RNAi pathways contribute to developmental history-dependent phenotypic plasticity in C. elegans

Abstract

Early environmental experiences profoundly influence adult phenotypes through complex mechanisms that are poorly understood. We previously showed that adult Caenorhabditis elegans that transiently passed through the stress-induced dauer larval stage (post-dauer adults) exhibit significant changes in gene expression profiles, chromatin states, and life history traits when compared with adults that bypassed the dauer stage (control adults). These wild-type, isogenic animals of equivalent developmental stages exhibit different signatures of molecular marks that reflect their distinct developmental trajectories. To gain insight into the mechanisms that contribute to these developmental history-dependent phenotypes, we profiled small RNAs from post-dauer and control adults by deep sequencing. RNA interference (RNAi) pathways are known to regulate genome-wide gene expression both at the chromatin and post-transcriptional level. By quantifying changes in endogenous small interfering RNA (endo-siRNA) levels in post-dauer as compared with control animals, our analyses identified a subset of genes that are likely targets of developmental history-dependent reprogramming through a complex RNAi-mediated mechanism. Mutations in specific endo-siRNA pathways affect expected gene expression and chromatin state changes for a subset of genes in post-dauer animals, as well as disrupt their increased brood size phenotype. We also find that both chromatin state and endo-siRNA distribution in dauers are unique, and suggest that remodeling in dauers provides a template for the subsequent establishment of adult post-dauer profiles. Our results indicate a role for endo-siRNA pathways as a contributing mechanism to early experience-dependent phenotypic plasticity in adults, and describe how developmental history can program adult physiology and behavior via epigenetic mechanisms.

Endogenous RNAi Pathways Are Required in Neurons for Dauer Formation in Caenorhabditis elegans

“…Although dauer-inducing environmental conditions are detected by a complex network of chemosensory neurons found in the head of worms, little is known about the concurrent integration of these signals, and whether the dauer formation triggers may have distinct effects at a molecular level. We have shown previously that postdauer adults that experienced high pheromone conditions are phenotypically distinct from adults that bypassed the dauer stage, and that these effects are partially dependent upon RNAi pathways (Hall et al 2010(Hall et al , 2013. Our data presented here suggest the intriguing possibility that RNAi pathways may mediate distinct effects on gene expression in postdauer animals that experienced different environmental stresses.…”

“…Although adults that passed through, or bypassed, the dauer stage appear morphologically similar, we previously showed that C. elegans retain a cellular memory of their developmental history that is reflected in changes in gene expression, genome-wide chromatin states, and life history traits (Hall et al 2010). Furthermore, we have shown that RNAi pathways are a major contributor to developmental history-dependent phenotypes in adults (Hall et al 2013). However, the role of RNAi pathways in regulating environmentally induced phenotypic plasticity during early larval stages is unknown.…”

Screening and analysis of Hc-ubq and Hc-gst related to desiccation survival of infective Haemonchus contortus larvae

“…In nature, normal C. elegans harbors low desiccation tolerance, while diapausing worms own high tolerance (Erkut et al, 2011;Hall et al, 2013). Diapausing C. elegans enter a state of anhydrobiosis to maintain subsistence under dry conditions.…”

Developmental and Cell Cycle Quiescence Is Mediated by the Nuclear Hormone Receptor Coregulator DIN-1S in the Caenorhabditis elegans Dauer Larva

“…elegans is capable of spending an extensive period in the dauer stage without adverse effects on its postrecovery reproductive fitness. In fact, studies have demonstrated that lifespan and brood size are both marginally, yet significantly, enhanced following passage through dauer (Hall et al 2010(Hall et al , 2013.…”

“…elegans is capable of spending an extensive period in the dauer stage without adverse effects on its postrecovery reproductive fitness. In fact, studies have demonstrated that lifespan and brood size are both marginally, yet significantly, enhanced following passage through dauer (Hall et al 2010(Hall et al , 2013.Over 90% of daf-2 control animals recover from the dauer stage to become healthy, egg-laying adults regardless of whether they have previously spent 1, 3, or 7 days as dauer larvae (Figure 4). Although din-1S; daf-2 animals typically grow to become healthy adults, they display severe reproductive defects during the adult stage if they transit through dauer.…”