Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

The evolutionary origin of plant and animal microRNAs

Abstract

MicroRNAs (miRNAs) are a unique class of short endogenous RNAs, which have become known in the past few decades as major players in gene regulation at the post-transcriptional level. Their regulatory roles make miRNAs crucial for normal development and physiology in several distinct groups of eukaryotes including plants and animals. The common notion is that miRNAs have evolved independently in those distinct lineages, but recent evidence from non-bilaterian metazoans, plants, and various algae raise the possibility that the last common ancestor of these lineages might already have employed an miRNA pathway for post-transcriptional regulation. In this Review we present the commonalities and differences of the miRNA pathways in various eukaryotes and discuss the contrasting scenarios of their possible evolutionary origin and their proposed link to organismal complexity and multicellularity.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Differences between miRNAs and siRNAs.
Figure 2: Phylogenetic tree of the major eukaryotic groups showing presence of miRNA systems.
Figure 3: Scheme describing the plant and animal canonical miRNA biogenesis pathways.
Figure 4: Schematic comparison of miRNA network topology in land plants and bilaterian animals.
Figure 5: A possible scenario of miRNA evolution in plants and animals where their last common ancestor possessed an miRNA system.

Similar content being viewed by others

References

  1. Ameres, S. L. & Zamore, P. D. Diversifying microRNA sequence and function. Nat. Rev. Mol. Cell Biol. 14, 475–488 (2013).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  3. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297 (2004).

    Article  CAS  PubMed  Google Scholar 

  4. Bartel, D. P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Reinhart, B. J., Weinstein, E. G., Rhoades, M. W., Bartel, B. & Bartel, D. P. MicroRNAs in plants. Genes Dev. 16, 1616–1626 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Iwasaki, Y. W., Siomi, M. C. & Siomi, H. PIWI-interacting RNA: its biogenesis and functions. Annu. Rev. Biochem. 84, 405–433 (2015).

    Article  CAS  PubMed  Google Scholar 

  7. Kim, V. N., Han, J. & Siomi, M. C. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10, 126–139 (2009).

    Article  CAS  PubMed  Google Scholar 

  8. Lee, R. C., Feinbaum, R. L. & Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854 (1993).

  9. Wightman, B., Ha, I. & Ruvkun, G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855–862 (1993).

  10. Giraldez, A. J. et al. MicroRNAs regulate brain morphogenesis in zebrafish. Science 308, 833–838 (2005).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  12. Peterson, K. J., Dietrich, M. R. & McPeek, M. A. MicroRNAs and metazoan macroevolution: insights into canalization, complexity, and the Cambrian explosion. Bioessays 31, 736–747 (2009).

    Article  CAS  PubMed  Google Scholar 

  13. Grimson, A. et al. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455, 1193–1197 (2008).

    Article  CAS  PubMed  Google Scholar 

  14. Tarver, J. E. et al. microRNAs and the evolution of complex multicellularity: identification of a large, diverse complement of microRNAs in the brown alga Ectocarpus. Nucleic Acids Res. 43, 6384–6398 (2015).

    Article  CAS  PubMed  Google Scholar 

  15. Erwin, D. H. et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097 (2011).

    Article  CAS  PubMed  Google Scholar 

  16. Axtell, M. J., Westholm, J. O. & Lai, E. C. Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol. 12, 221 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Robinson, J. M. et al. The identification of microRNAs in calcisponges: independent evolution of microRNAs in basal metazoans. J. Exp. Zool. B 320, 84–93 (2013).

    Article  CAS  Google Scholar 

  18. Maxwell, E. K., Ryan, J. F., Schnitzler, C. E., Browne, W. E. & Baxevanis, A. D. MicroRNAs and essential components of the microRNA processing machinery are not encoded in the genome of the ctenophore Mnemiopsis leidyi. BMC Genomics 13, 714 (2012).

    Article  CAS  PubMed  Google Scholar 

  19. Ryan, J. F. et al. The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342, 1242592 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Moroz, L. L. et al. The ctenophore genome and the evolutionary origins of neural systems. Nature 510, 109–114 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Tarver, J. E., Donoghue, P. C. & Peterson, K. J. Do miRNAs have a deep evolutionary history? Bioessays 34, 857–866 (2012).

    Article  CAS  PubMed  Google Scholar 

  22. Molnár, A., Schwach, F., Studholme, D. J., Thuenemann, E. C. & Baulcombe, D. C. miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447, 1126–1129 (2007).

    Article  PubMed  CAS  Google Scholar 

  23. Alaba, S. et al. The liverwort Pellia endiviifolia shares microtranscriptomic traits that are common to green algae and land plants. New Phytol. 206, 352–367 (2015).

    Article  CAS  PubMed  Google Scholar 

  24. Fromm, B. et al. A uniform system for the annotation of human microRNA genes and the evolution of the human microRNAome. Annu. Rev. Genet. 49, 213–242 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Millar, A. A. & Waterhouse, P. M. Plant and animal microRNAs: similarities and differences. Funct. Integr. Genomics 5, 129–135 (2005).

    Article  CAS  PubMed  Google Scholar 

  27. Ghildiyal, M. & Zamore, P. D. Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10, 94–108 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Jones-Rhoades, M. W., Bartel, D. P. & Bartel, B. MicroRNAs and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19–53 (2006).

    Article  CAS  PubMed  Google Scholar 

  29. Zhao, T. et al. A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev. 21, 1190–1203 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Avesson, L., Reimegård, J., Wagner, E. G. H. & Söderbom, F. MicroRNAs in Amoebozoa: deep sequencing of the small RNA population in the social amoeba Dictyostelium discoideum reveals developmentally regulated microRNAs. RNA 18, 1771–1782 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hinas, A. et al. The small RNA repertoire of Dictyostelium discoideum and its regulation by components of the RNAi pathway. Nucleic Acids Res. 35, 6714–6726 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Huang, P.-J. et al. Identification of putative miRNAs from the deep-branching unicellular flagellates. Genomics 99, 101–107 (2012).

    Article  CAS  PubMed  Google Scholar 

  33. Cuperus, J. T., Fahlgren, N. & Carrington, J. C. Evolution and functional diversification of MIRNA genes. Plant Cell 23, 431–442 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Fahlgren, N. et al. MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell 22, 1074–1089 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Axtell, M. J., Snyder, J. A. & Bartel, D. P. Common functions for diverse small RNAs of land plants. Plant Cell 19, 1750–1769 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Li, J., Wu, Y. & Qi, Y. MicroRNAs in a multicellular green alga Volvox carteri. Sci. China Life Sci. 57, 36–45 (2014).

    Article  PubMed  CAS  Google Scholar 

  37. Herron, M. D., Hackett, J. D., Aylward, F. O. & Michod, R. E. Triassic origin and early radiation of multicellular volvocine algae. Proc. Natl Acad. Sci. USA 106, 3254–3258 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Thomson, R. C., Plachetzki, D. C., Mahler, D. L. & Moore, B. R. A critical appraisal of the use of microRNA data in phylogenetics. Proc. Natl Acad. Sci. USA 111, E3659–E3668 (2014).

  39. Fromm, B., Worren, M. M., Hahn, C., Hovig, E. & Bachmann, L. Substantial loss of conserved and gain of novel microRNA families in flatworms. Mol. Biol. Evol. 30, 2619–2628 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Lu, J. et al. The birth and death of microRNA genes in Drosophila. Nat. Genet. 40, 351–355 (2008).

    Article  CAS  PubMed  Google Scholar 

  41. Berezikov, E. et al. Evolutionary flux of canonical microRNAs and mirtrons in Drosophila. Nature Genet. 42, 6–9 (2010).

    Article  CAS  PubMed  Google Scholar 

  42. Shaw, W. R., Armisen, J., Lehrbach, N. J. & Miska, E. A. The conserved miR-51 microRNA family is redundantly required for embryonic development and pharynx attachment in Caenorhabditis elegans. Genetics 185, 897–905 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Chen, K. & Rajewsky, N. The evolution of gene regulation by transcription factors and microRNAs. Nat. Rev. Genet. 8, 93–103 (2007).

    Article  CAS  PubMed  Google Scholar 

  44. Krishna, S. et al. Deep sequencing reveals unique small RNA repertoire that is regulated during head regeneration in Hydra magnipapillata. Nucleic Acids Res. 41, 599–616 (2013).

    Article  CAS  PubMed  Google Scholar 

  45. Moran, Y. et al. Cnidarian microRNAs frequently regulate targets by cleavage. Genome Res. 24, 651–663 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Arazi, T. et al. Cloning and characterization of micro-RNAs from moss. Plant J. 43, 837–848 (2005).

    Article  CAS  PubMed  Google Scholar 

  47. Schwab, R. et al. Specific effects of microRNAs on the plant transcriptome. Dev. Cell 8, 517–527 (2005).

    Article  CAS  PubMed  Google Scholar 

  48. Lin, S. et al. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350, 691–694 (2015).

    Article  CAS  PubMed  Google Scholar 

  49. Saraiya, A. A. & Wang, C. C. snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog. 4, e1000224 (2008).

  50. de Jong, D. et al. Multiple dicer genes in the early-diverging metazoa. Mol. Biol. Evol. 26, 1333–1340 (2009).

    Article  CAS  PubMed  Google Scholar 

  51. Ding, S.-W. RNA-based antiviral immunity. Nat. Rev. Immunol. 10, 632–644 (2010).

    Article  CAS  PubMed  Google Scholar 

  52. Kwon, S. C. et al. Structure of Human DROSHA. Cell 164, 81–90 (2016).

    Article  CAS  PubMed  Google Scholar 

  53. Valli, A. A. et al. Most microRNAs in the single-cell alga Chlamydomonas reinhardtii are produced by Dicer-like 3-mediated cleavage of introns and untranslated regions of coding RNAs. Genome Res. 26, 519–529 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Moran, Y., Praher, D., Fredman, D. & Technau, U. The evolution of microRNA pathway protein components in Cnidaria. Mol. Biol. Evol. 30, 2541–2552 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Burger, K. & Gullerova, M. Swiss army knives: non-canonical functions of nuclear Drosha and Dicer. Nat. Rev. Mol. Cell Biol. (2015).

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

    Article  CAS  PubMed  Google Scholar 

  57. Han, M.-H., Goud, S., Song, L. & Fedoroff, N. The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc. Natl Acad. Sci. USA 101, 1093–1098 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Sabin, L. R. et al. Ars2 regulates both miRNA-and siRNA-dependent silencing and suppresses RNA virus infection in Drosophila. Cell 138, 340–351 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Lee, Y. et al. The role of PACT in the RNA silencing pathway. EMBO J. 25, 522–532 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Forstemann, K. et al. Normal microRNA maturation and germ-line stem cell maintenance requires Loquacious, a double-stranded RNA-binding domain protein. PLoS Biol. 3, 1187 (2005).

    Article  CAS  Google Scholar 

  61. Chendrimada, T. P. et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436, 740–744 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Allen, E. et al. Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat. Genet. 36, 1282–1290 (2004).

    Article  CAS  PubMed  Google Scholar 

  63. Kim, V. N. & Nam, J.-W. Genomics of microRNA. Trends Genet. 22, 165–173 (2006).

    Article  CAS  PubMed  Google Scholar 

  64. Merchan, F., Boualem, A., Crespi, M. & Frugier, F. Plant polycistronic precursors containing non-homologous microRNAs target transcripts encoding functionally related proteins. Genome Biol. 10, R136 (2009).

  65. Rodriguez, A., Griffiths-Jones, S., Ashurst, J. L. & Bradley, A. Identification of mammalian microRNA host genes and transcription units. Genome Res. 14, 1902–1910 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Rajagopalan, R., Vaucheret, H., Trejo, J. & Bartel, D. P. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20, 3407–3425 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zhu, Q.-H. et al. A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res. 18, 1456–1465 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Joshi, P. K. et al. Identification of mirtrons in rice using MirtronPred: a tool for predicting plant mirtrons. Genomics 99, 370–375 (2012).

    Article  CAS  PubMed  Google Scholar 

  69. Ameres, S. L. et al. Target RNA–directed trimming and tailing of small silencing RNAs. Science 328, 1534–1539 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Yu, B. et al. Methylation as a crucial step in plant microRNA biogenesis. Science 307, 932–935 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Swarts, D. C. et al. The evolutionary journey of Argonaute proteins. Nat. Struct. Mol. Biol. 21, 743–753 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Ryan, J. F. & Chiodin, M. Where is my mind? How sponges and placozoans may have lost neural cell types. Phil. Trans. R. Soc. B 370, 20150059 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  73. Drinnenberg, I. A., Fink, G. R. & Bartel, D. P. Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333, 1592–1592 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Hutvagner, G. & Simard, M. J. Argonaute proteins: key players in RNA silencing. Nat. Rev. Mol. Cell Biol. 9, 22–32 (2008).

    Article  CAS  PubMed  Google Scholar 

  75. Meister, G. Argonaute proteins: functional insights and emerging roles. Nat Rev. Genet. 14, 447–459 (2013).

    Article  CAS  PubMed  Google Scholar 

  76. Okamura, K., Ishizuka, A., Siomi, H. & Siomi, M. C. Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev. 18, 1655–1666 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Swarts, D. C. et al. DNA-guided DNA interference by a prokaryotic Argonaute. Nature 507, 258–261 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Song, J.-J., Smith, S. K., Hannon, G. J. & Joshua-Tor, L. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305, 1434–1437 (2004).

    Article  CAS  PubMed  Google Scholar 

  79. Wang, Y. et al. Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456, 921–926 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Olovnikov, I., Chan, K., Sachidanandam, R., Newman, D. K. & Aravin, A. A. Bacterial argonaute samples the transcriptome to identify foreign DNA. Mol. Cell 51, 594-605 (2013).

  81. Carthew, R. W. & Sontheimer, E. J. Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642–655 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Rhoades, M. W. et al. Prediction of plant microRNA targets. Cell 110, 513–520 (2002).

    Article  CAS  PubMed  Google Scholar 

  83. Iwakawa, H.-o . & Tomari, Y. Molecular insights into microRNA-mediated translational repression in plants. Mol. Cell 52, 591–601 (2013).

    Article  CAS  PubMed  Google Scholar 

  84. Liu, Q., Wang, F. & Axtell, M. J. Analysis of complementarity requirements for plant microRNA targeting using a Nicotiana benthamiana quantitative transient assay. Plant Cell 26, 741–753 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Burki, F., Okamoto, N., Pombert, J.-F. & Keeling, P. J. The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins. Proc. R. Soc. Lon. B 279, 2255–2261 (2012).

    Article  Google Scholar 

  86. Philippe, H. et al. Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol. 9, e1000602 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Selbach, M. et al. Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58–63 (2008).

    Article  CAS  PubMed  Google Scholar 

  88. Baek, D. et al. The impact of microRNAs on protein output. Nature 455, 64–71 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Muddashetty, R. S. et al. Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol. Cell 42, 673–688 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Bhattacharyya, S. N., Habermacher, R., Martine, U., Closs, E. I. & Filipowicz, W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111–1124 (2006).

    Article  CAS  PubMed  Google Scholar 

  91. Fabian, M. R. & Sonenberg, N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat. Struct. Mol. Biol. 19, 586–593 (2012).

    Article  CAS  PubMed  Google Scholar 

  92. Huntzinger, E. & Izaurralde, E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12, 99–110 (2011).

    Article  CAS  PubMed  Google Scholar 

  93. Chekulaeva, M. et al. miRNA repression involves GW182-mediated recruitment of CCR4–NOT through conserved W-containing motifs. Nat. Struct. Mol. Biol. 18, 1218–1226 (2011).

    Article  CAS  PubMed  Google Scholar 

  94. Meister, G. et al. Identification of novel argonaute-associated proteins. Curr. Biol. 15, 2149–2155 (2005).

    Article  CAS  PubMed  Google Scholar 

  95. Kuzuoğlu-Öztürk, D., Huntzinger, E., Schmidt, S. & Izaurralde, E. The Caenorhabditis elegans GW182 protein AIN-1 interacts with PAB-1 and subunits of the PAN2-PAN3 and CCR4-NOT deadenylase complexes. Nucleic Acids Res. 40, 5651–5665 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Hutvágner, G. & Zamore, P. D. A microRNA in a multiple-turnover RNAi enzyme complex. Science 297, 2056–2060 (2002).

    Article  PubMed  CAS  Google Scholar 

  97. Brodersen, P. et al. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185–1190 (2008).

    Article  CAS  PubMed  Google Scholar 

  98. Reis, R. S., Hart-Smith, G., Eamens, A. L., Wilkins, M. R. & Waterhouse, P. M. Gene regulation by translational inhibition is determined by Dicer partnering proteins. Nat. Plants 1, 14027 (2015).

    Article  CAS  PubMed  Google Scholar 

  99. Yang, L., Wu, G. & Poethig, R. S. Mutations in the GW-repeat protein SUO reveal a developmental function for microRNA-mediated translational repression in Arabidopsis. Proc. Natl Acad. Sci. USA 109, 315–320 (2012).

    Article  CAS  PubMed  Google Scholar 

  100. Karginov, F. V. et al. Diverse endonucleolytic cleavage sites in the mammalian transcriptome depend upon microRNAs, Drosha, and additional nucleases. Mol. Cell 38, 781–788 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Shin, C. et al. Expanding the microRNA targeting code: functional sites with centered pairing. Mol. Cell 38, 789–802 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Faehnle, C. R., Elkayam, E., Haase, A. D., Hannon, G. J. & Joshua-Tor, L. The making of a slicer: activation of human Argonaute-1. Cell Rep. 3, 1901–1909 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Hauptmann, J. et al. Turning catalytically inactive human Argonaute proteins into active slicer enzymes. Nat. Struct. Mol. Biol. 20, 814–817 (2013).

    Article  CAS  PubMed  Google Scholar 

  104. Cheloufi, S., Dos Santos, C. O., Chong, M. M. & Hannon, G. J. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 465, 584–589 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Nakayashiki, H., Kadotani, N. & Mayama, S. Evolution and diversification of RNA silencing proteins in fungi. J. Mol. Evol. 63, 127–135 (2006).

    Article  CAS  PubMed  Google Scholar 

  106. Salomon, W. E., Jolly, S. M., Moore, M. J., Zamore, P. D. & Serebrov, V. Single-molecule imaging reveals that Argonaute reshapes the binding properties of its nucleic acid guides. Cell 162, 84–95 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Jones-Rhoades, M. W. & Bartel, D. P. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14, 787–799 (2004).

    Article  CAS  PubMed  Google Scholar 

  108. Niklas, K. J. & Newman, S. A. The origins of multicellular organisms. Evol. Dev. 15, 41–52 (2013).

    Article  PubMed  Google Scholar 

  109. Trillo, I. R. & Nedelcu, A. M. Evolutionary Transitions to Multicellular Life: Principles and mechanisms Vol. 2 (Springer, 2015).

    Google Scholar 

  110. Michod, R. E. & Roze, D. Cooperation and conflict in the evolution of multicellularity. Heredity 86, 1–7 (2001).

    Article  CAS  PubMed  Google Scholar 

  111. Michod, R. E., Viossat, Y., Solari, C. A., Hurand, M. & Nedelcu, A. M. Life-history evolution and the origin of multicellularity. J. Theor. Biol. 239, 257–272 (2006).

    Article  PubMed  Google Scholar 

  112. Olsen, P. H. & Ambros, V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671–680 (1999).

    Article  CAS  PubMed  Google Scholar 

  113. Ambros, V. A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell 57, 49–57 (1989).

    Article  CAS  PubMed  Google Scholar 

  114. Aukerman, M. J. & Sakai, H. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15, 2730–2741 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Chen, Y. & Stallings, R. L. Differential patterns of microRNA expression in neuroblastoma are correlated with prognosis, differentiation, and apoptosis. Cancer Res. 67, 976–983 (2007).

    Article  CAS  PubMed  Google Scholar 

  116. Melton, C., Judson, R. L. & Blelloch, R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 463, 621–626 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Rosa, A. et al. The interplay between the master transcription factor PU. 1 and miR-424 regulates human monocyte/macrophage differentiation. Proc. Natl Acad. Sci. USA 104, 19849–19854 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Schoolmeesters, A. et al. Functional profiling reveals critical role for miRNA in differentiation of human mesenchymal stem cells. PLoS ONE 4, e5605 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  119. Flynt, A. S. & Lai, E. C. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat. Rev. Genet. 9, 831–842 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Hornstein, E. & Shomron, N. Canalization of development by microRNAs. Nat. Genet. 38, S20–S24 (2006).

    Article  CAS  PubMed  Google Scholar 

  121. Baumgarten, S. et al. Integrating microRNA and mRNA expression profiling in Symbiodinium microadriaticum, a dinoflagellate symbiont of reef-building corals. BMC Genom. 14, 1 (2013).

    Article  CAS  Google Scholar 

  122. Ratcliff, W. C. et al. Experimental evolution of an alternating uni-and multicellular life cycle in Chlamydomonas reinhardtii. Nat. Commun. 4, 2742 (2013).

  123. Lee, H.-C. et al. Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol. Cell 38, 803–814 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Heimberg, A. M., Sempere, L. F., Moy, V. N., Donoghue, P. C. & Peterson, K. J. MicroRNAs and the advent of vertebrate morphological complexity. Proc. Natl Acad. Sci. USA 105, 2946–2950 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Sempere, L. F., Cole, C. N., Mcpeek, M. A. & Peterson, K. J. The phylogenetic distribution of metazoan microRNAs: insights into evolutionary complexity and constraint. J. Exp. Zool. Part B 306, 575–588 (2006).

    Article  CAS  Google Scholar 

  126. Wheeler, B. M. et al. The deep evolution of metazoan microRNAs. Evol. Dev. 11, 50–68 (2009).

    Article  CAS  PubMed  Google Scholar 

  127. Londin, E. et al. Analysis of 13 cell types reveals evidence for the expression of numerous novel primate-and tissue-specific microRNAs. Proc. Natl Acad. Sci. USA 112, E1106–E1115 (2015).

    Article  CAS  Google Scholar 

  128. Putnam, N. H. et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86–94 (2007).

    Article  CAS  PubMed  Google Scholar 

  129. Sperling, E. A. et al. MicroRNAs resolve an apparent conflict between annelid systematics and their fossil record. Proc. R. Soc. B 276, 4315–4322 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Small RNA research in the Moran lab is supported by a European Research Council Starting Grant (CNIDARIAMICRORNA, 637456) and a Young Investigator Grant by the German–Israeli Foundation for Scientific Research and Development (I-1058-203.7-2013). Research in the Technau group is supported by grants of the Austrian Research Fund FWF (P24858 and P22618).

Author information

Authors and Affiliations

Authors

Contributions

Y.M. and U.T. conceived the manuscript, Y.M., M.A., D.P. and U.T. wrote the paper.

Corresponding authors

Correspondence to Yehu Moran or Ulrich Technau.

Ethics declarations

Competing interests

The author declares no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moran, Y., Agron, M., Praher, D. et al. The evolutionary origin of plant and animal microRNAs. Nat Ecol Evol 1, 0027 (2017). https://doi.org/10.1038/s41559-016-0027

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41559-016-0027

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing