An Orchestrated Intron Retention Program in Meiosis Controls Timely Usage of Transcripts during Germ Cell Differentiation

Publication date: Available online 30 March 2017
Source:Developmental Cell
Author(s): Chiara Naro, Ariane Jolly, Sara Di Persio, Pamela Bielli, Niclas Setterblad, Antonio J. Alberdi, Elena Vicini, Raffaele Geremia, Pierre De la Grange, Claudio Sette
Global transcriptome reprogramming during spermatogenesis ensures timely expression of factors in each phase of male germ cell differentiation. Spermatocytes and spermatids require particularly extensive reprogramming of gene expression to switch from mitosis to meiosis and to support gamete morphogenesis. Here, we uncovered an extensive alternative splicing program during this transmeiotic differentiation. Notably, intron retention was largely the most enriched pattern, with spermatocytes showing generally higher levels of retention compared with spermatids. Retained introns are characterized by weak splice sites and are enriched in genes with strong relevance for gamete function. Meiotic intron-retaining transcripts (IRTs) were exclusively localized in the nucleus. However, differently from other developmentally regulated IRTs, they are stable RNAs, showing longer half-life than properly spliced transcripts. Strikingly, fate-mapping experiments revealed that IRTs are recruited onto polyribosomes days after synthesis. These studies reveal an unexpected function for regulated intron retention in modulation of the timely expression of select transcripts during spermatogenesis.

Teaser

Transcription during mammalian spermatogenesis is discontinuous and ceases in late post-meiotic stages. Naro et al. show that regulated intron retention in male meiotic germ cells generates long-lived intron-retaining transcripts that are preserved for days after their synthesis and can be timely translated by transcriptionally inactive post-meiotic germ cells.


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