Synergistic and Independent Actions of Multiple Terminal Nucleotidyl Transferases in the 3’ Tailing of Small RNAs in Arabidopsis

PLoS Genetics

Volumn 11, Issue 4, 2015, Pages

  Wang, Xiaoyan ^a   Zhang, Shuxin ^b   Dou, Yongchao ^b   Zhang, Chi ^b   Chen, Xuemei ^c   Yu, Bin ^b   Ren, Guodong ^a  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 1 PROTEIN; HEXOSE 1 PHOSPHATE URIDYLYLTRANSFERASE; MICRORNA; NUCLEOTIDYLTRANSFERASE; RNA; SMALL INTERFERING RNA; SMALL RNA; UNCLASSIFIED DRUG; URIDINE TRIPHOSPHATE RNA URIDYLYLTRANSFERASE; AGO1 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; ARGONAUTE PROTEIN; HEN1 PROTEIN, ARABIDOPSIS; HESO1 PROTEIN, ARABIDOPSIS; RNA POLYMERASE; URIDINE; URT1 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; CHEMICAL MODIFICATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC REGULATION; NONHUMAN; POINT MUTATION; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA STABILITY; URIDYLATION; ENZYMOLOGY; GENETICS; METABOLISM;

ANIMALIA; ARABIDOPSIS; CAENORHABDITIS ELEGANS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARGONAUTE PROTEINS; MICRORNAS; NUCLEOTIDYLTRANSFERASES; RNA NUCLEOTIDYLTRANSFERASES; RNA STABILITY; RNA, SMALL INTERFERING; URIDINE;

EID: 84930372546     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005091     Document Type: Article

References (36)

1. Chen XM, (2009) Small RNAs and Their Roles in Plant Development. Annu Rev Cell Dev Biol 25: 21–44. doi: 10.1146/annurev.cellbio.042308.113417 19575669
2. Ren G, Yu B, (2012) Critical roles of RNA-binding proteins in miRNA biogenesis in Arabidopsis. RNA Biol 9: 1424–1428. doi: 10.4161/rna.22740 23135480
3. Werner S, Wollmann H, Schneeberger K, Weigel D, (2010) Structure determinants for accurate processing of miR172a in Arabidopsis thaliana. Curr Biol 20: 42–48. doi: 10.1016/j.cub.2009.10.073 20015654
4. Mateos JL, Bologna NG, Chorostecki U, Palatnik JF, (2010) Identification of microRNA processing determinants by random mutagenesis of Arabidopsis MIR172a precursor. Curr Biol 20: 49–54. doi: 10.1016/j.cub.2009.10.072 20005105
5. 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 19816405
6. Yu B, Yang Z, Li J, Minakhina S, Yang M, et al. (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307: 932–935. 15705854
7. Baumberger N, Baulcombe DC, (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits rnicroRNAs and short interfering RNAs. Proc Natl Acad Sci U S A 102: 11928–11933. 16081530
8. Li J, Yang Z, Yu B, Liu J, Chen X, (2005) Methylation protects miRNAs and siRNAs from a 3'-end uridylation activity in Arabidopsis. Curr Biol 15: 1501–1507. 16111943
9. Montgomery TA, Rim YS, Zhang C, Dowen RH, Phillips CM, et al. (2012) PIWI associated siRNAs and piRNAs specifically require the Caenorhabditis elegans HEN1 ortholog henn-1. PLoS Genet 8: e1002616. doi: 10.1371/journal.pgen.1002616 22536158
10. Kamminga LM, van Wolfswinkel JC, Luteijn MJ, Kaaij LJ, Bagijn MP, et al. (2012) Differential impact of the HEN1 homolog HENN-1 on 21U and 26G RNAs in the germline of Caenorhabditis elegans. PLoS Genet 8: e1002702. doi: 10.1371/journal.pgen.1002702 22829772
11. Billi AC, Alessi AF, Khivansara V, Han T, Freeberg M, et al. (2012) The Caenorhabditis elegans HEN1 ortholog, HENN-1, methylates and stabilizes select subclasses of germline small RNAs. PLoS Genet 8: e1002617. doi: 10.1371/journal.pgen.1002617 22548001
12. Kamminga LM, Luteijn MJ, den Broeder MJ, Redl S, Kaaij LJT, et al. (2010) Hen1 is required for oocyte development and piRNA stability in zebrafish. Embo J 29: 3688–3700. doi: 10.1038/emboj.2010.233 20859253
13. Horwich MD, Li C, Matranga C, Vagin V, Farley G, et al. (2007) The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr Biol 17: 1265–1272. 17604629
14. Saito K, Sakaguchi Y, Suzuki T, Siomi H, Siomi MC, (2007) Pimet, the Drosophila homolog of HEN1, mediates 2'-O-methylation of Piwi- interacting RNAs at their 3' ends. Genes Dev 21: 1603–1608. 17606638
15. Kirino Y, Mourelatos Z, (2007) The mouse homolog of HEN1 is a potential methylase for Piwi-interacting RNAs. RNA 13: 1397–1401. 17652135
16. Ohara T, Sakaguchi Y, Suzuki T, Ueda H, Miyauchi K, et al. (2007) The 3' termini of mouse Piwi-interacting RNAs are 2'-O-methylated. Nat Struct Mol Biol 14: 349–350. 17384646
17. Ren G, Chen X, Yu B, (2012) Uridylation of miRNAs by HEN1 SUPPRESSOR1 in Arabidopsis. Curr Biol 22: 695–700. doi: 10.1016/j.cub.2012.02.052 22464191
18. Zhao Y, Yu Y, Zhai J, Ramachandran V, Dinh TT, et al. (2012) The Arabidopsis nucleotidyl transferase HESO1 uridylates unmethylated small RNAs to trigger their degradation. Curr Biol 22: 689–694. doi: 10.1016/j.cub.2012.02.051 22464194
19. Sement FM, Ferrier E, Zuber H, Merret R, Alioua M, et al. (2013) Uridylation prevents 3' trimming of oligoadenylated mRNAs. Nucleic Acids Res 41: 7115–7127. doi: 10.1093/nar/gkt465 23748567
20. Yu B, Bi L, Zhai J, Agarwal M, Li S, et al. (2010) siRNAs compete with miRNAs for methylation by HEN1 in Arabidopsis. Nucleic Acids Res 38: 5844–5850. doi: 10.1093/nar/gkq348 20448024
21. Zhai J, Zhao Y, Simon SA, Huang S, Petsch K, et al. (2013) Plant MicroRNAs Display Differential 3’- Truncation and Tailing, Modifications Which Are ARGONAUTE1-Dependent and Conserved Across Species. Plant Cell 25: 2417–2428. doi: 10.1105/tpc.113.114603 23839787
22. Liu C, Axtell MJ, Fedoroff NV, (2012) The helicase and RNaseIIIa domains of Arabidopsis Dicer-Like1 modulate catalytic parameters during microRNA biogenesis. Plant Physiol 159: 748–758. doi: 10.1104/pp.112.193508 22474216
23. Heo I, Ha M, Lim J, Yoon MJ, Park JE, et al. (2012) Mono-Uridylation of Pre-MicroRNA as a Key Step in the Biogenesis of Group II let-7 MicroRNAs. Cell 151: 521–532. doi: 10.1016/j.cell.2012.09.022 23063654
24. Ren GD, Xie M, Zhang SX, Vinovskis C, Chen XM, et al. (2014) Methylation protects microRNAs from an AGO1-associated activity that uridylates 5' RNA fragments generated by AGO1 cleavage. Proc Natl Acad Sci USA 111: 6365–6370. doi: 10.1073/pnas.1405083111 24733911
25. Kwak JE, Wickens M, (2007) A family of poly(U) polymerases. Rna 13: 860–867. 17449726
26. Zhang X, Yuan YR, Pei Y, Lin SS, Tuschl T, et al. (2006) Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev 20: 3255–3268. 17158744
27. Pomeranz MC, Hah C, Lin PC, Kang SG, Finer JJ, et al. (2010) The Arabidopsis Tandem Zinc Finger Protein AtTZF1 Traffics between the Nucleus and Cytoplasmic Foci and Binds Both DNA and RNA. Plant Physiol 152: 151–165. doi: 10.1104/pp.109.145656 19897605
28. Tu B, Xu C, Liu L, Zhai JX, Li S, et al. (2014) Distinct and cooperative activities of HESO1 and URT1 nucleotidyl transferases in microRNA turnover in Arabidopsis. PLoS Genet 11: e1005119.
29. Ramachandran V, Chen X, (2008) Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 321: 1490–1492. doi: 10.1126/science.1163728 18787168
30. 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 23881412
31. Chen X, Liu J, Cheng Y, Jia D, (2002) HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129: 1085–1094. 11874905
32. Weigel D, Glazebrook J, (2002) Arabidopsis. A Laboratory Manual.
33. Curtis MD, Grossniklaus U, (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462–469. 14555774
34. Clough SJ, Bent AF, (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743. 10069079
35. Ren GD, Xie M, Dou YC, Zhang SX, Zhang C, et al. (2012) Regulation of miRNA abundance by RNA binding protein TOUGH in Arabidopsis. Proc Natl Acad Sci USA 109: 12817–12821. doi: 10.1073/pnas.1204915109 22802657
36. Tanaka Y, Nakamura S, Kawamukai M, Koizumi N, Nakagawa T, (2011) Development of a series of gateway binary vectors possessing a tunicamycin resistance gene as a marker for the transformation of Arabidopsis thaliana. Biosci Biotechnol Biochem 75: 804–807. 21512216