The Evolution of Line-1 in Vertebrates

Abstract

The abundance and diversity of the LINE-1 (L1) retrotransposon differ greatly among vertebrates. Mammalian genomes contain hundreds of thousands L1s that have accumulated since the origin of mammals. A single group of very similar elements is active at a time in mammals, thus a single lineage of active families has evolved in this group. In contrast, non-mammalian genomes (fish, amphibians, reptiles) harbor a large diversity of concurrently transposing families, which are all represented by very small number of recently inserted copies. Why the pattern of diversity and abundance of L1 is so different among vertebrates remains unknown. To address this issue, we performed a detailed analysis of the evolution of active L1 in 14 mammals and in 3 non-mammalian vertebrate model species. We examined the evolution of base composition and codon bias, the general structure, and the evolution of the different domains of L1 (5′UTR, ORF1, ORF2, 3′UTR). L1s differ substantially in length, base composition, and structure among vertebrates. The most variation is found in the 5′UTR, which is longer in amniotes, and in the ORF1, which tend to evolve faster in mammals. The highly divergent L1 families of lizard, frog, and fish share species-specific features suggesting that they are subjected to the same functional constraints imposed by their host. The relative conservation of the 5′UTR and ORF1 in non-mammalian vertebrates suggests that the repression of transposition by the host does not act in a sequence-specific manner and did not result in an arms race, as is observed in mammals.

The Mobilome of Reptiles: Evolution, Structure, and Function

“…A relationship between transposition and reproduction is implicit since the spread of TEs and the increase in copy number requires transposition to occur in the germline or in early embryogenesis. In non-LTR retrotransposons, the phylogeny of the elements tends to recapitulate the phylogeny of the host, which is consistent with a strict model of vertical transmission [Malik et al, 1999;Kordis et al, 2006;Waters et al, 2007;Boissinot and Sookdeo, 2016]. This appears to be the case in the L1 and CR1 clades of LINEs, which have persisted and amplified in reptile genomes since the origin of amniotes, with no evidence of lateral transfer [Suh et al, 2014].…”

“…Consequently, most mammalian genomes contain a single active family of L1 element at a time. In contrast, L1 in A. carolinensis is represented by at least 20 concurrently active families, which diverged from each other before the split between mammals and reptiles [Novick et al, 2009;Boissinot and Sookdeo, 2016]. This situation is comparable to that of fish and frog genomes, where L1 is represented by multiple active families, thus indicating that the reduction in diversity of L1 is a mammalian specific feature Furano et al, 2004;Boissinot and Sookdeo, 2016;Ivancevic et al, 2016].…”

“…The evolution of L1 in A. carolinensis does not fit this pattern. In fact the 5 ′ untranslated region of the lizard L1 is extremely conserved, even across highly divergent L1 families, and the first open reading frame does not show any evidence of adaptive evolution or structural instability [Boissinot and Sookdeo, 2016]. This suggests that the control mechanisms of L1 in A. carolinensis are not acting in a family-specific manner.…”

“…In contrast, L1 in A. carolinensis is represented by at least 20 concurrently active families, which diverged from each other before the split between mammals and reptiles [Novick et al, 2009;Boissinot and Sookdeo, 2016]. This situation is comparable to that of fish and frog genomes, where L1 is represented by multiple active families, thus indicating that the reduction in diversity of L1 is a mammalian specific feature Furano et al, 2004;Boissinot and Sookdeo, 2016;Ivancevic et al, 2016]. This pattern is not limited to L1 since the L2 clade is represented in anole by 17 simultaneously active families, although L2 families are not as divergent from each other as L1 families are [Novick et al, 2009].…”

“…This suggests that the control mechanisms of L1 in A. carolinensis are not acting in a family-specific manner. We proposed that it is unlikely that family-specific transposition repressors evolved in an organism like the green anole, which harbors an extremely rich and diverse TE landscape, and that a more general repression mechanism constitutes a more effective way to control the large number of TE families that are simultaneously active in this genome [Boissinot and Sookdeo, 2016]. This aspect of reptile biology is however in dire need of investigation.…”