Dynamics and functional interplay of histone lysine butyrylation, crotonylation, and acetylation in rice under starvation and submergence.

Yue Lu, Qiutao Xu, Yuan Liu, Yue Yu, Zhong-Yi Cheng, Yu Zhao, Dao-Xiu Zhou
Author Information
  1. Yue Lu: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  2. Qiutao Xu: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  3. Yuan Liu: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  4. Yue Yu: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  5. Zhong-Yi Cheng: Jingjie PTM BioLab Co. Ltd, Hangzhou, 310018, China.
  6. Yu Zhao: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  7. Dao-Xiu Zhou: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China. dao-xiu.zhou@u-psud.fr. ORCID

Abstract

BACKGROUND: Histone lysine acylations by short-chain fatty acids are distinct from the widely studied histone lysine acetylation in chromatin, although both modifications are regulated by primary metabolism in mammalian cells. It remains unknown whether and how histone acylation and acetylation interact to regulate gene expression in plants that have distinct regulatory pathways of primary metabolism.
RESULTS: We identify 4 lysine butyrylation (Kbu) sites (H3K14, H4K12, H2BK42, and H2BK134) and 45 crotonylation (Kcr) sites on rice histones by mass spectrometry. Comparative analysis of genome-wide Kbu and Kcr and H3K9ac in combination with RNA sequencing reveals 25,306 genes marked by Kbu and Kcr in rice and more than 95% of H3K9ac-marked genes are marked by both. Kbu and Kcr are enriched at the 5' region of expressed genes. In rice under starvation and submergence, Kbu and Kcr appear to be less dynamic and display changes in different sets of genes compared to H3K9ac. Furthermore, Kbu seems to preferentially poise gene activation by external stresses, rather than internal circadian rhythm which has been shown to be tightly associated with H3K9ac. In addition, we show that rice sirtuin histone deacetylase (SRT2) is involved in the removal of Kcr.
CONCLUSION: Kbu, Kcr, and H3K9ac redundantly mark a large number of active genes but display different responses to external and internal signals. Thus, the proportion of rice histone lysine acetylation and acylation is dynamically regulated by environmental and metabolic cues, which may represent an epigenetic mechanism to fine-tune gene expression for plant adaptation.

MeSH Term

Acetylation
Gene Expression Regulation, Plant
Histones
Lysine
Oryza
Plant Proteins
Protein Processing, Post-Translational
Sirtuins
Stress, Physiological

Chemicals

Histones
Plant Proteins
Sirtuins
Lysine