Abstract
MicroRNAs, or miRNAs, are posttranscriptional regulators of gene expression. A wealth of observations and findings suggest highly complex, multicomponent, and intermingled pathways governing miRNA biogenesis and miRNA-mediated gene silencing. Plant miRNA genes are usually found as individual entities scattered around the intergenic and—to a much lesser extent—intragenic space, while miRNA gene clusters, formed by tandem or segmental duplications, also exist in plant genomes. Genome duplications are proposed to contribute to miRNA family expansions, as well. Evolutionarily young miRNAs retaining extensive homology to their loci of origin deliver important clues into miRNA origins and evolution. Additionally, imprecisely processed miRNAs evidence noncanonical routes of biogenesis, which may affect miRNA expression levels or targeting capabilities. Majority of the knowledge regarding miRNAs comes from model plant species. As ongoing research progressively expands into nonmodel systems, our understanding of miRNAs and miRNA-related pathways changes which opens up new perspectives and frontiers in miRNA research.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Appels R, Nystrom J, Webster H, Keeble-Gagnere G (2015) Discoveries and advances in plant and animal genomics. Funct Integr Genomics. doi:10.1007/s10142-015-0434-3
Arteaga-Vázquez M, Caballero-Pérez J, Vielle-Calzada J-P (2006) A family of microRNAs present in plants and animals. Plant Cell 18:3355–3369. doi:10.1105/tpc.106.044420
Axtell MJ, Westholm JO, Lai EC (2011) Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol 12:221. doi:10.1186/gb-2011-12-4-221
Bandiera S, Rüberg S, Girard M et al (2011) Nuclear outsourcing of RNA interference components to human mitochondria. PLoS One 6:e20746. doi:10.1371/journal.pone.0020746
Barrey E, Saint-Auret G, Bonnamy B et al (2011) Pre-microRNA and mature microRNA in human mitochondria. PLoS One 6:e20220. doi:10.1371/journal.pone.0020220
Bian Z, Li L-M, Tang R et al (2010) Identification of mouse liver mitochondria-associated miRNAs and their potential biological functions. Cell Res 20:1076–1078. doi:10.1038/cr.2010.119
Bologna NG, Mateos JL, Bresso EG, Palatnik JF (2009) A loop-to-base processing mechanism underlies the biogenesis of plant microRNAs miR319 and miR159. EMBO J 28:3646–3656. doi:10.1038/emboj.2009.292
Bonnet E, Wuyts J, Rouzé P, Van de Peer Y (2004) Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proc Natl Acad Sci U S A 101:11511–11516. doi:10.1073/pnas.0404025101
Budak H, Akpinar BA (2011) Dehydration stress-responsive miRNA in Brachypodium distachyon: evident by genome-wide screening of microRNAs expression. OMICS J Integr Biol 15(11):791–799. doi:10.1089/omi.2011.0073
Budak H, Kantar M (2015) Harnessing NGS and big data optimally: comparison of miRNA prediction from assembled versus non-assembled sequencing data—the case of the grass Aegilops tauschii complex genome. OMICS: International Journal of Plant Biology
Budak H, Khan Z, Kantar M (2014) History and current status of wheat miRNAs using next-generation sequencing and their roles in development and stress. Brief Funct Genomics. doi:10.1093/bfgp/elu021
Budak H, Bulut R, Kantar M, Alptekin B (2015a) MicroRNA nomenclature and the need for a revised naming prescription. Brief Funct Genomics
Budak H, Kantar M, Bulut R, Akpinar BA (2015b) Stress responsive miRNAs and isomiRs in cereals. Plant Sci in press:1–13. doi:10.1016/j.plantsci.2015.02.008
Campo S, Peris-Peris C, Siré C et al (2013) Identification of a novel microRNA (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (Natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. New Phytol 199:212–227. doi:10.1111/nph.12292
Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025. doi:10.1126/science.1088060
Chuck G, Whipple C, Jackson D, Hake S (2010) The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137:1243–1250. doi:10.1242/dev.048348
Colaiacovo M, Lamontanara A, Bernardo L et al (2012) On the complexity of miRNA-mediated regulation in plants: novel insights into the genomic organization of plant miRNAs. Biol Direct 7:15. doi:10.1186/1745-6150-7-15
Cui X, Xu SM, Mu DS, Yang ZM (2009) Genomic analysis of rice microRNA promoters and clusters. Gene 431:61–66. doi:10.1016/j.gene.2008.11.016
Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23:431–442. doi:10.1105/tpc.110.082784
Das S, Ferlito M, Kent OA et al (2012) Nuclear miRNA regulates the mitochondrial genome in the heart. Circ Res 110:1596–1603. doi:10.1161/CIRCRESAHA.112.267732
de Felippes FF, Schneeberger K, Dezulian T et al (2008) Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA 14:2455–2459. doi:10.1261/rna.1149408
Deng P, Nie X, Wang L et al (2014) Computational identification and comparative analysis of miRNAs in wheat group 7 chromosomes. Plant Mol Biol Report 32:487–500. doi:10.1007/s11105-013-0669-x
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:e219. doi:10.1371/journal.pone.0000219
He H, Liang G, Li Y et al (2014) Two young MicroRNAs originating from target duplication mediate nitrogen starvation adaptation via regulation of glucosinolate synthesis in Arabidopsis thaliana. Plant Physiol 164:853–865. doi:10.1104/pp. 113.228635
Jagtap S, Shivaprasad PV (2014) Diversity, expression and mRNA targeting abilities of Argonaute-targeting miRNAs among selected vascular plants. BMC Genomics 15:1049. doi:10.1186/1471-2164-15-1049
Jia J, Zhao S, Kong X et al (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95. doi:10.1038/nature12028
Joshi PK, Gupta D, Nandal UK et al (2012) Identification of mirtrons in rice using MirtronPred: a tool for predicting plant mirtrons. Genomics 99:370–375. doi:10.1016/j.ygeno.2012.04.002
Kantar M, Akpınar BA, Valárik M et al (2012) Subgenomic analysis of microRNAs in polyploid wheat. Funct Integr Genomics 12:465–479. doi:10.1007/s10142-012-0285-0
Kren BT, Wong PY-P, Sarver A et al (2009) MicroRNAs identified in highly purified liver-derived mitochondria may play a role in apoptosis. RNA Biol 6:65–72. doi:10.4161/rna.6.1.7534
Kurtoglu KY, Kantar M, Lucas SJ, Budak H (2013) Unique and conserved microRNAs in wheat chromosome 5D revealed by next-generation sequencing. PLoS One 8:e69801. doi:10.1371/journal.pone.0069801
Kurtoglu KY, Kantar M, Budak H (2014) New wheat microRNA using whole-genome sequence. Funct Integr Genomics. doi:10.1007/s10142-013-0357-9
Li A, Mao L (2007) Evolution of plant microRNA gene families. Cell Res 17:212–218. doi:10.1038/sj.cr.7310113
Li T, Li H, Zhang Y-X, Liu J-Y (2011a) Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Res 39:2821–2833. doi:10.1093/nar/gkq1047
Li Y, Li C, Xia J, Jin Y (2011b) Domestication of transposable elements into MicroRNA genes in plants. PLoS One 6:e19212. doi:10.1371/journal.pone.0019212
Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS One 7:e48951. doi:10.1371/journal.pone.0048951
Ling H-Q, Zhao S, Liu D et al (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496:87–90. doi:10.1038/nature11997
Liu Q (2012) Novel miRNAs in the control of arsenite levels in rice. Funct Integr Genomics 12:649–658. doi:10.1007/s10142-012-0282-3
Liu Q, Feng Y, Zhu Z (2009) Dicer-like (DCL) proteins in plants. Funct Integr Genomics 9:277–286. doi:10.1007/s10142-009-0111-5
Liu W, Yu W, Hou L et al (2014) Analysis of miRNAs and their targets during adventitious shoot organogenesis of Acacia crassicarpa. PLoS One 9:e93438. doi:10.1371/journal.pone.0093438
Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. 14:1605–1619. doi: 10.1105/tpc.003210.ruses
Lung B, Zemann A, Madej MJ et al (2006) Identification of small non-coding RNAs from mitochondria and chloroplasts. Nucleic Acids Res 34:3842–3852. doi:10.1093/nar/gkl448
Luo Y, Guo Z, Li L (2013) Evolutionary conservation of microRNA regulatory programs in plant flower development. Dev Biol 380:133–144. doi:10.1016/j.ydbio.2013.05.009
Marker C, Zemann A, Terhörst T et al (2002) Experimental RNomics. Curr Biol 12:2002–2013. doi:10.1016/S0960-9822(02)01304-0
Meng Y, Shao C (2012) Large-scale identification of mirtrons in Arabidopsis and rice. PLoS One 7:e31163. doi:10.1371/journal.pone.0031163
Merchan F, Boualem A, Crespi M, Frugier F (2009) Plant polycistronic precursors containing non-homologous microRNAs target transcripts encoding functionally related proteins. Genome Biol 10:R136. doi:10.1186/gb-2009-10-12-r136
Nozawa M, Miura S, Nei M (2012) Origins and evolution of microRNA genes in plant species. Genome Biol Evol 4:230–239. doi:10.1093/gbe/evs002
Park MY, Wu G, Gonzalez-Sulser A et al (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci U S A 102:3691–3696. doi:10.1073/pnas.0405570102
Pashkovskiy PP, Ryazansky SS (2013) Biogenesis, evolution, and functions of plant microRNAs. Biochem Biokhimii͡a 78:627–637. doi:10.1134/S0006297913060084
Patanun O, Lertpanyasampatha M, Sojikul P et al (2013) Computational identification of microRNAs and their targets in cassava (Manihot esculenta Crantz.). Mol Biotechnol 53:257–269. doi:10.1007/s12033-012-9521-z
Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425. doi:10.1101/gad.1476406
Ramachandran V, Chen X (2008) Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 321:1490–1492. doi:10.1126/science.1163728
Ren Y, Chen L, Zhang Y et al (2012) Identification of novel and conserved Populus tomentosa microRNA as components of a response to water stress. Funct Integr Genomics 12:327–339. doi:10.1007/s10142-012-0271-6
Ren G, Chen X, Yu B (2015) Small RNAs meet their targets: when methylation defends miRNAs from uridylation. RNA Biol 11:1099–1104. doi:10.4161/rna.36243
Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25:2383–2399. doi:10.1105/tpc.113.113159
Ruby JG, Jan CH, Bartel DP (2007) Intronic microRNA precursors that bypass Drosha processing. Nature 448:83–86. doi:10.1038/nature05983
Sobkowiak L, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2012) Non-canonical processing of Arabidopsis pri-miR319a/b/c generates additional microRNAs to target one RAP2.12 mRNA isoform. Front Plant Sci 3:46. doi:10.3389/fpls.2012.00046
Sorin C, Declerck M, Christ A et al (2014) A miR169 isoform regulates specific NF-YA targets and root architecture in Arabidopsis. New Phytol 202:1197–1211. doi:10.1111/nph.12735
Sripada L, Tomar D, Prajapati P et al (2012a) Systematic analysis of small RNAs associated with human mitochondria by deep sequencing: detailed analysis of mitochondrial associated miRNA. PLoS One 7:e44873. doi:10.1371/journal.pone.0044873
Sripada L, Tomar D, Singh R (2012b) Mitochondria: one of the destinations of miRNAs. Mitochondrion 12:593–599. doi:10.1016/j.mito.2012.10.009
Sun J, Zhou M, Mao Z, Li C (2012) Characterization and evolution of microRNA genes derived from repetitive elements and duplication events in plants. PLoS One 7:e34092. doi:10.1371/journal.pone.0034092
Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019. doi:10.1105/tpc.104.022830
Taylor RS, Tarver JE, Hiscock SJ, Donoghue PCJ (2014) Evolutionary history of plant microRNAs. Trends Plant Sci 19:175–182. doi:10.1016/j.tplants.2013.11.008
Wang X-J, Reyes JL, Chua N-H, Gaasterland T (2004) Prediction and identification of Arabidopsis thaliana microRNAs and their mRNA targets. Genome Biol 5:R65. doi:10.1186/gb-2004-5-9-r65
Wang L, Yu X, Wang H et al (2011) A novel class of heat-responsive small RNAs derived from the chloroplast genome of Chinese cabbage (Brassica rapa). BMC Genomics 12:289. doi:10.1186/1471-2164-12-289
Wang M, Wang Q, Zhang B (2013) Response of miRNAs and their targets to salt and drought stresses in cotton (Gossypium hirsutum L.). Gene 530:26–32. doi:10.1016/j.gene.2013.08.009
Wang R, Xu L, Zhu X et al (2014) Transcriptome-wide characterization of novel and heat-stress-responsive microRNAs in radish (Raphanus sativus L.) using next-generation sequencing. Plant Mol Biol Report. doi:10.1007/s11105-014-0786-1
Yi F, Xie S, Liu Y et al (2013) Genome-wide characterization of microRNA in foxtail millet (Setaria italica). BMC Plant Biol 13:212. doi:10.1186/1471-2229-13-212
Yu B, Yang Z, Li J et al (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307:932–935. doi:10.1126/science.1107130
Yu M, Carver BF, Yan L (2014) TamiR1123 originated from a family of miniature inverted-repeat transposable elements (MITE) including one inserted in the Vrn-A1a promoter in wheat. Plant Sci 215–216:117–123. doi:10.1016/j.plantsci.2013.11.007
Yumul RE, Kim YJ, Liu X et al (2013) POWERDRESS and diversified expression of the MIR172 gene family bolster the floral stem cell network. PLoS Genet 9:e1003218. doi:10.1371/journal.pgen.1003218
Zhao M, Meyers BC, Cai C, et al (2015) Evolutionary patterns and coevolutionary consequences of MIRNA genes and MicroRNA targets triggered by multiple mechanisms of genomic duplications in soybean. Plant Cell Online 27:tpc.15.00048. doi: 10.1105/tpc.15.00048
Zhou ZS, Zeng HQ, Liu ZP, Yang ZM (2012) Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ 35:86–99. doi:10.1111/j.1365-3040.2011.02418.x
Zhu H, Zhou Y, Castillo-González C et al (2013) Bidirectional processing of pri-miRNAs with branched terminal loops by Arabidopsis Dicer-like1. Nat Struct Mol Biol 20:1106–1115. doi:10.1038/nsmb.2646
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Budak, H., Akpinar, B.A. Plant miRNAs: biogenesis, organization and origins. Funct Integr Genomics 15, 523–531 (2015). https://doi.org/10.1007/s10142-015-0451-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-015-0451-2