A piggyBac transposase expressed from a germline-limited sequence is required for precise excision in Tetrahymena genome rearrangement

In the ciliated protozoan Tetrahymena thermophila, programmed genome rearrangement accompanies the differentiation of the somatic macronucleus (MAC) from the germline micronucleus (MIC). Internal eliminated sequences (IES) are excised, followed by rejoining of MAC-destined sequences, while fragmentation occurs at conserved chromosome breakage sequences (CBS), followed by de novo telomere addition. Here we demonstrate that although most fragments bounded by CBS are kept as MAC chromosomes, some—referred to as non-maintained chromosomes (NMC)—are lost after MAC differentiation. Importantly, large NMC contain genes specifically expressed during MAC differentiation and implicated in development-specific roles. In particular, TPB3, a domesticated piggyBac transposase, is required for precise excision of a special class of IES interrupting host genes with important functions. Our results reveal a novel exaptation of programmed genome rearrangement to achieve a development-specific gene expression pattern, which may be a recurring theme in eukaryotic organisms experiencing programmed genome rearrangement during germline to soma differentiation.