Cold-induced retrotransposition of fish LINEs

Chen, Shue; Yu, Mengchao; Chu, Xiangxiang; Li, Wenhao; Yin, Xiujuan; Chen, Liangbiao

doi:10.1016/j.jgg.2017.07.002

Cited by 14 publications

(13 citation statements)

References 62 publications

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“…This estimated timing of LINE burst expansion correlated with the radiation of the majority of the modern Antarctic notothenioid clades beginning in the late Miocene when seawater temperatures steadily declined [9]. In contrast, no burst expansion of LINEs was detected in the E. maclovinus genome, supporting an Antarctic/cold-specific LINE burst in the toothfish, and corroborating our prior empirical evidence for an increase in retrotransposition activity of D. mawsoni LINE-1, resulting in more copies in the transfected cells when subjected to stress from nonphysiologically low incubation temperature [42].…”

Section: Resultssupporting

confidence: 77%

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The genomic basis for colonizing the freezing Southern Ocean revealed by Antarctic toothfish and Patagonian robalo genomes

Chen

et al. 2019

GigaScience

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Background The Southern Ocean is the coldest ocean on Earth but a hot spot of evolution. The bottom-dwelling Eocene ancestor of Antarctic notothenioid fishes survived polar marine glaciation and underwent adaptive radiation, forming >120 species that fill all water column niches today. Genome-wide changes enabling physiological adaptations and the rapid expansion of the Antarctic notothenioids remain poorly understood. Results We sequenced and compared 2 notothenioid genomes—the cold-adapted and neutrally buoyant Antarctic toothfish Dissostichus mawsoni and the basal Patagonian robalo Eleginops maclovinus , representing the temperate ancestor. We detected >200 protein gene families that had expanded and thousands of genes that had evolved faster in the toothfish, with diverse cold-relevant functions including stress response, lipid metabolism, protein homeostasis, and freeze resistance. Besides antifreeze glycoprotein, an eggshell protein had functionally diversified to aid in cellular freezing resistance. Genomic and transcriptomic comparisons revealed proliferation of selcys–transfer RNA genes and broad transcriptional upregulation across anti-oxidative selenoproteins, signifying their prominent role in mitigating oxidative stress in the oxygen-rich Southern Ocean. We found expansion of transposable elements, temporally correlated to Antarctic notothenioid diversification. Additionally, the toothfish exhibited remarkable shifts in genetic programs towards enhanced fat cell differentiation and lipid storage, and promotion of chondrogenesis while inhibiting osteogenesis in bone development, collectively contributing to the achievement of neutral buoyancy and pelagicism. Conclusions Our study revealed a comprehensive landscape of evolutionary changes essential for Antarctic notothenioid cold adaptation and ecological expansion. The 2 genomes are valuable resources for further exploration of mechanisms underlying the spectacular notothenioid radiation in the coldest marine environment.

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Section: Resultssupporting

confidence: 77%

“…The seed sequences of the long interspersed TEs (LINEs) [42] were aligned against the D. mawsoni and E. maclovinus draft genomes, respectively, using BlastN at E-value of 1e-10. According to loci of the alignments, the sequences were extracted from the genomes, which were considered as the candidates of the LINEs.…”

Section: Methodsmentioning

confidence: 99%

The genomic basis for colonizing the freezing Southern Ocean revealed by Antarctic toothfish and Patagonian robalo genomes

Chen

et al. 2019

GigaScience

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“…To evaluate the representation of some DIRS1 , Gypsy , and Copia families in nototheniid genomes in the absence of a well-assembled genome available to run exhaustive computational analyses, we tried to estimate their copy number using qPCR approaches relative to two single copy gene standards. Despite the repeated nature of the TE sequences, this approach has already been used to estimate TE copy number on genomic DNA [ 62 , 75 , 76 ]. The same TE families quantified by qPCR were also mapped on nototheniid chromosomes using FISH.…”

Section: Discussionmentioning

confidence: 99%

“…According to recent time-calibrated molecular phylogeny analyses [ 45 , 51 ], the Trematomus species diversification occurred in the middle – late Miocene (− 17 to − 5 My), corresponding to a cooling of shallow Antarctic shelf waters, followed by rapid switches between glacial and interglacial conditions [ 42 – 44 , 91 ]. This could have led to transpositional waves through genomes [ 11 , 21 , 62 ] possibly linked to species diversification [ 2 , 3 ]. On the contrary, B. diacanthus , E. maclovinus , P. fluviatilis (non AFGP-bearing species chosen as outgroups) were not exposed to series of environmental changes with cooling at sub-zero temperatures [ 42 , 43 ], and do not reveal any regions of TE accumulation on their chromosomes for the studied TEs (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…The tractable species number of the monophyletic genus Trematomus , the history of thermal perturbations of the taxon, its remarkable inter- and intraspecific chromosomal diversity, and its plethora of TEs [ 58 – 62 ] make the group ideal to investigate whether mobilization of TEs in response to environmental change may have played a role in the chromosomal diversification that often accompanies rapid speciation events. In the present multi-strategy study, we focus on DIRS - and LTR-order retrotransposons, specifically the diversity, distribution, chromosomal locations, and quantification of the pol region of the DIRS1 , Gypsy , and Copia elements, which we find to be widely distributed in the genomes of Trematomus and other nototheniid species.…”

Section: Introductionmentioning

confidence: 99%

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Mobilization of retrotransposons as a cause of chromosomal diversification and rapid speciation: the case for the Antarctic teleost genus Trematomus

et al. 2018

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BackgroundThe importance of transposable elements (TEs) in the genomic remodeling and chromosomal rearrangements that accompany lineage diversification in vertebrates remains the subject of debate. The major impediment to understanding the roles of TEs in genome evolution is the lack of comparative and integrative analyses on complete taxonomic groups. To help overcome this problem, we have focused on the Antarctic teleost genus Trematomus (Notothenioidei: Nototheniidae), as they experienced rapid speciation accompanied by dramatic chromosomal diversity. Here we apply a multi-strategy approach to determine the role of large-scale TE mobilization in chromosomal diversification within Trematomus species.ResultsDespite the extensive chromosomal rearrangements observed in Trematomus species, our measurements revealed strong interspecific genome size conservation. After identifying the DIRS1, Gypsy and Copia retrotransposon superfamilies in genomes of 13 nototheniid species, we evaluated their diversity, abundance (copy numbers) and chromosomal distribution. Four families of DIRS1, nine of Gypsy, and two of Copia were highly conserved in these genomes; DIRS1 being the most represented within Trematomus genomes. Fluorescence in situ hybridization mapping showed preferential accumulation of DIRS1 in centromeric and pericentromeric regions, both in Trematomus and other nototheniid species, but not in outgroups: species of the Sub-Antarctic notothenioid families Bovichtidae and Eleginopsidae, and the non-notothenioid family Percidae.ConclusionsIn contrast to the outgroups, High-Antarctic notothenioid species, including the genus Trematomus, were subjected to strong environmental stresses involving repeated bouts of warming above the freezing point of seawater and cooling to sub-zero temperatures on the Antarctic continental shelf during the past 40 millions of years (My). As a consequence of these repetitive environmental changes, including thermal shocks; a breakdown of epigenetic regulation that normally represses TE activity may have led to sequential waves of TE activation within their genomes. The predominance of DIRS1 in Trematomus species, their transposition mechanism, and their strategic location in “hot spots” of insertion on chromosomes are likely to have facilitated nonhomologous recombination, thereby increasing genomic rearrangements. The resulting centric and tandem fusions and fissions would favor the rapid lineage diversification, characteristic of the nototheniid adaptive radiation.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4714-x) contains supplementary material, which is available to authorized users.

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