Removal of Retained Introns Regulates Translation in the Rapidly Developing Gametophyte of Marsilea vestita

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. ⺠The microspore of the fern M. vestita stores RNA that is translationally repressed ⺠Many RNAs stored in the dry microspore are intron-retaining transcripts (IRTs) ⺠IRTs encode essential proteins for spermatogenesis ⺠Removal of retained introns precedes translation critical for gamete development