A dynamic intron retention program regulates the expression of several hundred genes during pollen meiosis.

Abstract

Key message: Intron retention is a stage-specific mechanism of functional attenuation of a subset of co-regulated, functionally related genes during early stages of pollen development. To improve our understanding of the gene regulatory mechanisms that drive developmental processes, we performed a genome-wide study of alternative splicing and isoform switching during five key stages of pollen development in field mustard, Brassica rapa. Surprisingly, for several hundred genes (12.3% of the genes analysed), isoform switching results in stage-specific expression of intron-retaining transcripts at the meiotic stage of pollen development. In such cases, we report temporally regulated switching between expression of a canonical, translatable isoform and an intron-retaining transcript that is predicted to produce a truncated and presumably inactive protein. The results suggest a new pervasive mechanism underlying modulation of protein levels in a plant developmental program. The effect is not based on gene expression induction but on the type of transcript produced. We conclude that intron retention is a stage-specific mechanism of functional attenuation of a subset of co-regulated, functionally related genes during meiosis, especially genes related to ribosome biogenesis, mRNA transport and nuclear envelope architecture. We also propose that stage-specific expression of a non-functional isoform of Brassica rapa BrSDG8, a non-redundant member of histone methyltransferase gene family, linked to alternative splicing regulation, may contribute to the intron retention observed.