What can PIWI-interacting RNA research learn from chickens, and vice versa?

Xin Zhiguo Li,J. Plaizier

doi:10.1139/cjas-2018-0252

Abstract

P-element induced wimpy testis (PIWI) interacting RNA (piRNA) are essential for fertility, by protecting the integrity of the germ-line genome via silencing of transposable elements (TE). Because new TE are constantly invading the host genome, piRNA-producing loci are under continuous pressure to undergo rapid evolution. This arms race between TE and piRNA is a prime example of the genome being more plastic than previously thought. Historically, the study of piRNA and TE has benefited from the use of diverse model organisms, including worms, fruit fly, zebrafish, frogs, and mice. In domestic chickens, we recently identified a new mode of piRNA acquisition in which the host hijacks and converts a pre-existing provirus into a piRNA-producing locus to defend against Avian leukosis virus, an adaptive immune strategy similar to the prokaryotic CRISPR–Cas [clustered regularly interspaced short palindromic repeats (CRISPR) and CRISPR-associated (Cas)] system. This finding reveals a previously unrecognized mechanism of the host piRNA repertoire to rapidly evolve and target TE specifically. In this review, we will focus on both the unique and common features of chicken piRNA, as well as the advantages of using chickens as a model system, to address fundamental questions regarding piRNA acquisition in hosts. We will also comment on the potential application of piRNA for improving poultry health and reproductive efficiency.

Highlights

The capacity of PIWI-interacting RNAs (piRNAs) to mediate both transcriptional and post-transcriptional regulation distinguishes them from widely used miRNA/siRNA treatments and gives them great potential to serve as an innovative tool for gene-specific repression
Akin to piRNA reads from adult mouse testis, 70% of piRNA reads from roosters uniquely map to unannotated intergenic regions
Such feature of dual-strand piRNA clusters was thought to be specific to fruit flies (Brennecke et al 2007; Malone et al 2009; Czech et al 2018), which is due to noncanonical transcription machinery (Andersen et al 2017)

Summary

Chicken piRNAs

We and others have pioneered piRNA studies in chickens (Li et al 2013; Rengaraj et al 2014; Chirn et al 2015; Chang et al 2018), uncovering the unique features of the chicken piRNA pathway, as well as its commonalities with that of other organisms. Mapped piRNAs are derived from both strands Such feature of dual-strand piRNA clusters was thought to be specific to fruit flies (Brennecke et al 2007; Malone et al 2009; Czech et al 2018), which is due to noncanonical transcription machinery (Andersen et al 2017). The mechanism underlying convergent transcription of chicken piRNA clusters is unclear. We detected robust piRNA-mediated post-transcriptional silencing of TEs (Li et al 2013; Sun et al 2017). Some features of chicken piRNAs resemble mammalian system, while some of them resemble other model organisms (Table 1), the use of chickens for piRNA studies may unify distinct features from diverse model organisms and shed light on the evolution of piRNA pathway

TEs in chickens

New piRNA acquisition

The advantages of using chickens as model organisms

Findings

Utilizing piRNAs to improve reproductive health in the poultry industry