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Conservation and divergence in plant microRNAs

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Abstract

MicroRNAs (miRNAs) are a class of small, non-coding RNAs that regulate gene expression in eukaryotic cells. The past decade has seen an explosion in our understanding of the sets of miRNA genes encoded in the genomes in different species of plants and the mechanisms by which miRNAs interact with target RNAs. A subset of miRNA families (and their binding sites in target RNAs) are conserved between angiosperms and basal plants, suggesting they predate the divergence of existing lineages of plants. However, the majority of miRNA families expressed by any given plant species have a narrow phylogenetic distribution. As a group, these “young” miRNAs genes appear to be evolutionarily fluid and lack clearly understood biological function. The goal of this review is to summarize our understanding of the sets of miRNA genes and miRNA targets that exist in various plant species and to discuss hypotheses that explain the patterns of conservation and divergence observed among microRNAs in plants.

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References

  • Adai A, Johnson C, Mlotshwa S et al (2005) Computational prediction of miRNAs in Arabidopsis thaliana. Genome Res 15(1):78–91

    Article  PubMed  CAS  Google Scholar 

  • Addo-Quaye C, Eshoo T, Bartel D, Axtell M (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18:1–5

    Article  Google Scholar 

  • Addo-Quaye C, Snyder JA, Park YB, Li YF, Sunkar R, Axtell MJ (2009) Sliced microRNA targets and precise loop-first processing of MIR319 hairpins revealed by analysis of the Physcomitrella patens degradome. RNA 15(12):2112–2121

    Article  PubMed  CAS  Google Scholar 

  • Allen E, Howell MD (2010) miRNAs in the biogenesis of trans-acting siRNAs in higher plants. Semin Cell Dev Biol 21:798–804

    Article  PubMed  CAS  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Sung GH, Spatafora JW, Carrington JC (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36(12):1282–1290

    Article  PubMed  CAS  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121(2):207–221

    Article  PubMed  CAS  Google Scholar 

  • Ambros V, Bartel B, Bartel DP et al (2003) A uniform system for microRNA annotation. RNA 9(3):277–279

    Article  PubMed  CAS  Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15(11):2730–2741

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ (2008) Evolution of microRNAs and their targets: are all microRNAs biologically relevant? Biochim Biophys Acta 1779(11):725–734

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17(6):1658–1673

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Bowman JL (2008) Evolution of plant microRNAs and their targets. Trends Plant Sci 13(7):343–349

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19(6):1750–1769

    Article  PubMed  CAS  Google Scholar 

  • Baker CC, Sieber P, Wellmer F, Meyerowitz EM (2005) The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in Arabidopsis. Curr Biol 15(4):303–315

    Article  PubMed  CAS  Google Scholar 

  • Barakat A, Wall K, Leebens-Mack J, Wang YJ, Carlson JE, Depamphilis CW (2007) Large-scale identification of microRNAs from a basal eudicot (Eschscholzia californica) and conservation in flowering plants. Plant J 51(6):991–1003

    Article  PubMed  CAS  Google Scholar 

  • Bartel D (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233

    Article  PubMed  CAS  Google Scholar 

  • Beauclair L, Yu A, Bouche N (2010) MicroRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. Plant J 62(3):454–462

    Article  PubMed  CAS  Google Scholar 

  • Braun L, Cannella D, Ortet P et al (2010) A complex small RNA repertoire is generated by a plant/fungal-like machinery and effected by a metazoan-like Argonaute in the single-cell human parasite Toxoplasma gondii. PLoS Pathog 6(5):e1000920

    Article  PubMed  Google Scholar 

  • Brodersen P, Voinnet O (2009) Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 10(2):141–148

    Article  PubMed  CAS  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M et al (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320(5880):1185–1190

    Article  PubMed  CAS  Google Scholar 

  • Cerutti H, Casas-Mollano J (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet 50(2):81–99

    Article  PubMed  CAS  Google Scholar 

  • Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8(11):884–896

    Article  PubMed  CAS  Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303(5666):2022–2025

    Article  PubMed  CAS  Google Scholar 

  • Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44

    Article  PubMed  Google Scholar 

  • Cock J, Sterck L, Rouze P et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465(7298):617–621

    Article  PubMed  CAS  Google Scholar 

  • Dugas D, Bartel B (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67:403–417

    Article  PubMed  CAS  Google Scholar 

  • Ehrenreich IM, Purugganan MD (2008) Sequence variation of MicroRNAs and their binding sites in Arabidopsis. Plant Physiol 146(4):1974–1982

    Article  PubMed  CAS  Google Scholar 

  • Fahlgren N, Howell MD, Kasschau KD et al (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2(2):e219

    Article  PubMed  Google Scholar 

  • Fahlgren N, Jogdeo S, Kasschau KD et al (2010) MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell 22(4):1074–1089

    Article  PubMed  CAS  Google Scholar 

  • Felippes FF, Schneeberger K, Dezulian T, Huson DH, Weigel D (2008) Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA 14(12):2455–2459

    Article  PubMed  Google Scholar 

  • Finet C, Timme R, Delwiche C, Marletaz F (2010) Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr Biol 20(24):2217–2222

    Article  PubMed  CAS  Google Scholar 

  • Floyd SK, Bowman JL (2004) Gene regulation: ancient microRNA target sequences in plants. Nature 428(6982):485–486

    Article  PubMed  CAS  Google Scholar 

  • Floyd SK, Zalewski CS, Bowman JL (2006) Evolution of class III homeodomain-leucine zipper genes in streptophytes. Genetics 173(1):373–388

    Article  PubMed  CAS  Google Scholar 

  • Franco-Zorrilla J, Valli A, Todesco M et al (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39(8):1033–1037

    Article  PubMed  CAS  Google Scholar 

  • Friedman R, Farh K, Burge C, Bartel D (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1):92–105

    Article  PubMed  CAS  Google Scholar 

  • Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15(22):2038–2043

    Article  PubMed  CAS  Google Scholar 

  • German MA, Pillay M, Jeong DH et al (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 26(8):941–946

    Article  PubMed  CAS  Google Scholar 

  • Guddeti S, Zhang DC, Li AL et al (2005) Molecular evolution of the rice miR395 gene family. Cell Res 15(8):631–638

    Article  PubMed  CAS  Google Scholar 

  • Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17(5):1376–1386

    Article  PubMed  CAS  Google Scholar 

  • Hinas A, Reimegard J, Wagner E, Nellen W, Ambros V, Soderbom F (2007) The small RNA repertoire of Dictyostelium discoideum and its regulation by components of the RNAi pathway. Nucleic Acids Res 35(20):6714–6726

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14(6):787–799

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  PubMed  CAS  Google Scholar 

  • Kasschau KD, Xie Z, Allen E et al (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction. Dev Cell 4(2):205–217

    Article  PubMed  CAS  Google Scholar 

  • Klevebring D, Street NR, Fahlgren N et al (2009) Genome-wide profiling of Populus small RNAs. BMC Genomics 10:620

    Article  PubMed  Google Scholar 

  • Kutter C, Schob H, Stadler M, Meins F, Si-Ammour A (2007) MicroRNA-mediated regulation of stomatal development in Arabidopsis. Plant Cell 19(8):2417–2429

    Article  PubMed  CAS  Google Scholar 

  • Lee H, Li L, Gu W et al (2010) Diverse pathways generate microRNA-like RNAs and dicer-independent small interfering RNAs in fungi. Mol Cell 38(6):803–814

    Article  PubMed  CAS  Google Scholar 

  • Lelandais-Briere C, Naya L, Sallet E et al (2009) Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 21(9):2780–2796

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Zheng Y, Addo-Quaye C et al (2010) Transcriptome-wide identification of microRNA targets in rice. Plant J 62(5):742–759

    Article  PubMed  CAS  Google Scholar 

  • Lim LP, Lau NC, Garrett-Engele P et al (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433(7027):769–773

    Article  PubMed  CAS  Google Scholar 

  • Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52(1):133–146

    Article  PubMed  CAS  Google Scholar 

  • Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14(7):1605–1619

    Article  PubMed  CAS  Google Scholar 

  • Lu C, Tej S, Luo S, Haudenschild C, Meyers B, Green P (2005) Elucidation of the small RNA component of the transcriptome. Science 309(5740):1567–1569

    Article  PubMed  CAS  Google Scholar 

  • Lu C, Jeong DH, Kulkarni K et al (2008) Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc Natl Acad Sci USA 105(12):4951–4956

    Article  PubMed  CAS  Google Scholar 

  • Ma Z, Coruh C, Axtell MJ (2010) Arabidopsis lyrata small RNAs: transient MIRNA and small interfering RNA loci within the Arabidopsis genus. Plant Cell 22(4):1090–1103

    Article  PubMed  CAS  Google Scholar 

  • Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16(4):510–519

    Article  PubMed  CAS  Google Scholar 

  • Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17(5):1360–1375

    Article  PubMed  CAS  Google Scholar 

  • Mallory AC, Hinze A, Tucker MR et al (2009) Redundant and specific roles of the ARGONAUTE proteins AGO1 and ZLL in development and small RNA-directed gene silencing. PLoS Genet 5(9):e1000646

    Article  PubMed  Google Scholar 

  • Meyers BC, Axtell MJ, Bartel B et al (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20(12):3186–3190

    Article  PubMed  CAS  Google Scholar 

  • Mi S, Cai T, Hu Y et al (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133(1):116–127

    Article  PubMed  CAS  Google Scholar 

  • Molnar A, Schwach F, Studholme D, Thuenemann E, Baulcombe D (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447(7148):1126–1129

    Article  PubMed  CAS  Google Scholar 

  • Nikovics K, Blein T, Peaucelle A et al (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18(11):2929–2945

    Article  PubMed  CAS  Google Scholar 

  • Nodine M, Bartel D (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24(23):2678–2692

    Article  PubMed  CAS  Google Scholar 

  • Palatnik JF, Allen E, Wu X et al (2003) Control of leaf morphogenesis by microRNAs. Nature 425(6955):257–263

    Article  PubMed  CAS  Google Scholar 

  • Palatnik J, Wollmann H, Schommer C et al (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev Cell 13(1):115–125

    Article  PubMed  CAS  Google Scholar 

  • Pantaleo V, Szittya G, Moxon S et al (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 62(6):960–976

    PubMed  CAS  Google Scholar 

  • Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12(17):1484–1495

    Article  PubMed  CAS  Google Scholar 

  • Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20(24):3407–3425

    Article  PubMed  CAS  Google Scholar 

  • Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K (2008) Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant J 55(1):65–76

    Article  PubMed  CAS  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16(13):1616–1626

    Article  PubMed  CAS  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110(4):513–520

    Article  PubMed  CAS  Google Scholar 

  • Roger A, Hug L (2006) The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation. Philos Trans R Soc Lond B Biol Sci 361(1470):1039–1054

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510

    Article  PubMed  CAS  Google Scholar 

  • Schauer SE, Jacobsen SE, Meinke DW, Ray A (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci 7(11):487–491

    Article  PubMed  CAS  Google Scholar 

  • Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of MicroRNAs on the plant transcriptome. Dev Cell 8(4):517–527

    Article  PubMed  CAS  Google Scholar 

  • Shin H, Shin H, Chen R, Harrison M (2006) Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J 45(5):712–726

    Article  PubMed  CAS  Google Scholar 

  • Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM (2007) Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development 134(6):1051–1060

    Article  PubMed  CAS  Google Scholar 

  • Song C, Wang C, Zhang C et al (2010) Deep sequencing discovery of novel and conserved microRNAs in trifoliate orange (Citrus trifoliata). BMC Genomics 11:431

    Article  PubMed  Google Scholar 

  • Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16(8):2001–2019

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17(5):1397–1411

    Article  PubMed  CAS  Google Scholar 

  • Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17(1):49–63

    Article  PubMed  CAS  Google Scholar 

  • Todesco M, Rubio-Somoza I, Paz-Ares J, Weigel D (2010) A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genet 6(7):e1001031

    Article  PubMed  Google Scholar 

  • Vaucheret H (2008) Plant ARGONAUTES. Trends Plant Sci 13(7):350–358

    Article  PubMed  CAS  Google Scholar 

  • Vaucheret H, Vazquez F, Crete P, Bartel DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18(10):1187–1197

    Article  PubMed  CAS  Google Scholar 

  • Vazquez F, Gasciolli V, Crete P, Vaucheret H (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr Biol 14(4):346–351

    PubMed  CAS  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17(8):2204–2216

    Article  PubMed  CAS  Google Scholar 

  • Xie Z, Johansen LK, Gustafson AM et al (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2(5):E104

    Article  PubMed  Google Scholar 

  • Zhang J, Xu Y, Huan Q, Chong K (2009a) Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genomics 10:449

    Article  PubMed  Google Scholar 

  • Zhang L, Chia JM, Kumari S et al (2009b) A genome-wide characterization of microRNA genes in maize. PLoS Genet 5(11):e1000716

    Article  PubMed  Google Scholar 

  • Zhao T, Li G, Mi S et al (2007) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21(10):1190–1203

    Article  PubMed  CAS  Google Scholar 

  • Zhao CZ, Xia H, Frazier TP et al (2010) Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol 10:3

    Article  PubMed  Google Scholar 

  • Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61:4157–4168

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Matthew W. Jones-Rhoades.

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Jones-Rhoades, M.W. Conservation and divergence in plant microRNAs. Plant Mol Biol 80, 3–16 (2012). https://doi.org/10.1007/s11103-011-9829-2

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