Histone H3 lysine 36 methylation affects temperature-induced alternative splicing and flowering in plants

Abstract

Background: Global warming severely affects flowering time and reproductive success of plants. Alternative splicing of pre-messenger RNA (mRNA) is an important mechanism underlying ambient temperature-controlled responses in plants, yet its regulation is poorly understood. An increase in temperature promotes changes in plant morphology as well as the transition from the vegetative to the reproductive phase in Arabidopsis thaliana via changes in splicing of key regulatory genes. Here we investigate whether a particular histone modification affects ambient temperature-induced alternative splicing and flowering time.Results: We use a genome-wide approach and perform RNA-sequencing (RNA-seq) analyses and histone H3 lysine 36 tri-methylation (H3K36me3) chromatin immunoprecipitation sequencing (ChIP-seq) in plants exposed to different ambient temperatures. Analysis and comparison of these datasets reveal that temperature-induced differentially spliced genes are enriched in H3K36me3. Moreover, we find that reduction of H3K36me3 deposition causes alteration in temperature-induced alternative splicing. We also show that plants with mutations in H3K36me3 writers, eraser, or readers have altered high ambient temperature-induced flowering. Conclusions: Our results show a key role for the histone mark H3K36me3 in splicing regulation and plant plasticity to fluctuating ambient temperature. Our findings open new perspectives for the breeding of crops that can better cope with environmental changes due to climate change.

Histone modifications during the life cycle of the brown alga Ectocarpus

“…H3K36me3 is catalysed by SETD2, which is associated with Pol II and is therefore directly linked to transcript elongation. H3K36me3 has also been shown to be involved in alternative splicing in animals and plants [49,50]. The position of H3K36me3 within Ectocarpus genes and the positive correlation with transcript abundance are consistent with an evolutionarily conserved role associated with transcript elongation.…”

Empirical patterns of environmental variation favor adaptive transgenerational plasticity

“…Experimental studies have identified adaptive plastic responses to temperature changes, both within and across generations. For example, ambient temperature in Arabidopsis thaliana has been shown to influence the expression and splicing of hundreds of genes, leading to changes in histone methylation (Pajoro, Severing, Angenent, & Immink, ), and shifts in flowering time (Donohue, ) and other phenotypes (Adams, Stewart, Cohu, Muller, & Demmig‐Adams, ) in genotype‐specific ways. Additionally, recent work has demonstrated that effects of temperature on A. thaliana plants persist for multiple generations (Groot et al, ; Suter & Widmer, , ; Whittle et al, ).…”

Chromatin-mediated alternative splicing regulates cocaine reward behavior

“…We next sought to build on previous evidence that links Set2-dependent H3K36me3 to alternative splicing (De Almeida et al, 2011;Luco et al, 2010;Pajoro et al, 2017;Sessa et al, 2019;Xu et al, 2017;Yuan et al, 2017;Zhou et al, 2012). Although in higher eukaryotes multiple H3K36 methyltransferases catalyze H3K36me1 and H3K36me2, the yeast Set2 homolog is specific to H3K36me3 (McDaniel and Strahl, 2017;Sorenson et al, 2016;Strahl et al, 2002).…”

“…Recent bioinformatic studies find that epigenetic features may be more important than gene sequence in differentiating splicing patterns (De Almeida et al, 2011;Bonev et al, 2017;Pajoro et al, 2017;Yuan et al, 2017;Zhou et al, 2012). Using agnostic classical statistical and machine-learning methods we previously found that histone H3 lysing 36 trimethylation (H3K36me3) is the most informative histone post-translational modification (hPTM) in predicting splicing events in the nucleus accumbens (NAc), a key brain reward region (Hu et al, 2017), and in multiple tissues across development .…”