Evolution of Plant MicroRNAs

Abstract

Microribonucleic acids (miRNAs) are small noncoding regulatory molecules encoded in the genome and generated through several processing steps. They recognise specific messenger RNAs and regulate their expression by cleavage or by translational inhibition. MiRNAs were only discovered approximately 10 years ago but it quickly became evident that they play an important role in development and stress responses. Initially it was thought that all miRNAs are conserved in plants because the technology only allowed to sequence the most abundant miRNAs. However, the development of next generation sequencing technologies allowed researchers to generate millions of sequencing reads in a sample, which resulted in the identification of the less abundant miRNAs. Analysis of large‐scale sequencing data revealed that the number of nonconserved miRNAs is much larger than previously thought. This review focuses on the evolution of plant MIRNA genes from protein‐coding genes by describing the difference between conserved and nonconserved MIRNA families.

Key Concepts:

  • MicroRNAs are small noncoding regulatory molecules.

  • Primary miRNA transcripts are folded into a stem–loop secondary structure, which is cleaved twice by DICER‐LIKE1 releasing the microRNA duplex.

  • One strand of the microRNA duplex is incorporated into an ARGONAUTE complex and guides the complex to specific mRNAs.

  • The ARGONAUTE complex usually cleaves the target mRNA but it also suppresses the translation of noncleaved mRNAs.

  • Some MIRNA genes are ancient and conserved in all embryophytes but there are nonconserved MIRNA families that are only in angiosperms or specific to monocots or dicots. A large number of MIRNA families are even divergent between dicot families.

  • New MIRNA genes can potentially evolve from any inverted repeats but the most evidence exists for generation from inverse duplication of protein‐coding genes followed by deletions and mutations.

  • Indirect evidence suggests rapid birth and death of MIRNA genes: approximately 1–3 MIRNA genes per million years in the Arabidopsis lineage.

  • Nonconserved MIRNA genes are weakly expressed, imprecisely processed, show uniform nucleotide divergence and many lack targets, suggesting that they are evolving neutrally.

  • Nonconserved MIRNA genes could be a source of ‘regulatory diversity’, which can be selected for if they acquire target genes and that is advantageous for the plant, maybe in a new environment.

Keywords: microRNA; evolution; small noncoding RNA; gene expression regulation; siRNA

Figure 1.

Biogenesis of miRNAs. MIRNA genes are transcribed by RNA polymerase II in the nucleus where the pri‐miRNA is capped and polyadenylated. DCL1, with the aid of the cap binding complex (CBP20 and ABH1/CBP80), HYL1, DDL and SE, recognises the characteristic hairpin structure and trims off the flanking regions. The resulting pre‐miRNA is cleaved again by DCL1 releasing the miRNA duplex. The 3′ end of the duplex is methylated by HEN1 and the duplex moves to the cytoplasm where one of the strands is taken up by RISC. MiRNA guides RISC to target mRNAs, which are cleaved by AGO1 (or other AGO family members).

Figure 2.

Generation of new MIRNA genes. The ancestral protein‐coding gene is inverse duplicated to generate a long inverted repeat. Since the protein is expressed from the other copy, deletions and mutations can occur in the inverted repeat. The older the inverted duplication event, the more deletions/mutations can be accumulated. There are examples for the different stages, such as the MIR822 and MIR839 loci, which represent a transition between siRNA and miRNA producing loci, young MIRNA genes, where the stem sequences outside the miRNA α duplexes are still similar to the ancestral genes and finally the conserved MIRNA genes, where only the miRNA duplex resembles to the target gene. The promoter sequences may also drift. For example miR395 is expressed mainly in the phloem companion cells whereas one of its targets (SULTR2;1) is mainly expressed in the xylem parenchyma cells (Kawashima et al., ).

close

References

Addo‐Quaye C, Eshoo TW, Bartel DP and Axtell MJ (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Current Biology 18: 758–762.

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

Allen E, Xie Z, Gustafson AM et al. (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nature Genetics 36: 1282–1290.

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

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

Baumberger N and Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proceedings of the National Academy of Sciences of the USA 102: 11928–11933.

Ben Amor B, Wirth S, Merchan F et al. (2009) Novel long non‐protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Research 19: 57–69.

Berezikov E, Liu N, Flynt AS et al. (2010) Evolutionary flux of canonical microRNAs and mirtrons in Drosophila. Nature Genetics 42: 6–9.

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

Bureau TE and Wessler SR (1992) Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 4: 1283–1294.

Carmell MA and Hannon GJ (2004) RNase III enzymes and the initiation of gene silencing. Nature Structural and Molecular Biology 11: 214–218.

Cuperus JT, Fahlgren N and Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23: 431–442.

de Meaux J, Hu JY, Tartler U and Goebel U (2008) Structurally different alleles of the ath‐MIR824 microRNA precursor are maintained at high frequency in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the USA 105: 8994–8999.

Ehrenreich IM and Purugganan MD (2008) Sequence variation of microRNAs and their binding sites in Arabidopsis. Plant Physiology 146: 1974–1982.

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.

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

Fang Y and Spector DL (2007) Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Current Biology 17: 818–823.

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

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

Griffiths‐Jones S, Hui JH, Marco A and Ronshaugen M (2011) MicroRNA evolution by arm switching. EMBO Reports 12: 172–177.

Grigg SP, Canales C, Hay A and Tsiantis M (2005) SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437: 1022–1026.

Hammond SM, Bernstein E, Beach D and Hannon GJ (2000) An RNA‐directed nuclease mediates post‐transcriptional gene silencing in Drosophila cells. Nature 404: 293–296.

Hutvagner G and Simard MJ (2008) ARGONAUTE proteins: key players in RNA silencing. Nature Reviews of Molecular and Cell Biology 9: 22–32.

Jones‐Rhoades MW and Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stressinduced miRNA. Molecular Cell 14: 787–799.

Kawashima CG, Yoshimoto N, Maruyama‐Nakashita A et al. (2009) Sulphur starvation induces the expression of microRNA‐395 and one of its target genes but in different cell types. Plant Journal 57: 313–321.

Kurihara Y and Watanabe Y (2004) Arabidopsis micro‐RNA biogenesis through DICER‐LIKE 1 protein functions. Proceedings of the National Academy of Sciences of the USA 101: 12753–12758.

Kurihara Y, Takashi Y and Watanabe Y (2006) The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri‐miRNA in plant microRNA biogenesis. RNA 12: 206–212.

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

Laubinger S, Sachsenberg T, Zeller G et al. (2008) Dual roles of the nuclear capbinding complex and SERRATE in pre‐mRNA splicing and microRNA processing in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the USA 105: 8795–8800.

Lu SS, Tej S, Luo CD et al. (2005) Elucidation of the small RNA component of the transcriptome. Science 309: 1567–1569.

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

Mallory A and Vaucheret H (2010) Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22: 3879–3889.

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

Molnar A, Schwach F, Studholme DJ, Thuenemann EC and Baulcombe DC (2007) miRNAs control gene expression in the single‐cell alga Chlamydomonas reinhardtii. Nature 447: 1126–1129.

Moxon S, Jing R, Szittya G et al. (2008) Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Research 18: 1602–1609.

Ossowski S, Schneeberger K, Lucas‐Lledo JI et al. (2010) The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327: 92–94.

Park MY, Wu G, Gonzalez‐Sulser A, Vaucheret H and Poethig RS (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 102: 3691–3696.

Piriyapongsa J and Jordan IK (2008) Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14: 814–821.

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

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

Ronemus M, Vaughn MW and Martienssen RA (2006) Micro‐RNA‐targeted and small interfering RNA‐mediated mRNA degradation is regulated by ARGONAUTE, DICER, and RNA‐dependent RNA polymerase in Arabidopsis. Plant Cell 18: 1559–1574.

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

Tomari Y, Matranga C, Haley B, Martinez N and Zamore PD (2004) A protein sensor for siRNA asymmetry. Science 306: 1377–1380.

Vazquez F, Blevins T, Ailhas J, Boller T and Meins F Jr (2008) Evolution of Arabidopsis MIR genes generates novel micro‐RNA classes. Nucleic Acids Research 36: 6429–6438.

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

Warthmann N, Das S, Lanz C and Weigel D (2008) Comparative analysis of the MIR319a microRNA locus in Arabidopsis and related Brassicaceae. Molecular Biology and Evolution 25: 892–902.

Xie Z, Allen E, Fahlgren N et al. (2005) Expression of Arabidopsis MIRNA genes. Plant Physiology 138: 2145–2154.

Yang L, Liu Z, Lu F, Dong A and Huang H (2006) SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant Journal 47: 841–850.

Yu B, Bi L, Zheng B et al. (2008) The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. Proceedings of the National Academy of Sciences of the USA 105: 10073–10078.

Yu B, Yang Z, Li J et al. (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307: 932–935.

Further Reading

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

Rubio‐Somoza I, Cuperus JT, Weigel D and Carrington JC (2009) Regulation and functional specialization of small RNA‐target nodes during plant development. Current Opinion in Plant Biology 12(5): 622–627.

Rubio‐Somoza I and Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends in Plant Science 16(5): 258–264.

Shabalina SA and Koonin EV (2008) Origins and evolution of eukaryotic RNA interference. Trends in Ecology & Evolution 23(10): 578–587.

Tang G (2011) Plant microRNAs: an insight into their gene structures and evolution. Seminars in Cell & Developmental Biology 21(8): 782–789.

Willmann MR and Poethig RS (2007) Conservation and evolution of miRNA regulatory programs in plant development. Current Opinion in Plant Biology 10(5): 503–511.

Xie Z, Khanna K and Ruan S (2010) Expression of microRNAs and its regulation in plants. Seminars in Cell & Developmental Biology 21(8): 790–797.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Tamas, Dalmay(Apr 2012) Evolution of Plant MicroRNAs. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023756]