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MBE Advance Access originally published online on October 31, 2003
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Mol. Biol. Evol. 21(1):129-140. 2004
DOI: 10.1093/molbev/msh005
© 2004 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038

The Evolution of Homing Endonuclease Genes and Group I Introns in Nuclear rDNA

Peik Haugen*, Valérie Reeb{dagger}, François Lutzoni{dagger} and Debashish Bhattacharya*

* Department of Biological Sciences and Center for Comparative Genomics, University of Iowa
{dagger} Department of Biology, Duke University

E-mail: dbhattac{at}blue.weeg.uiowa.edu.

Group I introns are autonomous genetic elements that can catalyze their own excision from pre-RNA. Understanding how group I introns move in nuclear ribosomal (r)DNA remains an important question in evolutionary biology. Two models are invoked to explain group I intron movement. The first is termed homing and results from the action of an intron-encoded homing endonuclease that recognizes and cleaves an intronless allele at or near the intron insertion site. Alternatively, introns can be inserted into RNA through reverse splicing. Here, we present the sequences of two large group I introns from fungal nuclear rDNA, which both encode putative full-length homing endonuclease genes (HEGs). Five remnant HEGs in different fungal species are also reported. This brings the total number of known nuclear HEGs from 15 to 22. We determined the phylogeny of all known nuclear HEGs and their associated introns. We found evidence for intron-independent HEG invasion into both homologous and heterologous introns in often distantly related lineages, as well as the "switching" of HEGs between different intron peripheral loops and between sense and antisense strands of intron DNA. These results suggest that nuclear HEGs are frequently mobilized. HEG invasion appears, however, to be limited to existing introns in the same or neighboring sites. To study the intron-HEG relationship in more detail, the S943 group I intron in fungal small-subunit rDNA was used as a model system. The S943 HEG is shown to be widely distributed as functional, inactivated, or remnant ORFs in S943 introns.

Key Words: Group I introns • homing endonucleases • HEGs • intron mobility • ribosomal RNA


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