Abstract
Main conclusion
Nonsense-mediated mRNA decay in eukaryotes is vital to cellular homeostasis. Further knowledge of its putative role in plant RNA metabolism under stress is pivotal to developing fitness-optimizing strategies.
Abstract
Nonsense-mediated mRNA decay (NMD), part of the mRNA surveillance pathway, is an evolutionarily conserved form of gene regulation in all living organisms. Degradation of mRNA-bearing premature termination codons and regulation of physiological RNA levels highlight NMD’s role in shaping the cellular transcriptome. Initially regarded as purely a tool for cellular RNA quality control, NMD is now considered to mediate various aspects of plant developmental processes and responses to environmental changes. Here we offer a basic understanding of NMD in eukaryotes by explaining the concept of premature termination codon recognition and NMD complex formation. We also provide a detailed overview of the NMD mechanism and its role in gene regulation. The potential role of effectors, including ABCE1, in ribosome recycling during the translation process is also explained. Recent reports of alternatively spliced variants of corresponding genes targeted by NMD in Arabidopsis thaliana are provided in tabular format. Detailed figures are also provided to clarify the NMD concept in plants. In particular, accumulating evidence shows that NMD can serve as a novel alternative strategy for genetic manipulation and can help design RNA-based therapies to combat stress in plants. A key point of emphasis is its function as a gene regulatory mechanism as well as its dynamic regulation by environmental and developmental factors. Overall, a detailed molecular understanding of the NMD mechanism can lead to further diverse applications, such as improving cellular homeostasis in living organisms.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analysed during this study are included in this published article.
Abbreviations
- ABCE1:
-
ATP binding cassette E1
- AS:
-
Alternative splicing
- CBC:
-
Cap-binding complex
- eIF:
-
Eukaryotic translation initiation factor
- EJC:
-
Exon-junction complex
- IR:
-
Intron retention
- NMD:
-
Nonsense-mediated mRNA decay
- P-body:
-
Processing body
- PTC:
-
Premature termination codon
- SR:
-
Serine–arginine
- SURF:
-
SMG1–UPF1–eRF
- UPF:
-
Up-frameshift protein
References
Ajamian L, Abel K, Rao S, Vyboh K, García-de-Gracia F, Soto-Rifo R, Kulozik AE, Gehring NH, Mouland AJ (2015) HIV-1 recruits UPF1 but excludes UPF2 to promote nucleocytoplasmic export of the genomic RNA. Biomolecules 5(4):2808–2839. https://doi.org/10.3390/biom5042808
Annibaldis G, Domanski M, Dreos R, Contu L, Carl S, Kläy N, Mühlemann O (2020) Readthrough of stop codons under limiting ABCE1 concentration involves frameshifting and inhibits nonsense-mediated mRNA decay. Nucleic Acids Res 48(18):10259–10279. https://doi.org/10.1093/nar/gkaa758
Ashton-Beaucage D, Udell CM, Lavoie H, Baril C, Lefrançois M, Chagnon P, Gendron P, Caron-Lizotte O, Bonneil É, Thibault P (2010) The exon junction complex controls the splicing of MAPK and other long intron-containing transcripts in Drosophila. Cell 143(2):251–262. https://doi.org/10.1016/j.cell.2010.09.014
Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet 2(7):e106. https://doi.org/10.1371/journal.pgen.0020106
Balistreri G, Bognanni C, Mühlemann O (2017) Virus escape and manipulation of cellular nonsense-mediated mRNA decay. Viruses 9(1):24. https://doi.org/10.3390/v9010024
Belgrader P, Cheng J, Zhou X, Stephenson LS, Maquat LE (1994) Mammalian nonsense codons can be cis effectors of nuclear mRNA half-life. Mol Cell Biol 14(12):8219–8228. https://doi.org/10.1128/mcb.14.12.8219-8228.1994
Buchwald G, Ebert J, Basquin C, Sauliere J, Jayachandran U, Bono F, Le Hir H, Conti E (2010) Insights into the recruitment of the NMD machinery from the crystal structure of a core EJC-UPF3b complex. Proc Natl Acad Sci USA 107(22):10050–10055. https://doi.org/10.1073/pnas.1000993107
Bühler M, Steiner S, Mohn F, Paillusson A, Mühlemann O (2006) EJC-independent degradation of nonsense immunoglobulin-μ mRNA depends on 3′ UTR length. Nat Struct Mol Biol 13(5):462–464. https://doi.org/10.1038/nsmb1081
Calixto CP, Guo W, James AB, Tzioutziou NA, Entizne JC, Panter PE, Knight H, Nimmo HG, Zhang R, Brown JW (2018) Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome. Plant Cell 30(7):1424–1444. https://doi.org/10.1105/tpc.18.00177
Celik A, Kervestin S, Jacobson A (2015) NMD: at the crossroads between translation termination and ribosome recycling. Biochimie 114:2–9. https://doi.org/10.1016/j.biochi.2014.10.027
Cesari S (2018) Multiple strategies for pathogen perception by plant immune receptors. New Phytol 219(1):17–24. https://doi.org/10.1111/nph.14877
Chakrabarti S, Jayachandran U, Bonneau F, Fiorini F, Basquin C, Domcke S, Le Hir H, Conti E (2011) Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. Mol Cell 41(6):693–703. https://doi.org/10.1016/j.molcel.2011.02.010
Chamieh H, Ballut L, Bonneau F, Le Hir H (2008) NMD factors UPF2 and UPF3 bridge UPF1 to the exon junction complex and stimulate its RNA helicase activity. Nat Struct Mol Biol 15(1):85–93. https://doi.org/10.1038/nsmb1330
Chaudhary S, Khokhar W, Jabre I, Reddy AS, Byrne LJ, Wilson CM, Syed NH (2019) Alternative splicing and protein diversity: plants versus animals. Front Plant Sci 10:708. https://doi.org/10.3389/fpls.2019.00708
Chazal P-E, Daguenet E, Wendling C, Ulryck N, Tomasetto C, Sargueil B, Le Hir H (2013) EJC core component MLN51 interacts with eIF3 and activates translation. Proc Natl Acad Sci USA 110(15):5903–5908. https://doi.org/10.1073/pnas.121873211
Cheng J, Maquat LE (1993) Nonsense codons can reduce the abundance of nuclear mRNA without affecting the abundance of pre-mRNA or the half-life of cytoplasmic mRNA. Mol Cell Biol 13(3):1892–1902. https://doi.org/10.1128/mcb.13.3.1892-1902.1993
Chiba Y, Green PJ (2009) mRNA degradation machinery in plants. J Plant Biol 52:114–124. https://doi.org/10.1007/s12374-009-9021-2
Choe J, Oh N, Park S, Lee YK, Song O-K, Locker N, Chi S-G, Kim YK (2012) Translation initiation on mRNAs bound by nuclear cap-binding protein complex CBP80/20 requires interaction between CBP80/20-dependent translation initiation factor and eukaryotic translation initiation factor 3g. J Biol Chem 287(22):18500–18509. https://doi.org/10.1074/jbc.M111.327528
Choe J, Ahn SH, Kim YK (2014) The mRNP remodeling mediated by UPF1 promotes rapid degradation of replication-dependent histone mRNA. Nucleic Acids Res 42(14):9334–9349. https://doi.org/10.1093/nar/gku610
Cruz TM, Carvalho RF, Richardson DN, Duque P (2014) Abscisic acid (ABA) regulation of Arabidopsis SR protein gene expression. Int J Mol Sci 15(10):17541–17564. https://doi.org/10.3390/ijms151017541
Cymerman M, Saul H, Farhi R, Vexler K, Gottlieb D, Berezin I, Shaul O (2022) Plant transcripts with long or structured uORFs in NDL2 5’UTR can escape NMD in a reinitiation independent manner. J Exp Bot 74(1):91–103. https://doi.org/10.1093/jxb/erac385
Dai Y, Li W, An L (2016) NMD mechanism and the functions of Upf proteins in plant. Plant Cell Rep 35:5–15. https://doi.org/10.1007/s00299-015-1867-9
Desai A, Hu Z, French CE, Lloyd JP, Brenner SE (2020) Networks of splice factor regulation by unproductive splicing coupled with nonsense mediated mRNA decay. bioRxiv:2020.2005. 2020.107375. https://doi.org/10.1101/2020.05.20.107375
Diem MD, Chan CC, Younis I, Dreyfuss G (2007) PYM binds the cytoplasmic exon-junction complex and ribosomes to enhance translation of spliced mRNAs. Nat Struct Mol Biol 14(12):1173–1179. https://doi.org/10.1038/nsmb1321
Dostie J, Dreyfuss G (2002) Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr Biol 12(13):1060–1067. https://doi.org/10.1016/S0960-9822(02)00902-8
Drechsel G, Kahles A, Kesarwani AK, 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(10):3726–3742. https://doi.org/10.1105/tpc.113.115485
Durand S, Franks TM, Lykke-Andersen J (2016) Hyperphosphorylation amplifies UPF1 activity to resolve stalls in nonsense-mediated mRNA decay. Nat Commun 7(1):12434. https://doi.org/10.1038/ncomms12434
Dzikiewicz-Krawczyk A, Piontek P, Szweykowska-Kulińska Z, Jarmołowski A (2008) The nuclear cap-binding protein complex is not essential for nonsense-mediated mRNA decay (NMD) in plants. Acta Biochim Polonica 55(4):825–828. https://doi.org/10.18388/abp.2008_3047
Feng Q, Jagannathan S, Bradley RK (2017) The RNA surveillance factor UPF1 represses myogenesis via its E3 ubiquitin ligase activity. Mol Cell 67(2):239-251.e6. https://doi.org/10.1016/j.molcel.2017.05.034
Filichkin SA, Hamilton M, Dharmawardhana PD, Singh SK, Sullivan C, Ben-Hur A, Reddy AS, Jaiswal P (2018) Abiotic stresses modulate landscape of poplar transcriptome via alternative splicing, differential intron retention, and isoform ratio switching. Front Plant Sci 9:5. https://doi.org/10.3389/fpls.2018.00005
Fiorini F, Robin J-P, Kanaan J, Borowiak M, Croquette V, Le Hir H, Jalinot P, Mocquet V (2018) HTLV-1 Tax plugs and freezes UPF1 helicase leading to nonsense-mediated mRNA decay inhibition. Nat Commun 9(1):431. https://doi.org/10.1038/s41467-017-02793-6
Franks TM, Singh G, Lykke-Andersen J (2010) Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense-mediated mRNA decay. Cell 143(6):938–950. https://doi.org/10.1016/j.cell.2010.11.043
Garcia D, Garcia S, Voinnet O (2014) Nonsense-mediated decay serves as a general viral restriction mechanism in plants. Cell Host Microbe 16(3):391–402. https://doi.org/10.1016/j.chom.2014.08.001
Gatfield D, Unterholzner L, Ciccarelli FD, Bork P, Izaurralde E (2003) Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. EMBO J22(15):3960–3970. https://doi.org/10.1093/emboj/cdg371
Green RE, Lewis BP, Hillman RT, Blanchette M, Lareau LF, Garnett AT, Rio DC, Brenner SE (2003) Widespread predicted nonsense-mediated mRNA decay of alternatively-spliced transcripts of human normal and disease genes. Bioinformatics 19(suppl_1):i118–i121. https://doi.org/10.1093/bioinformatics/btg1015
Halstead JM, Lionnet T, Wilbertz JH, Wippich F, Ephrussi A, Singer RH, Chao JA (2015) An RNA biosensor for imaging the first round of translation from single cells to living animals. Science 347(6228):1367–1671. https://doi.org/10.1126/science.aaa3380
Hamid FM, Makeyev EV (2014) Emerging functions of alternative splicing coupled with nonsense-mediated decay. Biochem Soc Trans 42(4):1168–1173. https://doi.org/10.1042/BST20140066
He F, Brown AH, Jacobson A (1997) Upf1p, Nmd2p, and Upf3p are interacting components of the yeast nonsense-mediated mRNA decay pathway. Mol Cell Biol 17(3):1580–1594. https://doi.org/10.1128/MCB.17.3.1580
Hellen CU (2018) Translation termination and ribosome recycling in eukaryotes. Cold Spring Harb Perspect Biol 10(10):a032656. https://doi.org/10.1101/cshperspect.a032656
Hodgkin J, Papp A, Pulak R, Ambros V, Anderson P (1989) A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics 123(2):301–313. https://doi.org/10.1093/genetics/123.2.301
Hoek TA, Khuperkar D, Lindeboom RG, Sonneveld S, Verhagen BM, Boersma S, Vermeulen M, Tanenbaum ME (2019) Single-molecule imaging uncovers rules governing nonsense-mediated mRNA decay. Mol Cell 75(2):324-339.e311. https://doi.org/10.1016/j.molcel.2019.05.008
Hogg JR, Goff SP (2010) Upf1 senses 3′ UTR length to potentiate mRNA decay. Cell 143(3):379–389. https://doi.org/10.1016/j.cell.2010.10.005
Hori K, Watanabe Y (2007) Context analysis of termination codons in mRNA that are recognized by plant NMD. Plant Cell Physiol 48(7):1072–1078. https://doi.org/10.1093/pcp/pcm075
Hosoda N, Kim YK, Lejeune F, Maquat LE (2005) CBP80 promotes interaction of Upf1 with Upf2 during nonsense-mediated mRNA decay in mammalian cells. Nat Struct Mol Biol 12(10):893–901. https://doi.org/10.1038/nsmb995
Hua J (2013) Modulation of plant immunity by light, circadian rhythm, and temperature. Curr Opin Plant Biol 16(4):406–413. https://doi.org/10.1016/j.pbi.2013.06.017
Hug N, Caceres JF (2014) The RNA helicase DHX34 activates NMD by promoting a transition from the surveillance to the decay-inducing complex. Cell Rep 8(6):1845–1856. https://doi.org/10.1016/j.celrep.2014.08.020
Hug N, Longman D, Cáceres JF (2016) Mechanism and regulation of the nonsense-mediated decay pathway. Nucleic Acids Res 44(4):1483–1495. https://doi.org/10.1093/nar/gkw010
Hurt JA, Robertson AD, Burge CB (2013) Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay. Genome Res 23(10):1636–1650. https://doi.org/10.1101/gr.157354.113
Imamachi N, Salam KA, Suzuki Y, Akimitsu N (2017) A GC-rich sequence feature in the 3′ UTR directs UPF1-dependent mRNA decay in mammalian cells. Genome Res 27(3):407–418. https://doi.org/10.1101/gr.206060.116
Isken O, Kim YK, Hosoda N, Mayeur GL, Hershey JW, Maquat LE (2008) Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133(2):314–327. https://doi.org/10.1016/j.cell.2008.02.030
Jang YH, Park HY, Lee KC, Thu MP, Kim SK, Suh MC, Kang H, Kim JK (2014) A homolog of splicing factor SF1 is essential for development and is involved in the alternative splicing of pre-mRNA in Arabidopsis thaliana. Plant J78:591–603. https://doi.org/10.1111/tpj.12491
Jeong H-J, Kim YJ, Kim SH, Kim Y-H, Lee I-J, Kim YK, Shin JS (2011) Nonsense-mediated mRNA decay factors, UPF1 and UPF3, contribute to plant defense. Plant Cell Physiol 52(12):2147–2156. https://doi.org/10.1093/pcp/pcr144
Joazeiro CA (2017) Ribosomal stalling during translation: providing substrates for ribosome-associated protein quality control. Annu Rev Cell Dev Biol 33:343–368. https://doi.org/10.1146/annurev-cellbio-111315-125249
Kalyna M, Simpson CG, Syed NH, Lewandowska D, Marquez Y, Kusenda B, Marshall J, Fuller J, Cardle L, McNicol J (2012) Alternative splicing and nonsense-mediated decay modulate expression of important regulatory genes in Arabidopsis. Nucleic Acids Res 40(6):2454–2469. https://doi.org/10.1093/nar/gkr932
Karousis ED, Gurzeler L-A, Annibaldis G, Dreos R, Mühlemann O (2020) Human NMD ensues independently of stable ribosome stalling. Nat Commun 11(1):4134. https://doi.org/10.1038/s41467-020-17974-z
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(3):355–367. https://doi.org/10.1101/gad.1389006
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 J27(11):1585–1595. https://doi.org/10.1038/emboj.2008.88
Kerenyi F, Wawer I, Sikorski PJ, Kufel J, Silhavy D (2013) Phosphorylation of the N-and C-terminal UPF 1 domains plays a critical role in plant nonsense-mediated m RNA decay. Plant J 76(5):836–848. https://doi.org/10.1111/tpj.12346
Kertesz S, Kerenyi Z, Merai Z, Bartos I, Palfy 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(21):6147–6157. https://doi.org/10.1093/nar/gkl737
Kervestin S, Jacobson A (2012) NMD: a multifaceted response to premature translational termination. Nat Rev Mol Cell Biol 13(11):700–712. https://doi.org/10.1038/nrm3454
Kim YK, Maquat LE (2019) UPFront and center in RNA decay: UPF1 in nonsense-mediated mRNA decay and beyond. RNA 25(4):407–422. https://doi.org/10.1261/rna.070136.118
Kim VN, Kataoka N, Dreyfuss G (2001) Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon junction complex. Science 293(5536):1832–1836. https://doi.org/10.1126/science.1062829
Kim YK, Furic L, DesGroseillers L, Maquat LE (2005) Mammalian Staufen1 recruits Upf1 to specific mRNA 3′ UTRs so as to elicit mRNA decay. Cell 120(2):195–208. https://doi.org/10.1016/j.cell.2004.11.050
Kugler W, Enssle J, Hentze MW, Kulozik AE (1995) Nuclear degradation of nonsense mutated β-globin mRNA: a post-transcriptional mechanism to protect heterozygotes from severe clinical manifestations of β-thalassemia? Nucleic Acids Res 23(3):413–418. https://doi.org/10.1093/nar/23.3.413
Kumar V, Singh T (2021) Genome recoding: a review of basic concepts, current research and future prospects of virus attenuation for controlling plant viral diseases. J Plant Biochem Biotechnol 30:221–232. https://doi.org/10.1007/s13562-020-00583-8
Kurosaki T, Li W, Hoque M, Popp MW-L, Ermolenko DN, Tian B, Maquat LE (2014) A post-translational regulatory switch on UPF1 controls targeted mRNA degradation. Genes Dev 28(17):1900–1916. https://doi.org/10.1093/nar/23.3.413
Kurosaki T, Hoque M, Maquat LE (2018) Identifying cellular nonsense-mediated mRNA decay (NMD) targets: immunoprecipitation of phosphorylated UPF1 followed by RNA sequencing (p-UPF1 RIP−Seq). Methods Mol Biol 1720:175–186. https://doi.org/10.1007/978-1-4939-7540-2_13
Kurosaki T, Popp MW, Maquat LE (2019) Quality and quantity control of gene expression by nonsense-mediated mRNA decay. Nat Rev Mol Cell Biol 20(7):406–420. https://doi.org/10.1038/s41580-019-0126-2
Laloum T, Martín G, Duque P (2018) Alternative splicing control of abiotic stress responses. Trends Plant Sci 23(2):140–150. https://doi.org/10.1016/j.tplants.2017.09.019
Le Hir H, Izaurralde E, Maquat LE, Moore MJ (2000) The spliceosome deposits multiple proteins 20–24 nucleotides upstream of mRNA exon–exon junctions. EMBO J 19(24):6860–6869. https://doi.org/10.1093/emboj/19.24.6860
Le Hir H, Gatfield D, Izaurralde E, Moore MJ (2001) The exon–exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J20(17):4987–4997. https://doi.org/10.1093/emboj/20.17.4987
Lee SR, Pratt GA, Martinez FJ, Yeo GW, Lykke-Andersen J (2015) Target discrimination in nonsense-mediated mRNA decay requires Upf1 ATPase activity. Mol Cell 59(3):413–425. https://doi.org/10.1016/j.molcel.2015.06.036
Lejeune F, Li X, Maquat LE (2003) Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol Cell 12(3):675–687. https://doi.org/10.1016/s1097-2765(03)00349-6
Lewis BP, Green RE, Brenner SE (2003) Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc Natl Acad Sci USA 100(1):189–192. https://doi.org/10.1073/pnas.013677010
Liu C, Karam R, Zhou Y, Su F, Ji Y, Li G, Xu G, Lu L, Wang C, Song M, Zhu J, Wang Y, Zhao Y, Foo W, Zou M, Valasek M, Javle M, WilkinsonM LuY (2014) The UPF1 RNA surveillance gene is commonly mutated in pancreatic adenosquamous carcinoma. Nat Med 20(6):596–598. https://doi.org/10.1038/nm.3548
Lykke-Andersen J, Shu M-D, Steitz JA (2000) Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103(7):1121–1131. https://doi.org/10.1016/s0092-8674(00)00214-2
Mabin JW, Woodward LA, Patton RD, Yi Z, Jia M, Wysocki VH, Bundschuh R, Singh G (2018) The exon junction complex undergoes a compositional switch that alters mRNP structure and nonsense-mediated mRNA decay activity. Cell Rep 25(9):2431-2446.e2437. https://doi.org/10.1016/j.celrep.2018.11.046
Mandadi KK, Scholthof K-BG (2015) Genome-wide analysis of alternative splicing landscapes modulated during plant-virus interactions in Brachypodium distachyon. Plant Cell 27(1):71–85. https://doi.org/10.1105/tpc.114.133991
Maquat LE, Carmichael GG (2001) Quality control of mRNA function. Cell 104(2):173–176. https://doi.org/10.1016/S0092-8674(01)00202-1
Maquat LE, Tarn W-Y, Isken O (2010) The pioneer round of translation: features and functions. Cell 142(3):368–374. https://doi.org/10.1016/j.cell.2010.07.022
Matsuda D, Hosoda N, Kim YK, Maquat LE (2007) Failsafe nonsense-mediated mRNA decay does not detectably target eIF4E-bound mRNA. Nat Struct Mol Biol 14(10):974–979. https://doi.org/10.1038/nsmb1297
May JP, Yuan X, Sawicki E, Simon AE (2018) RNA virus evasion of nonsense-mediated decay. PLoS Pathog 14(11):e1007459. https://doi.org/10.1371/journal.ppat.1007459
May JP, Johnson PZ, Ilyas M, Gao F, Simon AE (2020) The multifunctional long-distance movement protein of Pea enation mosaic virus 2 protects viral and host transcripts from nonsense-mediated decay. Mbio 11(2):e00204-e220. https://doi.org/10.1128/mbio.00204-20
Mendell JT, Medghalchi SM, Lake RG, Noensie EN, Dietz HC (2000) Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol Cell Biol 20(23):8944–8957. https://doi.org/10.1128/MCB.20.23.8944-8957.2000
Mendell JT, Sharifi NA, Meyers JL, Martinez-Murillo F, Dietz HC (2004) Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat Genet 36(10):1073–1078. https://doi.org/10.1038/ng1429
Mérai Z, Benkovics AH, Nyikó T, Debreczeny M, Hiripi L, Kerényi Z, Kondorosi É, Silhavy D (2013) The late steps of plant nonsense-mediated mRNA decay. Plant J 73(1):50–62. https://doi.org/10.1111/tpj.12015
Meriin AB, Narayanan A, Meng L, Alexandrov I, Varelas X, Cissé II, Sherman MY (2018) Hsp70–Bag3 complex is a hub for proteotoxicity-induced signaling that controls protein aggregation. Proc Natl Acad Sci USA 115(30):E7043–E7052. https://doi.org/10.1073/pnas.1803130115
Mocquet V, Durand S, Jalinot P (2015) How retroviruses escape the nonsense-mediated mRNA decay. AIDS Res Hum Retrovir 31(10):948–958. https://doi.org/10.1089/aid.2014.0326
Mufarrege EF, Gonzalez DH, Curi GC (2011) Functional interconnections of Arabidopsis exon junction complex proteins and genes at multiple steps of gene expression. J Exp Bot 62(14):5025–5036. https://doi.org/10.1093/jxb/err202
Nagarajan VK, Kukulich PM, von Hagel B, Green PJ (2019) RNA degradomes reveal substrates and importance for dark and nitrogen stress responses of Arabidopsis XRN4. Nucleic Acids Res 47(17):9216–9230. https://doi.org/10.1093/nar/gkz712
Nagy E, Maquat LE (1998) A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem Sci 23(6):198–199. https://doi.org/10.1016/S0968-0004(98)01208-0
Neumann A, Meinke S, Goldammer G, Strauch M, Schubert D, Timmermann B, Heyd F, Preußner M (2020) Alternative splicing coupled mRNA decay shapes the temperature-dependent transcriptome. EMBO Rep 21(12):e51369. https://doi.org/10.15252/embr.202051369
Neu-Yilik G, Raimondeau E, Eliseev B, Yeramala L, Amthor B, Deniaud A, Huard K, Kerschgens K, Hentze MW, Schaffitzel C (2017) Dual function of UPF3B in early and late translation termination. EMBO J 36(20):2968–2986. https://doi.org/10.15252/embj.201797079
Nyikó T, Sonkoly B, Mérai Z, Benkovics AH, Silhavy D (2009) Plant upstream ORFs can trigger nonsense-mediated mRNA decay in a size-dependent manner. Plant Mol Biol 71:367–378. https://doi.org/10.1007/s11103-009-9528-4
Nyikó T, Kerenyi F, Szabadkai L, Benkovics AH, Major P, Sonkoly B, Merai Z, Barta E, Niemiec E, Kufel J (2013) Plant nonsense-mediated mRNA decay is controlled by different autoregulatory circuits and can be induced by an EJC-like complex. Nucleic Acids Res 41(13):6715–6728. https://doi.org/10.1093/nar/gkt366
Ohnishi T, Yamashita A, Kashima I, Schell T, Anders KR, Grimson A, Hachiya T, Hentze MW, Anderson P, Ohno S (2003) Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol Cell 12(5):1187–1200. https://doi.org/10.1016/s1097-2765(03)00443-x
Ohtani M, Wachter A (2019) NMD-based gene regulation—a strategy for fitness enhancement in plants? Plant Cell Physiol 60(9):1953–1960. https://doi.org/10.1093/pcp/pcz090
Okada-Katsuhata Y, Yamashita A, Kutsuzawa K, Izumi N, Hirahara F, Ohno S (2012) N-and C-terminal Upf1 phosphorylations create binding platforms for SMG-6 and SMG-5: SMG-7 during NMD. Nucleic Acids Res 40(3):1251–1266. https://doi.org/10.1093/nar/gkr791
Park Y, Park J, Hwang HJ, Kim B, Jeong K, Chang J, Lee J-B, Kim YK (2020) Nonsense-mediated mRNA decay factor UPF1 promotes aggresome formation. Nat Commun 11(1):3106. https://doi.org/10.1038/s41467-020-16939-6
Peccarelli M, Kebaara BW (2014) Regulation of natural mRNAs by the nonsense-mediated mRNA decay pathway. Eukaryot Cell 13(9):1126–1135. https://doi.org/10.1128/ec.00090-14
Pervouchine D, Popov Y, Berry A, Borsari B, Frankish A, Guigó R (2019) Integrative transcriptomic analysis suggests new autoregulatory splicing events coupled with nonsense-mediated mRNA decay. Nucleic Acids Res 47(10):5293–5306. https://doi.org/10.1093/nar/gkz193
Pisarev AV, Skabkin MA, Pisareva VP, Skabkina OV, Rakotondrafara AM, Hentze MW, Hellen CU, Pestova TV (2010) The role of ABCE1 in eukaryotic posttermination ribosomal recycling. Mol Cell 37(2):196–210. https://doi.org/10.1016/j.molcel.2009.12.034
Popp MW-L, Maquat LE (2013) Organizing principles of mammalian nonsense-mediated mRNA decay. Annu Rev Genet 47:139–165. https://doi.org/10.1146/annurev-genet-111212-133424
Popp MW-L, Maquat LE (2014) The dharma of nonsense-mediated mRNA decay in mammalian cells. Mol Cells 37(1):1–8. https://doi.org/10.14348/molcells.2014.2193
Popp MW, Maquat LE (2015) A TRICK’n way to see the pioneer round of translation. Science 347(6228):1316–1317. https://doi.org/10.1126/science.aaa9484
Popp MW, Maquat LE (2018) Nonsense-mediated mRNA decay and cancer. Curr Opin Genet Dev 48:44–50. https://doi.org/10.1016/j.gde.2017.10.007
Pulak R, Anderson P (1993) mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev 7(10):1885–1897. https://doi.org/10.1101/gad.7.10.1885
Raxwal VK, Riha K (2016) Nonsense mediated RNA decay and evolutionary capacitance. Biochim Biophys Acta 1859(12):1538–1543. https://doi.org/10.1016/j.bbagrm.2016.09.001
Raxwal VK, Riha K (2023) The biological functions of nonsense-mediated mRNA decay in plants: RNA quality control and beyond. Biochem Soc Trans 51(1):31–39. https://doi.org/10.1042/BST20211231
Raxwal VK, Simpson CG, Gloggnitzer J, Entinze JC, Guo W, Zhang R, Brown JW, Riha K (2020) Nonsense-mediated RNA decay factor UPF1 is critical for posttranscriptional and translational gene regulation in Arabidopsis. Plant Cell 32(9):2725–2741. https://doi.org/10.1105/tpc.20.00244
Roignant J-Y, Treisman JE (2010) Exon junction complex subunits are required to splice Drosophila MAP kinase, a large heterochromatic gene. Cell 143(2):238–250. https://doi.org/10.1016/j.cell.2010.09.036
Ruggiero A, Punzo P, Van Oosten MJ, Cirillo V, Esposito S, Costa A, Maggio A, Grillo S, Batelli G (2022) Transcriptomic and splicing changes underlying tomato responses to combined water and nutrient stress. Front Plant Sci 13:974048. https://doi.org/10.3389/fpls.2022.974048
Sato H, Maquat LE (2009) Remodeling of the pioneer translation initiation complex involves translation and the karyopherin importin β. Genes Dev 23(21):2537–2550. https://doi.org/10.1101/gad.1817109
Saul H, Elharrar E, Gaash R, Eliaz D, Valenci M, Akua T, Avramov M, Frankel N, Berezin I, Gottlieb D (2009) The upstream open reading frame of the Arabidopsis AtMHX gene has a strong impact on transcript accumulation through the nonsense-mediated mRNA decay pathway. Plant J 60(6):1031–1042. https://doi.org/10.1111/j.1365-313X.2009.04021.x
Schmidt U, Richter K, Berger AB, Lichter P (2006) In vivo BiFC analysis of Y14 and NXF1 mRNA export complexes: preferential localization within and around SC35 domains. J Cell Biol 172(3):373–381. https://doi.org/10.1083/jcb.200503061
Schuller AP, Zinshteyn B, Enam SU, Green R (2018) Directed hydroxyl radical probing reveals Upf1 binding to the 80S ribosomal E site rRNA at the L1 stalk. Nucleic Acids Res 46(4):2060–2073. https://doi.org/10.1093/nar/gkx1263
Schweingruber C, Rufener SC, Zünd D, Yamashita A, Mühlemann O (2013) Nonsense-mediated mRNA decay—mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim Biophys Acta 1829(6–7):612–623. https://doi.org/10.1016/j.bbagrm.2013.02.005
Serin G, Gersappe A, Black JD, Aronoff R, Maquat LE (2001) Identification and characterization of human orthologues to Saccharomyces cerevisiae Upf2 protein and Upf3 protein (Caenorhabditis elegans SMG-4). Mol Cell Biol 21(1):209–223. https://doi.org/10.1128/MCB.21.1.209-223.2001
Shi Y, Su Z, Yang H, Wang W, Jin G, He G, Siddique AN, Zhang L, Zhu A, Xue R (2019) Alternative splicing coupled to nonsense-mediated mRNA decay contributes to the high-altitude adaptation of maca (Lepidium meyenii). Gene 694:7–18. https://doi.org/10.1016/j.gene.2018.12.082
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(4):e111. https://doi.org/10.1371/journal.pbio.0060111
Singh G, Kucukural A, Cenik C, Leszyk JD, Shaffer SA, Weng Z, Moore MJ (2012) The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 151(4):750–764. https://doi.org/10.1016/j.cell.2012.10.007
Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12(2):89–100. https://doi.org/10.1038/nri3141
Staiger D, Brown JW (2013) Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell 25(10):3640–3656. https://doi.org/10.1105/tpc.113.113803
Stalder L, Mühlemann O (2009) Processing bodies are not required for mammalian nonsense-mediated mRNA decay. RNA 15(7):1265–1273. https://doi.org/10.1261/rna.1672509
Sureshkumar S, Dent C, Seleznev A, Tasset C, Balasubramanian S (2016) Nonsense-mediated mRNA decay modulates FLM-dependent thermosensory flowering response in Arabidopsis. Nat Plants 2(5):1–7. https://doi.org/10.1038/nplants.2016.55
Sybilska E, Daszkowska-Golec A (2023) Alternative splicing in ABA signaling during seed germination. Front Plant Sci 14:1144990. https://doi.org/10.3389/fpls.2023.1144990
Szakonyi D, Duque P (2018) Alternative splicing as a regulator of early plant development. Front Plant Sci 9:1174. https://doi.org/10.3389/fpls.2018.01174
Tran GVQ, Kleinehr J, Preugschas HF, Anhlan D, Mohamed FF, Ehrhardt C, Ludwig S, Hrincius ER (2021) Nonsense-mediated mRNA decay does not restrict influenza A virus propagation. Cell Microbiol 23(6):e13323. https://doi.org/10.1111/cmi.13323
Trcek T, Sato H, Singer RH, Maquat LE (2013) Temporal and spatial characterization of nonsense-mediated mRNA decay. Genes Dev 27(5):541–551. https://doi.org/10.1101/gad.209635.112
van Gent M, Reich A, Velu SE, Gack MU (2021) Nonsense-mediated decay controls the reactivation of the oncogenic herpesviruses EBV and KSHV. PLoS Biol 19(2):e3001097. https://doi.org/10.1371/journal.pbio.3001097
Wang W, Czaplinski K, Rao Y, Peltz SW (2001) The role of Upf proteins in modulating the translation read-through of nonsense-containing transcripts. EMBO J20(4):880–890. https://doi.org/10.1093/emboj/20.4.880
Wang J, Gudikote JP, Olivas OR, Wilkinson MF (2002) Boundary-independent polar nonsense-mediated decay. EMBO Rep 3(3):274–279. https://doi.org/10.1093/embo-reports/kvf036
Wang Z, Murigneux V, Le Hir H (2014) Transcriptome-wide modulation of splicing by the exon junction complex. Genome Biol 15:1–18. https://doi.org/10.1186/s13059-014-0551-7
Wang J, Liu J, Guo Z (2023) Natural uORF variation in plants. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2023.07.005.10.1016/j.tplants.2023.07.005
Weischenfeldt J, Damgaard I, Bryder D, Theilgaard-Mönch K, Thoren LA, Nielsen FC, Jacobsen SEW, Nerlov C, Porse BT (2008) NMD is essential for hematopoietic stem and progenitor cells and for eliminating by-products of programmed DNA rearrangements. Genes Dev 22(10):1381–1396. https://doi.org/10.1101/gad.468808
Wengrod J, Martin L, Wang D, Frischmeyer-Guerrerio P, Dietz HC, Gardner LB (2013) Inhibition of nonsense-mediated RNA decay activates autophagy. Mol Cell Biol 33(11):2128–2135. https://doi.org/10.1128/MCB.00174-13
Wissink EM, Vihervaara A, Tippens ND, Lis JT (2019) Nascent RNA analyses: tracking transcription and its regulation. Nat Rev Genet 20(12):705–723. https://doi.org/10.1038/s41576-019-0159-6
Woodward LA, Mabin JW, Gangras P, Singh G (2017) The exon junction complex: a life long guardian of mRNA fate. Wiley Interdiscip Rev iRNA 8(3):e1411. https://doi.org/10.1002/wrna.1411
Xu J, Chua N-H (2011) Processing bodies and plant development. Curr Opin Plant Biol 14(1):88–93. https://doi.org/10.1016/j.pbi.2010.10.003
Yamashita A, Ohnishi T, Kashima I, Taya Y, Ohno S (2001) Human SMG-1, a novel phosphatidylinositol 3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsense-mediated mRNA decay. Genes Dev 15(17):2215–2228. https://doi.org/10.1101/gad.913001
Yoine M, Ma O, Onai K, Mita S, Nakamura K (2006) The lba1 mutation of UPF1 RNA helicase involved in nonsense-mediated mRNA decay causes pleiotropic phenotypic changes and altered sugar signalling in Arabidopsis. Plant J 47(1):49–62. https://doi.org/10.1111/j.1365-313X.2006.02771.x
Yu X, Li B, Jang GJ, Jiang S, Jiang D, Jang JC, Wu SH, Shan L, He P (2019) Orchestration of processing body dynamics and mRNA decay in Arabidopsis immunity. Cell Rep 28(8):2194–2205. https://doi.org/10.1016/j.celrep.2019.07.054
Zhang J, Sun X, Qian Y, LaDuca JP, Maquat LE (1998) At least one intron is required for the nonsense-mediated decay of triosephosphate isomerase mRNA: a possible link between nuclear splicing and cytoplasmic translation. Mol Cell Biol 18(9):5272–5283. https://doi.org/10.1128/MCB.18.9.5272
Zhu X, Zhang H, Mendell JT (2020) Ribosome recycling by ABCE1 links lysosomal function and iron homeostasis to 3ʹ UTR-directed regulation and nonsense-mediated decay. Cell Rep 32(2):107895. https://doi.org/10.1016/j.celrep.2020.107895
Acknowledgements
The authors thank the Vice-Chancellor of Central University of Punjab, India for providing support for the present assignment. Varnika Rana acknowledges the SERB for fellowship. The authors also acknowledge the SERB funding agency for financial help under project CRG/2020/000368. All figure contents were created using Biorender.com. AV is an incumbent of the Wolfson Chair in Floriculture.
Author information
Authors and Affiliations
Contributions
VK and AV conceived and designed the study. VK, RL and VR analysed data. RL, VR and VK wrote the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Gerhard Leubner.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Luha, R., Rana, V., Vainstein, A. et al. Nonsense-mediated mRNA decay pathway in plants under stress: general gene regulatory mechanism and advances. Planta 259, 51 (2024). https://doi.org/10.1007/s00425-023-04317-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04317-7