Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
BB/P009751/1
Biotechnology and Biological Sciences Research Council - United Kingdom
PubMed
32665305
PubMed Central
PMC7474300
DOI
10.1105/tpc.20.00244
PII: tpc.20.00244
Knihovny.cz E-zdroje
- MeSH
- alternativní sestřih MeSH
- Arabidopsis genetika metabolismus MeSH
- mutace MeSH
- nonsense mediated mRNA decay * MeSH
- posttranslační úpravy proteinů MeSH
- proteiny huseníčku genetika metabolismus MeSH
- proteosyntéza MeSH
- regulace genové exprese u rostlin MeSH
- RNA-helikasy genetika metabolismus MeSH
- transportní proteiny genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- proteiny huseníčku MeSH
- RNA-helikasy MeSH
- RPS6 protein, Arabidopsis MeSH Prohlížeč
- SMG7 protein, Arabidopsis MeSH Prohlížeč
- transportní proteiny MeSH
- UPF1 protein, Arabidopsis MeSH Prohlížeč
- UPF3 protein, Arabidopsis MeSH Prohlížeč
Nonsense-mediated RNA decay (NMD) is an RNA control mechanism that has also been implicated in the broader regulation of gene expression. Nevertheless, a role for NMD in genome regulation has not yet been fully assessed, partially because NMD inactivation is lethal in many organisms. Here, we performed an in-depth comparative analysis of Arabidopsis (Arabidopsis thaliana) mutants lacking the NMD-related proteins UPF3, UPF1, and SMG7. We found different impacts of these proteins on NMD and the Arabidopsis transcriptome, with UPF1 having the biggest effect. Transcriptome assembly in UPF1-null plants revealed genome-wide changes in alternative splicing, suggesting that UPF1 functions in splicing. The inactivation of UPF1 led to translational repression, as manifested by a global shift in mRNAs from polysomes to monosomes and the downregulation of genes involved in translation and ribosome biogenesis. Despite these global changes, NMD targets and mRNAs expressed at low levels with short half-lives were enriched in the polysomes of upf1 mutants, indicating that UPF1/NMD suppresses the translation of aberrant RNAs. Particularly striking was an increase in the translation of TIR domain-containing, nucleotide binding, leucine-rich repeat (TNL) immune receptors. The regulation of TNLs via UPF1/NMD-mediated mRNA stability and translational derepression offers a dynamic mechanism for the rapid activation of TNLs in response to pathogen attack.
Cell and Molecular Sciences James Hutton Institute Dundee DD2 5DA United Kingdom
Central European Institute of Technology Masaryk University 625 00 Brno Czech Republic
Gregor Mendel Institute Austrian Academy of Sciences 1030 Vienna Austria
Information and Computational Sciences James Hutton Institute Dundee DD2 5DA United Kingdom
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Aliouat A., Hatin I., Bertin P., Francois P., Stierle V., Namy O., Salhi S., Jean-Jean O.(2020). Divergent effects of translation termination factor eRF3A and nonsense-mediated mRNA decay factor UPF1 on the expression of uORF carrying mRNAs and ribosome protein genes. RNA Biol. 17: 227–239. PubMed PMC
Amrani N., Ganesan R., Kervestin S., Mangus D.A., Ghosh S., Jacobson A.(2004). A faux 3′-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature 432: 112–118. PubMed
Arciga-Reyes L., Wootton L., Kieffer M., Davies B.(2006). UPF1 is required for nonsense-mediated mRNA decay (NMD) and RNAi in Arabidopsis. Plant J. 47: 480–489. PubMed
Ashburner M., et al. (2000). Gene Ontology: Tool for the unification of biology. Nat. Genet. 25: 25–29. PubMed PMC
Avery P., Vicente-Crespo M., Francis D., Nashchekina O., Alonso C.R., Palacios I.M.(2011). Drosophila Upf1 and Upf2 loss of function inhibits cell growth and causes animal death in a Upf3-independent manner. RNA 17: 624–638. PubMed PMC
Benkovics A.H., Nyikó T., Mérai Z., Silhavy D., Bisztray G.D.(2011). Functional analysis of the grapevine paralogs of the SMG7 NMD factor using a heterolog VIGS-based gene depletion-complementation system. Plant Mol. Biol. 75: 277–290. PubMed
Bray N.L., Pimentel H., Melsted P., Pachter L.(2016). Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34: 525–527. PubMed
Calixto C.P.G., Guo W., James A.B., Tzioutziou N.A., Entizne J.C., Panter P.E., Knight H., Nimmo H.G., Zhang R., Brown J.W.S.(2018). Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome. Plant Cell 30: 1424–1444. PubMed PMC
Capitao C., Shukla N., Wandrolova A., Mittelsten Scheid O., Riha K.(2018). Functional characterization of SMG7 paralogs in Arabidopsis thaliana. Front. Plant Sci. 9: 1602. PubMed PMC
Carbon S., et al. (2019). The Gene Ontology Resource: 20 years and still GOing strong. Nucleic Acids Res. 47: D330–D338. PubMed PMC
Celik A., Baker R., He F., Jacobson A.(2017). High-resolution profiling of NMD targets in yeast reveals translational fidelity as a basis for substrate selection. RNA 23: 735–748. PubMed PMC
Chiam N.C., Fujimura T., Sano R., Akiyoshi N., Hiroyama R., Watanabe Y., Motose H., Demura T., Ohtani M.(2019). Nonsense-mediated mRNA decay deficiency affects the auxin response and shoot regeneration in Arabidopsis. Plant Cell Physiol. 60: 2000–2014. PubMed
Chicois C., Scheer H., Garcia S., Zuber H., Mutterer J., Chicher J., Hammann P., Gagliardi D., Garcia D.(2018). The UPF1 interactome reveals interaction networks between RNA degradation and translation repression factors in Arabidopsis. Plant J. 96: 119–132. PubMed
Colombo M., Karousis E.D., Bourquin J., Bruggmann R., Mühlemann O.(2017). Transcriptome-wide identification of NMD-targeted human mRNAs reveals extensive redundancy between SMG6- and SMG7-mediated degradation pathways. RNA 23: 189–201. PubMed PMC
Cui H., Tsuda K., Parker J.E.(2015). Effector-triggered immunity: From pathogen perception to robust defense. Annu. Rev. Plant Biol. 66: 487–511. PubMed
Degtiar E., Fridman A., Gottlieb D., Vexler K., Berezin I., Farhi R., Golani L., Shaul O.(2015). The feedback control of UPF3 is crucial for RNA surveillance in plants. Nucleic Acids Res. 43: 4219–4235. PubMed PMC
de Turris V., Nicholson P., Orozco R.Z., Singer R.H., Mühlemann O.(2011). Cotranscriptional effect of a premature termination codon revealed by live-cell imaging. RNA 17: 2094–2107. PubMed PMC
Dobin A., Davis C.A., Schlesinger F., Drenkow J., Zaleski C., Jha S., Batut P., Chaisson M., Gingeras T.R.(2013). STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29: 15–21. PubMed PMC
Drechsel G., Kahles A., Kesarwani A.K., Stauffer E., Behr J., Drewe P., Rätsch G., Wachter A.(2013). Nonsense-mediated decay of alternative precursor mRNA splicing variants is a major determinant of the Arabidopsis steady state transcriptome. Plant Cell 25: 3726–3742. PubMed PMC
Galili T., O’Callaghan A., Sidi J., Sievert C.(2018). heatmaply: An R package for creating interactive cluster heatmaps for online publishing. Bioinformatics 34: 1600–1602. PubMed PMC
Gloggnitzer J., Akimcheva S., Srinivasan A., Kusenda B., Riehs N., Stampfl H., Bautor J., Dekrout B., Jonak C., Jiménez-Gómez J.M., Parker J.E., Riha K.(2014). Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. Cell Host Microbe 16: 376–390. PubMed
Gout J.F., et al. (2017). The landscape of transcription errors in eukaryotic cells. Sci. Adv. 3: e1701484. PubMed PMC
Gu Z., Eils R., Schlesner M.(2016). Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32: 2847–2849. PubMed
Guo W., Tzioutziou N., Stephen G., Milne I., Calixto C., Waugh R., Brown J.W.S., Zhang R.(2019). 3D RNA-seq: A powerful and flexible tool for rapid and accurate differential expression and alternative splicing analysis of RNA-seq data for biologists. bioRxiv 656686. PubMed PMC
He F., Jacobson A.(1995). Identification of a novel component of the nonsense-mediated mRNA decay pathway by use of an interacting protein screen. Genes Dev. 9: 437–454. PubMed
He F., Jacobson A.(2015). Nonsense-mediated mRNA decay: Degradation of defective transcripts is only part of the story. Annu. Rev. Genet. 49: 339–366. PubMed PMC
Heyer E.E., Moore M.J.(2016). Redefining the translational status of 80S monosomes. Cell 164: 757–769. PubMed
Hoek T.A., Khuperkar D., Lindeboom R.G.H., Sonneveld S., Verhagen B.M.P., Boersma S., Vermeulen M., Tanenbaum M.E.(2019). Single-molecule imaging uncovers rules governing nonsense-mediated mRNA decay. Mol. Cell 75: 324–339.e311. PubMed PMC
Hogg J.R., Goff S.P.(2010). Upf1 senses 3’UTR length to potentiate mRNA decay. Cell 143: 379–389. PubMed PMC
Hori K., Watanabe Y.(2005). UPF3 suppresses aberrant spliced mRNA in Arabidopsis. Plant J. 43: 530–540. PubMed
Hurt J.A., Robertson A.D., Burge C.B.(2013). Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay. Genome Res. 23: 1636–1650. PubMed PMC
Hwang J., Maquat L.E.(2011). Nonsense-mediated mRNA decay (NMD) in animal embryogenesis: To die or not to die, that is the question. Curr. Opin. Genet. Dev. 21: 422–430. PubMed PMC
Isken O., Kim Y.K., Hosoda N., Mayeur G.L., Hershey J.W., Maquat L.E.(2008). Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133: 314–327. PubMed PMC
Jeong H.J., Kim Y.J., Kim S.H., Kim Y.H., Lee I.J., Kim Y.K., Shin J.S.(2011). Nonsense-mediated mRNA decay factors, UPF1 and UPF3, contribute to plant defense. Plant Cell Physiol. 52: 2147–2156. PubMed
Jirage D., Tootle T.L., Reuber T.L., Frost L.N., Feys B.J., Parker J.E., Ausubel F.M., Glazebrook J.(1999). Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl. Acad. Sci. USA 96: 13583–13588. PubMed PMC
Jung H.W., et al. (2020). Pathogen-associated molecular pattern-triggered immunity involves proteolytic degradation of core nonsense-mediated mRNA decay factors during the early defense response. Plant Cell 32: 1081–1101. PubMed PMC
Juntawong P., Hummel M., Bazin J., Bailey-Serres J.(2015). Ribosome profiling: A tool for quantitative evaluation of dynamics in mRNA translation. Methods Mol. Biol. 1284: 139–173. PubMed
Kalyna M., et al. (2012). Alternative splicing and nonsense-mediated decay modulate expression of important regulatory genes in Arabidopsis. Nucleic Acids Res. 40: 2454–2469. PubMed PMC
Kang Y.J., Yang D.C., Kong L., Hou M., Meng Y.Q., Wei L., Gao G.(2017). CPC2: A fast and accurate coding potential calculator based on sequence intrinsic features. Nucleic Acids Res. 45: W12–W16. PubMed PMC
Karousis E.D., Nasif S., Mühlemann O.(2016). Nonsense-mediated mRNA decay: Novel mechanistic insights and biological impact. Wiley Interdiscip. Rev. RNA 7: 661–682. PubMed PMC
Kashima I., Yamashita A., Izumi N., Kataoka N., Morishita R., Hoshino S., Ohno M., Dreyfuss G., Ohno S.(2006). Binding of a novel SMG-1-Upf1-eRF1-eRF3 complex (SURF) to the exon junction complex triggers Upf1 phosphorylation and nonsense-mediated mRNA decay. Genes Dev. 20: 355–367. PubMed PMC
Kerényi Z., Mérai Z., Hiripi L., Benkovics A., Gyula P., Lacomme C., Barta E., Nagy F., Silhavy D.(2008). Inter-kingdom conservation of mechanism of nonsense-mediated mRNA decay. EMBO J. 27: 1585–1595. PubMed PMC
Kertész S., Kerényi Z., Mérai Z., Bartos I., Pálfy T., Barta E., Silhavy D.(2006). Both introns and long 3′-UTRs operate as cis-acting elements to trigger nonsense-mediated decay in plants. Nucleic Acids Res. 34: 6147–6157. PubMed PMC
Kesarwani A.K., Lee H.C., Ricca P.G., Sullivan G., Faiss N., Wagner G., Wunderling A., Wachter A.(2019). Multifactorial and species-specific feedback regulation of the RNA surveillance pathway nonsense-mediated decay in plants. Plant Cell Physiol. 60: 1986–1999. PubMed
Kim Y.K., Maquat L.E.(2019). UPFront and center in RNA decay: UPF1 in nonsense-mediated mRNA decay and beyond. RNA 25: 407–422. PubMed PMC
Kurihara Y., et al. (2009). Genome-wide suppression of aberrant mRNA-like noncoding RNAs by NMD in Arabidopsis. Proc. Natl. Acad. Sci. USA 106: 2453–2458. PubMed PMC
Kurosaki T., Popp M.W., Maquat L.E.(2019). Quality and quantity control of gene expression by nonsense-mediated mRNA decay. Nat. Rev. Mol. Cell Biol. 20: 406–420. PubMed PMC
Kwon Y.J., Park M.J., Kim S.G., Baldwin I.T., Park C.M.(2014). Alternative splicing and nonsense-mediated decay of circadian clock genes under environmental stress conditions in Arabidopsis. BMC Plant Biol. 14: 136. PubMed PMC
Lai Y., Eulgem T.(2018). Transcript-level expression control of plant NLR genes. Mol. Plant Pathol. 19: 1267–1281. PubMed PMC
Larsson O., Sonenberg N., Nadon R.(2010). Identification of differential translation in genome wide studies. Proc. Natl. Acad. Sci. USA 107: 21487–21492. PubMed PMC
Law C.W., Chen Y., Shi W., Smyth G.K.(2014). voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 15: R29. PubMed PMC
Lewandowska D., ten Have S., Hodge K., Tillemans V., Lamond A.I., Brown J.W.(2013). Plant SILAC: Stable-isotope labelling with amino acids of Arabidopsis seedlings for quantitative proteomics. PLoS One 8: e72207. PubMed PMC
Livak K.J., Schmittgen T.D.(2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402–408. PubMed
Loh B., Jonas S., Izaurralde E.(2013). The SMG5-SMG7 heterodimer directly recruits the CCR4-NOT deadenylase complex to mRNAs containing nonsense codons via interaction with POP2. Genes Dev. 27: 2125–2138. PubMed PMC
Lykke-Andersen J.(2002). Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol. Cell. Biol. 22: 8114–8121. PubMed PMC
Medghalchi S.M., Frischmeyer P.A., Mendell J.T., Kelly A.G., Lawler A.M., Dietz H.C.(2001). Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum. Mol. Genet. 10: 99–105. PubMed
Mendell J.T., Sharifi N.A., Meyers J.L., Martinez-Murillo F., Dietz H.C.(2004). Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 36: 1073–1078. PubMed
Merai Z., Benkovics A.H., Nyiko T., Debreczeny M., Hiripi L., Kerenyi Z., Kondorosi E., Silhavy D.(2013). The late steps of plant nonsense-mediated mRNA decay. Plant J. 73: 50–62. PubMed
Merchante C., Brumos J., Yun J., Hu Q., Spencer K.R., Enríquez P., Binder B.M., Heber S., Stepanova A.N., Alonso J.M.(2015). Gene-specific translation regulation mediated by the hormone-signaling molecule EIN2. Cell 163: 684–697. PubMed
Metzstein M.M., Krasnow M.A.(2006). Functions of the nonsense-mediated mRNA decay pathway in Drosophila development. PLoS Genet. 2: e180. PubMed PMC
Mi H., Huang X., Muruganujan A., Tang H., Mills C., Kang D., Thomas P.D.(2017). PANTHER version 11: Expanded annotation data from Gene Ontology and reactome pathways, and data analysis tool enhancements. Nucleic Acids Res. 45: D183–D189. PubMed PMC
Mustroph A., Juntawong P., Bailey-Serres J.(2009). Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods. Methods Mol. Biol. 553: 109–126. PubMed
Nagarajan V.K., Kukulich P.M., von Hagel B., Green P.J.(2019). RNA degradomes reveal substrates and importance for dark and nitrogen stress responses of Arabidopsis XRN4. Nucleic Acids Res. 47: 9216–9230. PubMed PMC
Nelson J.O., Förster D., Frizzell K.A., Luschnig S., Metzstein M.M.(2018). Multiple nonsense-mediated mRNA processes require Smg5 in Drosophila. Genetics 209: 1073–1084. PubMed PMC
Nelson J.O., Moore K.A., Chapin A., Hollien J., Metzstein M.M.(2016). Degradation of Gadd45 mRNA by nonsense-mediated decay is essential for viability. eLife 5: e12876. PubMed PMC
Nicholson P., Gkratsou A., Josi C., Colombo M., Mühlemann O.(2018). Dissecting the functions of SMG5, SMG7, and PNRC2 in nonsense-mediated mRNA decay of human cells. RNA 24: 557–573. PubMed PMC
Peltz S.W., Brown A.H., Jacobson A.(1993). mRNA destabilization triggered by premature translational termination depends on at least three cis-acting sequence elements and one trans-acting factor. Genes Dev. 7: 1737–1754. PubMed
Pertea M., Pertea G.M., Antonescu C.M., Chang T.C., Mendell J.T., Salzberg S.L.(2015). StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33: 290–295. PubMed PMC
Raxwal V.K., Riha K.(2016). Nonsense mediated RNA decay and evolutionary capacitance. Biochim. Biophys. Acta 1859: 1538–1543. PubMed
Rayson S., Arciga-Reyes L., Wootton L., De Torres Zabala M., Truman W., Graham N., Grant M., Davies B.(2012). A role for nonsense-mediated mRNA decay in plants: Pathogen responses are induced in Arabidopsis thaliana NMD mutants. PLoS One 7: e31917. PubMed PMC
Riehs N., Akimcheva S., Puizina J., Bulankova P., Idol R.A., Siroky J., Schleiffer A., Schweizer D., Shippen D.E., Riha K.(2008). Arabidopsis SMG7 protein is required for exit from meiosis. J. Cell Sci. 121: 2208–2216. PubMed
Riehs-Kearnan N., Gloggnitzer J., Dekrout B., Jonak C., Riha K.(2012). Aberrant growth and lethality of Arabidopsis deficient in nonsense-mediated RNA decay factors is caused by autoimmune-like response. Nucleic Acids Res. 40: 5615–5624. PubMed PMC
Risso D., Ngai J., Speed T.P., Dudoit S.(2014). Normalization of RNA-seq data using factor analysis of control genes or samples. Nat. Biotechnol. 32: 896–902. PubMed PMC
Serdar L.D., Whiteside D.L., Baker K.E.(2016). ATP hydrolysis by UPF1 is required for efficient translation termination at premature stop codons. Nat. Commun. 7: 14021. PubMed PMC
Simpson C.G., Fuller J., Maronova M., Kalyna M., Davidson D., McNicol J., Barta A., Brown J.W.(2008). Monitoring changes in alternative precursor messenger RNA splicing in multiple gene transcripts. Plant J. 53: 1035–1048. PubMed
Singh A.K., Choudhury S.R., De S., Zhang J., Kissane S., Dwivedi V., Ramanathan P., Petric M., Orsini L., Hebenstreit D., Brogna S.(2019). The RNA helicase UPF1 associates with mRNAs co-transcriptionally and is required for the release of mRNAs from gene loci. eLife 8: e41444. PubMed PMC
Singh G., Rebbapragada I., Lykke-Andersen J.(2008). A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol. 6: e111. PubMed PMC
Sorenson R.S., Deshotel M.J., Johnson K., Adler F.R., Sieburth L.E.(2018). Arabidopsis mRNA decay landscape arises from specialized RNA decay substrates, decapping-mediated feedback, and redundancy. Proc. Natl. Acad. Sci. USA 115: E1485–E1494. PubMed PMC
Sulkowska A., Auber A., Sikorski P.J., Silhavy D., Auth M., Sitkiewicz E., Jean V., Merret R., Bousquet-Antonelli C., Kufel J.(2020). RNA helicases from the DEA(D/H)-box family contribute to plant NMD efficiency. Plant Cell Physiol.. 61: 144–157. PubMed
Trapnell C., Roberts A., Goff L., Pertea G., Kim D., Kelley D.R., Pimentel H., Salzberg S.L., Rinn J.L., Pachter L.(2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7: 562–578. PubMed PMC
Unterholzner L., Izaurralde E.(2004). SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell 16: 587–596. PubMed
Wickham H.(2009). Ggplot2: Elegant Graphics for Data Analysis. (Cham, Switzerland: Springer; ).
Wittkopp N., Huntzinger E., Weiler C., Saulière J., Schmidt S., Sonawane M., Izaurralde E.(2009). Nonsense-mediated mRNA decay effectors are essential for zebrafish embryonic development and survival. Mol. Cell. Biol. 29: 3517–3528. PubMed PMC
Yoine M., Nishii T., Nakamura K.(2006). Arabidopsis UPF1 RNA helicase for nonsense-mediated mRNA decay is involved in seed size control and is essential for growth. Plant Cell Physiol. 47: 572–580. PubMed
Yu X., Willmann M.R., Anderson S.J., Gregory B.D.(2016). Genome-wide mapping of uncapped and cleaved transcripts reveals a role for the nuclear mRNA cap-binding complex in cotranslational RNA decay in Arabidopsis. Plant Cell 28: 2385–2397. PubMed PMC
Zhang R., et al. (2017). A high quality Arabidopsis transcriptome for accurate transcript-level analysis of alternative splicing. Nucleic Acids Res. 45: 5061–5073. PubMed PMC
Zhang W., Murphy C., Sieburth L.E.(2010). Conserved RNaseII domain protein functions in cytoplasmic mRNA decay and suppresses Arabidopsis decapping mutant phenotypes. Proc. Natl. Acad. Sci. USA 107: 15981–15985. PubMed PMC
Zünd D., Gruber A.R., Zavolan M., Mühlemann O.(2013). Translation-dependent displacement of UPF1 from coding sequences causes its enrichment in 3′ UTRs. Nat. Struct. Mol. Biol. 20: 936–943. PubMed
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