Genome gymnastics: unique modes of dna evolution and processing in ciliates . Nat Rev Genet 1, 191–198 (2000). https://doi.org/10.1038/35042057

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