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

Abstract

Vernalisation is the process in which long-term cold exposure makes plants competent to flower. In vernalisation of Arabidopsis thaliana, a floral repressor, AtFLC, undergoes epigenetic silencing. Although the silencing of AtFLC is maintained under warm conditions after a sufficient duration of cold, FLC orthologues are reactivated under the same conditions in perennial plants, such as A. halleri. In contrast to the abundant knowledge on cold requirements in AtFLC silencing, it has remained unknown how cold duration affects the reactivation of perennial FLC. Here, we analysed the dynamics of A. halleri FLC (AhgFLC) mRNA, H3K4me3, and H3K27me3 over 8 weeks and 14 weeks cold followed by warm conditions. We showed that the minimum levels of AhgFLC mRNA and H3K4me3 were similar between 8 and 14 weeks vernalisation; however, the maximum level of H3K27me3 was higher after 14 weeks than after 8 weeks vernalisation. Combined with mathematical modelling, we showed that H3K27me3 prevents a rapid increase in AhgFLC expression in response to warm temperatures after vernalisation, which controls AhgFT expression and the initiation of flowering. Thus, the duration of cold defines the rate of AhgFLC reactivation via the buffering function of H3K27me3 against temperature increase.

The Flowering Season-Meter at FLOWERING LOCUS C Across Life Histories in Crucifers

“…A group of over 30 nucleosomes of the AtFLC locus appears to be structured in three regions with distinct H3K4me3/H3K27me3 dynamics ( Finnegan and Dennis, 2007 ; Yang et al, 2014 ). We note that all three domains can also be distinguished in A. halleri ( Nishio et al, 2020a , b ). The few nucleosomes spanning the short first exon and part of the first intron form a chromatin domain termed the nucleation region, NR.…”

“…These results indicate that AhgFLC serves as a memory of seasonal temperature throughout the year, not just during the cold season and that all four AhgFLC quadrants manifest stability characteristic of PcG/TrxG states. Notably, stability of AhgFLC dial-up and dial-down states was supported further: intermediate AhgFLC dial-up levels are maintained when plants were transplanted to cold ( Nishio et al, 2020a ), and the AhgFLC dial-down levels are proportional with the length of cold treatments ( Nishio et al, 2020b ), as known from A. thaliana ( Sheldon et al, 2006 ) and Arabis alpina ( Wang et al, 2009 ).…”

“…The greater bulk of nucleosomes along the coding region, including the long first intron, which is generally termed the gene body (GB). Finally, the distal end of FLC , encompassing the promoter and the 5′ end of the antisense non-coding RNA COOLAIR ( Swiezewski et al, 2009 ), marks the third domain, later termed distal Nucleation Region (dNR) ( Nishio et al, 2020a , b ).…”

“…The perennial life cycle in Arabidopsis halleri ssp. gemmifera ( A. halleri ) is unique in that all developing meristems first become reproductive, then revert to the vegetative phase by developing aerial rosettes, which then propagate clonally ( Aikawa et al, 2010 ; Satake et al, 2013 ; Nishio et al, 2016 , 2020a , b ; Honjo and Kudoh, 2019 ). These characteristics confer experimental advantages, especially in studies in the natural environment.…”

Digital paradigm for Polycomb epigenetic switching and memory

“…The seasonal dynamics of histone modifications at FLC were recently studied in a natural population of the perennial Arabidopsis halleri [ 27 •• , 28 ]. Mathematical modelling was also used to interpret the H3K27me3 dynamics in terms of cis-mediated digital nucleation and spreading: like in the closely related A. thaliana , AhFLC shows H3K27me3 nucleation close to the transcriptional start site during the winter months and delayed spreading of the repressive mark across the locus with increasing temperatures in late winter and spring.…”