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.
Abstract
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.
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Acknowledgements
The research was supported by ARC Discovery grant DP0988972 (PB), McKenzie Fellowship (AG) and to the University of Melbourne Research Scholarship (NL). This research was supported by Spartan HPC (Lev Lafayette GS, Linh Vu, Bernard Meade October 27, 2016) at the University of Melbourne, Australia.
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AAG designed the bioinformatics pipeline, analysed the sequencing data and wrote the manuscript; ADA initiated and standardized the pollen developmental stages, and prepared plant material for sequencing; WL performed RT-PCR validation; NL prepared independent replicate plant material and IGV view of the genes; MBS conceived research and wrote the manuscript; PLB conceived and designed the research, supervised and wrote the manuscript.
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Golicz, A.A., Allu, A.D., Li, W. et al. A dynamic intron retention program regulates the expression of several hundred genes during pollen meiosis. Plant Reprod 34, 225–242 (2021). https://doi.org/10.1007/s00497-021-00411-6
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DOI: https://doi.org/10.1007/s00497-021-00411-6