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

Haruki Nishio,Hiroshi Kudoh,Koji Iwayama

doi:10.1038/s41598-020-72566-7

Haruki Nishio, Hiroshi Kudoh + Show 1 more

Open Access

https://doi.org/10.1038/s41598-020-72566-7

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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.

Highlights

Vernalisation is the process in which long-term cold exposure makes plants competent to flower
In the 14 weeks vernalisation treatment, bolting started after 10 weeks of cold, while flowering and reversion started only after transfer to the warm condition (Fig. 1i). These data indicate that AhgFLC mRNA levels and the H3K4me[3] levels at the nucleation region were saturated after 8 weeks of cold, and the minimum levels were similar between the 8 weeks and 14 weeks vernalisation treatments
Our time series data showed that the H3K27me[3] levels at all regions of AhgFLC were not saturated even after 8 weeks of cold, and continued to increase up to 14 weeks of cold. These results are similar to those reported for the Lov-1 accession of A. thaliana[18,19]; differences between annual and perennial plants exist in the response to warm conditions following exposure to long-term cold

Summary

Introduction

Vernalisation is the process in which long-term cold exposure makes plants competent to flower. 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 the AtFLC silencing process, the effect of cold duration on the upregulation of perennial FLC orthologues on return to warm has remained to be determined. FLC orthologues are silenced in a quantitative manner under cold conditions as well as A. thaliana; they are upregulated under warm conditions following vernalisation in perennial plants, Arabidopsis. It is expected that an insufficient cold duration would affect flowering through the perturbation of perennial FLC upregulation

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