Ancient origin and recent innovations of RNA polymerase IV and V
Abstract
Small RNA-mediated chromatin modification is a conserved feature of eukaryotes. In flowering plants, the short interfering (si)RNAs that direct transcriptional silencing are abundant and subfunctionalization has led to specialized machinery responsible for synthesis and action of these small RNAs. In particular, plants possess polymerase (Pol) IV and Pol V, multi-subunit homologs of the canonical DNA-dependent RNA Pol II, as well as specialized members of the RNA-dependent RNA Polymerase (RDR), Dicer-like (DCL), and Argonaute (AGO) families. Together these enzymes are required for production and activity of Pol IV-dependent (p4-)siRNAs, which trigger RNA-directed DNA methylation (RdDM) at homologous sequences. p4-siRNAs accumulate highly in developing endosperm, a specialized tissue found only in flowering plants, and are rare in nonflowering plants, suggesting that the evolution of flowers might coincide with the emergence of specialized RdDM machinery. Through comprehensive identification of RdDM genes from species representing the breadth of the land plant phylogeny, we describe the ancient origin of Pol IV and Pol V, suggesting that a nearly complete and functional RdDM pathway could have existed in the earliest land plants. We also uncover innovations in these enzymes that are coincident with the emergence of seed plants and flowering plants, and recent duplications that mightmore »
- Authors:
-
- Univ. of Arizona, Tucson, AZ (United States)
- Univ. Veracruzana, Veracruz (Mexico)
- Univ. of California, Riverside, CA (United States)
- Univ. Autonoma de Queretaro, Queretaro (Mexico)
- Publication Date:
- Research Org.:
- Univ. of Arizona, Tucson, AZ (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1344524
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Molecular Biology and Evolution
- Additional Journal Information:
- Journal Volume: 32; Journal Issue: 7; Journal ID: ISSN 0737-4038
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; escape from adaptive conflict; gene duplication; RNA polymerase IV; RNA polymerase V; RNA silencing; small RNA-directed DNA methylation
Citation Formats
Huang, Yi, Kendall, Timmy, Forsythe, Evan S., Dorantes-Acosta, Ana, Li, Shaofang, Caballero-Perez, Juan, Chen, Xuemei, Arteaga-Vazquez, Mario, Beilstein, Mark A., and Mosher, Rebecca A. Ancient origin and recent innovations of RNA polymerase IV and V. United States: N. p., 2015.
Web. doi:10.1093/molbev/msv060.
Huang, Yi, Kendall, Timmy, Forsythe, Evan S., Dorantes-Acosta, Ana, Li, Shaofang, Caballero-Perez, Juan, Chen, Xuemei, Arteaga-Vazquez, Mario, Beilstein, Mark A., & Mosher, Rebecca A. Ancient origin and recent innovations of RNA polymerase IV and V. United States. https://doi.org/10.1093/molbev/msv060
Huang, Yi, Kendall, Timmy, Forsythe, Evan S., Dorantes-Acosta, Ana, Li, Shaofang, Caballero-Perez, Juan, Chen, Xuemei, Arteaga-Vazquez, Mario, Beilstein, Mark A., and Mosher, Rebecca A. Thu .
"Ancient origin and recent innovations of RNA polymerase IV and V". United States. https://doi.org/10.1093/molbev/msv060. https://www.osti.gov/servlets/purl/1344524.
@article{osti_1344524,
title = {Ancient origin and recent innovations of RNA polymerase IV and V},
author = {Huang, Yi and Kendall, Timmy and Forsythe, Evan S. and Dorantes-Acosta, Ana and Li, Shaofang and Caballero-Perez, Juan and Chen, Xuemei and Arteaga-Vazquez, Mario and Beilstein, Mark A. and Mosher, Rebecca A.},
abstractNote = {Small RNA-mediated chromatin modification is a conserved feature of eukaryotes. In flowering plants, the short interfering (si)RNAs that direct transcriptional silencing are abundant and subfunctionalization has led to specialized machinery responsible for synthesis and action of these small RNAs. In particular, plants possess polymerase (Pol) IV and Pol V, multi-subunit homologs of the canonical DNA-dependent RNA Pol II, as well as specialized members of the RNA-dependent RNA Polymerase (RDR), Dicer-like (DCL), and Argonaute (AGO) families. Together these enzymes are required for production and activity of Pol IV-dependent (p4-)siRNAs, which trigger RNA-directed DNA methylation (RdDM) at homologous sequences. p4-siRNAs accumulate highly in developing endosperm, a specialized tissue found only in flowering plants, and are rare in nonflowering plants, suggesting that the evolution of flowers might coincide with the emergence of specialized RdDM machinery. Through comprehensive identification of RdDM genes from species representing the breadth of the land plant phylogeny, we describe the ancient origin of Pol IV and Pol V, suggesting that a nearly complete and functional RdDM pathway could have existed in the earliest land plants. We also uncover innovations in these enzymes that are coincident with the emergence of seed plants and flowering plants, and recent duplications that might indicate additional subfunctionalization. Phylogenetic analysis reveals rapid evolution of Pol IV and Pol V subunits relative to their Pol II counterparts and suggests that duplicates were retained and subfunctionalized through Escape from Adaptive Conflict. Finally, evolution within the carboxy-terminal domain of the Pol V largest subunit is particularly striking, where illegitimate recombination facilitated extreme sequence divergence.},
doi = {10.1093/molbev/msv060},
journal = {Molecular Biology and Evolution},
number = 7,
volume = 32,
place = {United States},
year = {Thu Mar 12 00:00:00 EDT 2015},
month = {Thu Mar 12 00:00:00 EDT 2015}
}
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Identification and characterization of small non-coding RNAs from Chinese fir by high throughput sequencing
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Conifers have a unique small RNA silencing signature
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Genome-Wide Profiling and Analysis of Arabidopsis siRNAs
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- PLoS Biology, Vol. 5, Issue 3
Physcomitrella patens DCL3 Is Required for 22–24 nt siRNA Accumulation, Suppression of Retrotransposon-Derived Transcripts, and Normal Development
journal, December 2008
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- PLoS Genetics, Vol. 4, Issue 12
A Functional Phylogenomic View of the Seed Plants
journal, December 2011
- Lee, Ernest K.; Cibrian-Jaramillo, Angelica; Kolokotronis, Sergios-Orestis
- PLoS Genetics, Vol. 7, Issue 12
AGO6 Functions in RNA-Mediated Transcriptional Gene Silencing in Shoot and Root Meristems in Arabidopsis thaliana
journal, October 2011
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The iPlant Collaborative: Cyberinfrastructure for Plant Biology
journal, January 2011
- Goff, Stephen A.; Vaughn, Matthew; McKay, Sheldon
- Frontiers in Plant Science, Vol. 2
Pol IV-Dependent siRNA Production is Reduced in Brassica rapa
journal, September 2013
- Huang, Yi; Kendall, Timmy; Mosher, Rebecca
- Biology, Vol. 2, Issue 4
Deep Conservation of Human Protein Tandem Repeats within the Eukaryotes
text, January 2014
- Schaper, Elke; Gascuel, Olivier; Anisimova, Maria
- ETH Zurich
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24-nt reproductive phasiRNAs are broadly present in angiosperms
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Evidence for a Unique DNA-Dependent RNA Polymerase in Cereal Crops
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An Insect Counteradaptation against Host Plant Defenses Evolved through Concerted Neofunctionalization
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Construction and characterization of a knock-down RNA interference line of OsNRPD1 in rice ( Oryza sativa ssp japonica cv Nipponbare)
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Arabidopsis RNA Polymerase IV generates 21–22 nucleotide small RNAs that can participate in RNA-directed DNA methylation and may regulate genes
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Arabidopsis RNA Polymerase IV generates 21-22 nucleotide small RNAs that can participate in RNA-directed DNA methylation and may regulate genes
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Tissue-specific transposon-associated small RNAs in the gymnosperm tree, Norway spruce
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Conservation and divergence of small RNA pathways and microRNAs in land plants
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Draft genome of the living fossil Ginkgo biloba
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Metagenomic sequencing suggests a diversity of RNA interference-like responses to viruses across multicellular eukaryotes
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Evidence for a unique DNA-dependent RNA polymerase in cereal crops
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Four putative SWI2/SNF2 chromatin remodelers have dual roles in regulating DNA methylation in Arabidopsis
journal, October 2018
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24-nt reproductive phasiRNAs are broadly present in angiosperms
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An Insect Counteradaptation against Host Plant Defenses Evolved through Concerted Neofunctionalization
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- Molecular Biology and Evolution, Vol. 36, Issue 5
Catalytic properties of RNA polymerases IV and V: accuracy, nucleotide incorporation and rNTP/dNTP discrimination
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The NRPD1 N-terminus contains a Pol IV-specific motif that is critical for genome surveillance in Arabidopsis
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- Ferrafiat, Laura; Pflieger, David; Singh, Jasleen
- Nucleic Acids Research, Vol. 47, Issue 17
siRNA biogenesis, DNA methylation and target locus silencing are distinct and separable Pol IV sub-functions differentially dependent on the largest subunit's CTD
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Metagenomic sequencing suggests a diversity of RNA interference-like responses to viruses across multicellular eukaryotes
posted_content, March 2018
- Waldron, Fergal M.; Stone, Graham N.; Obbard, Darren J.
- bioRxiv
Evidence for a unique DNA-dependent RNA polymerase in cereal crops
posted_content, February 2018
- Trujillo, Joshua T.; Seetharam, Arun S.; Hufford, Matthew B.
- bioRxiv
Tracing the origin and evolution history of methylation-related genes in plants
journal, July 2019
- Pei, Liuling; Zhang, Lin; Li, Jianying
- BMC Plant Biology, Vol. 19, Issue 1
Evolution of plant genome architecture
journal, March 2016
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- Genome Biology, Vol. 17, Issue 1
Conservation and divergence of small RNA pathways and microRNAs in land plants
journal, August 2017
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- Genome Biology, Vol. 18, Issue 1
Draft genome of the living fossil Ginkgo biloba
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