Advances on the Molecular Action Mechanisms of Plant miRNA

doi:10.13560/j.cnki.biotech.bull.1985.2020-0262

Abstract

Abstract: microRNAs（miRNAs）are a class of 20- to 24-nucleotide（nt）endogenous noncoding single-stranded RNAs widely exisitng in eukaryote. miRNAs in plants negatively regulate the expressions of target genes through mRNA cleavage or translation repression and play important roles in cell proliferation and differentiation,growth and development of an individual,and responses to environmental stresses. Since the first identification of plant miRNAs in 2002,research on miRNAs has become a hotspot in the field of plant molecular biology. Decades of research have elucidated the mechanisms of miRNA biogenesis and degradation and revealed the regulatory roles of miRNAs in numerous biological processes in plants. However,mechanisms underpinning the action of plant miRNAs are still not well understood,especially with respect to miRNA-mediated translation repression. This review summarizes both historical perspectives and the latest progress on the plant miRNAs-mediated mRNA cleavage and translation repression,discusses the influencing factors and relationship of two mechanisms,and suggests the research direction and thoughts in future,aiming at providing a theoretical basis for in-depth understanding of the mechanism of plant miRNA and promoting the basic research and practical application of miRNA.

Key words: miRNA, mRNA cleavage, translation repression, phasiRNA

ZHANG Cui-ju, MO Bei-xin, CHEN Xue-mei, CUI Jie. Advances on the Molecular Action Mechanisms of Plant miRNA[J]. Biotechnology Bulletin, 2020, 36(7): 1-14.

References

[1] Lee RC, Feinbaum RL, Ambres V.The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14[J]. Cell, 1993, 75(5):843-854.
[2] Reinhart BJ, Slack FJ, Basson M, et al.The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans[J]. Nature, 2000, 403(6772):901-906.
[3] Reinhart BJ, Weinstein EG, Rhoades MW, et al.MicroRNAs in plants[J]. Genes & Development, 2002, 16(13):1616-1626.
[4] Llave C.Cleavage of scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA[J]. Science, 2002, 297(5589):2053-2056.
[5] Park W, Li J, Song R, et al.CARPEL FACTORY, a dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana[J]. Current Biology, 2002, 12(17):1484-1495.
[6] Kozomara A, Birgaoanu M, Griffiths-Jones S. miRBase:from microRNA sequences to function[J]. Nucleic Acids Research, 2019, 47(1):D155-D162.
[7] Hamilton AJ, Baulcombe DC.A species of small antisense RNA in posttranscriptional gene silencing in plants[J]. Science, 1999, 286(5441):950-952.
[8] Aukerman MJ, Sakai H.Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes[J]. The Plant Cell, 2003, 15(11):2730-2741.
[9] Chen X.A MicroRNA as a translational repressor of APETALA2 in Arabidopsis flower development[J]. Science, 2004, 303(5666):2022-2025.
[10] Gandikota M, Birkenbihl RP, Höhmann S, et al.The miRNA156/157 recognition element in the 3' UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings[J]. The Plant Journal, 2007, 49(4):683-693.
[11] Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, et al.Widespread translational inhibition by plant miRNAs and siRNAs[J]. Science, 2008, 320(5880):1185-1190.
[12] 熊雪梅, 吴莹, 王洋. 植物体内调控miRNA合成与功能的机制研究进展[J]. 植物研究, 2014, 34(2):282-288.
[13] 郭韬, 李广林, 魏强, 等. 植物MicroRNA功能的研究进展[J]. 西北植物学报, 2011, 31(11):2347-2354.
[14] 许硕, 胡正, 姜奇彦, 等. 植物microRNA功能及其在逆境条件下的研究进展[J]. 生物技术通报, 2012(2):1-7.
[15] 张俊红, 张守攻, 齐力旺. 植物成熟microRNA转录后修饰与降解的研究进展[J]. 植物学报, 2014, 49(4):483-489.
[16] Yu Y, Jia T, Chen X.The ‘how’ and ‘where’ of plant microRNAs[J]. The New Phytologist, 2017, 216(4):1002-1017.
[17] Ipsaro JJ, Joshua-Tor L.From guide to target:molecular insights into eukaryotic RNA-interference machinery[J]. Nature Structural & Molecular Biology, 2015, 22(1):20-28.
[18] Iwakawa HO, Tomari Y.The functions of microRNAs:mRNA decay and translational repression[J]. Trends in Cell Biology, 2015, 25(11):651-665.
[19] Iwakawa HO, Tomari Y.Molecular insights into microRNA-mediated translational repression in plants[J]. Molecular Cell, 2013, 52(4):591-601.
[20] Arribas-Hernández L, Kielpinski LJ, Brodersen P. mRNA decay of most Arabidopsis miRNA targets requires slicer activity of AGO1[J]. Plant Physiology, 2016, 171(4):2620-2632.
[21] German MA, Pillay M, Jeong DH, et al.Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends[J]. Nature Biotechnology, 2008, 26(8):941-946.
[22] Höck J, Meister G.The Argonaute protein family[J]. Genome Biology, 2008, 9(2):210.
[23] Baumberger N, Baulcombe DC.Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs[J]. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(33):11928-11933.
[24] Qi Y, Denli AM, Hannon GJ.Biochemical specialization within Arabidopsis RNA silencing pathways[J]. Molecular Cell, 2005, 19(3):421-428.
[25] Mi S, Cai T, Hu Y, et al.Sorting of small RNAs into Arabidopsis Argonaute complexes is directed by the 5' terminal nucleotide[J]. Cell, 2008, 133(1):116-127.
[26] Montgomery TA, Howell MD, Cuperus JT, et al.Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation[J]. Cell, 2008, 133(1):128-141.
[27] Takeda A, Iwasaki S, Watanabe T, et al.The mechanism selecting the guide strand from small RNA duplexes is different among Argonaute proteins[J]. Plant and Cell Physiology, 2008, 49(4):493-500.
[28] Ji L, Liu X, Yan J, et al.ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis[J]. PLoS Genetics, 2011, 7(3):e1001358.
[29] Maunoury N, Vaucheret H.AGO1 and AGO2 act redundantly in miR408-mediated plantacyanin regulation[J]. PLoS One, 2011, 6(12):e28729.
[30] Zhu H, Hu F, Wang R, et al.Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development[J]. Cell, 2011, 145(2):242-256.
[31] Hutvagner G, Simard MJ.Argonaute proteins:key players in RNA silencing[J]. Nature Reviews Molecular Cell Biology, 2008, 9(1):22-32.
[32] Elbashir SM, Lendeckel W, Tuschl T.RNA interference is mediated by 21- and 22-nucleotide RNAs[J]. Genes & Development, 2001, 15(2):188-200.
[33] Souret FF, Kastenmayer JP, Green PJ.AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets[J]. Molecular Cell, 2004, 15(2):173-183.
[34] Ibrahim F, Rohr J, Jeong WJ, et al.Untemplated oligoadenylation promotes degradation of RISC-cleaved transcripts[J]. Science, 2006, 314(5807):1893-1893.
[35] Ren G, Xie M, Zhang S, et al.Methylation protects microRNAs from an AGO1-associated activity that uridylates 5' RNA fragments generated by AGO1 cleavage[J]. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(17):6365-6370.
[36] Wang X, Zhang S, Dou Y, et al.Synergistic and independent actions of multiple terminal nucleotidyl transferases in the 3' tailing of small RNAs in Arabidopsis[J]. PLoS Genetics, 2015, 11(4):e1005091.
[37] Zhang Z, Hu F, Sung MW, et al.RISC-interacting clearing 3'-5' exoribonucleases(RICEs)degrade uridylated cleavage fragments to maintain functional RISC in Arabidopsis thaliana[J]. eLife, 2017, 6:e24466.
[38] Branscheid A, Marchais A, Schott G, et al.SKI2 mediates degradation of RISC 5'-cleavage fragments and prevents secondary siRNA production from miRNA targets in Arabidopsis[J]. Nucleic Acids Research, 2015, 43(22):10975-10988.
[39] Orban TI, Izaurralde E.Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome[J]. RNA, 2005, 11(4):459-469.
[40] Alonso-Peral MM, Li J, Li Y, et al.The microRNA159-regulated GAMYB-like genes inhibit growth and promote programmed cell death in Arabidopsis[J]. Plant Physiology, 2010, 154(2):757-771.
[41] Li S, Liu L, Zhuang X, et al.MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis[J]. Cell, 2013, 153(3):562-574.
[42] Liu MJ, Wu SH, Wu JF, et al.Translational landscape of photomorphogenic Arabidopsis[J]. The Plant Cell, 2013, 25(10):3699-3710.
[43] Reis RS, Hart-Smith G, Eamens AL, et al.Gene regulation by translational inhibition is determined by Dicer partnering proteins[J]. Nature Plants, 2015, 1:14027.
[44] Zekri L, Kuzuoğlu-Öztürk D, Izaurralde E. GW182 proteins cause PABP dissociation from silenced miRNA targets in the absence of deadenylation[J]. The EMBO Journal, 2013, 32(7):1052-1065.
[45] Huntzinger E, Izaurralde E.Gene silencing by microRNAs:contributions of translational repression and mRNA decay[J]. Nature Reviews Genetics, 2011, 12(2):99-110.
[46] Iki T, Yoshikawa M, Nishikiori M, et al.In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90[J]. Molecular Cell, 2010, 39(2):282-291.
[47] Iki T, Yoshikawa M, Meshi T, et al.Cyclophilin 40 facilitates HSP90-mediated RISC assembly in plants[J]. The EMBO Journal, 2012, 31(2):267-278.
[48] Cui Y, Fang X, Qi Y.TRANSPORTIN1 promotes the association of microRNA with ARGONAUTE1 in Arabidopsis[J]. The Plant Cell, 2016, 28(10):2576-2585.
[49] Yang L, Wu G, Poethig RS.Mutations in the GW-repeat protein SUO reveal a developmental function for microRNA-mediated translational repression in Arabidopsis[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(1):315-320.
[50] Pomeranz M, Lin PC, Finer J, et al.AtTZF gene family localizes to cytoplasmic foci[J]. Plant Signaling & Behavior, 2010, 5(2):190-192.
[51] Weber C, Nover L, Fauth M.Plant stress granules and mRNA processing bodies are distinct from heat stress granules[J]. The Plant Journal, 2008, 56(4):517-530.
[52] Rogers K, Chen X.Biogenesis, turnover, and mode of action of plant microRNAs[J]. The Plant Cell, 2013, 25(7):2383-2399.
[53] Lanet E, Delannoy E, Sormani R, et al.Biochemical evidence for translational repression by Arabidopsis microRNAs[J]. The Plant Cell, 2009, 21(6):1762-1768.
[54] Ma X, Ibrahim F, Kim EJ, et al.An ortholog of the Vasa intronic gene is required for small RNA-mediated translation repression in Chlamydomonas reinhardtii[J]. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117(1):761-770.
[55] Van Dyke N, Pickering BF, Van Dyke MW.Stm1p alters the ribosome association of eukaryotic elongation factor 3 and affects translation elongation[J]. Nucleic Acids Research, 2009, 37(18):6116-6125.
[56] Bolger GB.The RNA-binding protein SERBP1 interacts selectively with the signaling protein RACK1[J]. Cell Signaling, 2017, 35:256-263.
[57] Jannot G, Bajan S, Giguère NJ, et al.The ribosomal protein RACK1 is required for microRNA function in both C. elegans and humans[J]. EMBO Reports, 2011, 12(6):581-586.
[58] Speth C, Willing EM, Rausch S, et al.RACK1 scaffold proteins influence miRNA abundance in Arabidopsis[J]. The Plant Journal, 2013, 76(3):433-445.
[59] Yekta S, Shih IH, Bartel DP.MicroRNA-directed cleavage of HOXB8 mRNA[J]. Science, 2004, 304(5670):594-596.
[60] Hausser J, Syed AP, Bilen B, et al.Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation[J]. Genome Research, 2013, 23(4):604-615.
[61] Yamasaki T, Voshall A, Kim EJ et al. Complementarity to an miRNA seed region is sufficient to induce moderate repression of a target transcript in the unicellular green alga Chlamydomonas reinhardtii[J]. The Plant Journal, 2013, 76(6):1045-1056.
[62] Liu Q, Wang F, Axtell MJ.Analysis of complementarity requirements for plant microRNA targeting using a Nicotiana benthamiana quantitative transient assay[J]. The Plant Cell, 2014, 26(2):741-753.
[63] Li JF, Chung HS, Niu Y, et al.Comprehensive protein-based artificial microRNA screens for effective gene silencing in plants[J]. The Plant Cell, 2013, 25(5):1507-1522.
[64] Hou CY, Lee WC, Chou HC, et al.Global analysis of truncated RNA ends reveals new insights into ribosome stalling in plants[J]. The Plant Cell, 2016, 28(10):2398-2416.
[65] Fei Q, Xia R, Meyers BC.Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks[J]. The Plant Cell, 2013, 25(7):2400-2415.
[66] Johnson C, Kasprzewska A, Tennessen K, et al.Clusters and superclusters of phased small RNAs in the developing inflorescence of rice[J]. Genome Research, 2009, 19(8):1429-1440.
[67] International Brachypodium Initiative.Genome sequencing and analysis of the model grass Brachypodium distachyon[J]. Nature, 2010, 463(7282):763-768.
[68] Song X, Li P, Zhai J, et al.Roles of DCL4 and DCL3b in rice phased small RNA biogenesis[J]. The Plant Journal, 2012, 69(3):462-474.
[69] Yoshikawa M.A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis[J]. Genes & Development, 2005, 19(18):2164-2175.
[70] Allen E, Xie Z, Gustafson AM, et al.MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants[J]. Cell, 2005, 121(2):207-221.
[71] Axtell M J, Jan C, Rajagopalan R, et al.A two-hit trigger for siRNA biogenesis in plants[J]. Cell, 2006, 127(3):565-577.
[72] Zhai J, Jeong DH, De Paoli E, et al.MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs[J]. Genes & Development, 2011, 25(23):2540-2553.
[73] Xia R, Meyers BC, Liu Z, et al.MicroRNA superfamilies descended from miR390 and their roles in secondary small interfering RNA Biogenesis in Eudicots[J]. The Plant Cell, 2013, 25(5):1555-1572.
[74] Chen HM, Chen LT, Patel K, et al.22-nucleotide RNAs trigger secondary siRNA biogenesis in plants[J]. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(34):15269-15274.
[75] Cuperus JT, Carbonell A, Fahlgren N, et al.Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis[J]. Nature Structural & Molecular Biology, 2010, 17(8):997-1003.
[76] Zhai J, Zhao Y, Simon SA, et al.Plant microRNAs display differential 3' truncation and tailing modifications that are ARGONAUTE1 dependent and conserved across species[J]. The Plant Cell, 2013, 25(7):2417-2428.
[77] Manavella P, Hagmann J, Ott F, et al.Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1[J]. Cell, 2012, 151(4):859-870.
[78] Zhang C, Ng WK, Lu J, et al.Roles of target site location and sequence complementarity in trans-acting siRNA formation in Arabidopsis[J]. The Plant Journal, 2012, 69(2):217-226.
[79] Yoshikawa M, Iki T, Numa H, et al.A short open reading frame encompassing the microRNA173 target site plays a role in trans-acting small interfering RNA biogenesis[J]. Plant Physiology, 2016, 171(1):359-368.
[80] Li S, Le B, Ma X, et al.Biogenesis of phased siRNAs on membrane-bound polysomes in Arabidopsis[J]. eLife, 2016, 5:e22750.
[81] Arribas-Hernandez L, Marchais A, Poulsen C, et al.The slicer activity of ARGONAUTE1 is required specifically for the phasing, not production, of trans-acting short interfering RNAs in Arabidopsis[J]. The Plant Cell, 2016, 28(7):1563-1580.
[82] Bajczyk M, Bhat SS, Szewc L, et al.Novel nuclear functions of Arabidopsis ARGONAUTE1:beyond RNA interference[J]. Plant Physiology, 2019, 179(3):1030-1039.
[83] Derrien B, Baumberger N, Schepetilnikov M, et al.Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(39):15942-15946.
[84] Xu J, Chua NH.Processing bodies and plant development[J]. Current Opinion in Plant Biology, 2011, 14(1):88-93.
[85] Teixeira D, Sheth U, Valencia-Sanchez MA, et al.Processing bodies require RNA for assembly and contain nontranslating mRNAs[J]. RNA, 2005, 11(4):371-382.
[86] Brodersen P, Sakvarelidzeachard L, Schaller H, et al.Isoprenoid biosynthesis is required for miRNA function and affects membrane association of ARGONAUTE 1 in Arabidopsis[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(5):1778-1783.
[87] Yu X, Willmann MR, Anderson SJ, et al.Genome-wide mapping of uncapped and cleaved transcripts reveals a role for the nuclear mRNA cap-binding complex in cotranslational RNA decay in Arabidopsis[J]. The Plant Cell, 2016, 28(10):2385-2397.
[88] Liu L, Chen X.Intercellular and systemic trafficking of RNAs in plants[J]. Nature Plants, 2018, 4(11):869-878.
[89] Wilczynska A, Bushell M.The complexity of miRNA-mediated repression[J]. Cell Death and Differentiation, 2015, 22(1):22-33.
[90] Earley K, Smith M, Weber R, et al.An endogenous F-box protein regulates ARGONAUTE1 in Arabidopsis thaliana[J]. Silence, 2010, 1(1):15.
[91] Csorba T, Lózsa R, Hutvágner G, et al.Polerovirus protein P0 prevents the assembly of small RNA-containing RISC complexes and leads to degradation of ARGONAUTE1[J]. The Plant Journal, 2010, 62(3):463-472.
[92] Beauclair L, Yu A, Bouché N. microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis[J]. The Plant Journal, 2010, 62(3):454-462.
[93] Bhattacharyya SN, Habermacher R, Martine U, et al.Stress-induced reversal of microRNA repression and mRNA P-body localization in human cells[J]. Cold Spring Harbor Symposia on Quantitative Biology, 2006, 71:513-521.
[94] Muddashetty RS, Nalavadi VC, Gross C, et al.Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling[J]. Molecular Cell, 2011, 42(5):673-688.
[95] Mazumder A, Bose M, Chakraborty A, et al.A transient reversal of miRNA-mediated repression controls macrophage activation[J]. EMBO Report, 2013, 14(11):1008-1016.
[96] Voinnet O.Origin, biogenesis, and activity of plant microRNAs[J]. Cell, 2009, 136(4):669-687.
[97] Reynoso E, Nesci A, Allegretti P, et al.Kinetic and mechanistic aspects of sensitized photodegradation of β-lactam antibiotics:microbiological implications[J]. Redox Report, 2012, 17(6):275-283.