The Roles of CDF2 in Transcriptional and Posttranscriptional Regulation of Primary MicroRNAs

English version České info

CDFs were identified to play roles in the blue light signaling. This study reveals that CDF2 acts as a transcriptional activator or repressor of a group of microRNA (miRNA) genes and binds to the pri-miRNA transcripts. This study demonstrates that CDF2 interacts with the Dicer-like 1 (DCL1) complex and suppresses the processing of primary miRNAs. Genetic analysis shows that CDF2 works in the same pathway as miR156 or miR172 to control flowering. The finding that the miRNA accumulation is regulated by a factor at both the transcriptional and posttranscriptional levels may have a broad impact on the miRNA biogenesis field. The regulation of miRNA abundance by CDF2 sheds light on the roles of miRNAs in the light signaling pathways.

Vyšlo v časopise: The Roles of CDF2 in Transcriptional and Posttranscriptional Regulation of Primary MicroRNAs. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005598
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005598

Souhrn

Zdroje

1. Vazquez F, Legrand S, Windels D (2010) The biosynthetic pathways and biological scopes of plant small RNAs. Trends in Plant Science 15: 337–345. doi: 10.1016/j.tplants.2010.04.001 20427224

2. Chapman E, Carrington J (2007) Specialization and evolution of endogenous small RNA pathways. Nature Reviews Genetics 8: 884–896. 17943195

3. Yu B, Bi L, Zheng B, Ji L, Chevalier D, et al. (2008) The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. Proc Natl Acad Sci U S A 105: 10073–10078. doi: 10.1073/pnas.0804218105 18632581

4. Jones-Rhoades M, Bartel D, Bartel B (2006) MicroRNAs and Their Regulatory Roles in Plants. Annu Rev Plant Biol 57: 19–53. 16669754

5. Han M, Goud S, Song L, Fedoroff N (2004) The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proceedings of the National Academy of Sciences 101: 1093–1098.

6. Lobbes D, Rallapalli G, Schmidt D, Martin C, Clarke J (2006) SERRATE: a new player on the plant microRNA scene. EMBO reports 7: 1052–1058. 16977334

7. Manavella P, Hagmann J, Ott F, Laubinger S, Franz M, et al. (2012) Fast-Forward Genetics Identifies Plant CPL Phosphatases as Regulators of miRNA Processing Factor HYL1. Cell 151: 859–870. doi: 10.1016/j.cell.2012.09.039 23141542

8. Laubinger S, Sachsenberg T, Zeller G, Busch W, Lohmann JU, et al. (2008) Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc Natl Acad Sci U S A 105: 8795–8800. doi: 10.1073/pnas.0802493105 18550839

9. Ren G, Xie M, Dou Y, Zhang S, Zhang C, et al. (2012) Regulation of miRNA abundance by RNA binding protein TOUGH in Arabidopsis. Proc Natl Acad Sci U S A 109: 12817–12821. doi: 10.1073/pnas.1204915109 22802657

10. Wu X, Shi Y, Li J, Xu L, Fang Y, et al. (2013) A role for the RNA-binding protein MOS2 in microRNA maturation in Arabidopsis. Cell Res 23: 645–657. doi: 10.1038/cr.2013.23 23399598

11. Fornara F, Panigrahi K, Gissot L, Sauerbrunn N, Rühl M, et al. (2009) Arabidopsis DOF Transcription Factors Act Redundantly to Reduce CONSTANS Expression and Are Essential for a Photoperiodic Flowering Response. Developmental Cell 17: 75–86. doi: 10.1016/j.devcel.2009.06.015 19619493

12. Moreno-Risueno M, Martínez M, Vicente-Carbajosa J, Carbonero P (2007) The family of DOF transcription factors: from green unicellular algae to vascular plants. Molecular Genetics and Genomics 277: 379–390. 17180359

13. Papi M, Sabatini S, Bouchez D, Camilleri C, Costantino P, et al. (2000) Identification and disruption of an Arabidopsis zinc finger gene controlling seed germination. Genes Development 14: 28–33. 10640273

14. Gualberti G, Papi M, Bellucci L, Ricci I, Bouchez D, et al. (2002) Mutations in the Dof Zinc Finger Genes DAG2 and DAG1 Influence with Opposite Effects the Germination of Arabidopsis Seeds. The Plant Cell Online 14: 1253–1263.

15. Kang H, Singh K (2000) Characterization of salicylic acid-responsive, arabidopsis Dof domain proteins: overexpression of OBP3 leads to growth defects. The Plant Journal 21: 329–339. 10758484

16. Park D, Lim P, Kim J, Cho D, Hong S, et al. (2003) The Arabidopsis COG1 gene encodes a Dof domain transcription factor and negatively regulates phytochrome signaling. The Plant Journal 34: 161–171. 12694592

17. Peng Z, Lu Y, Li L, Zhao Q, Feng Q, et al. (2013) The draft genome of the fast-growing non-timber forest species moso bamboo (Phyllostachys heterocycla) Nat Genet 45: 456–461. doi: 10.1038/ng.2569 23435089

18. Imaizumi T, Schultz TF, Harmon FG, Ho LA, SA. K (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309: 293–297. 16002617

19. Wang L, Song X, Gu L, Li X, Cao S, et al. (2013) NOT2 proteins promote polymerase II-dependent transcription and interact with multiple MicroRNA biogenesis factors in Arabidopsis. Plant Cell 25: 715–727. doi: 10.1105/tpc.112.105882 23424246

20. Zhang S XM, Ren G, Yu B. (2013) CDC5, a DNA binding protein, positively regulates posttranscriptional processing and/or transcription of primary microRNA transcripts. Proc Natl Acad Sci U S A 110: 17588–17593. doi: 10.1073/pnas.1310644110 24101471

21. Cheng TL WZ, Liao Q, Zhu Y, Zhou WH, Xu W, Qiu Z. (2014) MeCP2 suppresses nuclear microRNA processing and dendritic growth by regulating the DGCR8/Drosha complex. Dev Cell 28: 547–560. doi: 10.1016/j.devcel.2014.01.032 24636259

22. Wagschal A, Rousset E, Basavarajaiah P, Contreras X, Harwig A, et al. (2012) Microprocessor, Setx, Xrn2, and Rrp6 co-operate to induce premature termination of transcription by RNAPII. cell 150: 1147–1157. doi: 10.1016/j.cell.2012.08.004 22980978

23. Liu F, Bakht S, C. D (2012) Cotranscriptional role for Arabidopsis DICER-LIKE 4 in transcription termination. science 335: 1621–1623. doi: 10.1126/science.1214402 22461611

24. Fang Y, Spector D (2007) Identification of Nuclear Dicing Bodies Containing Proteins for MicroRNA Biogenesis in Living Arabidopsis Plants Curr Biol 17: 818–823. 17442570

25. Liu Q, Yan Q, Liu Y, Hong F, Sun Z, et al. (2013) Complementation of HYPONASTIC LEAVES1 by double-strand RNA-binding domains of DICER-LIKE1 in nuclear dicing bodies. Plant Physiol 163: 108–117. doi: 10.1104/pp.113.219071 23886622

26. Fang Y, DL S (2007) Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr Biol 17: 818–823. 17442570

27. Eisen M, Spellman P, Brown P, D B (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci 95: 14863–14868. 9843981

28. Yanagisawa S (2002) The Dof family of plant transcription factors. TRENDS in Plant Science 7: 555–560. 12475498

29. Mena M, Cejudo F, Isabel-Lamoneda I, Carbonero P (2002) A Role for the DOF Transcription Factor BPBF in the Regulation of Gibberellin-Responsive Genes in Barley Aleurone. Plant Physiology 130: 111–119. 12226491

30. Fang X, Cui Y, Li Y, Qi Y. (2015) Transcription and processing of primary microRNAs are coupled by Elongator complex in Arabidopsis. NATURE PLANTS

31. Kawahara Y, Zinshteyn B, Sethupathy P, Iizasa H, Hatzigeorgiou AG, et al. (2007) Science. Redirection of silencing targets by adenosine-to-inosine editing of miRNAs 315: 1137–1140. 17322061

32. Yamagata K, Fujiyama S, Ito S, Ueda T, Murata T, et al. (2009) Maturation of MicroRNA Is Hormonally Regulated by a Nuclear Receptor. Molecular Cell 36: 340–347. doi: 10.1016/j.molcel.2009.08.017 19854141

33. Heo I, Joo C, Kim YK, Ha M, Yoon MJ, et al. (2009) TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 138: 696–708. doi: 10.1016/j.cell.2009.08.002 19703396

34. Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, et al. (2008) A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 10: 987–993. doi: 10.1038/ncb1759 18604195

35. Viswanathan SR, Daley GQ, RI. G (2008) Selective blockade of microRNA processing by Lin28. Science 320: 97–100 doi: 10.1126/science.1154040 18292307

36. Heo I, Joo C, Kim Y, Ha M, Yoon M, et al. (2009) TUT4 in Concert with Lin28 Suppresses MicroRNA Biogenesis through Pre-MicroRNA Uridylation. Cell 138: 696–708. doi: 10.1016/j.cell.2009.08.002 19703396

37. Hagan J, Piskounova E, Gregory R (2009) Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat Struct Mol Biol 16: 1021–1025. doi: 10.1038/nsmb.1676 19713958

38. Luo Y, Guo Z, L. 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 23707900

39. Cho SK, Chaabane SB, Shah P, Poulsen CP, SW. Y (2014) COP1 E3 ligase protects HYL1 to retain microRNA biogenesis. Nat Commun 23: doi: 10.1038/ncomms6867

40. Wang JW, Czech B, W D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: 738–749 doi: 10.1016/j.cell.2009.06.014 19703399

41. Wang JW, Czech B, D. W (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: 738–749. doi: 10.1016/j.cell.2009.06.014 19703399

42. Yang Z, Wang X, Gu S, Hu Z, Xu H, et al. (2008) Comparative study of SBP-box gene family in Arabidopsis and rice. Gene 407: 1–11. 17629421

43. Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development Science 303: 2022–2025. 12893888

44. Lu C, Fedoroff NV (2000) A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12: 2351–2366. 11148283

45. Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, et al. (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16: 69–79. 15469823

46. Jacobsen S, Running M, Meyerowitz E (1999) Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126: 5231–5243. 10556049

47. Clough S, Bent A (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743. 10069079

48. Liu Q, Yan Q, Liu Y, Hong F, Sun Z, et al. (2013) Complementation of HYPONASTIC LEAVES1 by double-strand RNA-binding domains of DICER-LIKE1 in nuclear dicing bodies. Plant Physiol 163: 108–117. doi: 10.1104/pp.113.219071 23886622

49. Ning J, Zhang B, Wang N, Zhou Y, L. X (2011) Increased leaf angle1, a Raf-like MAPKKK that interacts with a nuclear protein family, regulates mechanical tissue formation in the Lamina joint of rice. Plant Cell 23: 4334–4347. doi: 10.1105/tpc.111.093419 22207574

50. Siurkus J, Panula-Perälä J, Horn U, Kraft M, Rimseliene R, et al. (2010) Novel approach of high cell density recombinant bioprocess development: optimisation and scale-up from microliter to pilot scales while maintaining the fed-batch cultivation mode of E. coli cultures. Microb Cell Fact 9.

51. Wang M, Gu D, Liu T, Wang Z, Guo X, et al. (2007) Overexpression of a putative maize calcineurin B-like protein in Arabidopsis confers salt tolerance. Plant Mol Biol 65: 733–746. 17882512

52. Livak KJS, Thomas D. (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods 25: 402–408. 11846609

53. Saleh A, Alvarez-Venegas R, Z. A (2008) An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat Protoc 3: 1018–1025. doi: 10.1038/nprot.2008.66 18536649

54. Jefferson R.A., Kavanagh T.A., and Bevan MW (1987) GUS fusions: Beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907. 3327686

55. Langmead B, Trapnell C, Pop M, Salzberg S (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10: R25. doi: 10.1186/gb-2009-10-3-r25 19261174

56. Griffiths-Jones S, Saini H, van Dongen S, Enright A (2008) miRBase: tools for microRNA genomics. Nucleic Acids Research 36: D154–D158. 17991681

57. Terzi LC, and Simpson GG (2009) Arabidopsis RNA immunoprecipitation. Plant J 59: 163–168. doi: 10.1111/j.1365-313X.2009.03859.x 19419533