Heat stress-induced activation of MAPK pathway attenuates Atf1-dependent epigenetic inheritance of heterochromatin in fission yeast

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Abstract

Eukaryotic cells are constantly exposed to various environmental stimuli. It remains largely unexplored how environmental cues bring about epigenetic fluctuations and affect heterochromatin stability. In the fission yeast Schizosaccharomyces pombe, heterochromatic silencing is quite stable at pericentromeres but unstable at the mating-type (mat) locus under chronic heat stress, although both loci are within the major constitutive heterochromatin regions. Here, we found that the compromised gene silencing at the mat locus at elevated temperature is linked to the phosphorylation status of Atf1, a member of the ATF/CREB superfamily. Constitutive activation of MAPK signaling disrupts epigenetic maintenance of heterochromatin at the mat locus even under normal temperature. Mechanistically, phosphorylation of Atf1 impairs its interaction with heterochromatin protein Swi6^HP1, resulting in lower site-specific Swi6^HP1 enrichment. Expression of non-phosphorylatable Atf1, tethering Swi6^HP1 to the mat3M-flanking site or absence of the anti-silencing factor Epe1 can largely or partially rescue heat stress-induced defective heterochromatic maintenance at the mat locus.

Data availability

The authors confirm that all data supporting the findings of this study are available within the manuscript main figures, supplemental figures, supplementary tables and source data files. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD048330.

The following data sets were generated

1. Sun L
2. Liu L
3. Song C
4. Wang Y
5. Jin QW
(2024) Sty1 kinase-dependent phosphosite mapping on Atf1
ProteomeXchange, PXD048330.

https://www.ebi.ac.uk/pride/archive/projects/PXD048330

Article and author information

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Li Sun

State Key Laboratory of Cellular Stress Biology, Xiamen University, Xiamen, China

Competing interests
The authors declare that no competing interests exist.
Libo Liu

State Key Laboratory of Cellular Stress Biology, Xiamen University, Xiamen, China

Competing interests
The authors declare that no competing interests exist.
Chunlin Song

State Key Laboratory of Cellular Stress Biology, Xiamen University, Xiamen, China

Competing interests
The authors declare that no competing interests exist.
Yamei Wang

State Key Laboratory of Cellular Stress Biology, Xiamen University, Xiamen, China

For correspondence
wangyamei@xmu.edu.cn

Competing interests
The authors declare that no competing interests exist.
Quan-wen Jin

State Key Laboratory of Cellular Stress Biology, Xiamen University, Xiamen, China

For correspondence
jinquanwen@xmu.edu.cn

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6146-6910

Funding

National Natural Science Foundation of China (32170731)

Quan-wen Jin

National Natural Science Foundation of China (30871376)

Quan-wen Jin

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.