Abstract
BackgroundIntron retention (IR), the most prevalent alternative splicing form in plants, plays a critical role in gene expression during plant development and stress response. However, the molecular mechanisms underlying IR regulation remain largely unknown.ResultsKnockdown of SDG725, a histone H3 lysine 36 (H3K36)-specific methyltransferase in rice, leads to alterations of IR in more than 4700 genes. Surprisingly, IR events are globally increased at the 5′ region but decreased at the 3′ region of the gene body in the SDG725-knockdown mutant. Chromatin immunoprecipitation sequencing analyses reveal that SDG725 depletion results in a genome-wide increase of the H3K36 mono-methylation (H3K36me1) but, unexpectedly, promoter-proximal shifts of H3K36 di- and tri-methylation (H3K36me2 and H3K36me3). Consistent with the results in animals, the levels of H3K36me1/me2/me3 in rice positively correlate with gene expression levels, whereas shifts of H3K36me2/me3 coincide with position-specific alterations of IR. We find that either H3K36me2 or H3K36me3 alone contributes to the positional change of IR caused by SDG725 knockdown, although IR shift is more significant when both H3K36me2 and H3K36me3 modifications are simultaneously shifted.ConclusionsOur results revealed that SDG725 modulates IR in a position-specific manner, indicating that H3K36 methylation plays a role in RNA splicing, probably by marking the retained introns in plants.
Highlights
Intron retention (IR), the most prevalent alternative splicing form in plants, plays a critical role in gene expression during plant development and stress response
SDG725 regulates a global shift of intron retention in rice Since H3K36 methylation has been proposed for splicing regulation in animals, we sought to investigate whether a similar mechanism is employed in plants
We found that the intron retention index (IRI)-up introns were favored at the 5′ portion of the gene body while the IRI-down introns were preferred at the 3′ portion of the gene body when comparing 725Ri-1 to WT rice plants using stringent coverage requirements (Fig. 1b, Additional file 1: Figure S3)
Summary
Intron retention (IR), the most prevalent alternative splicing form in plants, plays a critical role in gene expression during plant development and stress response. Intron retention (IR), a specific form of pre-messenger RNA (pre-mRNA) alternative splicing (AS), has attracted increasing attention given its role in global gene expression regulation in both animals and plants [1,2,3,4,5,6]. During Arabidopsis gametophyte development, IR regulates translation in a transcription-independent and spliceosome-dependent manner [14]. Taken together, all these findings underscore the importance of IR in plant growth and development
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