The METHYLTRANSFERASE B–SERRATE interaction mediates the reciprocal regulation of microRNA biogenesis and RNA m6A modification

doi:10.1111/jipb.13770

J Integr Plant Biol. ›› 2024, Vol. 66 ›› Issue (12): 2613-2631.DOI: 10.1111/jipb.13770 cstr: 32098.14.jipb.13770

• Cell and Developmental Biology • Previous Articles Next Articles

The METHYLTRANSFERASE B–SERRATE interaction mediates the reciprocal regulation of microRNA biogenesis and RNA m⁶A modification

Haiyan Bai^1†, Yanghuan Dai^1†, Panting Fan^2†, Yiming Zhou¹, Xiangying Wang¹, Jingjing Chen¹, Yuzhe Jiao¹, Chang Du¹, Zhuoxi Huang¹, Yuting Xie¹, Xiaoyu Guo¹, Xiaoqiang Lang^3,4, Yongqing Ling^1,3,4, Yizhen Deng⁵, Qi Liu^3,4*, Shengbo He^2* and Zhonghui Zhang^1*

1. Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Science, South China Normal University, Guangzhou 510631, China
2. Guangdong Laboratory for Lingnan Modern Agriculture, State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources, Guangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou 510642, China
3. Key Laboratory of Genetics and Breeding of High Quality Rice in Southern China (Co‐construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Guangzhou 510640, China
4. Guangdong Key Laboratory of New Technology in Rice Breeding, Guangdong Rice Engineering Laboratory, Rice Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
5. Guangdong Province Key Laboratory of Microbial Signals and Disease, State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources, South China Agricultural University, Guangzhou 510642, China
^†These authors contributed equally to this work.
^*Correspondence: Shengbo He (shengbo.he@scau.edu.cn); Qi Liu (rnainfor@gmail.com); Zhonghui Zhang (zhzhang@m.scnu.edu.cn, Dr. Zhang is responsible for the distribution of all materials associated with this article)

Received:2024-06-22 Accepted:2024-08-10 Online:2024-08-29 Published:2024-12-01
Supported by:
This work was supported by the National Natural Science Foundation of China (32170593 and 31771349), the Guangdong Provincial Pearl River Talent Plan (2019QN01N108), the National Science Foundation of Guangdong Province, China (Grant No. 2020B1515020007), and the State Key Laboratory for Conservation and Utilization of Subtropical Agro‐bioresources (SKLCUSA‐b202006) to Z.Z.; a double first‐class discipline promotion project of Guangdong province (2021B10564001) and the Guangdong Provincial Pearl River Talent Plan (2021QN020536) to S.H.; the Elite Rice Plan of Rice Research Institute, Guangdong Academy of Agricultural Sciences (2022YG01) to Q.L.

Abstract

Abstract: In eukaryotes, RNA N⁶-methyladenosine (m⁶A) modification and microRNA (miRNA)-mediated RNA silencing represent two critical epigenetic regulatory mechanisms. The m⁶A methyltransferase complex (MTC) and the microprocessor complex both undergo liquid–liquid phase separation to form nuclear membraneless organelles. Although m⁶A methyltransferase has been shown to positively regulate miRNA biogenesis, a mechanism of reciprocal regulation between the MTC and the microprocessor complex has remained elusive. Here, we demonstrate that the MTC and the microprocessor complex associate with each other through the METHYLTRANSFERASE B (MTB)–SERRATE (SE) interacting module. Knockdown of MTB impaired miRNA biogenesis by diminishing microprocessor complex binding to primary miRNAs (pri-miRNAs) and their respective MIRNA loci. Additionally, loss of SE function led to disruptions in transcriptome-wide m⁶A modification. Further biochemical assays and fluorescence recovery after photobleaching (FRAP) assay indicated that SE enhances the liquid–liquid phase separation and solubility of the MTC. Moreover, the MTC exhibited enhanced retention on chromatin and diminished binding to its RNA substrates in the se mutant background. Collectively, our results reveal the substantial regulatory interplay between RNA m⁶A modification and miRNA biogenesis.

Key words: iquid–liquid phase separation, microRNA biogenesis, MTB, RNA m⁶A modification, SE

Haiyan Bai, Yanghuan Dai, Panting Fan, Yiming Zhou, Xiangying Wang, Jingjing Chen, Yuzhe Jiao, Chang Du, Zhuoxi Huang, Yuting Xie, Xiaoyu Guo, Xiaoqiang Lang, Yongqing Ling, Yizhen Deng, Qi Liu, Shengbo He, Zhonghui Zhang. The METHYLTRANSFERASE B–SERRATE interaction mediates the reciprocal regulation of microRNA biogenesis and RNA m⁶A modification[J]. J Integr Plant Biol., 2024, 66(12): 2613-2631.

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The METHYLTRANSFERASE B–SERRATE interaction mediates the reciprocal regulation of microRNA biogenesis and RNA m⁶A modification

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