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Volume 29, No 5, May 2019

ISSN: 1001-0602 
EISSN: 1748-7838 2018 
impact factor 17.848* 
(Clarivate Analytics, 2019)

Volume 29 Issue 5, May 2019: 379-390   |  Open Access

ORIGINAL ARTICLES

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

Junzhong Liu 1, Lili Feng 1,2,3, Xueting Gu 1,2, Xian Deng 4, Qi Qiu 2,4, Qun Li 1, Yingying Zhang 1, Muyang Wang 1,5, Yiwen Deng 1, Ertao Wang 1, Yuke He 1, Isabel Bäurle 6, Jianming Li 5,7, Xiaofeng Cao 2,4,8 and Zuhua He 1,3

1 National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology & Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China; 2University of the Chinese Academy of Sciences, Beijing 100049, China; 3School of Life Science and Technology, Shanghai Tech University, Shanghai 201210, China; 4State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; 5Shanghai Center for Plant Stress Biology, Chinese Academy of Sciences, Shanghai 201602, China; 6Institute of Biochemistry and Biology, University of Potsdam, Potsdam, Germany; 7Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA and 8CAS Center for Excellence in Molecular Plant Sciences, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
 Correspondence: Xiaofeng Cao (xfcao@genetics.ac.cn) or Zuhua He (zhhe@sibs.ac.cn)These authors contributed equally: Junzhong Liu, Lili Feng, Xueting Gu, Xian Deng

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.


https://doi.org/10.1038/s41422-019-0145-8

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