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The utilization of stored RNA is a driving force in rapid development. Here, we show that retention and subsequent removal of introns from pre-mRNAs regulate temporal patterns of translation during rapid and posttranscriptionally controlled spermatogenesis of the fern Marsilea vestita. Analysis of RNAseq-derived transcriptomes revealed a large subset of intron-retaining transcripts (IRTs) that encode proteins essential for gamete development. Genomic and IRT sequence comparisons show that other introns have been previously removed from the IRT pre-mRNAs. Fully spliced isoforms appear at distinct times during development in a spliceosome-dependent and transcription-independent manner. RNA interference knockdowns of 17/17 IRTs produced anomalies after the time points when those transcripts would normally be spliced. Intron retention is a functional mechanism for forestalling precocious translation of transcripts in the male gametophyte of M. vestita. These results have broad implications for plant gene regulation, where intron retention is widespread.
► The microspore of the fern M. vestita stores RNA that is translationally repressed ► Many RNAs stored in the dry microspore are intron-retaining transcripts (IRTs) ► IRTs encode essential proteins for spermatogenesis ► Removal of retained introns precedes translation critical for gamete development
Studying posttranscriptional regulation of spermatogenesis in the fern Marsilea vestita, Boothby et al. show that intron retention is an essential regulator of rapid plant development. Removal of introns from pre-mRNAs in the microspore during male gametophyte development provides key temporal control of translation and gene expression.