Spontaneous germline excision ofTol1, a DNA-based transposable element naturally occurring in the medaka fish genome

Abstract

DNA-based transposable elements are ubiquitous constituents of eukaryotic genomes. Vertebrates are, however, exceptional in that most of their DNA-based elements appear to be inactivated. The Tol1 element of the medaka fish, Oryzias latipes, is one of the few elements for which copies containing an undamaged gene have been found. Spontaneous transposition of this element in somatic cells has previously been demonstrated, but there is only indirect evidence for its germline transposition. Here, we show direct evidence of spontaneous excision in the germline. Tyrosinase is the key enzyme in melanin biosynthesis. In an albino laboratory strain of medaka fish, which is homozygous for a mutant tyrosinase gene in which a Tol1 copy is inserted, we identified de novo reversion mutations related to melanin pigmentation. The gamete-based reversion rate was as high as 0.4%. The revertant fish carried the tyrosinase gene from which the Tol1 copy had been excised. We previously reported the germline transposition of Tol2, another DNA-based element that is thought to be a recent invader of the medaka fish genome. Tol1 is an ancient resident of the genome. Our results indicate that even an old element can contribute to genetic variation in the host genome as a natural mutator.

A chromosome-level, haplotype-resolved genome assembly and annotation for the Eurasian minnow (Leuciscidae: Phoxinus phoxinus) provide evidence of haplotype diversity

“…The Kimura substitution level is correlated with the age of transposition activity: low substitution levels indicate recent transposition events; higher substitution levels suggest old transposition events. The repeat landscape of the annotated P. phoxinus genome (Figure 2) indicates a high level of active, i.e., recent, transposition bursts (Watanabe et al, 2014). In fish genomes, active transposons accumulate at a faster rate than they decline (Shao et al, 2019), leading to an abundance of active transposons with low Kimura substitution levels (Böhne et al, 2012; Gao et al, 2016; Sotero-Caio et al, 2017), an exact pattern observed in TEs in the P. phoxinus genome.…”

TRT, a Vertebrate and ProtozoanTc1-Like Transposon: Current Activity and Horizontal Transfer

“…To date, only some Tc1 -like elements (such as Tol1 , Tol2 , Passport , and Tana1 ) that were identified in bony fishes have been demonstrated to be transpositionally active ( Koga et al 2006 ; Clark et al 2009 ; Pujolar et al 2013 ; Watanabe et al 2014 ). Previous studies showed that most Tc1 -like elements in fishes are inactive because of stop codons, deletions, or frameshifts within their sequences ( Radice et al 1994 ; Reed 1999 ).…”

“…Importantly, active Tc1/mariner transposons may be potentially used as molecular tools for transgenesis and insertion mutagenesis ( Pavlopoulos et al 2007 ; Voigt et al 2016 ). To date, only some Tc1 -like elements (such as Tol1 , Tol2 , Passport , and Tana1 ) in bony fishes are known to be both intact in their native form and transpositionally active ( Koga et al 2006 ; Clark et al 2009 ; Pujolar et al 2013 ; Watanabe et al 2014 ).…”

TE studies in Japan: the fourth Japanese meeting on host–transposon interactions

“…These findings suggest that the small DNA insertions and deletions detected in related genes among different species could have been generated by an ancient “paste-and-cut” transposition. Even almost fossilized DNA transposons, such as the medaka Tol1 element, are capable of undergoing transposition bursts [8]. Based on these findings, A. Koga proposed that DNA transposons, by acting as the major source of small DNA insertions and deletions, could have a more significant role in the evolution of their host genomes than was previously postulated.…”