Mechanism of siRNA production by a plant Dicer-RNA complex in dicing-competent conformation
In the biogenesis of small RNAs, the Dicer family endonucleases act as a molecular ruler to cut the substrate RNA into defined lengths. Wang et al . report a structure of the dicing-competent state of plant DICER LIKE PROTEIN 3 (DCL3) in complex with a pre–small interfering RNA (pre-siRNA). Toward o...
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| Published in | Science (American Association for the Advancement of Science) Vol. 374; no. 6571; pp. 1152 - 1157 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
26.11.2021
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| Subjects | |
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| Abstract | In the biogenesis of small RNAs, the Dicer family endonucleases act as a molecular ruler to cut the substrate RNA into defined lengths. Wang
et al
. report a structure of the dicing-competent state of plant DICER LIKE PROTEIN 3 (DCL3) in complex with a pre–small interfering RNA (pre-siRNA). Toward one end of the pre-siRNA, DCL3 uses a positively charged pocket and an aromatic cap to specifically recognize the 5′-phosphorylated adenosine of the guide strand and the 3′ overhang of the complementary strand, respectively. On the other end, the paired ribonuclease III domains of DCL3 cut both strands of the RNA, determining the precise length of the product small RNA. —DJ
Structural studies, complemented by functional data, elucidate the dicing principle for Dicer endonucleases in plants and more widely.
In eukaryotes, small RNAs (sRNAs) play critical roles in multiple biological processes. Dicer endonucleases are a central part of sRNA biogenesis. In plants, DICER-LIKE PROTEIN 3 (DCL3) produces 24-nucleotide (nt) small interfering RNAs (siRNAs) that determine the specificity of the RNA-directed DNA methylation pathway. Here, we determined the structure of a DCL3–pre-siRNA complex in an active dicing-competent state. The 5′-phosphorylated A1 of the guide strand and the 1-nt 3′ overhang of the complementary strand are specifically recognized by a positively charged pocket and an aromatic cap, respectively. The 24-nt siRNA length dependence relies on the separation between the 5′-phosphorylated end of the guide RNA and dual cleavage sites formed by the paired ribonuclease III domains. These structural studies, complemented by functional data, provide insight into the dicing principle for Dicers in general. |
|---|---|
| AbstractList | In eukaryotes, small RNAs (sRNAs) play critical roles in multiple biological processes. Dicer endonucleases are central to sRNA biogenesis. In plants, DICER-LIKE PROTEIN 3 (DCL3) produces 24-nt small interfering RNAs (siRNAs) that determine the specificity of the RNA-directed DNA methylation (RdDM) pathway. Here, we determined structure of a DCL3-pre-siRNA complex in an active dicing-competent state. The 5’-phosphorylated-A1 of the guide strand and the 1-nt 3’-overhang of the complementary strand are specifically recognized by a positively charged pocket and an aromatic cap, respectively. The 24-nt siRNA length dependence relies on the separation between the 5’-phosphorylated-end of the guide RNA and dual cleavage sites formed by the paired RNaseIII domains. These structural studies, complemented by functional data, reveal insights into the dicing principle for Dicers in general.
Mechanistic understanding of the terminus-specific, length-dependent, and strand-biased 24-nt siRNA production by Arabidopsis DCL3. In the biogenesis of small RNAs, the Dicer family endonucleases act as a molecular ruler to cut the substrate RNA into defined lengths. Wang et al . report a structure of the dicing-competent state of plant DICER LIKE PROTEIN 3 (DCL3) in complex with a pre–small interfering RNA (pre-siRNA). Toward one end of the pre-siRNA, DCL3 uses a positively charged pocket and an aromatic cap to specifically recognize the 5′-phosphorylated adenosine of the guide strand and the 3′ overhang of the complementary strand, respectively. On the other end, the paired ribonuclease III domains of DCL3 cut both strands of the RNA, determining the precise length of the product small RNA. —DJ Structural studies, complemented by functional data, elucidate the dicing principle for Dicer endonucleases in plants and more widely. In eukaryotes, small RNAs (sRNAs) play critical roles in multiple biological processes. Dicer endonucleases are a central part of sRNA biogenesis. In plants, DICER-LIKE PROTEIN 3 (DCL3) produces 24-nucleotide (nt) small interfering RNAs (siRNAs) that determine the specificity of the RNA-directed DNA methylation pathway. Here, we determined the structure of a DCL3–pre-siRNA complex in an active dicing-competent state. The 5′-phosphorylated A1 of the guide strand and the 1-nt 3′ overhang of the complementary strand are specifically recognized by a positively charged pocket and an aromatic cap, respectively. The 24-nt siRNA length dependence relies on the separation between the 5′-phosphorylated end of the guide RNA and dual cleavage sites formed by the paired ribonuclease III domains. These structural studies, complemented by functional data, provide insight into the dicing principle for Dicers in general. In eukaryotes, small RNAs (sRNAs) play critical roles in multiple biological processes. Dicer endonucleases are a central part of sRNA biogenesis. In plants, DICER-LIKE PROTEIN 3 (DCL3) produces 24-nucleotide (nt) small interfering RNAs (siRNAs) that determine the specificity of the RNA-directed DNA methylation pathway. Here, we determined the structure of a DCL3–pre-siRNA complex in an active dicing-competent state. The 5′-phosphorylated A1 of the guide strand and the 1-nt 3′ overhang of the complementary strand are specifically recognized by a positively charged pocket and an aromatic cap, respectively. The 24-nt siRNA length dependence relies on the separation between the 5′-phosphorylated end of the guide RNA and dual cleavage sites formed by the paired ribonuclease III domains. These structural studies, complemented by functional data, provide insight into the dicing principle for Dicers in general. In eukaryotes, small RNAs (sRNAs) play critical roles in multiple biological processes. Dicer endonucleases are a central part of sRNA biogenesis. In plants, DICER-LIKE PROTEIN 3 (DCL3) produces 24-nucleotide (nt) small interfering RNAs (siRNAs) that determine the specificity of the RNA-directed DNA methylation pathway. Here, we determined the structure of a DCL3–pre-siRNA complex in an active dicing-competent state. The 5′-phosphorylated A1 of the guide strand and the 1-nt 3′ overhang of the complementary strand are specifically recognized by a positively charged pocket and an aromatic cap, respectively. The 24-nt siRNA length dependence relies on the separation between the 5′-phosphorylated end of the guide RNA and dual cleavage sites formed by the paired ribonuclease III domains. These structural studies, complemented by functional data, provide insight into the dicing principle for Dicers in general.In eukaryotes, small RNAs (sRNAs) play critical roles in multiple biological processes. Dicer endonucleases are a central part of sRNA biogenesis. In plants, DICER-LIKE PROTEIN 3 (DCL3) produces 24-nucleotide (nt) small interfering RNAs (siRNAs) that determine the specificity of the RNA-directed DNA methylation pathway. Here, we determined the structure of a DCL3–pre-siRNA complex in an active dicing-competent state. The 5′-phosphorylated A1 of the guide strand and the 1-nt 3′ overhang of the complementary strand are specifically recognized by a positively charged pocket and an aromatic cap, respectively. The 24-nt siRNA length dependence relies on the separation between the 5′-phosphorylated end of the guide RNA and dual cleavage sites formed by the paired ribonuclease III domains. These structural studies, complemented by functional data, provide insight into the dicing principle for Dicers in general. Ready to diceIn the biogenesis of small RNAs, the Dicer family endonucleases act as a molecular ruler to cut the substrate RNA into defined lengths. Wang et al. report a structure of the dicing-competent state of plant DICER LIKE PROTEIN 3 (DCL3) in complex with a pre–small interfering RNA (pre-siRNA). Toward one end of the pre-siRNA, DCL3 uses a positively charged pocket and an aromatic cap to specifically recognize the 5′-phosphorylated adenosine of the guide strand and the 3′ overhang of the complementary strand, respectively. On the other end, the paired ribonuclease III domains of DCL3 cut both strands of the RNA, determining the precise length of the product small RNA. —DJIn eukaryotes, small RNAs (sRNAs) play critical roles in multiple biological processes. Dicer endonucleases are a central part of sRNA biogenesis. In plants, DICER-LIKE PROTEIN 3 (DCL3) produces 24-nucleotide (nt) small interfering RNAs (siRNAs) that determine the specificity of the RNA-directed DNA methylation pathway. Here, we determined the structure of a DCL3–pre-siRNA complex in an active dicing-competent state. The 5′-phosphorylated A1 of the guide strand and the 1-nt 3′ overhang of the complementary strand are specifically recognized by a positively charged pocket and an aromatic cap, respectively. The 24-nt siRNA length dependence relies on the separation between the 5′-phosphorylated end of the guide RNA and dual cleavage sites formed by the paired ribonuclease III domains. These structural studies, complemented by functional data, provide insight into the dicing principle for Dicers in general. |
| Author | Harris, C. Jake Zhang, Laixing Wu, Zhe Zhai, Jixian Yang, Zhenlin Zhong, Zhenhui Du, Jiamu Wang, Changshi Yang, Maojun Wang, Qian Xiao, Lifan Li, Sisi Jacobsen, Steven E. Feng, Suhua Xue, Yan |
| AuthorAffiliation | 4 Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK 3 Ministry of Education Key Laboratory of Protein Science, Tsinghua-Peking Center for Life Sciences, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, China 6 Howard Hughes Medical Institute, University of California, Los Angeles, CA 90095 2 Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA 1 Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Institute of Plant and Food Science, School of Life Science, Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong 518055, China 5 Department of Biochemistry and Molecular Biology, International Cancer Center, Shenzhen University Health Science Center, Shenzhen, 518060, China |
| AuthorAffiliation_xml | – name: 2 Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – name: 3 Ministry of Education Key Laboratory of Protein Science, Tsinghua-Peking Center for Life Sciences, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, China – name: 4 Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK – name: 5 Department of Biochemistry and Molecular Biology, International Cancer Center, Shenzhen University Health Science Center, Shenzhen, 518060, China – name: 6 Howard Hughes Medical Institute, University of California, Los Angeles, CA 90095 – name: 1 Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Institute of Plant and Food Science, School of Life Science, Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong 518055, China |
| Author_xml | – sequence: 1 givenname: Qian orcidid: 0000-0002-6369-6899 surname: Wang fullname: Wang, Qian organization: Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Institute of Plant and Food Science, School of Life Science, Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong 518055, China – sequence: 2 givenname: Yan orcidid: 0000-0003-0871-8853 surname: Xue fullname: Xue, Yan organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – sequence: 3 givenname: Laixing orcidid: 0000-0001-9552-3848 surname: Zhang fullname: Zhang, Laixing organization: Ministry of Education Key Laboratory of Protein Science, Tsinghua-Peking Center for Life Sciences, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, China – sequence: 4 givenname: Zhenhui orcidid: 0000-0002-8438-0375 surname: Zhong fullname: Zhong, Zhenhui organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – sequence: 5 givenname: Suhua surname: Feng fullname: Feng, Suhua organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – sequence: 6 givenname: Changshi orcidid: 0000-0001-5206-9737 surname: Wang fullname: Wang, Changshi organization: Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Institute of Plant and Food Science, School of Life Science, Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong 518055, China – sequence: 7 givenname: Lifan orcidid: 0000-0002-4252-0421 surname: Xiao fullname: Xiao, Lifan organization: Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Institute of Plant and Food Science, School of Life Science, Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong 518055, China – sequence: 8 givenname: Zhenlin surname: Yang fullname: Yang, Zhenlin organization: Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Institute of Plant and Food Science, School of Life Science, Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong 518055, China – sequence: 9 givenname: C. Jake orcidid: 0000-0001-5120-0377 surname: Harris fullname: Harris, C. Jake organization: Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK – sequence: 10 givenname: Zhe surname: Wu fullname: Wu, Zhe organization: Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Institute of Plant and Food Science, School of Life Science, Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong 518055, China – sequence: 11 givenname: Jixian orcidid: 0000-0002-0217-0666 surname: Zhai fullname: Zhai, Jixian organization: Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Institute of Plant and Food Science, School of Life Science, Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong 518055, China – sequence: 12 givenname: Maojun orcidid: 0000-0002-6798-3094 surname: Yang fullname: Yang, Maojun organization: Ministry of Education Key Laboratory of Protein Science, Tsinghua-Peking Center for Life Sciences, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, China – sequence: 13 givenname: Sisi orcidid: 0000-0002-7290-8128 surname: Li fullname: Li, Sisi organization: Department of Biochemistry and Molecular Biology, International Cancer Center, Shenzhen University Health Science Center, Shenzhen 518060, China – sequence: 14 givenname: Steven E. orcidid: 0000-0001-9483-138X surname: Jacobsen fullname: Jacobsen, Steven E. organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA., Howard Hughes Medical Institute, University of California, Los Angeles, CA 90095, USA – sequence: 15 givenname: Jiamu orcidid: 0000-0002-1337-0786 surname: Du fullname: Du, Jiamu organization: Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Institute of Plant and Food Science, School of Life Science, Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong 518055, China |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34648373$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These authors contributed equally. Author contributions Q.W. C.W., L.X., and Z.Y. performed the biochemical and structural experiments. Y.X. Z.Z., S.F., and C.H. performed the functional experiments. L.Z contributed to the cryo-EM data processing. Z.W., J.Z., and M.Y. provided helpful discussions. S.L. directed the in vitro assay. S.L., S.E.J., and J.D. supervised the project and wrote the manuscript. |
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| Snippet | In the biogenesis of small RNAs, the Dicer family endonucleases act as a molecular ruler to cut the substrate RNA into defined lengths. Wang
et al
. report a... In eukaryotes, small RNAs (sRNAs) play critical roles in multiple biological processes. Dicer endonucleases are a central part of sRNA biogenesis. In plants,... Ready to diceIn the biogenesis of small RNAs, the Dicer family endonucleases act as a molecular ruler to cut the substrate RNA into defined lengths. Wang et... In eukaryotes, small RNAs (sRNAs) play critical roles in multiple biological processes. Dicer endonucleases are central to sRNA biogenesis. In plants,... |
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| SubjectTerms | Adenosine Arabidopsis - chemistry Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - chemistry Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Biological activity Biosynthesis Cryoelectron Microscopy DNA methylation Domains Eukaryotes Models, Molecular Mutagenesis Nucleic Acid Conformation Nucleotides Phosphorylation Protein Binding Protein Conformation Protein Domains Proteins Ribonuclease III Ribonuclease III - chemistry Ribonuclease III - genetics Ribonuclease III - metabolism Ribonucleic acid RNA RNA, Plant - chemistry RNA, Plant - metabolism RNA, Small Interfering - chemistry RNA, Small Interfering - metabolism siRNA Substrates |
| Title | Mechanism of siRNA production by a plant Dicer-RNA complex in dicing-competent conformation |
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