The transcription and export complex THO/TREX contributes to transcription termination in plants
Autoři:
Ghazanfar Abbas Khan aff001; Jules Deforges aff001; Rodrigo S. Reis aff001; Yi-Fang Hsieh aff001; Jonatan Montpetit aff001; Wojciech Antosz aff003; Luca Santuari aff001; Christian S. Hardtke aff001; Klaus D. Grasser aff003; Yves Poirier aff001
Působiště autorů:
Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland
aff001; School of Biosciences, University of Melbourne, Melbourne, Australia
aff002; Department of Cell Biology & Plant Biochemistry, Biochemistry Centre, University of Regensburg, Regensburg, Germany
aff003
Vyšlo v časopise:
The transcription and export complex THO/TREX contributes to transcription termination in plants. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008732
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008732
Souhrn
Transcription termination has important regulatory functions, impacting mRNA stability, localization and translation potential. Failure to appropriately terminate transcription can also lead to read-through transcription and the synthesis of antisense RNAs which can have profound impact on gene expression. The Transcription-Export (THO/TREX) protein complex plays an important role in coupling transcription with splicing and export of mRNA. However, little is known about the role of the THO/TREX complex in the control of transcription termination. In this work, we show that two proteins of the THO/TREX complex, namely TREX COMPONENT 1 (TEX1 or THO3) and HYPER RECOMBINATION1 (HPR1 or THO1) contribute to the correct transcription termination at several loci in Arabidopsis thaliana. We first demonstrate this by showing defective termination in tex1 and hpr1 mutants at the nopaline synthase (NOS) terminator present in a T-DNA inserted between exon 1 and 3 of the PHO1 locus in the pho1-7 mutant. Read-through transcription beyond the NOS terminator and splicing-out of the T-DNA resulted in the generation of a near full-length PHO1 mRNA (minus exon 2) in the tex1 pho1-7 and hpr1 pho1-7 double mutants, with enhanced production of a truncated PHO1 protein that retained phosphate export activity. Consequently, the strong reduction of shoot growth associated with the severe phosphate deficiency of the pho1-7 mutant was alleviated in the tex1 pho1-7 and hpr1 pho1-7 double mutants. Additionally, we show that RNA termination defects in tex1 and hpr1 mutants leads to 3’UTR extensions in several endogenous genes. These results demonstrate that THO/TREX complex contributes to the regulation of transcription termination.
Klíčová slova:
Arabidopsis thaliana – DNA transcription – Gene expression – Messenger RNA – Phenotypes – RNA sequencing – Shoot growth – Transcriptional termination
Zdroje
1. Chen FX, Smith ER, Shilatifard A. Born to run: control of transcription elongation by RNA polymerase II. Nat Rev Mol Cell Biol. 2018;19(7):464–478. doi: 10.1038/s41580-018-0010-5 29740129
2. Herzel L, Ottoz DSM, Alpert T, Neugebauer KM. Splicing and transcription touch base: co-transcriptional spliceosome assembly and function. Nat Rev Mol Cell Biol. 2017;18(10):637–650. doi: 10.1038/nrm.2017.63 28792005
3. Richard P, Manley JL. Transcription termination by nuclear RNA polymerases. Genes Dev. 2009;23(11):1247–1269. doi: 10.1101/gad.1792809 19487567
4. Hsin J-P, Manley JL. The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev. 2012;26(19):2119–2137. doi: 10.1101/gad.200303.112 23028141
5. Nagarajan VK, Jones CI, Newbury SF, Green PJ. XRN 5 ' -> 3 ' exoribonucleases: Structure, mechanisms and functions. Biochim Biophys Acta. 2013;1829(6–7):590–603. doi: 10.1016/j.bbagrm.2013.03.005 23517755
6. Chen W, Jia Q, Song Y, Fu H, Wei G, Ni T. Alternative Polyadenylation: Methods, Findings, and Impacts. Genom Proteom Bioinf. 2017;15(5):287–300.
7. Mapendano CK, Lykke-Andersen S, Kjems J, Bertrand E, Jensen TH. Crosstalk between mRNA 3 ' End Processing and Transcription Initiation. Mol Cell. 2010;40(3):410–422. doi: 10.1016/j.molcel.2010.10.012 21070967
8. Sun H-X, Li Y, Niu Q-W, Chua N-H. Dehydration stress extends mRNA 3 ' untranslated regions with noncoding RNA functions in Arabidopsis. Genome Res. 2017;27(8):1427–1436. doi: 10.1101/gr.218669.116 28522613
9. Katahira J. mRNA export and the TREX complex. Biochim Biophys Acta. 2012;1819(6):507–513. doi: 10.1016/j.bbagrm.2011.12.001 22178508
10. Heath CG, Viphakone N, Wilson SA. The role of TREX in gene expression and disease. Biochem J. 2016;473:2911–2935. doi: 10.1042/BCJ20160010 27679854
11. Meinel DM, Burkert-Kautzsch C, Kieser A, O'Duibhir E, Siebert M, Mayer A, Cramer P, Soding J, Holstege FCP, Straesser K. Recruitment of TREX to the Transcription Machinery by Its Direct Binding to the Phospho-CTD of RNA Polymerase II. PLoS Genet. 2013;9(11).
12. Gomez-Gonzalez B, Garcia-Rubio M, Bermejo R, Gaillard H, Shirahige K, Marin A, Foiani M, Aguilera A. Genome-wide function of THO/TREX in active genes prevents R-loop-dependent replication obstacles. EMBO J. 2011;30(15):3106–3119. doi: 10.1038/emboj.2011.206 21701562
13. Ehrnsberger HF, Grasser M, Grasser KD. Nucleocytosolic mRNA transport in plants: export factors and their influence on growth and development. J Exp Bot. 2019; doi: 10.1093/jxb/erz173 30972423
14. Yelina NE, Smith LM, Jones AME, Patel K, Kelly KA, Baulcombe DC. Putative Arabidopsis THO/TREX mRNA export complex is involved in transgene and endogenous siRNA biosynthesis. Proc Natl Acad Sci USA. 2010;107(31):13948–13953. doi: 10.1073/pnas.0911341107 20634427
15. Jauvion V, Elmayan T, Vaucheret H. The Conserved RNA Trafficking Proteins HPR1 and TEX1 Are Involved in the Production of Endogenous and Exogenous Small Interfering RNA in Arabidopsis. Plant Cell. 2010;22(8):2697–2709. doi: 10.1105/tpc.110.076638 20798330
16. Tao S, Zhang Y, Wang X, Xu L, Fang X, Lu ZJ, Liu D. The THO/TREX Complex Active in miRNA Biogenesis Negatively Regulates Root-Associated Acid Phosphatase Activity Induced by Phosphate Starvation. Plant Physiol. 2016;171(4):2841–2853. doi: 10.1104/pp.16.00680 27329222
17. Francisco-Mangilet AG, Karlsson P, Kim M-H, Eo HJ, Oh SA, Kim JH, Kulcheski FR, Park SK, Andres Manavella P. THO2, a core member of the THO/TREX complex, is required for microRNA production in Arabidopsis. Plant J. 2015;82(6):1018–1029. doi: 10.1111/tpj.12874 25976549
18. Furumizu C, Tsukaya H, Komeda Y. Characterization of EMU, the Arabidopsis homolog of the yeast THO complex member HPR1. RNA. 2010;16(9):1809–1817. doi: 10.1261/rna.2265710 20668032
19. Sorensen BB, Ehrnsberger HF, Esposito S, Pfab A, Bruckmann A, Hauptmann J, Meister G, Merkl R, Schubert T, Laengst G et al. The Arabidopsis THO/TREX component TEX1 functionally interacts with MOS11 and modulates mRNA export and alternative splicing events. Plant Mol Biol. 2017;93(3):283–298. doi: 10.1007/s11103-016-0561-9 28004241
20. Xu C, Zhou X, Wen C-K. HYPER RECOMBINATION1 of the THO/TREX Complex Plays a Role in Controlling Transcription of the REVERSION-TO-ETHYLENE SENSITIVITY1 Gene in Arabidopsis. PLoS Genet. 2015;11(2).
21. Arpat AB, Magliano P, Wege S, Rouached H, Stefanovic A, Poirier Y. Functional expression of PHO1 to the Golgi and trans-Golgi network and its role in export of inorganic phosphate. Plant J. 2012;71:479–491. doi: 10.1111/j.1365-313X.2012.05004.x 22449068
22. Hamburger D, Rezzonico E, MacDonald-Comber Petétot J, Somerville C, Poirier Y. Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell. 2002;14:889–902. doi: 10.1105/tpc.000745 11971143
23. Poirier Y, Thoma S, Somerville C, Schiefelbein J. A mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol. 1991;97:1087–1093. doi: 10.1104/pp.97.3.1087 16668493
24. Stefanovic A, Arpat AB, Bligny R, Gout E, Vidoudez C, Bensimon M, Poirier Y. Overexpression of PHO1 in Arabidopsis leaves reveals its role in mediating phosphate efflux. Plant J. 2011;66:689–699. doi: 10.1111/j.1365-313X.2011.04532.x 21309867
25. Rouached H, Stefanovic A, Secco D, Arpat AB, Gout E, Bligny R, Poirier Y. Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in Arabidopsis. Plant J. 2011;65:557–570. doi: 10.1111/j.1365-313X.2010.04442.x 21288266
26. Secco D, Baumann A, Poirier Y. Charcaterization of the rice PHO1 gene family reveals a key role for OsPHO1;2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons. Plant Physiol. 2010;152:1693–1704. doi: 10.1104/pp.109.149872 20081045
27. Wege S, Khan GA, Jung J-Y, Vogiatzaki E, Pradervand S, Aller I, Meyer AJ, Poirier Y. The EXS domain of PHO1 participates in the response of shoots to phosphate deficiency via a root-to-shoot signal. Plant Physiol. 2016;170(1):385–400. doi: 10.1104/pp.15.00975 26546667
28. Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS. SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev. 2004;18(19):2368–2379. doi: 10.1101/gad.1231804 15466488
29. Ronemus M, Vaughn MW, Martienssen RA. MicroRNA-targeted and small interfering RNA-mediated mRNA degradation is regulated by Argonaute, Dicer, and RNA-dependent RNA polymerase in Arabidopsis. Plant Cell. 2006;18(7):1559–1574. doi: 10.1105/tpc.106.042127 16798886
30. Loke JC, Stahlberg EA, Strenski DG, Haas BJ, Wood PC, Li QQ. Compilation of mRNA polyadenylation signals in Arabidopsis revealed a new signal element and potential secondary structures. Plant Physiol. 2005;138(3):1457–1468. doi: 10.1104/pp.105.060541 15965016
31. Sherstnev A, Duc C, Cole C, Zacharaki V, Hornyik C, Ozsolak F, Milos PM, Barton GJ, Simpson GG. Direct sequencing of Arabidopsis thaliana RNA reveals patterns of cleavage and polyadenylation. Nat Struct Mol Biol. 2012;19(8):845–852. doi: 10.1038/nsmb.2345 22820990
32. Wu XH, Liu M, Downie B, Liang C, Ji GL, Li QQ, Hunt AG. Genome-wide landscape of polyadenylation in Arabidopsis provides evidence for extensive alternative polyadenylation. Proc Natl Acad Sci USA. 2011;108(30):12533–12538. doi: 10.1073/pnas.1019732108 21746925
33. Doan Duy Hai T, Saran S, Williamson AJK, Pierce A, Dittrich-Breiholz O, Wiehlmann L, Koch A, Whetton AD, Tamura T. THOC5 controls 3 ' end- processing of immediate early genes via interaction with polyadenylation specific factor 100 (CPSF100). Nucleic Acids Res. 2014;42(19):12249–12260. doi: 10.1093/nar/gku911 25274738
34. Katahira J, Okuzaki D, Inoue H, Yoneda Y, Maehara K, Ohkawa Y. Human TREX component Thoc5 affects alternative polyadenylation site choice by recruiting mammalian cleavage factor I. Nucleic Acids Res. 2013;41(14):7060–7072. doi: 10.1093/nar/gkt414 23685434
35. Pak V, Eifler TT, Jaeger S, Krogan NJ, Fujinaga K, Peterlin BM. CDK11 in TREX/THOC Regulates HIV mRNA 3 ' End Processing. Cell Host Microbe. 2015;18(5):560–570. doi: 10.1016/j.chom.2015.10.012 26567509
36. Pan H, Liu S, Tang D. HPR1, a component of the THO/TREX complex, plays an important role in disease resistance and senescence in Arabidopsis. Plant J. 2012;69(5):831–843. doi: 10.1111/j.1365-313X.2011.04835.x 22035198
37. Doll S, Kuhlmann M, Rutten T, Mette MF, Scharfenberg S, Petridis A, Berreth DC, Mock HP. Accumulation of the coumarin scopolin under abiotic stress conditions is mediated by the Arabidopsis thaliana THO/TREX complex. Plant J. 2018;93(3):431–444. doi: 10.1111/tpj.13797 29222952
38. Su Z, Zhao L, Zhao Y, Li S, Won S, Cai H, Wang L, Li Z, Chen P, Qin Y et al. The THO Complex Non-Cell-Autonomously Represses Female Germline Specification through the TAS3-ARF3 Module. Curr Biol. 2017;27(11):1597–+. doi: 10.1016/j.cub.2017.05.021 28552357
39. Tian B, Hu J, Zhang HB, Lutz CS. A large-scale analysis of mRNA polyadenylation of human and mouse genes. Nucleic Acids Res. 2005;33(1):201–212. doi: 10.1093/nar/gki158 15647503
40. Depicker A, Stachel S, Dhaese P, Zambryski PC, Goodman H. Nopaline synthase: transcript mapping and DNA sequence. J Mol Appl Genet. 1982;6:561–573.
41. Beyene G, Buenrostro-Nava MT, Damaj MB, Gao SJ, Molina J, Mirkov TE. Unprecedented enhancement of transient gene expression from minimal cassettes using a double terminator. Plant Cell Rep. 2011;30(1):13–25. doi: 10.1007/s00299-010-0936-3 20967448
42. Nagaya S, Kawamura K, Shinmyo A, Kato K. The HSP Terminator of Arabidopsis thaliana Increases Gene Expression in Plant Cells. Plant Cell Physiol. 2010;51(2):328–332. doi: 10.1093/pcp/pcp188 20040586
43. Richter LJ, Thanavala Y, Arntzen CJ, Mason HS. Production of hepatitis B surface antigen in transgenic plants for oral immunization. Nat Biotechnol. 2000;18(11):1167–1171. doi: 10.1038/81153 11062435
44. Rosenthal SH, Diamos AG, Mason HS. An intronless form of the tobacco extensin gene terminator strongly enhances transient gene expression in plant leaves. Plant Mol Biol. 2018;96(4–5):429–443. doi: 10.1007/s11103-018-0708-y 29429129
45. Mayr C. Regulation by 3 ‘-untranslated regions. Ann Rev Genet. 2017;51:171–194. doi: 10.1146/annurev-genet-120116-024704 28853924
46. Kindgren P, Ard R, Ivanov M, Marquardt S. Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation. Nature Comm. 2018;9.
47. Cuerda-Gil D, Slotkin RK. Non-canonical RNA-directed DNA methylation. Nature Plants. 2016;2(11):e16163.
48. Mathieu O, Bouche N. Interplay between chromatin and RNA processing. Curr Opin Plant Biol. 2014;18:60–65. doi: 10.1016/j.pbi.2014.02.006 24631845
49. Jung J-Y, Ried MK, Hothorn M, Poirier Y. Control of plant phosphate homeostasis by inositol pyrophosphates and the SPX domain. Curr Opin Biotechnol. 2018;49:156–162. doi: 10.1016/j.copbio.2017.08.012 28889038
50. Wild R, Gerasimaite R, Jung J-Y, Truffault V, Pavlovic I, Schmidt A, Saiardi A, Jessen HJ, Poirier Y, Hothorn M et al. Control of eukaryotic phosphate homeostasis by inositol polyphosphate sensor domains. Science. 2016;352(6288):986–990. doi: 10.1126/science.aad9858 27080106
51. Liu T-Y, Huang T-K, Tseng C-Y, Lai Y-S, Lin S-I, Lin W-Y, Chen J-W, Chiou T-J. PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell. 2012;24(5):2168–2183. doi: 10.1105/tpc.112.096636 22634761
52. Khan GA, Vogiatzaki E, Glauser G, Poirier Y. Phosphate Deficiency Induces the Jasmonate Pathway and Enhances Resistance to Insect Herbivory. Plant Physiol. 2016;171(1):632–644. doi: 10.1104/pp.16.00278 27016448
53. Ames BN. Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol. 1966;8:115–118.
54. Curtis MD, Grossniklaus U. A gateway cloning vectors set for high-throughput functional analysis of genes in planta. Plant Physiol. 2003;133:462–469. doi: 10.1104/pp.103.027979 14555774
55. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;6:735–743.
56. Deforges J, Reis RS, Jacquet P, Sheppard S, Geadekar VP, Hart-Smith G, Tanzer A, Hofacker IL, Iseli C, Xenarios I et al. Control of cognate mRNA translation by cis-natural antisense. Plant Physiol. 2019;180(1):305–322. doi: 10.1104/pp.19.00043 30760640
57. Kim D, Landmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12(4):357–360. doi: 10.1038/nmeth.3317 25751142
58. Anders S, Pyl PT, Huber W. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31(2):166–169. doi: 10.1093/bioinformatics/btu638 25260700
59. Love M, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. doi: 10.1186/s13059-014-0550-8 25516281
60. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. Integrative genomics viewer. Nat Biotechnol. 2011;29(1):24–26. doi: 10.1038/nbt.1754 21221095
61. Yoo S-D, Cho Y-H, Sheen J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc. 2007;2(7):1565–1572. doi: 10.1038/nprot.2007.199 17585298
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 4
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- „Jednohubky“ z klinického výzkumu – 2024/44
Nejčtenější v tomto čísle
- Analysis of genes within the schizophrenia-linked 22q11.2 deletion identifies interaction of night owl/LZTR1 and NF1 in GABAergic sleep control
- High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements
- Molecular genetics of maternally-controlled cell divisions
- Spastin mutations impair coordination between lipid droplet dispersion and reticulum
