Global transcriptome analysis reveals circadian control of splicing events in Arabidopsis thaliana.
Arabidopsis thaliana
SPF30
alternative splicing
circadian clock
circadian rhythms
splicing factors
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
13
01
2020
revised:
26
03
2020
accepted:
01
04
2020
pubmed:
22
4
2020
medline:
6
3
2021
entrez:
22
4
2020
Statut:
ppublish
Résumé
The circadian clock of Arabidopsis thaliana controls many physiological and molecular processes, allowing plants to anticipate daily changes in their environment. However, developing a detailed understanding of how oscillations in mRNA levels are connected to oscillations in co/post-transcriptional processes, such as splicing, has remained a challenge. Here we applied a combined approach using deep transcriptome sequencing and bioinformatics tools to identify novel circadian-regulated genes and splicing events. Using a stringent approach, we identified 300 intron retention, eight exon skipping, 79 alternative 3' splice site usage, 48 alternative 5' splice site usage, and 350 multiple (more than one event type) annotated events under circadian regulation. We also found seven and 721 novel alternative exonic and intronic events. Depletion of the circadian-regulated splicing factor AtSPF30 homologue resulted in the disruption of a subset of clock-controlled splicing events. Altogether, our global circadian RNA-seq coupled with an in silico, event-centred, splicing analysis tool offers a new approach for studying the interplay between the circadian clock and the splicing machinery at a global scale. The identification of many circadian-regulated splicing events broadens our current understanding of the level of control that the circadian clock has over this co/post-transcriptional regulatory layer.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
889-902Informations de copyright
© 2020 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Agarwal, A., Koppstein, D., Rozowsky, J., Sboner, A., Habegger, L., Hillier, L.W., Sasidharan, R., Reinke, V., Waterston, R.H. and Gerstein, M. (2010) Comparison and calibration of transcriptome data from RNA-Seq and tiling arrays. BMC Genom. 11, 383.
Ameur, A., Zaghlool, A., Halvardson, J., Wetterbom, A., Gyllensten, U., Cavelier, L. and Feuk, L. (2011) Total RNA sequencing reveals nascent transcription and widespread co-transcriptional splicing in the human brain. Nat. Struct. Mol. Biol. 18, 1435-1440.
Bardou, F., Ariel, F., Simpson, C.G., Romero-Barrios, N., Laporte, P., Balzergue, S., Brown, J.W. and Crespi, M. (2014) Long noncoding RNA modulates alternative splicing regulators in Arabidopsis. Dev. Cell, 30, 166-176.
Beckwith, E.J., Hernando, C.E., Polcownuk, S., Bertolin, A.P., Mancini, E., Ceriani, M.F. and Yanovsky, M.J. (2017) Rhythmic behavior is controlled by the SRm160 splicing factor in Drosophila melanogaster. Genetics, 207, 593-607.
Cote, J. and Richard, S. (2005) Tudor domains bind symmetrical dimethylated arginines. J. Biol. Chem. 280, 28 476-28 483.
Covington, M.F., Maloof, J.N., Straume, M., Kay, S.A. and Harmer, S.L. (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 9, R130.
Cui, Z., Xu, Q. and Wang, X. (2014) Regulation of the circadian clock through pre-mRNA splicing in Arabidopsis. J. Exp. Bot. 65, 1973-1980.
De Maio, F.A., Risso, G., Iglesias, N.G. et al. (2016) The dengue virus NS5 protein intrudes in the cellular spliceosome and modulates splicing. PLoS Pathog. 12, e1005841.
Deckard, A., Anafi, R.C., Hogenesch, J.B., Haase, S.B. and Harer, J. (2013) Design and analysis of large-scale biological rhythm studies: a comparison of algorithms for detecting periodic signals in biological data. Bioinformatics, 29, 3174-3180.
Dodd, A.N., Salathia, N., Hall, A., Kevei, E., Toth, R., Nagy, F., Hibberd, J.M., Millar, A.J. and Webb, A.A. (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science, 309, 630-633.
Dunlap, J.C., Loros, J.J. and DeCoursey, P.J. (2004) Chronobiology: Biological Timekeeping. Sunderland, MA: Sinauer Associates.
Fernandez-Pozo, N., Haas, F.B., Meyberg, R. et al. (2019) PEATmoss (Physcomitrella Expression Atlas Tool): a unified gene expression atlas for the model plant Physcomitrella patens. Plant J. 102, 165-177.
Filichkin, S.A., Cumbie, J.S., Dharmawardhana, P., Jaiswal, P., Chang, J.H., Palusa, S.G., Reddy, A.S., Megraw, M. and Mockler, T.C. (2015) Environmental stresses modulate abundance and timing of alternatively spliced circadian transcripts in Arabidopsis. Mol. Plant, 8, 207-227.
Filichkin, S.A., Priest, H.D., Givan, S.A., Shen, R., Bryant, D.W., Fox, S.E., Wong, W.K. and Mockler, T.C. (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res. 20, 45-58.
Freese, N.H., Norris, D.C. and Loraine, A.E. (2016) Integrated genome browser: visual analytics platform for genomics. Bioinformatics, 32, 2089-2095.
Genov, N., Basti, A., Abreu, M., Astaburuaga, R. and Relogio, A. (2019) A bioinformatic analysis identifies circadian expression of splicing factors and time-dependent alternative splicing events in the HD-MY-Z cell line. Sci. Rep. 9, 11 062.
Gouy, M., Guindon, S. and Gascuel, O. (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27, 221-224.
Green, R.M., Tingay, S., Wang, Z.Y. and Tobin, E.M. (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol. 129, 576-584.
Gueroussov, S., Gonatopoulos-Pournatzis, T., Irimia, M., Raj, B., Lin, Z.Y., Gingras, A.C. and Blencowe, B.J. (2015) An alternative splicing event amplifies evolutionary differences between vertebrates. Science, 349, 868-873.
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. and Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321.
Harmer, S.L., Panda, S. and Kay, S.A. (2001) Molecular bases of circadian rhythms. Annu. Rev. Cell Dev. Biol. 17, 215-253.
Hazen, S.P., Naef, F., Quisel, T., Gendron, J.M., Chen, H., Ecker, J.R., Borevitz, J.O. and Kay, S.A. (2009) Exploring the transcriptional landscape of plant circadian rhythms using genome tiling arrays. Genome Biol. 10, R17.
Henriques, R., Wang, H., Liu, J., Boix, M., Huang, L.F. and Chua, N.H. (2017) The antiphasic regulatory module comprising CDF5 and its antisense RNA FLORE links the circadian clock to photoperiodic flowering. New Phytol. 216, 854-867.
Hernando, C.E., Romanowski, A. and Yanovsky, M.J. (2017) Transcriptional and post-transcriptional control of the plant circadian gene regulatory network. Biochim. Biophys. Acta Gene Regul. Mech. 1860, 84-94.
Hong, X., Scofield, D.G. and Lynch, M. (2006) Intron size, abundance, and distribution within untranslated regions of genes. Mol. Biol. Evol. 23, 2392-2404.
Hsu, P.Y. and Harmer, S.L. (2012) Circadian phase has profound effects on differential expression analysis. PLoS ONE, 7, e49853.
Hughes, M.E., DiTacchio, L., Hayes, K.R., Vollmers, C., Pulivarthy, S., Baggs, J.E., Panda, S. and Hogenesch, J.B. (2009) Harmonics of circadian gene transcription in mammals. PLoS Genet. 5, e1000442.
Hughes, M.E., Grant, G.R., Paquin, C., Qian, J. and Nitabach, M.N. (2012) Deep sequencing the circadian and diurnal transcriptome of Drosophila brain. Genome Res. 22, 1266-1281.
Hughes, M.E., Hogenesch, J.B. and Kornacker, K. (2010) JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J. Biol. Rhythms, 25, 372-380.
James, A.B., Syed, N.H., Bordage, S., Marshall, J., Nimmo, G.A., Jenkins, G.I., Herzyk, P., Brown, J.W. and Nimmo, H.G. (2012a) Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell, 24, 961-981.
James, A.B., Syed, N.H., Brown, J.W. and Nimmo, H.G. (2012b) Thermoplasticity in the plant circadian clock: how plants tell the time-perature. Plant Signal. Behav. 7, 1219-1223.
Jones, M.A., Williams, B.A., McNicol, J., Simpson, C.G., Brown, J.W. and Harmer, S.L. (2012) Mutation of Arabidopsis spliceosomal timekeeper locus1 causes circadian clock defects. Plant Cell, 24, 4066-4082.
Katari, M.S., Nowicki, S.D., Aceituno, F.F. et al. (2010) VirtualPlant: a software platform to support systems biology research. Plant Physiol. 152, 500-515.
Keegan, K.P., Pradhan, S., Wang, J.P. and Allada, R. (2007) Meta-analysis of Drosophila circadian microarray studies identifies a novel set of rhythmically expressed genes. PLoS Comput. Biol. 3, e208.
Khodor, Y.L., Rodriguez, J., Abruzzi, K.C., Tang, C.H., Marr, M.T. 2nd and Rosbash, M. (2011) Nascent-seq indicates widespread cotranscriptional pre-mRNA splicing in Drosophila. Genes Dev. 25, 2502-2512.
Kolesnikov, N., Hastings, E., Keays, M. et al. (2015) ArrayExpress update-simplifying data submissions. Nucleic Acids Res. 43, D1113-1116.
Kornblihtt, A.R., Schor, I.E., Allo, M., Dujardin, G., Petrillo, E. and Munoz, M.J. (2013) Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat. Rev. Mol. Cell Biol. 14, 153-165.
Kroiss, M., Schultz, J., Wiesner, J., Chari, A., Sickmann, A. and Fischer, U. (2008) Evolution of an RNP assembly system: a minimal SMN complex facilitates formation of UsnRNPs in Drosophila melanogaster. Proc. Natl Acad. Sci. USA, 105, 10 045-10 050.
Kwon, Y.J., Park, M.J., Kim, S.G., Baldwin, I.T. and 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.
Le, S.Q. and Gascuel, O. (2008) An improved general amino acid replacement matrix. Mol. Biol. Evol. 25, 1307-1320.
Li, S., Wang, Y., Zhao, Y., Zhao, X., Chen, X. and Gong, Z. (2020) Global Co-transcriptional splicing in Arabidopsis and the correlation with splicing regulation in mature RNAs. Mol. Plant, 13, 266-277.
Liu, K., Guo, Y., Liu, H. et al. (2012) Crystal structure of TDRD3 and methyl-arginine binding characterization of TDRD3, SMN and SPF30. PLoS ONE, 7, e30375.
Mancini, E., Iserte, J., Yanovsky, M. and Chernomoretz, A. (2019) ASpli: Analysis of alternative splicing using RNA-Seq. R package version 1.8.1. Bioconductor, Release (3.8).
Mancini, E., Sanchez, S.E., Romanowski, A., Schlaen, R.G., Sanchez-Lamas, M., Cerdan, P.D. and Yanovsky, M.J. (2016) Acute effects of light on alternative splicing in light-grown plants. Photochem. Photobiol. 92, 126-133.
Martin, M.L., Lechner, L., Zabaleta, E.J. and Salerno, G.L. (2013) A mitochondrial alkaline/neutral invertase isoform (A/N-InvC) functions in developmental energy-demanding processes in Arabidopsis. Planta, 237, 813-822.
Mateos, J.L., de Leone, M.J., Torchio, J., Reichel, M. and Staiger, D. (2018) Beyond transcription: fine-tuning of circadian timekeeping by post-transcriptional regulation. Genes, 9, 616.
McClung, C.R. (2006) Plant circadian rhythms. Plant Cell 18, 792-803.
McClung, C.R. (2014) Wheels within wheels: new transcriptional feedback loops in the Arabidopsis circadian clock. F1000Prime Rep. 6, 2.
Michael, T.P., Mockler, T.C., Breton, G. et al. (2008) Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLoS Genet. 4, e14.
Mier, P. and Perez-Pulido, A.J. (2012) Fungal Smn and Spf30 homologues are mainly present in filamentous fungi and genomes with many introns: implications for spinal muscular atrophy. Gene, 491, 135-141.
Millar, A.J. (2016) The intracellular dynamics of circadian clocks reach for the light of ecology and evolution. Annu. Rev. Plant Biol. 67, 595-618.
Millar, A.J. and Kay, S.A. (1991) Circadian Control of cab gene transcription and mRNA accumulation in Arabidopsis. Plant Cell, 3, 541-550.
Mockler, T.C., Michael, T.P., Priest, H.D., Shen, R., Sullivan, C.M., Givan, S.A., McEntee, C., Kay, S.A. and Chory, J. (2007) The DIURNAL project: DIURNAL and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harb. Symp. Quant. Biol. 72, 353-363.
Oesterreich, F.C., Herzel, L., Straube, K., Hujer, K., Howard, J. and Neugebauer, K.M. (2016) Splicing of Nascent RNA coincides with intron exit from RNA Polymerase II. Cell, 165, 372-381.
Papasaikas, P., Tejedor, J.R., Vigevani, L. and Valcarcel, J. (2015) Functional splicing network reveals extensive regulatory potential of the core spliceosomal machinery. Mol. Cell, 57, 7-22.
Perez-Santangelo, S., Schlaen, R.G. and Yanovsky, M.J. (2013) Genomic analysis reveals novel connections between alternative splicing and circadian regulatory networks. Brief. Funct. Genomics, 12, 13-24.
Pervouchine, D.D., Knowles, D.G. and Guigo, R. (2013) Intron-centric estimation of alternative splicing from RNA-seq data. Bioinformatics, 29, 273-274.
Plautz, J.D., Straume, M., Stanewsky, R., Jamison, C.F., Brandes, C., Dowse, H.B., Hall, J.C. and Kay, S.A. (1997) Quantitative analysis of Drosophila period gene transcription in living animals. J. Biol. Rhythms, 12, 204-217.
Preussner, M., Goldammer, G., Neumann, A., Haltenhof, T., Rautenstrauch, P., Muller-McNicoll, M. and Heyd, F. (2017) Body temperature cycles control rhythmic alternative splicing in mammals. Mol. Cell, 67, 433-446.e4.
Reddy, A.S., Marquez, Y., Kalyna, M. and Barta, A. (2013) Complexity of the alternative splicing landscape in plants. Plant Cell, 25, 3657-3683.
Rehrauer, H., Aquino, C., Gruissem, W. et al. (2010) AGRONOMICS1: a new resource for Arabidopsis transcriptome profiling. Plant Physiol. 152, 487-499.
Ritchie, M.E., Phipson, B., Wu, D., Hu, Y., Law, C.W., Shi, W. and Smyth, G.K. (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47.
Romanowski, A. and Yanovsky, M.J. (2015) Circadian rhythms and post-transcriptional regulation in higher plants. Front. Plant Sci. 6, 437.
Romero-Barrios, N., Legascue, M.F., Benhamed, M., Ariel, F. and Crespi, M. (2018) Splicing regulation by long noncoding RNAs. Nucleic Acids Res. 46, 2169-2184.
Saldi, T., Cortazar, M.A., Sheridan, R.M. and Bentley, D.L. (2016) Coupling of RNA Polymerase II transcription elongation with pre-mRNA splicing. J. Mol. Biol. 428, 2623-2635.
Saltzman, A.L., Pan, Q. and Blencowe, B.J. (2011) Regulation of alternative splicing by the core spliceosomal machinery. Genes Dev. 25, 373-384.
Sanchez, S.E., Petrillo, E., Beckwith, E.J. et al. (2010) A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature, 468, 112-116.
Schlaen, R.G., Mancini, E., Sanchez, S.E., Perez-Santangelo, S., Rugnone, M.L., Simpson, C.G., Brown, J.W., Zhang, X., Chernomoretz, A. and Yanovsky, M.J. (2015) The spliceosome assembly factor GEMIN2 attenuates the effects of temperature on alternative splicing and circadian rhythms. Proc. Natl Acad. Sci. USA, 112, 9382-9387.
Sievers, F., Wilm, A., Dineen, D. et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539.
Staiger, D. and Brown, J.W. (2013) Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell, 25, 3640-3656.
Staiger, D. and Green, R. (2011) RNA-based regulation in the plant circadian clock. Trends Plant Sci. 16, 517-523.
Syed, N.H., Kalyna, M., Marquez, Y., Barta, A. and Brown, J.W. (2012) Alternative splicing in plants-coming of age. Trends Plant Sci. 17, 616-623.
Talbot, K., Miguel-Aliaga, I., Mohaghegh, P., Ponting, C.P. and Davies, K.E. (1998) Characterization of a gene encoding survival motor neuron (SMN)-related protein, a constituent of the spliceosome complex. Hum. Mol. Genet. 7, 2149-2156.
Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
Wang, X., Wu, F., Xie, Q. et al. (2012) SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis. Plant Cell, 24, 3278-3295.
Wichert, S., Fokianos, K. and Strimmer, K. (2004) Identifying periodically expressed transcripts in microarray time series data. Bioinformatics, 20, 5-20.
Wijnen, H., Naef, F. and Young, M.W. (2005) Molecular and statistical tools for circadian transcript profiling. Methods Enzymol. 393, 341-365.
Xin, R., Zhu, L., Salome, P.A., Mancini, E., Marshall, C.M., Harmon, F.G., Yanovsky, M.J., Weigel, D. and Huq, E. (2017) SPF45-related splicing factor for phytochrome signaling promotes photomorphogenesis by regulating pre-mRNA splicing in Arabidopsis. Proc. Natl Acad. Sci. USA, 114, E7018-E7027.
Zhang, R., Calixto, C.P.G., Marquez, Y. et al. (2017) A high quality Arabidopsis transcriptome for accurate transcript-level analysis of alternative splicing. Nucleic Acids Res. 45, 5061-5073.
Zhu, D., Mao, F., Tian, Y., Lin, X., Gu, L., Gu, H., Qu, L.J., Wu, Y. and Wu, Z. (2020) The features and regulation of co-transcriptional splicing in Arabidopsis. Mol. Plant, 13, 278-294.