Transgenerational epigenetic inheritance of
sid-1 silencing (
sid-1 TEI) is one of the few well-characterized examples of TEI that manifests in both germline and somatic tissues. Somatic
sid-1 TEI requires chromatin-modifying factors, whereas germline silencing depends solely on RNAi factors indicating distinct mechanisms. To further characterize the roles and inter-dependency of nuclear and cytoplasmic RNAi machinery in the initiation and inheritance of
sid-1 TEI, we used a unigametic germline inheritance system. In this system, maternal and paternal pronuclei do not fuse at fertilization and correspondingly form AB and P1 cell lineages. In the case of an embryo produced by epigenetically silenced
sid-1 mother, the naive paternal pronucleus that forms germline cells is exposed to maternal cytoplasmic but not nuclear TEI factors. Therefore, F2-self progeny derived entirely from the paternal genome may inherit silencing provided by only cytoplasmic TEI information. We found these animals to be fully resistant to germline
dpy-11(RNAi) (
sid-1 silenced) for at least six generations. This result demonstrates nuclei-independent transmission of transgenerational
sid-1 germline silencing. Surprisingly, the germline-silenced F2 animals failed to show any resistance to somatic
dpy-11(RNAi). This result implies that nuclear TEI machinery is not required to transmit somatic
sid-1 silencing. Moreover, somatic
sid-1 silencing was not observed during the six generations of persistent germline silencing. This indicates that germline silencing is not sufficient to prime somatic silencing. Taken together, our results put forward a working hypothesis that nuclear factors from the silenced parent are required to establish somatic silencing and that somatic and germline silencing are initiated and maintained independently.