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 tRNALYS or from a tRNA species structurally related to tRNALyS. 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 protoSalmonidae 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.Gene duplication is believed to be of major importance in creating genetic diversity (1). The genes for immunoglobulins, histocompatibility complexes, and globins are examples of this gene duplication. This mechanism operates at the DNA level and probably has as old a history as DNA genomes themselves. Another mechanism for maintaining the fluidity of eukaryotic genomes is that recently characterized retroposition, in which information in nonviral cellular RNA can flow back into the genome via cDNA intermediates (2,3). Retroposition creates additional sequence combinations through dispersal of genetic information and can shape and reshape eukaryotic genomes in many different ways (3,4). The precise mechanism of retroposition is at present speculative. Recently, Weiner and Meizels (5) presented an interesting hypothesis concerning the mechanism of generation of duplex DNA at the beginning of the DNA world, proposing that duplex DNA genomes may have been derived from earlier DNA genomes that replicated like retroviruses through an RNA intermediate. This suggests that the mechanism of retroposition might be closely linked to that of replication of retroviruses (6).The highly repetitive sequences that are interspersed throughout eukaryotic genomes have been classified into two categories based on size: long interspersed repetitive elements (LINEs), which include Li sequences, and short interspersed repetitive elements (SINEs), such as the primate Alu and rodent type 1 or 2 Alu families (7). Previously, highly repetitive and transcribable sequences have been found in the genome of the chum salmon (Oncorhynchus keta) (8,9). Like all SINE families examined so far (10-14) other than Alu (15, 16), this Sma I family [formerly the salmon polymerase (Pol) III/SINE family] has been shown to be derived from a tRNA; moreover the Sma I family has several of the characteristic features of retroposons and appears to be the youngest SINE family characterized to date.The genus Oncorhynchus has many s...

SINE sequences detect DNA fingerprints in salmonid fishes

“…The distribution of Hpa as detected by the Hpa I 5' probe was consistent with that reported by Kido et al (1991). However, initial results with the oligonucleotide homologous to the 5' end of Fok I were not consistent with the distribution reported by Kido et a!.…”

“…1). The sequence on which these probes were based was obtained from the cherry salmon (Oncorhynchus masou) (Kido et al, 1991), thus this observation may reflect divergence in the sequence of the SINE among genera. There also might be fewer copies of the element in Salve/inus than in the other genera.…”

“…It thus seems unlikely that we are detecting a repetitive element other than the SINEs we have targeted. However, if 10000 copies of each of these elements are randomly distributed throughout the salmonid genome (Kido et a!., 1991), the detection of only 35-40 bands per individual is surprising. This observation has several possible interesting explanations which are currently difficult to evaluate.…”

“…The recognition sites for these enzymes are not found in the consensus sequence of either the Hpa I or Fok I SINEs reported by Kido et al (1991) and thus they should cut outside the SINEs, leaving intact elements in the digested DNA. Two jg of each sample were then loaded into either 0.8 or 1.0 per cent agarose gels and electrophoresed in 1 x TAE buffer at 50 volts for 24 h at 4°C with buffer recirculation.…”

“…(1991). This led us to hybridize membranes with probes derived from the 3' end of Fok I and subsequently Hpa I to determine which regions of the SINEs were responsible for the distributions reported by Kido et al (1991). In addition to the oligonucleotide probes, a 172 base pair segment of Hpa I was amplified and used as a probe.…”