Soma-derived 30-nt small RNAs are coupled with chromosome breakage and precisely target nontransposon DNA against elimination in Euplotes vannus.

Metazoans suppress transposons via small RNA-mediated silencing, but ciliates physically eliminate transposons from somatic genomes. Here, we report the high-quality germline genome assembly of a marine ciliate Euplotes vannus, where ~80% are transposons and other germline-specific DNA that has to be precisely eliminated during soma development. We demonstrate that a class of soma-derived 30-nucleotide small RNAs precisely targets nontransposon DNA against elimination during this process. Small RNA-mediated targeting remains functional across varying small RNA lengths and is compatible with heterozygous sites. These small RNAs are cleaved by Dicer-like ribonuclease from long noncoding RNAs, which are bidirectionally transcribed of somatic chromosomes, initiated at subtelomeric chromosome breakage sequences (5'-TTGAA-3'). On the basis of these findings and time-course transcriptomic profiling, we propose a model elucidating the molecular mechanism of DNA elimination in Euplotes. These findings provide insights into the role of small RNAs in transmitting genetic information across generations and maintaining genome stability.