Abstract
Chromatin regulation ensures stable repression of stress-inducible genes under non-stress conditions and transcriptional activation and memory of stress-related genes after stress exposure. However, there is only limited knowledge on how chromatin genes are regulated at the transcriptional and post-transcriptional level upon stress exposure and relief from stress. We reveal that the repressive modification histone H3 lysine 27 trimethylation (H3K27me3) targets genes which are quickly activated upon cold exposure, however, H3K27me3 is not necessarily lost during a longer time in the cold. In addition, we have set-up a quantitative reverse transcription polymerase chain reaction-based platform for high-throughput transcriptional profiling of a large set of chromatin genes. We find that the expression of many of these genes is regulated by cold. In addition, we reveal an induction of several DNA and histone demethylase genes and certain histone variants after plants have been shifted back to ambient temperature (deacclimation), suggesting a role in the memory of cold acclimation. We also re-analyze large scale transcriptomic datasets for transcriptional regulation and alternative splicing (AS) of chromatin genes, uncovering an unexpected level of regulation of these genes, particularly at the splicing level. This includes several vernalization regulating genes whose AS may result in cold-regulated protein diversity. Overall, we provide a profiling platform for the analysis of chromatin regulatory genes and integrative analyses of their regulation, suggesting a dynamic regulation of key chromatin genes in response to low temperature stress.
Highlights
Plants are exposed to a multitude of abiotic and biotic stresses during their lifetime and have evolved efficient mechanisms to cope with such events
By bioinformatics comparison of H3K27me3 target genes and a detailed kinetic analysis of cold-regulated genes, we revealed an enrichment of H3K27me3 target genes among the early inducible genes
As the early inducible genes are required to trigger a cascade of gene regulatory networks to permit cold acclimation, it is likely important to control their tight repression in non-stress conditions
Summary
Plants are exposed to a multitude of abiotic and biotic stresses during their lifetime and have evolved efficient mechanisms to cope with such events. Vernalization is defined as the acquisition of the competence to flower after prolonged cold treatment, allowing vernalizationresponsive plants to flower in spring, under favorable temperature conditions and the appropriate photoperiod. This process relies on epigenetic mechanisms, as cold induces a mitotically stable switch inhibiting the expression of the floral repressor FLOWERING LOCUS C (FLC). Changes in the chromatin state were previously described for cold-inducible genes not involved in vernalization, suggesting the involvement of dynamic chromatin regulation in the induction and repression of cold stress-responsive genes (Kwon et al, 2009; Park et al, 2018). The existence of memory of a cold priming event, including transcriptional memory, resulting in improved freezing tolerance after a subsequent triggering cold treatment was recently shown (Zuther et al, 2019)
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