Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Widespread Translational Inhibition by Plant miRNAs and siRNAs
Peter Brodersen,1
Lali Sakvarelidze-Achard,1
Marianne Bruun-Rasmussen,1
Patrice Dunoyer,1
Yoshiharu Y. Yamamoto,2
Leslie Sieburth,3
Olivier Voinnet1*
Abstract:
High complementarity between plant microRNAs (miRNAs) and theirmessenger RNA targets is thought to cause silencing, prevalentlyby endonucleolytic cleavage. We have isolated Arabidopsis mutantsdefective in miRNA action. Their analysis provides evidencethat plant miRNA–guided silencing has a widespread translationalinhibitory component that is genetically separable from endonucleolyticcleavage. We further show that the same is true of silencingmediated by small interfering RNA (siRNA) populations. Translationalrepression is effected in part by the ARGONAUTE proteins AGO1and AGO10. It also requires the activity of the microtubule-severingenzyme katanin, implicating cytoskeleton dynamics in miRNA action,as recently suggested from animal studies. Also as in animals,the decapping component VARICOSE (VCS)/Ge-1 is required fortranslational repression by miRNAs, which suggests that theunderlying mechanisms in the two kingdoms are related.
1 Institut de Biologie Moléculaire des Plantes du CNRS, Unité Propre de Recherche 2357, 12 rue du Général Zimmer, 67084 Strasbourg Cedex, France. 2 Center for Gene Research, Nagoya University, Furo-cho, Chikusa-ku, Nagoya Aichi, 464-8602, Japan. 3 Department of Biology, University of Utah, Salt Lake City, UT84112, USA.
* To whom correspondence should be addressed. E-mail: olivier.voinnet{at}ibmp-ulp.u-strasbg.fr
The editors suggest the following Related Resources on Science sites:
In Science Signaling
EDITORS' CHOICE
Guy Riddihough (3 June 2008) Sci. Signal.1 (22), ec210.
[DOI: 10.1126/scisignal.122ec210] |Abstract »
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation.
J. Hausser, A. P. Syed, B. Bilen, and M. Zavolan (2013)
Genome Res.
23, 604-615
|Abstract »|Full Text »|PDF »
Small Interfering RNA-Mediated Translation Repression Alters Ribosome Sensitivity to Inhibition by Cycloheximide in Chlamydomonas reinhardtii.
X. Ma, E.-J. Kim, I. Kook, F. Ma, A. Voshall, E. Moriyama, and H. Cerutti (2013)
PLANT CELL
25, 985-998
|Abstract »|Full Text »|PDF »
Tamoxifen Represses miR-200 MicroRNAs and Promotes Epithelial-to-Mesenchymal Transition by Up-Regulating c-Myc in Endometrial Carcinoma Cell Lines.
J.-X. Bai, B. Yan, Z.-N. Zhao, X. Xiao, W.-W. Qin, R. Zhang, L.-T. Jia, Y.-L. Meng, B.-Q. Jin, D.-M. Fan, et al. (2013)
Endocrinology
154, 635-645
|Abstract »|Full Text »|PDF »
Tissue-Specific Silencing of Arabidopsis SU(VAR)3-9 HOMOLOG8 by miR171a.
P. A. Manavella, D. Koenig, I. Rubio-Somoza, H. A. Burbano, C. Becker, and D. Weigel (2013)
Plant Physiology
161, 805-812
|Abstract »|Full Text »|PDF »
Identification and profiling of arsenic stress-induced microRNAs in Brassica juncea.
S. Srivastava, A. K. Srivastava, P. Suprasanna, and S. F. D'Souza (2013)
J. Exp. Bot.
64, 303-315
|Abstract »|Full Text »|PDF »
Lessons on RNA Silencing Mechanisms in Plants from Eukaryotic Argonaute Structures.
A Molecular Link between miRISCs and Deadenylases Provides New Insight into the Mechanism of Gene Silencing by MicroRNAs.
J. E. Braun, E. Huntzinger, and E. Izaurralde (2012)
Cold Spring Harb Perspect Biol
4, a012328
|Abstract »|Full Text »|PDF »
Two MicroRNAs Linked to Nodule Infection and Nitrogen-Fixing Ability in the Legume Lotus japonicus.
A. De Luis, K. Markmann, V. Cognat, D. B. Holt, M. Charpentier, M. Parniske, J. Stougaard, and O. Voinnet (2012)
Plant Physiology
160, 2137-2154
|Abstract »|Full Text »|PDF »
Ultradeep Sequencing Analysis of Population Dynamics of Virus Escape Mutants in RNAi-Mediated Resistant Plants.
F. Martinez, G. Lafforgue, M. J. Morelli, F. Gonzalez-Candelas, N.-H. Chua, J.-A. Daros, and S. F. Elena (2012)
Mol. Biol. Evol.
29, 3297-3307
|Abstract »|Full Text »|PDF »
Dissecting Functions of KATANIN and WRINKLED1 in Cotton Fiber Development by Virus-Induced Gene Silencing.
J. Qu, J. Ye, Y.-F. Geng, Y.-W. Sun, S.-Q. Gao, B.-P. Zhang, W. Chen, and N.-H. Chua (2012)
Plant Physiology
160, 738-748
|Abstract »|Full Text »|PDF »
Functional Analysis of Three Arabidopsis ARGONAUTES Using Slicer-Defective Mutants.
A. Carbonell, N. Fahlgren, H. Garcia-Ruiz, K. B. Gilbert, T. A. Montgomery, T. Nguyen, J. T. Cuperus, and J. C. Carrington (2012)
PLANT CELL
24, 3613-3629
|Abstract »|Full Text »|PDF »
IAA-Ala Resistant3, an Evolutionarily Conserved Target of miR167, Mediates Arabidopsis Root Architecture Changes during High Osmotic Stress.
N. Kinoshita, H. Wang, H. Kasahara, J. Liu, C. MacPherson, Y. Machida, Y. Kamiya, M. A. Hannah, and N.-H. Chua (2012)
PLANT CELL
24, 3590-3602
|Abstract »|Full Text »|PDF »
The MicroRNA Pathway Genes AGO1, HEN1 and HYL1 Participate in Leaf Proximal-Distal, Venation and Stomatal Patterning in Arabidopsis.
S. Jover-Gil, H. Candela, P. Robles, V. Aguilera, J. M. Barrero, J. L. Micol, and M. R. Ponce (2012)
Plant Cell Physiol.
53, 1322-1333
|Abstract »|Full Text »|PDF »
Complexity of miRNA-dependent regulation in root symbiosis.
J. Bazin, P. Bustos-Sanmamed, C. Hartmann, C. Lelandais-Briere, and M. Crespi (2012)
Phil Trans R Soc B
367, 1570-1579
|Abstract »|Full Text »|PDF »
Known and novel post-transcriptional regulatory sequences are conserved across plant families.
J. N. Vaughn, S. R. Ellingson, F. Mignone, and A. von Arnim (2012)
RNA
18, 368-384
|Abstract »|Full Text »|PDF »
A MicroRNA Superfamily Regulates Nucleotide Binding Site-Leucine-Rich Repeats and Other mRNAs.
P. V. Shivaprasad, H.-M. Chen, K. Patel, D. M. Bond, B. A. C. M. Santos, and D. C. Baulcombe (2012)
PLANT CELL
24, 859-874
|Abstract »|Full Text »|PDF »
Isoprenoid biosynthesis is required for miRNA function and affects membrane association of ARGONAUTE 1 in Arabidopsis.
P. Brodersen, L. Sakvarelidze-Achard, H. Schaller, M. Khafif, G. Schott, A. Bendahmane, and O. Voinnet (2012)
PNAS
109, 1778-1783
|Abstract »|Full Text »|PDF »
Mutations in the GW-repeat protein SUO reveal a developmental function for microRNA-mediated translational repression in Arabidopsis.
mirEX: a platform for comparative exploration of plant pri-miRNA expression data.
D. Bielewicz, J. Dolata, A. Zielezinski, S. Alaba, B. Szarzynska, M. W. Szczesniak, A. Jarmolowski, Z. Szweykowska-Kulinska, and W. M. Karlowski (2012)
Nucleic Acids Res.
40, D191-D197
|Abstract »|Full Text »|PDF »
Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa.
X. Yu, H. Wang, Y. Lu, M. de Ruiter, M. Cariaso, M. Prins, A. van Tunen, and Y. He (2012)
J. Exp. Bot.
63, 1025-1038
|Abstract »|Full Text »|PDF »
Suppression of Arabidopsis ARGONAUTE1-Mediated Slicing, Transgene-Induced RNA Silencing, and DNA Methylation by Distinct Domains of the Cucumber mosaic virus 2b Protein.
C.-G. Duan, Y.-Y. Fang, B.-J. Zhou, J.-H. Zhao, W.-N. Hou, H. Zhu, S.-W. Ding, and H.-S. Guo (2012)
PLANT CELL
24, 259-274
|Abstract »|Full Text »|PDF »
Massive Analysis of Rice Small RNAs: Mechanistic Implications of Regulated MicroRNAs and Variants for Differential Target RNA Cleavage.
D.-H. Jeong, S. Park, J. Zhai, S. G. R. Gurazada, E. De Paoli, B. C. Meyers, and P. J. Green (2011)
PLANT CELL
23, 4185-4207
|Abstract »|Full Text »|PDF »
The Regulatory Activities of Plant MicroRNAs: A More Dynamic Perspective.
Y. Meng, C. Shao, H. Wang, and M. Chen (2011)
Plant Physiology
157, 1583-1595
|Full Text »|PDF »
Toward microRNA-mediated gene regulatory networks in plants.
Tempo and Mode of Plant RNA Virus Escape from RNA Interference-Mediated Resistance.
G. Lafforgue, F. Martinez, J. Sardanyes, F. de la Iglesia, Q.-W. Niu, S.-S. Lin, R. V. Sole, N.-H. Chua, J.-A. Daros, and S. F. Elena (2011)
J. Virol.
85, 9686-9695
|Abstract »|Full Text »|PDF »
Differential expression of the microRNAs in superior and inferior spikelets in rice (Oryza sativa).
T. Peng, Q. Lv, J. Zhang, J. Li, Y. Du, and Q. Zhao (2011)
J. Exp. Bot.
62, 4943-4954
|Abstract »|Full Text »|PDF »
An Importin {beta} Protein Negatively Regulates MicroRNA Activity in Arabidopsis.
W. Wang, R. Ye, Y. Xin, X. Fang, C. Li, H. Shi, X. Zhou, and Y. Qi (2011)
PLANT CELL
23, 3565-3576
|Abstract »|Full Text »|PDF »
Stars and Symbiosis: MicroRNA- and MicroRNA*-Mediated Transcript Cleavage Involved in Arbuscular Mycorrhizal Symbiosis.
E. A. Devers, A. Branscheid, P. May, and F. Krajinski (2011)
Plant Physiology
156, 1990-2010
|Abstract »|Full Text »|PDF »
psRNATarget: a plant small RNA target analysis server.
Identification of an ARGONAUTE for Antiviral RNA Silencing in Nicotiana benthamiana.
H. B. Scholthof, V. Y. Alvarado, J. C. Vega-Arreguin, J. Ciomperlik, D. Odokonyero, C. Brosseau, M. Jaubert, A. Zamora, and P. Moffett (2011)
Plant Physiology
156, 1548-1555
|Abstract »|Full Text »|PDF »
MicroRNAs in the shoot apical meristem of soybean.
C. E. Wong, Y.-T. Zhao, X.-J. Wang, L. Croft, Z.-H. Wang, F. Haerizadeh, J. S. Mattick, M. B. Singh, B. J. Carroll, and P. L. Bhalla (2011)
J. Exp. Bot.
62, 2495-2506
|Abstract »|Full Text »|PDF »
Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica).
T. Li, H. Li, Y.-X. Zhang, and J.-Y. Liu (2011)
Nucleic Acids Res.
39, 2821-2833
|Abstract »|Full Text »|PDF »
ETOILE Regulates Developmental Patterning in the Filamentous Brown Alga Ectocarpus siliculosus.
A. Le Bail, B. Billoud, S. Le Panse, S. Chenivesse, and B. Charrier (2011)
PLANT CELL
23, 1666-1678
|Abstract »|Full Text »|PDF »
Computational analysis of miRNA targets in plants: current status and challenges.
Complex Regulation of Two Target Genes Encoding SPX-MFS Proteins by Rice miR827 in Response to Phosphate Starvation.
S.-I. Lin, C. Santi, E. Jobet, E. Lacut, N. El Kholti, W. M. Karlowski, J.-L. Verdeil, J. C. Breitler, C. Perin, S.-S. Ko, et al. (2010)
Plant Cell Physiol.
51, 2119-2131
|Abstract »|Full Text »|PDF »
MicroRNA Gene Regulation Cascades During Early Stages of Plant Development.
Global effects of the small RNA biogenesis machinery on the Arabidopsis thaliana transcriptome.
S. Laubinger, G. Zeller, S. R. Henz, S. Buechel, T. Sachsenberg, J.-W. Wang, G. Ratsch, and D. Weigel (2010)
PNAS
107, 17466-17473
|Abstract »|Full Text »|PDF »
The MicroRNA159-Regulated GAMYB-like Genes Inhibit Growth and Promote Programmed Cell Death in Arabidopsis.
M. M. Alonso-Peral, J. Li, Y. Li, R. S. Allen, W. Schnippenkoetter, S. Ohms, R. G. White, and A. A. Millar (2010)
Plant Physiology
154, 757-771
|Abstract »|Full Text »|PDF »
Conserved RNaseII domain protein functions in cytoplasmic mRNA decay and suppresses Arabidopsis decapping mutant phenotypes.
Small RNA Duplexes Function as Mobile Silencing Signals Between Plant Cells.
P. Dunoyer, G. Schott, C. Himber, D. Meyer, A. Takeda, J. C. Carrington, and O. Voinnet (2010)
Science
328, 912-916
|Abstract »|Full Text »|PDF »
Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis.
H. Lee, S. J. Yoo, J. H. Lee, W. Kim, S. K. Yoo, H. Fitzgerald, J. C. Carrington, and J. H. Ahn (2010)
Nucleic Acids Res.
38, 3081-3093
|Abstract »|Full Text »|PDF »
microRNA, seeds, and Darwin?: diverse function of miRNA in seed biology and plant responses to stress.
R. C. Martin, P.-P. Liu, N. A. Goloviznina, and H. Nonogaki (2010)
J. Exp. Bot.
61, 2229-2234
|Abstract »|Full Text »|PDF »
Arabidopsis lyrata Small RNAs: Transient MIRNA and Small Interfering RNA Loci within the Arabidopsis Genus.
Systems Biology Update: Cell Type-Specific Transcriptional Regulatory Networks.
L. Pu and S. Brady (2010)
Plant Physiology
152, 411-419
|Full Text »|PDF »
Conservation and divergence of microRNAs and their functions in Euphorbiaceous plants.
C. Zeng, W. Wang, Y. Zheng, X. Chen, W. Bo, S. Song, W. Zhang, and M. Peng (2010)
Nucleic Acids Res.
38, 981-995
|Abstract »|Full Text »|PDF »
Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis.
D. Moldovan, A. Spriggs, J. Yang, B. J. Pogson, E. S. Dennis, and I. W. Wilson (2010)
J. Exp. Bot.
61, 165-177
|Abstract »|Full Text »|PDF »
The Arabidopsis Tandem Zinc Finger Protein AtTZF1 Traffics between the Nucleus and Cytoplasmic Foci and Binds Both DNA and RNA.
M. C. Pomeranz, C. Hah, P.-C. Lin, S. G. Kang, J. J. Finer, P. J. Blackshear, and J.-C. Jang (2010)
Plant Physiology
152, 151-165
|Abstract »|Full Text »|PDF »
Sliced microRNA targets and precise loop-first processing of MIR319 hairpins revealed by analysis of the Physcomitrella patens degradome.
C. Addo-Quaye, J. A. Snyder, Y. B. Park, Y.-F. Li, R. Sunkar, and M. J. Axtell (2009)
RNA
15, 2112-2121
|Abstract »|Full Text »|PDF »
Uncovering Small RNA-Mediated Responses to Phosphate Deficiency in Arabidopsis by Deep Sequencing.
L.-C. Hsieh, S.-I. Lin, A. C.-C. Shih, J.-W. Chen, W.-Y. Lin, C.-Y. Tseng, W.-H. Li, and T.-J. Chiou (2009)
Plant Physiology
151, 2120-2132
|Abstract »|Full Text »|PDF »
Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis.
A. Mustroph, M. E. Zanetti, C. J. H. Jang, H. E. Holtan, P. P. Repetti, D. W. Galbraith, T. Girke, and J. Bailey-Serres (2009)
PNAS
106, 18843-18848
|Abstract »|Full Text »|PDF »
Deciphering the diversity of small RNAs in plants: the long and short of it.
F. Schwach, S. Moxon, V. Moulton, and T. Dalmay (2009)
Briefings in Functional Genomics
8, 472-481
|Abstract »|Full Text »|PDF »
Rice MicroRNA Effector Complexes and Targets.
L. Wu, Q. Zhang, H. Zhou, F. Ni, X. Wu, and Y. Qi (2009)
PLANT CELL
21, 3421-3435
|Abstract »|Full Text »|PDF »
MOSAIC FLORAL ORGANS1, an AGL6-Like MADS Box Gene, Regulates Floral Organ Identity and Meristem Fate in Rice.
S. Ohmori, M. Kimizu, M. Sugita, A. Miyao, H. Hirochika, E. Uchida, Y. Nagato, and H. Yoshida (2009)
PLANT CELL
21, 3008-3025
|Abstract »|Full Text »|PDF »
Graft-transmissible induction of potato tuberization by the microRNA miR172.
A. Martin, H. Adam, M. Diaz-Mendoza, M. Zurczak, N. D. Gonzalez-Schain, and P. Suarez-Lopez (2009)
Development
136, 2873-2881
|Abstract »|Full Text »|PDF »
Signals and prepatterns: new insights into organ polarity in plants.
A. Y. Husbands, D. H. Chitwood, Y. Plavskin, and M. C.P. Timmermans (2009)
Genes & Dev.
23, 1986-1997
|Abstract »|Full Text »|PDF »
Genome-Wide Medicago truncatula Small RNA Analysis Revealed Novel MicroRNAs and Isoforms Differentially Regulated in Roots and Nodules.
C. Lelandais-Briere, L. Naya, E. Sallet, F. Calenge, F. Frugier, C. Hartmann, J. Gouzy, and M. Crespi (2009)
PLANT CELL
21, 2780-2796
|Abstract »|Full Text »|PDF »
Transcriptome Analyses Revealed Diverse Expression Changes in ago1 and hyl1 Arabidopsis Mutants.
Y. Kurihara, E. Kaminuma, A. Matsui, M. Kawashima, M. Tanaka, T. Morosawa, J. Ishida, Y. Mochizuki, K. Shinozaki, T. Toyoda, et al. (2009)
Plant Cell Physiol.
50, 1715-1720
|Abstract »|Full Text »|PDF »
Analysis of Post-transcriptional Regulations by a Functional, Integrated, and Quantitative Method.
B. Laloo, D. Simon, V. Veillat, D. Lauzel, V. Guyonnet-Duperat, F. Moreau-Gaudry, F. Sagliocco, and C. Grosset (2009)
Mol. Cell. Proteomics
8, 1777-1788
|Abstract »|Full Text »|PDF »
Comprehensive prediction of novel microRNA targets in Arabidopsis thaliana.
L. Alves-Junior, S. Niemeier, A. Hauenschild, M. Rehmsmeier, and T. Merkle (2009)
Nucleic Acids Res.
37, 4010-4021
|Abstract »|Full Text »|PDF »
Defining the Functional Network of Epigenetic Regulators in Arabidopsis thaliana.
Identification of Nutrient-Responsive Arabidopsis and Rapeseed MicroRNAs by Comprehensive Real-Time Polymerase Chain Reaction Profiling and Small RNA Sequencing.
B. D. Pant, M. Musialak-Lange, P. Nuc, P. May, A. Buhtz, J. Kehr, D. Walther, and W.-R. Scheible (2009)
Plant Physiology
150, 1541-1555
|Abstract »|Full Text »|PDF »
Small RNA analysis in Petunia hybrida identifies unusual tissue-specific expression patterns of conserved miRNAs and of a 24mer RNA.
P. Tedder, E. Zubko, D. R. Westhead, and P. Meyer (2009)
RNA
15, 1012-1020
|Abstract »|Full Text »|PDF »
Biochemical Evidence for Translational Repression by Arabidopsis MicroRNAs.
E. Lanet, E. Delannoy, R. Sormani, M. Floris, P. Brodersen, P. Crete, O. Voinnet, and C. Robaglia (2009)
PLANT CELL
21, 1762-1768
|Abstract »|Full Text »|PDF »
Investigating Translational Repression by MicroRNAs in Arabidopsis.