Environmentally-induced epigenetic conversion of a piRNA cluster

Area of Science:

• Epigenetics
• RNA biology
• Genomics

Background:

• Transposable element (TE) activity in animal gonads is suppressed by PIWI-interacting RNAs (piRNAs).
• Germinal piRNA clusters are typically thought to be activated through maternal inheritance of piRNAs from the previous generation in flies.
• The precise mechanisms for initiating piRNA production from previously inactive clusters remain incompletely understood.

Purpose of the Study:

• To investigate the potential for environmental factors to initiate piRNA production from an inactive piRNA cluster.
• To explore the role of temperature and transcription in the de novo activation of piRNA clusters.
• To challenge the prevailing model of maternal inheritance for piRNA cluster activation.

Main Methods:

• Utilized a P-element derived transgene insertion in Drosophila melanogaster as a model for an inactive piRNA cluster.
• Exposed flies to elevated temperatures (29°C) compared to standard conditions (25°C).
• Analyzed piRNA production, antisense transcript levels, and the requirement for transcription of homologous sequences.

Main Results:

• High temperature (29°C) induced stable conversion of the inactive piRNA cluster into an active producer of functional piRNAs.
• Increased antisense transcripts were observed from the cluster at 29°C.
• Transcription of euchromatic homologous sequences was necessary for this de novo piRNA production, suggesting a role for double-stranded RNA.

Conclusions:

• Environmental changes, specifically elevated temperature, can trigger the establishment of active piRNA clusters.
• This study presents the first evidence of de novo piRNA cluster activation independent of maternal piRNA inheritance.
• The findings suggest a novel pathway for epigenetic regulation of transposable elements involving temperature-induced transcription and double-stranded RNA intermediates.