Selection on the Genes of Euplotes crassus Tec1 and Tec2 Transposons: Evolutionary Appearance of a Programmed Frameshift in a Tec2 Gene Encoding a Tyrosine Family Site-Specific Recombinase

Abstract

The Tec1 and Tec2 transposons of the ciliate Euplotes crassus carry a gene for a tyrosine-type site-specific recombinase. The expression of the Tec2 gene apparently uses a programmed ؉1 frameshift. To test this hypothesis, we first examined whether this gene has evolved under purifying selection in Tec1 and Tec2. Each element carries three genes, and each has evolved under purifying selection for the function of its encoded protein, as evidenced by a dearth of nonsynonymous changes. This distortion of divergence is apparent in codons both 5 and 3 of the frameshift site. Thus, Tec2 transposons have diverged from each other while using a programmed ؉1 frameshift to produce recombinase, the function of which is under purifying selection. What might this function be? Tyrosine-type site-specific recombinases are extremely rare in eukaryotes, and Tec elements are the first known eukaryotic type II transposons to encode a site-specific recombinase. Tec elements also encode a widespread transposase. The Tec recombinase might function in transposition, resolve products of transposition (bacterial replicative transposons use recombinase or resolvase to separate joined replicons), or provide a function that benefits the ciliate host. Transposons in ciliated protozoa are removed from the macronucleus, and it has been proposed that the transposons provide this "excisase" activity.We have studied the evolution of ciliate Tec transposon sequences to compare their evolution in Euplotes crassus to that of TBE1 transposons in Oxytricha ciliates (49) as well as to examine the appearance of a frameshift site in a Tec2 gene (22). We have confirmed that this frameshift has been a functional mechanism, and we demonstrate that this gene and its homolog in Tec1 elements encode a tyrosine-type site-specific recombinase.The Tec and TBE elements encode a DDE transposase (conserved Asp, Asp, Gln residues in the active site) (10) and appear to be type II elements ("cut-and-paste" or "DNAmediated" elements) (5). The evolution of eukaryotic type II transposons has proved difficult to understand: purifying selection for transposase function is not expected to act on the transposase genes of eukaryotic cut-and-paste transposons within a host population and is generally not found (36,37,48,49). However, TBE1 transposons are a notable exception to this expectation. TBE1 transposon genes have evolved under strong selection for the function of their encoded proteins within their host ciliates (49): that is, nonsynonymous-or missense-mutations have been selected against and so removed from the pool of transposons in the host genome, while synonymous mutations have accumulated unabated. The reason for this selection is at present unknown, but it has been proposed that TBE1 transposons are under selection for a specific host function (28,46,49).Ciliated protozoa are unique transposon hosts because they carry two types of nuclei, a micronucleus and a macronucleus. The macronucleus is a terminally differentiated version of the micronucleus and provides a...

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