Repressive chromatin modification underpins the long-term expression trend of a perennial flowering gene in nature

Abstract

Natural environments require organisms to possess robust mechanisms allowing responses to seasonal trends. In Arabidopsis halleri, the flowering regulator AhgFLC shows upregulation and downregulation phases along with long-term past temperature, but the underlying machinery remains elusive. Here, we investigate the seasonal dynamics of histone modifications, H3K27me3 and H3K4me3, at AhgFLC in a natural population. Our advanced modelling and transplant experiments reveal that H3K27me3-mediated chromatin regulation at AhgFLC provides two essential properties. One is the ability to respond to the long-term temperature trends via bidirectional interactions between H3K27me3 and H3K4me3; the other is the ratchet-like character of the AhgFLC system, i.e. reversible in the entire perennial life cycle but irreversible during the upregulation phase. Furthermore, we show that the longterm temperature trends are locally indexed at AhgFLC in the form of histone modifications. Our study provides a more comprehensive understanding of H3K27me3 function at AhgFLC in a complex natural environment.

Duration of cold exposure defines the rate of reactivation of a perennial FLC orthologue via H3K27me3 accumulation

“…1). As previously defined 24 , the AhgFLC locus was classified into three regions: the nucleation region, the linker region, Reversion, leaf formation at the reproductive shoot apical meristem. In (b-i), temperature regimes are represented by grey lines (4 °C in cold and 20/15 °C D/N in warm, shown by the average value).…”

“…In A. halleri, the influence of DNA replication on the reduction of H3K27me3 would be minimal, given the fact that we analysed AhgFLC H3K27me3 levels in fully expanded leaves wherein cell division and endoreduplication are inactive 35,36 . We previously revealed that AhgFLC transcription starts earlier than the reduction of H3K27me3 at the locus 24 , which might trigger the active removal of the modification by recruiting H3K27me3 demethylases. Similar processes have been proposed as a candidate mechanism of Lov-1 AtFLC reactivation 19 .…”

“…Therefore, our mathematical modelling indicates that H3K27me3 buffers sudden changes in AhgFLC mRNA level associated with temperature changes by the interaction with H3K4me3 at the two nucleation regions. In our mathematical modelling to simulate active and repressive histone modifications at the proximal/distal nucleation regions at AhgFLC, we needed to analyse H3K4me3 and H3K27me3 which accumulate at these regions 24 . However, as H3K36me3 is known to be antagonistic to H3K27me3 at AtFLC in A. thaliana 15,19 , modelling of AhgFLC H3K36me3 dynamics should be addressed in future studies.…”

“…www.nature.com/scientificreports/ halleri [20][21][22][23][24][25] , Arabidopsis lyrata 26 , and Arabis alpina [27][28][29] . H3K27me3 accumulates at perennial FLC orthologues under cold conditions and is removed from the locus in response to warm temperatures 24,25,27 . In perennial plants, the upregulation of FLC orthologues under warm conditions following vernalisation would antagonise the upregulation of FT orthologues and flowering.…”

Fine tuning of hormonal signaling is linked to dormancy status in sweet cherry flower buds

“…The next steps, in addition to the integration of GA signaling and its crosstalk with ABA, will be to provide information on temperaturemediated control of the regulatory cascades. Recent research led on Arabidopsis, allowed by highthroughput sequencing techniques, has hastened the pace for the incorporation of molecular data into phenology models (Satake et al 2013, Kudoh 2016, Antoniou-Kourounioti et al 2018, Nishio et al 2020), thus opening new roads for perennial studies.…”