Multiple Lineages of Ancient CR1 Retroposons Shaped the Early Genome Evolution of Amniotes

Suh, Alexander; Churakov, Gennady; Ramakodi, Meganathan P.; Platt, Roy N.; Jurka, Jerzy; Kojima, Kenji; Caballero, Juan; Smit, Arian F. A.; Vliet, Kent A.; Hoffmann, Federico G.; Brosius, Juergen; Green, Edward; Braun, Edward L.; Ray, David A.; Schmitz, Juergen

doi:10.1093/gbe/evu256

Cited by 61 publications

(89 citation statements)

References 74 publications

(161 reference statements)

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“…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]. However, another clade of LINEs called RTE seems to be prone to lateral transfer [Zupunski et al, 2001].…”

Section: Modes Of Transmission: Vertical Versus Horizontalsupporting

confidence: 64%

“…The majority of CR1 element activity predated the diversification of modern crocodilians [Suh et al, 2014]. However, in-depth analyses of crocodilian and bird genomes have uncovered interesting patterns of recent, but low, levels of activity.…”

Section: The Mobilome Of Archosaursmentioning

confidence: 99%

“…Among LINEs, CR1/L3 elements are the most abundant in turtles Tollis et al, 2017], which is similar to other reptiles. The high number of CR1 lineages in turtles likely reflects much of the CR1 ancestral diversity in amniotes [Suh et al, 2014]. Many CR1 subfamilies display a low divergence (<5%) from their con-Cytogenet Genome Res 2019;157:21-33 DOI: 10.1159/000496416 28 sensus sequence, suggesting a recent burst of activity [Tollis et al, 2017].…”

Section: The Mobilome Of Turtlesmentioning

confidence: 99%

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The Mobilome of Reptiles: Evolution, Structure, and Function

Boissinot¹,

Bourgeois²,

Manthey

et al. 2019

Cytogenet Genome Res

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Transposable elements (TE) constitute one of the most variable genomic features among vertebrates, impacting genome size, structure, and composition. Despite their important role in shaping genomic diversity, they have mostly been studied in mammals, which display one of the least diverse genomes in terms of TE diversity. Recent new resources in reptilian genomics have opened a broader perspective about TE evolution in amniotes. We discuss these recent results by showing that TE diversity is high in reptiles, particularly in squamates, with strong heterogeneity in the number of TE classes retained in each lineage, even at short evolutionary scales. More research is needed to uncover the exact mechanisms that regulate TE proliferation in reptiles and to what extent these selfish elements can play a role in local adaptation or in the emergence of barriers to gene flow.

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Section: Modes Of Transmission: Vertical Versus Horizontalsupporting

confidence: 64%

Section: The Mobilome Of Archosaursmentioning

confidence: 99%

Section: The Mobilome Of Turtlesmentioning

confidence: 99%

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The Mobilome of Reptiles: Evolution, Structure, and Function

Boissinot¹,

Bourgeois²,

Manthey

et al. 2019

Cytogenet Genome Res

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“…CR1 have been active at least since the common ancestor of birds, always with several subfamilies at the same time (110). This is because one CR1 lineage survived from the many lineages of LINE present in the common ancestor of birds and crocodilians (111). CR1 consensus sequences tend to be similar between ancient and recent families [e.g., families CR1-E and CR1-J across most of avian evolution (110)], which creates mis-annotations in the genome using RepeatMasker.…”

Section: Methodsmentioning

confidence: 99%

Dynamics of genome size evolution in birds and mammals

Kapusta

Suh

Feschotte

2017

Proc. Natl. Acad. Sci. U.S.A.

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355

358

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Genome size in mammals and birds shows remarkably little interspecific variation compared with other taxa. However, genome sequencing has revealed that many mammal and bird lineages have experienced differential rates of transposable element (TE) accumulation, which would be predicted to cause substantial variation in genome size between species. Thus, we hypothesize that there has been covariation between the amount of DNA gained by transposition and lost by deletion during mammal and avian evolution, resulting in genome size equilibrium. To test this model, we develop computational methods to quantify the amount of DNA gained by TE expansion and lost by deletion over the last 100 My in the lineages of 10 species of eutherian mammals and 24 species of birds. The results reveal extensive variation in the amount of DNA gained via lineage-specific transposition, but that DNA loss counteracted this expansion to various extents across lineages. Our analysis of the rate and size spectrum of deletion events implies that DNA removal in both mammals and birds has proceeded mostly through large segmental deletions (>10 kb). These findings support a unified "accordion" model of genome size evolution in eukaryotes whereby DNA loss counteracting TE expansion is a major determinant of genome size. Furthermore, we propose that extensive DNA loss, and not necessarily a dearth of TE activity, has been the primary force maintaining the greater genomic compaction of flying birds and bats relative to their flightless relatives.genome size evolution | DNA loss | transposable elements | amniotes | flight T he nature and relative importance of the molecular mechanisms and evolutionary forces underlying genome size variation has been the subject of intense research and debate (1-7). Variation in genome sizes may not always occur at a level where natural selection is strong enough to prevent genetic drift to determine their fate (neutral or effectively neutral variation) (3). Additionally, the fixation probability of slightly deleterious deletions or insertions would be higher in species with smaller effective population sizes, where natural selection acts less efficiently (3,8). On the other hand, a number of correlative associations between genome size and phenotypic traits, such as cell size (9, 10) and metabolic rate associated with powered flight (11, 12), suggest that natural selection and adaptive processes also shape genome size evolution. Teasing apart the relative importance of these two forces (drift and selection) requires a better understanding of the mode and processes by which DNA is gained and lost over long evolutionary periods in different taxa. Thus, establishing an integrated view of the contribution of gain and loss of DNA to genome size variation (or lack thereof) remains an important goal in genome biology (e.g., refs. 1, 2, 13, and 14).Most studies of genome size evolution have focused on taxa with extensive variation in genome sizes, such as flowering plants (15)(16)(17)(18)(19)(20), conifers (21), insects (22-...

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“…They dominate the landscape of transposable elements (TEs) in the genomes of all major lineages except mammals (Shedlock et al 2007;Suh et al 2015a) and comprise a large diversity that existed since the days of the amniote ancestor (Suh et al 2015a). Notably, CR1 elements are the only TEs that were active throughout avian evolution and have thus been widely used as phylogenetic markers [e.g., (Baker et al 2014;Haddrath and Baker 2012;Kaiser et al 2007;Kriegs et al 2007;Liu et al 2012;Suh et al 2011aSuh et al , b, 2012Suh et al , 2015a].…”

mentioning

confidence: 99%

The Specific Requirements for CR1 Retrotransposition Explain the Scarcity of Retrogenes in Birds

Suh

2015

J Mol Evol

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Chicken repeat 1 (CR1) retroposons are the most abundant superfamily of transposable elements in the genomes of birds, crocodilians, and turtles. However, CR1 mobilization remains poorly understood. In this article, I document that the diverse CR1 lineages of land vertebrates share a highly conserved hairpin structure and an octamer microsatellite motif at their very 3' ends. Together with the presence of these same motifs in the tails of CR1-mobilized short interspersed elements, this suggests that the minimum requirement for CR1 transcript recognition and retrotransposition is a complex >50-nt structure. Such a highly specific recognition sequence readily explains why CR1-dominated genomes generally contain very few retrogenes. Conversely, the mammalian richness in retrogenes results from CR1 extinction in their early evolution and subsequent establishment of L1 dominance.

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Multiple Lineages of Ancient CR1 Retroposons Shaped the Early Genome Evolution of Amniotes

Cited by 61 publications

References 74 publications

The Mobilome of Reptiles: Evolution, Structure, and Function

The Mobilome of Reptiles: Evolution, Structure, and Function

Dynamics of genome size evolution in birds and mammals

The Specific Requirements for CR1 Retrotransposition Explain the Scarcity of Retrogenes in Birds

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