Hyponastic Leaves 1 protects pri-miRNAs from nuclear exosome attack

Gao, Shuai; Wang, Jingyu; Jiang, Ning; Zhang, Shiting; Wang, Yuan; Zhang, Jun; Li, Ning; Fang, Yixiao; Yang, Lin; Chen, Susu; Yan, Bingbing; Huang, Tao; Benke, Kálmán; Wang, Yingxiang; Chang, Fang Rong; Ren, Guodong

doi:10.1073/pnas.2007203117

Cited by 27 publications

(28 citation statements)

References 54 publications

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“…Interestingly ID calculation showed a subtle but significant difference between these mutants and control plants regarding trimming or tailing ( Figure 2 A). Similarly, mutations of SUPPRESSOR OF HYL1 (SHY43), also known as SOP1, a cofactor of the nucleoplasmic exosome controlling pri-miRNA stability [ 43 ], affected miRNA tailing and trimming ( Figure 2 A). Plants overexpressing the HAWAIIAN SKIRT ( HWS ) gene but not the mutants in this gene also showed altered IDs ( Figure 2 A).…”

Section: Resultsmentioning

confidence: 99%

Extensive Analysis of miRNA Trimming and Tailing Indicates that AGO1 Has a Complex Role in miRNA Turnover

Giudicatti

Tomassi

Manavella

et al. 2021

Plants

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MicroRNAs are small regulatory RNAs involved in several processes in plants ranging from development and stress responses to defense against pathogens. In order to accomplish their molecular functions, miRNAs are methylated and loaded into one ARGONAUTE (AGO) protein, commonly known as AGO1, to stabilize and protect the molecule and to assemble a functional RNA-induced silencing complex (RISC). A specific machinery controls miRNA turnover to ensure the silencing release of targeted-genes in given circumstances. The trimming and tailing of miRNAs are fundamental modifications related to their turnover and, hence, to their action. In order to gain a better understanding of these modifications, we analyzed Arabidopsis thaliana small RNA sequencing data from a diversity of mutants, related to miRNA biogenesis, action, and turnover, and from different cellular fractions and immunoprecipitations. Besides confirming the effects of known players in these pathways, we found increased trimming and tailing in miRNA biogenesis mutants. More importantly, our analysis allowed us to reveal the importance of ARGONAUTE 1 (AGO1) loading, slicing activity, and cellular localization in trimming and tailing of miRNAs.

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Section: Resultsmentioning

confidence: 99%

Extensive Analysis of miRNA Trimming and Tailing Indicates that AGO1 Has a Complex Role in miRNA Turnover

Giudicatti

Tomassi

Manavella

et al. 2021

Plants

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“…The fact that miR168a and b and miR403 are dependent upon HYL1 for its maturation (Szarzynska et al , 2009) raises the question whether the down-regulation of these pre-microRNAs under TuMV infections is a consequence of TuMV alteration of miRNA processing via HYL1. Importantly, HYL1 can stabilize pri-miRNAs (Gao et al , 2020) and is downregulated by ABA (Lu and Fedoroff, 2000), which increases under TuMV infection (Manacorda et al , 2021). Further studies should elucidate the role that HYL1 or other components of the plant microprocessor machinery could have in the alteration of the biogenesis of microRNAs 168 and 403, among others, during viral infections.…”

Section: Discussionmentioning

confidence: 99%

TuMV infection alters miR168/AGO1 and miR403/AGO2 systems regulation in Arabidopsis

Manacorda

Tasselli

Maraño

et al. 2021

Preprint

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Viral infections trigger a strong response of the plant RNA silencing machinery. The cargo protein AGO1 has a well-established role in siRNA loading. Several plant viruses have convergently evolved a molecular counter-attack reliant on inactivation of the AGO1-based plant defense by altering the regulatory loop that comprises miR168 and AGO1. Upon viral infections, another AGO protein, AGO2, is induced. AGO2 is in turn post-transcriptionally regulated by miR403. The simultaneous study of both regulatory systems working along an infection time-frame is lacking. Here it is shown the molecular response of Arabidopsis Turnip Mosaic Virus (TuMV) infection from early to late stages post-infection. Molecular analyses confirmed that TuMV induced mature miR168 accumulation in Arabidopsis, as reported also for other plant-virus interactions. However, differently from reported plant-virus interactions, miRNA precursors pre-miR168a and b were down-regulated and no significant transcriptional effect was detected on miR168a promoter. AGO1 mRNA was induced, but AGO1 protein levels were unchanged. Analyses of the miR403/AGO2 system showed a similar pattern, except for an induction of AGO2 protein levels. Additionally, low molecular weight forms of AGO1 and 2 proteins were detected and relatively overaccumulated under TuMV infections. Our results suggest that TuMV alters the biogenesis of miR168 and miR403 at the processing step. Whilst TuMV induces both miR168 and miR403 overaccumulation, it fails to prevent overaccumulation of the antiviral AGO2 at both mRNA and protein levels.

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“…In addition, the capbinding proteins (Kim et al, 2008), DAWDLE (DDL, a forkhead-associated domain protein) (Yu et al, 2008), NOT2, TGH, CDC5, PLEIOTROPIC REGULATORY LOCUS 1 (PRL1; an RNA binding protein) (Zhang et al, 2014), SHORT VALVE 1 (a ribosomal protein) (Li et al, 2017), the THO/ TREX complex (Francisco-Mangilet et al, 2015), MODIFIER OF SNC1,2 (MOS2; an RNA-binding protein) (Wu et al, 2013), The RNA helicase MOS4-ASSOCIATED COMPLEX 7 (MAC7) (Jia et al, 2017), the ubiquitin ligase MAC3 (Li et al, 2018a), the RNA-binding protein MAC5 (Li et al, 2020) and Chromatin remodeling factor 2 (CHR2) (Wang et al, 2018) are dynamically associated with the DCL1 complex to modulate the efficient processing of pri-miRNAs. Recent studies also show that pri-miRNA stability plays a crucial role in miRNA biogenesis (Yu et al, 2008;Speth et al, 2013;Zhang et al, 2014;Fang et al, 2019;Li et al, 2020). For instance, increased pri-miRNA decay in ddl, mac3, mac5 and prl1 reduces miRNA levels (Yu et al, 2008;Zhang et al, 2014;Li et al, 2018aLi et al, , 2020.…”

Section: Introductionmentioning

confidence: 99%

“…Recent studies also show that pri-miRNA stability plays a crucial role in miRNA biogenesis (Yu et al, 2008;Speth et al, 2013;Zhang et al, 2014;Fang et al, 2019;Li et al, 2020). For instance, increased pri-miRNA decay in ddl, mac3, mac5 and prl1 reduces miRNA levels (Yu et al, 2008;Zhang et al, 2014;Li et al, 2018aLi et al, , 2020. Interestingly, HYL1, besides its role in processing, is able to protect pri-miRNAs from degradation from the nuclear exosome (Gao et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…For instance, increased pri-miRNA decay in ddl, mac3, mac5 and prl1 reduces miRNA levels (Yu et al, 2008;Zhang et al, 2014;Li et al, 2018aLi et al, , 2020. Interestingly, HYL1, besides its role in processing, is able to protect pri-miRNAs from degradation from the nuclear exosome (Gao et al, 2020). SE, another component of DCL1 complex, can mediate the decay of pri-miRNAs by nuclear localized exosome and 5 0 -to-3 0 exoribonuclease 2 and 3 (Bajczyk et al, 2020;Gao et al, 2020;Li et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Serrate‐Associated Protein 1, a splicing‐related protein, promotes miRNA biogenesis in Arabidopsis

Liu

Yang

et al. 2021

New Phytologist

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MicroRNAs (miRNAs) are essential regulators of gene expression in metazoans and plants. In plants, most miRNAs are generated from primary miRNA transcripts (pri-miRNAs), which are processed by the Dicer-like 1 (DCL1) complex along with accessory proteins.Serrate-Associated Protein 1 (SEAP1), a conserved splicing-related protein, has been studied in human and yeast. However, the functions of SEAP1 in plants remain elusive.Lack of SEAP1 results in embryo lethality and knockdown of SEAP1 by an artificial miRNA (amiR SEAP1 ) causes pleiotropic developmental defects and reduction in miRNA accumulation. SEAP1 associates with the DCL1 complex, and may promote the interaction of the DCL1 complexes with pri-miRNAs. SEAP1 also enhances pri-miRNA accumulation, but does not affect pri-miRNA transcription, suggesting it may indirectly or directly stabilize pri-miRNAs. In addition, SEAP1 affects the splicing of some pri-miRNAs and intron retention of messenger RNAs at global levels.Our findings uncover both conserved and novel functions of SEAP1 in plants. Besides the role as a splicing factor, SEPA1 may promote miRNA biogenesis by positively modulating pri-miRNA splicing, processing and/or stability.

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Hyponastic Leaves 1 protects pri-miRNAs from nuclear exosome attack

Cited by 27 publications

References 54 publications

Extensive Analysis of miRNA Trimming and Tailing Indicates that AGO1 Has a Complex Role in miRNA Turnover

Extensive Analysis of miRNA Trimming and Tailing Indicates that AGO1 Has a Complex Role in miRNA Turnover

TuMV infection alters miR168/AGO1 and miR403/AGO2 systems regulation in Arabidopsis

Serrate‐Associated Protein 1, a splicing‐related protein, promotes miRNA biogenesis in Arabidopsis

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