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.