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 long-term 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.

Highlights

  • Natural environments require organisms to possess robust mechanisms allowing responses to seasonal trends

  • Arabidopsis thaliana FLOWERING LOCUS C (FLC) undergoes epigenetic silencing during vernalisation — a process in which plants become competent to flower after experiencing a period of prolonged cold of winter — in its life cycle as an annual plant

  • We find that H3K27me[3] at the posterior region of the AhgFLC locus may contribute to the ratchet-like character of the AhgFLC system — reversible during the entire perennial life cycle but irreversible during the upregulation phase in spring

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Summary

Introduction

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. One is the ability to respond to the long-term temperature trends via bidirectional interactions between H3K27me[3] and H3K4me[3]; 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. We speculated that unexplored properties of AhgFLC regulation would permit the identification of long-term trends after short-term fluctuations were filtered out, allowing spring and autumn to be distinguished and preventing springtime AhgFLC repression. Arabidopsis thaliana FLC (hereafter AtFLC) undergoes epigenetic silencing during vernalisation — a process in which plants become competent to flower after experiencing a period of prolonged cold of winter — in its life cycle as an annual plant.

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