piRNA loss unleashes episodic transposition bursts

Area of Science:

• Genetics
• Molecular Biology
• Evolutionary Biology

Background:

• The piwi-interacting RNA (piRNA) pathway is crucial for suppressing transposable element (TE) expression in Metazoa.
• Disruption of the piRNA pathway leads to increased TE expression, but the consequences for actual transposition remain poorly understood.

Purpose of the Study:

• To investigate whether increased TE expression upon piRNA pathway loss results in actual transposition.
• To identify which TEs mobilize and their frequency following piRNA pathway disruption.
• To characterize the dynamics of TE mobilization across generations in Drosophila.

Main Methods:

• Development of a framework to track TE copy accumulation across generations in the Drosophila male germline.
• Utilizing single-fly Nanopore DNA sequencing to analyze TE insertions.
• Employing genomic DNA collection at each generation for validation and dating of TE insertions.
• Conducting phylogenetic analysis to study TE mobilization patterns.

Main Results:

• Multiple TE families, including copia, mdg3, and invader3, mobilized after 10-45 generations of piRNA pathway loss.
• The copia transposon was the most prolific, with dozens of new insertions distributed across chromosome arms.
• TE mobilization occurred in episodic bursts, deviating significantly from a Poisson process, indicating stochasticity.
• Direct evidence was obtained showing the piRNA pathway tightly suppresses germline transposition.

Conclusions:

• The piRNA pathway is essential for suppressing germline transposition in Drosophila.
• Disruption of the piRNA pathway triggers punctuated, stochastic bursts of TE movement, rather than a simple rate increase.
• These bursts can significantly alter the timing and magnitude of mutational input during evolution.