Remarkable compartmentalization of transposable elements and pseudogenes in the heterochromatin of the Tetraodon nigroviridis genome

^*Genoscope and Centre National de la Recherche Scientifique, Unité Mixte de Recherche 8030, 2 Rue Gaston Crémieux, 91057 Evry Cedex, France; and ^†Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, FR 1541, 43 Rue Cuvier, 75231 Paris Cedex 05, France

Edited by Margaret G. Kidwell, University of Arizona, Tucson, AZ, and approved August 9, 2002 (received for review May 13, 2002)

Abstract

Tetraodon nigroviridis is among the smallest known vertebrate genomes and as such represents an interesting model for studying genome architecture and evolution. Previous studies have shown that Tetraodon contains several types of tandem and dispersed repeats, but that their overall contribution is >10% of the genome. Using genomic library hybridization, fluorescent in situ hybridization, and whole genome shotgun and directed sequencing, we have investigated the global and local organization of repeat sequences in Tetraodon. We show that both tandem and dispersed repeat elements are compartmentalized in specific regions that correspond to the short arms of small subtelocentric chromosomes. The concentration of repeats in these heterochromatic regions is in sharp contrast to their paucity in euchromatin. In addition, we have identified a number of pseudogenes that have arisen through either duplication of genes or the retro-transcription of mRNAs. These pseudogenes are amplified to high numbers, some with more than 200 copies, and remain almost exclusively located in the same heterochromatic regions as transposable elements. The sequencing of one such heterochromatic region reveals a complex pattern of duplications and inversions, reminiscent of active and frequent rearrangements that can result in the truncation and hence inactivation of transposable elements. This tight compartmentalization of repeats and pseudogenes is absent in large vertebrate genomes such as mammals and is reminiscent of genomes that remain compact during evolution such as Drosophila and Arabidopsis.

Footnotes

↵ ‡ To whom correspondence should be addressed. E-mail: hrc{at}genoscope.cns.fr.
This paper was submitted directly (Track II) to the PNAS office.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AJ457054, AJ313481, AJ313482, and AJ313483).
Abbreviations:

WGS,

whole genome shotgun;

BAC,

bacterial artificial chromosome;

FISH,

fluorescent in situ hybridization;

iSET,

isolated SET;

TRAP,

translocom-associated protein;

E2H2,

enhancer of Zeste homolog 2;

LINE,

long interspersed element