An H3K27me3 demethylase-HSFA2 regulatory loop orchestrates transgenerational thermomemory in Arabidopsis

Junzhong Liu,Xiaofeng Cao,Ertao Wang,Yuke He,Qi Qiu,Xueting Gu,Yiwen Deng,Jianming Li,Yingying Zhang,Isabel Bäurle,Lili Feng,Xian Deng,Muyang Wang,Zuhua He,Qun Li

doi:10.1038/s41422-019-0145-8

Abstract

Global warming has profound effects on plant growth and fitness. Plants have evolved sophisticated epigenetic machinery to respond quickly to heat, and exhibit transgenerational memory of the heat-induced release of post-transcriptional gene silencing (PTGS). However, how thermomemory is transmitted to progeny and the physiological relevance are elusive. Here we show that heat-induced HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2) directly activates the H3K27me3 demethylase RELATIVE OF EARLY FLOWERING 6 (REF6), which in turn derepresses HSFA2. REF6 and HSFA2 establish a heritable feedback loop, and activate an E3 ubiquitin ligase, SUPPRESSOR OF GENE SILENCING 3 (SGS3)-INTERACTING PROTEIN 1 (SGIP1). SGIP1-mediated SGS3 degradation leads to inhibited biosynthesis of trans-acting siRNA (tasiRNA). The REF6-HSFA2 loop and reduced tasiRNA converge to release HEAT-INDUCED TAS1 TARGET 5 (HTT5), which drives early flowering but attenuates immunity. Thus, heat induces transmitted phenotypes via a coordinated epigenetic network involving histone demethylases, transcription factors, and tasiRNAs, ensuring reproductive success and transgenerational stress adaptation.

Highlights

Increasing global temperatures have diverse and profound effects on plant growth, development and reproduction, and greatly threaten global crop yields.[1,2] Plants have evolved sophisticated epigenetic machinery to respond quickly to heat.[3]
We found that parental Col plants grown at prolonged high temperature bolted earlier than those grown at 22 °C, and that most of their unstressed second generation progeny blotted earlier (Fig. 1a)
High temperatures induced PHYTOCHROME INTERACTING FACTOR4 (PIF4) expression, PIF4 upregulation was not detected in unstressed progeny, indicating that factors other than PIF4 are involved in the transgenerational thermomemory (Fig. 1b; Supplementary information, Fig. S1b, c)

Summary

Introduction

Increasing global temperatures have diverse and profound effects on plant growth, development and reproduction, and greatly threaten global crop yields.[1,2] Plants have evolved sophisticated epigenetic machinery to respond quickly to heat.[3]. It has been widely recognized that DNA methylation is not involved in the heatinduced release of gene silencing.[3]

Methods

Results

Conclusion