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Intrinsically disordered proteins SAID1/2 condensate on SERRATE for dual inhibition of miRNA biogenesis in Arabidopsis

Intrinsically disordered proteins (IDPs) SAID1/2 are hypothetic dentin sialophosphoprotein-like proteins, but their true functions are unknown. Here, we identified SAID1/2 as negative regulators of SERRATE (SE), a core factor in miRNA biogenesis complex (microprocessor). Loss-of-function double muta...

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Autores principales: Shang, Baoshuan, Wang, Lin, Yan, Xingxing, Li, Yanjun, Li, Changhao, Wu, Chaohua, Wang, Tian, Guo, Xiang, Choi, Suk Won, Zhang, Tianru, Wang, Ziying, Tong, Chun-Yip, Oh, Taerin, Zhang, Xiao, Wang, Zhiye, Peng, Xu, Zhang, Xiuren
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10083546/
https://www.ncbi.nlm.nih.gov/pubmed/36972460
http://dx.doi.org/10.1073/pnas.2216006120
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author Shang, Baoshuan
Wang, Lin
Yan, Xingxing
Li, Yanjun
Li, Changhao
Wu, Chaohua
Wang, Tian
Guo, Xiang
Choi, Suk Won
Zhang, Tianru
Wang, Ziying
Tong, Chun-Yip
Oh, Taerin
Zhang, Xiao
Wang, Zhiye
Peng, Xu
Zhang, Xiuren
author_facet Shang, Baoshuan
Wang, Lin
Yan, Xingxing
Li, Yanjun
Li, Changhao
Wu, Chaohua
Wang, Tian
Guo, Xiang
Choi, Suk Won
Zhang, Tianru
Wang, Ziying
Tong, Chun-Yip
Oh, Taerin
Zhang, Xiao
Wang, Zhiye
Peng, Xu
Zhang, Xiuren
author_sort Shang, Baoshuan
collection PubMed
description Intrinsically disordered proteins (IDPs) SAID1/2 are hypothetic dentin sialophosphoprotein-like proteins, but their true functions are unknown. Here, we identified SAID1/2 as negative regulators of SERRATE (SE), a core factor in miRNA biogenesis complex (microprocessor). Loss-of-function double mutants of said1; said2 caused pleiotropic developmental defects and thousands of differentially expressed genes that partially overlapped with those in se. said1; said2 also displayed increased assembly of microprocessor and elevated accumulation of microRNAs (miRNAs). Mechanistically, SAID1/2 promote pre-mRNA processing 4 kinase A-mediated phosphorylation of SE, causing its degradation in vivo. Unexpectedly, SAID1/2 have strong binding affinity to hairpin-structured pri-miRNAs and can sequester them from SE. Moreover, SAID1/2 directly inhibit pri-miRNA processing by microprocessor in vitro. Whereas SAID1/2 did not impact SE subcellular compartmentation, the proteins themselves exhibited liquid–liquid phase condensation that is nucleated on SE. Thus, we propose that SAID1/2 reduce miRNA production through hijacking pri-miRNAs to prevent microprocessor activity while promoting SE phosphorylation and its destabilization in Arabidopsis.
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spelling pubmed-100835462023-09-27 Intrinsically disordered proteins SAID1/2 condensate on SERRATE for dual inhibition of miRNA biogenesis in Arabidopsis Shang, Baoshuan Wang, Lin Yan, Xingxing Li, Yanjun Li, Changhao Wu, Chaohua Wang, Tian Guo, Xiang Choi, Suk Won Zhang, Tianru Wang, Ziying Tong, Chun-Yip Oh, Taerin Zhang, Xiao Wang, Zhiye Peng, Xu Zhang, Xiuren Proc Natl Acad Sci U S A Biological Sciences Intrinsically disordered proteins (IDPs) SAID1/2 are hypothetic dentin sialophosphoprotein-like proteins, but their true functions are unknown. Here, we identified SAID1/2 as negative regulators of SERRATE (SE), a core factor in miRNA biogenesis complex (microprocessor). Loss-of-function double mutants of said1; said2 caused pleiotropic developmental defects and thousands of differentially expressed genes that partially overlapped with those in se. said1; said2 also displayed increased assembly of microprocessor and elevated accumulation of microRNAs (miRNAs). Mechanistically, SAID1/2 promote pre-mRNA processing 4 kinase A-mediated phosphorylation of SE, causing its degradation in vivo. Unexpectedly, SAID1/2 have strong binding affinity to hairpin-structured pri-miRNAs and can sequester them from SE. Moreover, SAID1/2 directly inhibit pri-miRNA processing by microprocessor in vitro. Whereas SAID1/2 did not impact SE subcellular compartmentation, the proteins themselves exhibited liquid–liquid phase condensation that is nucleated on SE. Thus, we propose that SAID1/2 reduce miRNA production through hijacking pri-miRNAs to prevent microprocessor activity while promoting SE phosphorylation and its destabilization in Arabidopsis. National Academy of Sciences 2023-03-27 2023-04-04 /pmc/articles/PMC10083546/ /pubmed/36972460 http://dx.doi.org/10.1073/pnas.2216006120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Shang, Baoshuan
Wang, Lin
Yan, Xingxing
Li, Yanjun
Li, Changhao
Wu, Chaohua
Wang, Tian
Guo, Xiang
Choi, Suk Won
Zhang, Tianru
Wang, Ziying
Tong, Chun-Yip
Oh, Taerin
Zhang, Xiao
Wang, Zhiye
Peng, Xu
Zhang, Xiuren
Intrinsically disordered proteins SAID1/2 condensate on SERRATE for dual inhibition of miRNA biogenesis in Arabidopsis
title Intrinsically disordered proteins SAID1/2 condensate on SERRATE for dual inhibition of miRNA biogenesis in Arabidopsis
title_full Intrinsically disordered proteins SAID1/2 condensate on SERRATE for dual inhibition of miRNA biogenesis in Arabidopsis
title_fullStr Intrinsically disordered proteins SAID1/2 condensate on SERRATE for dual inhibition of miRNA biogenesis in Arabidopsis
title_full_unstemmed Intrinsically disordered proteins SAID1/2 condensate on SERRATE for dual inhibition of miRNA biogenesis in Arabidopsis
title_short Intrinsically disordered proteins SAID1/2 condensate on SERRATE for dual inhibition of miRNA biogenesis in Arabidopsis
title_sort intrinsically disordered proteins said1/2 condensate on serrate for dual inhibition of mirna biogenesis in arabidopsis
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10083546/
https://www.ncbi.nlm.nih.gov/pubmed/36972460
http://dx.doi.org/10.1073/pnas.2216006120
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