Phase separation of SERRATE drives dicing body assembly and promotes miRNA processing in Arabidopsis

Xie, Dan; Chen, Min; Niu, Jinrong; Wang, Liang; Li, Yan; Fang, Xiuqi; Li, Pilong; Qi, Yijun

doi:10.1038/s41556-020-00606-5

Cited by 119 publications

(81 citation statements)

References 44 publications

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“…Therefore, DEAD-box helicases may serve as a common scaffold for the assembly of many membraneless organelles. While this study was under review, another related work revealed that SEs can undergo phase separation and control the assembly of D-bodies ( 21 ), which supports our conclusion that scaffold RNA helicase proteins indeed interact with unique IDR-containing proteins of membraneless organelles and coordinately drive the formation of distinct membraneless organelles.…”

Section: Discussionsupporting

confidence: 82%

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DEAD-box helicases modulate dicing body formation in Arabidopsis

Liu

et al. 2021

Sci. Adv.

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Eukaryotic cells contain numerous membraneless organelles that are made from liquid droplets of proteins and nucleic acids and that provide spatiotemporal control of various cellular processes. However, the molecular mechanisms underlying the formation and rapid stress-induced alterations of these organelles are relatively uncharacterized. Here, we investigated the roles of DEAD-box helicases in the formation and alteration of membraneless nuclear dicing bodies (D-bodies) in Arabidopsis thaliana. We uncovered that RNA helicase 6 (RH6), RH8, and RH12 are previously unidentified D-body components. These helicases interact with and promote the phase separation of SERRATE, a key component of D-bodies, and drive the formation of D-bodies through liquid-liquid phase separations (LLPSs). The accumulation of these helicases in the nuclei decreases upon Turnip mosaic virus infections, which couples with the decrease of D-bodies. Our results thus reveal the key roles of RH6, RH8, and RH12 in modulating D-body formation via LLPSs.

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Section: Discussionsupporting

confidence: 82%

“…S5J). A study published while this study was under review also reported the phase separation property of SE ( 21 ). In contrast, phase separation of RH12 is ATP and RNA dependent ( Fig.…”

Section: Resultsmentioning

confidence: 99%

DEAD-box helicases modulate dicing body formation in Arabidopsis

Liu

et al. 2021

Sci. Adv.

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“…The long and structurally variable plant pri-miRNAs posed a challenge for such an event to happens. On top, the recent demonstration of pri-miRNA processing in SERRATE-containing liquid droplets, likely D-Bodies, and the absence of this protein in most MIRNA loci challenged the idea of co-transcriptional processing in plants (Speth et al, 2018; Xie et al, 2021). In this study we confirmed that pri-miRNAs are processed co-transcriptionally in plants and showed that this process co-exists with a post-transcriptional counterpart.…”

Section: Discussionmentioning

confidence: 99%

R-Loops between nascent pri-miRNAs and the encoding loci promote co-transcriptional processing of miRNAs in plants

Gonzalo

Tossolini

Gulanicz

et al. 2021

Preprint

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In most organisms, the maturation of nascent RNAs is coupled to transcription, undergoing many processing steps co-transcriptionally. Unlike in animals, the RNA polymerase II (RNAPII) transcribes microRNAs (miRNAs) as long and structurally variable pri-miRNAs in plants. Current evidence suggests that the miRNA biogenesis complex assembly initiates early during the transcription of pri-miRNAs in plants. However, it is unknown whether miRNA processing occurs co-transcriptionally. Here, we show that plant miRNA biogenesis is coupled to transcription in a process that relies on the formation of DNA:RNA hybrids (R-loops) between the nascent transcript and the encoding loci. We used native elongating transcript sequencing data and imaging techniques to demonstrate that plant miRNA biogenesis occurs co-transcriptionally. We found that the entire biogenesis occurs coupled to transcription for pri-miRNAs processed from the loop but requires a second nucleoplasmic step for those processed from the base of the hairpin. Furthermore, we found that co- and post-transcriptional miRNA processing mechanisms co-exist for most miRNAs in a dynamic balance. Notably, we discovered that R-loops between the 5'-end single-stranded arm of the pri-miRNAs and the encoding loci anchor the transcript, promoting co-transcriptional processing. Our data demonstrate the coupling of transcription and miRNA processing in plants and discovered an unexpected function for R-loops promoting RNA processing. Furthermore, our results suggest the neo-functionalization of co-transcriptionally processed miRNAs, boosting countless regulatory scenarios.

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“…More recently, dicing bodies in plants have been regarded as protein condensates formed using phase transitions. During an in vitro setup, SERRATE forms liquid-like droplets to recruit DCL1, HYL1, and pri/pre-miRNAs, promoting the processing activity, maturation, and export of miRNAs [107].…”

Section: Membrane-less Compartmentsmentioning

confidence: 99%

Subcellular Localization of miRNAs and Implications in Cellular Homeostasis

Jie

Feng

Huang

et al. 2021

Genes

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MicroRNAs (miRNAs) are thought to act as post-transcriptional regulators in the cytoplasm by either dampening translation or stimulating degradation of target mRNAs. With the increasing resolution and scope of RNA mapping, recent studies have revealed novel insights into the subcellular localization of miRNAs. Based on miRNA subcellular localization, unconventional functions and mechanisms at the transcriptional and post-transcriptional levels have been identified. This minireview provides an overview of the subcellular localization of miRNAs and the mechanisms by which they regulate transcription and cellular homeostasis in mammals, with a particular focus on the roles of phase-separated biomolecular condensates.

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Phase separation of SERRATE drives dicing body assembly and promotes miRNA processing in Arabidopsis

Cited by 119 publications

References 44 publications

DEAD-box helicases modulate dicing body formation in Arabidopsis

DEAD-box helicases modulate dicing body formation in Arabidopsis

R-Loops between nascent pri-miRNAs and the encoding loci promote co-transcriptional processing of miRNAs in plants

Subcellular Localization of miRNAs and Implications in Cellular Homeostasis

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