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Shaping and reshaping of salmonid genomes by amplification of tRNA-derived retroposons during evolution.

ABSTRACT: Three families of tRNA-derived repeated retroposons in the genomes of salmonid species have been isolated and characterized. These three families differ in sequence, but all are derived from a tRNA(Lys) or from a tRNA species structurally related to tRNA(Lys). The salmon Sma I family is present in the genomes of two species of the genus Oncorhynchus but not in other species, including five other species of the same genus. The charr Fok I family is present only in four species and subspecies of the genus Salvelinus. The third family, the salmonid Hpa I family, appears to be present in all salmonid species but is not present in species that are not members of the Salmonidae. Thus, the genome of proto-Salmonidae was originally shaped by amplification and dispersion of the salmonid Hpa I family and then reshaped by amplification of the Sma I and Fok I families in the more recently evolved species of salmon and charr, respectively. We speculate that amplification and dispersion of retroposons may have played a role in salmonid speciation.

SUBMITTER: Kido Y

PROVIDER: S-EPMC51224 | biostudies-other | 1991 Mar

REPOSITORIES: biostudies-other

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Shaping and reshaping of salmonid genomes by amplification of tRNA-derived retroposons during evolution.

Kido Y Y Aono M M Yamaki T T Matsumoto K K Murata S S Saneyoshi M M Okada N N

Proceedings of the National Academy of Sciences of the United States of America 19910301 6

Three families of tRNA-derived repeated retroposons in the genomes of salmonid species have been isolated and characterized. These three families differ in sequence, but all are derived from a tRNA(Lys) or from a tRNA species structurally related to tRNA(Lys). The salmon Sma I family is present in the genomes of two species of the genus Oncorhynchus but not in other species, including five other species of the same genus. The charr Fok I family is present only in four species and subspecies of t ...[more]

PMID: 1848699

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Project description:BackgroundIn gene-dense genomes, mobile elements are confronted with highly selective pressure to amplify without causing excessive damage to the host. The targeting of tRNA genes as potentially safe integration sites has been developed by retrotransposons in various organisms such as the social amoeba Dictyostelium discoideum and the yeast Saccharomyces cerevisiae. In D. discoideum, tRNA gene-targeting retrotransposons have expanded to approximately 3 % of the genome. Recently obtained genome sequences of species representing the evolutionary history of social amoebae enabled us to determine whether the targeting of tRNA genes is a generally successful strategy for mobile elements to colonize compact genomes.ResultsDuring the evolution of dictyostelids, different retrotransposon types independently developed the targeting of tRNA genes at least six times. DGLT-A elements are long terminal repeat (LTR) retrotransposons that display integration preferences ~15 bp upstream of tRNA gene-coding regions reminiscent of the yeast Ty3 element. Skipper elements are chromoviruses that have developed two subgroups: one has canonical chromo domains that may favor integration in centromeric regions, whereas the other has diverged chromo domains and is found ~100 bp downstream of tRNA genes. The integration of D. discoideum non-LTR retrotransposons ~50 bp upstream (TRE5 elements) and ~100 bp downstream (TRE3 elements) of tRNA genes, respectively, likely emerged at the root of dictyostelid evolution. We identified two novel non-LTR retrotransposons unrelated to TREs: one with a TRE5-like integration behavior and the other with preference ~4 bp upstream of tRNA genes.ConclusionsDictyostelid retrotransposons demonstrate convergent evolution of tRNA gene targeting as a probable means to colonize the compact genomes of their hosts without being excessively mutagenic. However, high copy numbers of tRNA gene-associated retrotransposons, such as those observed in D. discoideum, are an exception, suggesting that the targeting of tRNA genes does not necessarily favor the amplification of position-specific integrating elements to high copy numbers under the repressive conditions that prevail in most host cells.

Project description:Whole-genome duplication (WGD) was experienced twice by the vertebrate ancestor (2 rounds; 2R), again by the teleost fish ancestor (3R) and most recently in certain teleost lineages (4R). Consequently, vertebrate gene families are often expanded in 3R and 4R genomes. Arguably, many types of "functional divergence" present across 2R gene families will exceed that between 3R/4R paralogs of genes comprising 2R families. Accordingly, 4R offers a form of replication of 2R. Examining whether this concept has implications for molecular evolutionary research, we studied insulin-like growth factor (IGF) binding proteins (IGFBPs), whose six 2R family members carry IGF hormones and regulate interactions between IGFs and IGF1-receptors (IGF1Rs). Using phylogenomic approaches, we resolved the complete IGFBP repertoire of 4R-derived salmonid fishes (19 genes; 13 more than human) and established evolutionary relationships/nomenclature with respect to WGDs. Traits central to IGFBP action were determined for all genes, including atomic interactions in IGFBP-IGF1/IGF2 complexes regulating IGF-IGF1R binding. Using statistical methods, we demonstrate that attributes of these protein interfaces are overwhelming a product of 2R IGFBP family membership, explain 49-68% of variation in IGFBP mRNA concentration in several different tissues, and strongly predict the strength and direction of IGFBP transcriptional regulation under differing nutritional states. The results support a model where vertebrate IGFBP family members evolved divergent structural attributes to provide distinct competition for IGFs with IGF1Rs, predisposing different functions in the regulation of IGF signaling. Evolution of gene expression then acted to ensure the appropriate physiological production of IGFBPs according to their structural specializations, leading to optimal IGF-signaling according to nutritional-status and the endocrine/local mode of action. This study demonstrates that relatively recent gene family expansion can facilitate inference of functional evolution within ancient genetic systems.

Dataset Information

Shaping and reshaping of salmonid genomes by amplification of tRNA-derived retroposons during evolution.

Publications

Shaping and reshaping of salmonid genomes by amplification of tRNA-derived retroposons during evolution.

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