Extinction of LINE-1 activity coincident with a major mammalian radiation in
1,2Robert A. Grahn, 1,3Timothy A. Rinehart, 1Michael A. Cantrell and 1Holly A. Wichman
1University of Idaho Department of Biological Sciences, 443051 Moscow, ID 83844-3051
2Current address: College of Veterinary Medicine Department of Population Health and Reproduction University of California Davis, California 95616
3Current Address: USDA Small Fruit Research Station 306 South High Street P.O. Box 287 Poplarville, Mississippi 39470
Running Head:
LINE-1 extinction
Keywords:
LINE-1
Sigmodontinae transposable element evolution
Corresponding author:
Holly A Wichman Dept. of Bio. Sci. Univ. of Idaho Moscow ID 83844-3051 (208) 885-7805 (208) 885-7905 (fax) [email protected]
1
Abstract
LINE-1 transposable elements (L1s) are ubiquitous in mammals and are thought to have remained active since before the mammalian radiation. Only one L1 extinction event, in South
American rodents in the genus Oryzomys, has been convincingly demonstrated. Here we examine the phylogenetic limits and evolutionary tempo of that extinction event by characterizing L1s in related rodents. Fourteen genera from five tribes within the Sigmodontinae family were examined. Only the Sigmodontini, the most basal tribe in this group, demonstrate recent L1 activity. The Oryzomyini, Akodontini, Phyllotini, and Thomasomyini contain only
L1s that appear to have inserted long ago: their L1s lack open reading frames, have mutations at conserved amino acid residues, and show numerous private mutations. They also lack restriction site-defined L1 subfamilies specific to any species, genus or tribe examined, and fail to form monophyletic species, genus or tribal L1 clusters. We determine here that this L1 extinction event occurred roughly 8.8 million years ago, near the divergence of Sigmodon from the remaining Sigmodontinae species. These species appear to be ideal model organisms for studying the impact of L1 inactivity on mammalian genomes.
2
Introduction
The long interspersed element LINE-1 (L1) makes up a large component of the genome
in all mammalian species examined to date, with tens of thousands of copies present per genome
(Furano, 2000). Sequence analysis of mammalian genomes shows that they make up 17 % or
more of the human and mouse genomes (Lander et al., 2001; Waterston et al., 2002).
Hybridization of an L1 probe to genomic Southern blots from representatives of several orders of
mammals revealed a widespread distribution of these elements and lead to the suggestion that
L1s predate the mammalian radiation (Burton et al., 1986). L1s have been characterized at the
sequence level in numerous rodents (Martin et al., 1985; Hardies et al., 2000; Casavant and
Hardies, 1994b; Martin, 1995; Naas et al., 1998; D'Ambrosio et al., 1986; Casavant et al., 1996;
Casavant et al., 1998; Kass et al., 1992; Vanlerberghe et al., 1993; Kholodilov et al., 1993;
Mayorov et al., 1999), in several primates, especially humans (Fanning and Singer, 1987b;
Kazazian et al., 1988; Skowronski et al., 1988; Salem et al., 2003), in two carnivores (Choi et
al., 1999; Fanning and Singer, 1987a), rabbits (Fanning and Singer, 1987a), cattle (Plucienniczak
and Plucienniczak, 1999) and a marsupial (Dorner and Paabo, 1995).
Full length L1s range from 6.0 to 7.5 kb. (Loeb et al., 1986). They have 5' and 3'
untranslated regions that bound two open reading frames (ORFs), and a poly A tract of varying
length following the 3’ untranslated region. The first open reading frame (ORF 1