Abstract
Key message
Maize SWI3-type chromatin remodeler impacts alternative splicing contexts in response to osmotic stress by altering nucleosome density and affecting transcriptional elongation rate.
Abstract
Alternative splicing (AS) is commonly found in higher eukaryotes and is an important posttranscriptional regulatory mechanism to generate transcript diversity. AS has been widely accepted as playing essential roles in different biological processes including growth, development, signal transduction and responses to biotic and abiotic stresses in plants. However, whether and how chromatin remodeling complex functions in AS in plant under osmotic stress remains unknown. Here, we show that a maize SWI3D protein, ZmCHB101, impacts AS contexts in response to osmotic stress. Genome-wide analysis of mRNA contexts in response to osmotic stress using ZmCHB101-RNAi lines reveals that ZmCHB101 impacts alternative splicing contexts of a subset of osmotic stress-responsive genes. Intriguingly, ZmCHB101-mediated regulation of gene expression and AS is largely uncoupled, pointing to diverse molecular functions of ZmCHB101 in transcriptional and posttranscriptional regulation. We further found ZmCHB101 impacts the alternative splicing contexts by influencing alteration of chromatin and histone modification status as well as transcriptional elongation rates mediated by RNA polymerase II. Taken together, our findings suggest a novel insight of how plant chromatin remodeling complex impacts AS under osmotic stress .
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References
Alló M, Schor IE, Muñoz MJ et al (2010) Chromatin and alternative splicing. Cold Spring Harb Symp Quant Biol 75:103–111
Andersson R, Enroth S, Rada-Iglesias A, Wadelius C, Komorowski J (2009) Nucleosomes are well positioned in exons and carry characteristic histone modifications. Genome Res 19:1732–1741
Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet 2:e106
Batsché E, Yaniv M, Muchardt C (2006) The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nat Struct Mol Biol 13:22–29
Becker PB, Hörz W (2002) ATP-dependent nucleosome remodeling. Annu Rev Biochem 71:247–273
Ben Rejeb K, Lefebvre-De Vos D, Le Disquet I et al (2015) Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. New Phytol 208:1138–1148
Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72:291–336
Boudsocq M, Barbier-Brygoo H, Lauriere C (2004) Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J Biol Chem 279:41758–41766
Brown SJ, Stoilov P, Xing Y (2012) Chromatin and epigenetic regulation of pre-mRNA processing. Hum Mol Genet 21:R90–R96
Burckin T, Nagel R, Mandel-Gutfreund Y et al (2005) Exploring functional relationships between components of the gene expression machinery. Nat Struct Mol Biol 12:175–182
Cairns BR (2005) Chromatin remodeling complexes: strength in diversity, precision through specialization. Curr Opin Genet Dev 15:185–190
Cancer Genome Atlas Research N (2013) Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 499:43–49
Carrillo Oesterreich F, Bieberstein N, Neugebauer KM (2011) Pause locally, splice globally. Trends Cell Biol 21:328–335
Churbanov A, Winters-Hilt S, Koonin EV, Rogozin IB (2008) Accumulation of GC donor splice signals in mammals. Biol Direct 3:30
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
de la Mata M, Alonso CR, Kadener S et al (2003) A slow RNA polymerase II affects alternative splicing in vivo. Mol Cell 12:525–532
Dhami P, Saffrey P, Bruce AW et al (2010) Complex exon-intron marking by histone modifications is not determined solely by nucleosome distribution. PLoS One 5:e12339
Dinesh-Kumar SP, Baker BJ (2000) Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. Proc Natl Acad Sci USA 97:1908–1913
Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat Commun 3:740
Ding Y, Liu N, Virlouvet L, Riethoven JJ, Fromm M, Avramova Z (2013) Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol 13:229
Ding F, Cui P, Wang Z, Zhang S, Ali S, Xiong L (2014) Genome-wide analysis of alternative splicing of pre-mRNA under salt stress in Arabidopsis. BMC Genom 15:431
Dujardin G, Lafaille C, de la Mata M et al (2014) How slow RNA polymerase II elongation favors alternative exon skipping. Mol Cell 54:683–690
Egawa C, Kobayashi F, Ishibashi M, Nakamura T, Nakamura C, Takumi S (2006) Differential regulation of transcript accumulation and alternative splicing of a DREB2 homolog under abiotic stress conditions in common wheat. Genes Genet Syst 81:77–91
Estavillo GM, Crisp PA, Pornsiriwong W et al (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012
Feng J, Li J, Gao Z et al (2015) SKIP confers osmotic tolerance during salt stress by controlling alternative gene splicing in Arabidopsis. Mol Plant 8:1038–1052
Filichkin SA, Priest HD, Givan SA et al (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20:45–58
Foissac S, Sammeth M (2007) ASTALAVISTA: dynamic and flexible analysis of alternative splicing events in custom gene datasets. Nucleic Acids Res 35:W297–W299
Hamey JJ, Wilkins MR (2018) Methylation of elongation factor 1A: where, who, and why? Trends Biochem Sci 43:211–223
Han SK, Wu MF, Cui S, Wagner D (2015) Roles and activities of chromatin remodeling ATPases in plants. Plant J 83:62–77
Haring M, Offermann S, Danker T, Horst I, Peterhansel C, Stam M (2007) Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods 3:11
Hartmann L, Pedrotti L, Weiste C et al (2015) Crosstalk between two bZIP signaling pathways orchestrates salt-induced metabolic reprogramming in Arabidopsis roots. Plant Cell 27:2244–2260
Hon G, Wang W, Ren B (2009) Discovery and annotation of functional chromatin signatures in the human genome. PLoS Comput Biol 5:e1000566
Huang YC, Niu CY, Yang CR, Jinn TL (2016) The heat stress factor HSFA6b connects ABA signaling and ABA-mediated heat responses. Plant Physiol 172:1182–1199
Iida K, Go M (2006) Survey of conserved alternative splicing events of mRNAs encoding SR proteins in land plants. Mol Biol Evol 23:1085–1094
Jiang F, Guo M, Yang F et al (2012a) Mutations in an AP2 transcription factor-like gene affect internode length and leaf shape in maize. PLoS One 7:e37040
Jiang Y, Liang G, Yu D (2012b) Activated expression of WRKY57 confers drought tolerance in Arabidopsis. Mol Plant 5:1375–1388
Jordan T, Schornack S, Lahaye T (2002) Alternative splicing of transcripts encoding Toll-like plant resistance proteins—what’s the functional relevance to innate immunity? Trends Plant Sci 7:392–398
Kaminaka H, Näke C, Epple P et al (2006) bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. Embo j 25:4400–4411
Karali D, Oxley D, Runions J, Ktistakis N, Farmaki T (2012) The Arabidopsis thaliana immunophilin ROF1 directly interacts with PI(3)P and PI(3,5)P2 and affects germination under osmotic stress. PLoS One 7:e48241
Kazan K (2003) Alternative splicing and proteome diversity in plants: the tip of the iceberg has just emerged. Trends Plant Sci 8:468–471
Kelemen O, Convertini P, Zhang Z, Wen Y, Shen M, Falaleeva M, Stamm S (2013) Function of alternative splicing. Gene 514:1–30
Keren H, Lev-Maor G, Ast G (2010) Alternative splicing and evolution: diversification, exon definition and function. Nat Rev Genet 11:345–355
Keren-Shaul H, Lev-Maor G, Ast G (2013) Pre-mRNA splicing is a determinant of nucleosome organization. PLoS One 8:e53506
Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, Ahringer J (2009) Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 41:376–381
Kornberg RD, Lorch Y (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285–294
Kornblihtt AR, Schor IE, Allo M, Blencowe BJ (2009) When chromatin meets splicing. Nat Struct Mol Biol 16:902–903
Kumar D, Chattopadhyay S (2018) Glutathione modulates the expression of heat shock proteins via the transcription factors BZIP10 and MYB21 in Arabidopsis. J Exp Bot 69:3729–3743
Kuwahara Y, Wei D, Durand J, Weissman BE (2013) SNF5 reexpression in malignant rhabdoid tumors regulates transcription of target genes by recruitment of SWI/SNF complexes and RNAPII to the transcription start site of their promoters. Mol Cancer Res 11:251–260
Lareau LF, Green RE, Bhatnagar RS, Brenner SE (2004) The evolving roles of alternative splicing. Curr Opin Struct Biol 14:273–282
Levine M (2011) Paused RNA polymerase II as a developmental checkpoint. Cell 145:502–511
Li Y, Humbert S, Howell SH (2012) ZmbZIP60 mRNA is spliced in maize in response to ER stress. BMC Res Notes 5:144
Li W, Lin WD, Ray P, Lan P, Schmidt W (2013) Genome-wide detection of condition-sensitive alternative splicing in Arabidopsis roots. Plant Physiol 162:1750–1763
Li Q, Xiao G, Zhu YX (2014) Single-nucleotide resolution mapping of the Gossypium raimondii transcriptome reveals a new mechanism for alternative splicing of introns. Mol Plant 7:829–840
Luco RF, Pan Q, Tominaga K, Blencowe BJ, Pereira-Smith OM, Misteli T (2010) Regulation of alternative splicing by histone modifications. Science 327:996–1000
Maniatis T, Reed R (2002) An extensive network of coupling among gene expression machines. Nature 416:499–506
Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15
Marquez Y, Brown JW, Simpson C, Barta A, Kalyna M (2012) Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 22:1184–1195
Meng L, Lemaux PG (2012) A simple and rapid method for nuclear run-on transcription assays in plants. Plant Mol Biol Report 21:65–71
Naftelberg S, Schor IE, Ast G, Kornblihtt AR (2015) Regulation of alternative splicing through coupling with transcription and chromatin structure. Annu Rev Biochem 84:165–198
Narlikar GJ, Fan H-Y, Kingston RE (2002) Cooperation between complexes that regulate chromatin structure and transcription. Cell 108:475–487
Patrick KL, Ryan CJ, Xu J et al (2015) Genetic interaction mapping reveals a role for the SWI/SNF nucleosome remodeler in spliceosome activation in fission yeast. PLoS Genet 11:e1005074
Prado F, Jimeno-Gonzalez S, Reyes JC (2017) Histone availability as a strategy to control gene expression. RNA Biol 14:281–286
Proudfoot NJ, Furger A, Dye MJ (2002) Integrating mRNA processing with transcription. Cell 108:501–512
Reddy AS, Marquez Y, Kalyna M, Barta A (2013) Complexity of the alternative splicing landscape in plants. Plant Cell 25:3657–3683
Ricardi MM, Gonzalez RM, Iusem ND (2010) Protocol: fine-tuning of a Chromatin Immunoprecipitation (ChIP) protocol in tomato. Plant Methods 6:11
Saldi T, Cortazar MA, Sheridan RM, Bentley DL (2016) Coupling of RNA polymerase II transcription elongation with pre-mRNA splicing. J Mol Biol 428:2623–2635
Sarnowska E, Gratkowska DM, Sacharowski SP et al (2016) The role of SWI/SNF chromatin remodeling complexes in hormone crosstalk. Trends Plant Sci 21:594–608
Schor IE, Rascovan N, Pelisch F, Alló M, Kornblihtt AR (2009) Neuronal cell depolarization induces intragenic chromatin modifications affecting NCAM alternative splicing. Proc Natl Acad Sci USA 106:4325–4330
Schor IE, Lleres D, Risso GJ, Pawellek A, Ule J, Lamond AI, Kornblihtt AR (2012) Perturbation of chromatin structure globally affects localization and recruitment of splicing factors. PLoS One 7:e48084
Schwabish MA, Struhl K (2007) The Swi/Snf complex is important for histone eviction during transcriptional activation and RNA polymerase II elongation in vivo. Mol Cell Biol 27:6987–6995
Schwartz S, Ast G (2010) Chromatin density and splicing destiny: on the cross-talk between chromatin structure and splicing. Embo j 29:1629–1636
Shen Y, Zhou Z, Wang Z et al (2014) Global dissection of alternative splicing in paleopolyploid soybean. Plant Cell 26:996–1008
Spies N, Nielsen CB, Padgett RA, Burge CB (2009) Biased chromatin signatures around polyadenylation sites and exons. Mol Cell 36:245–254
Sturgill D, Malone JH, Sun X, Smith HE, Rabinow L, Samson ML, Oliver B (2013) Design of RNA splicing analysis null models for post hoc filtering of Drosophila head RNA-Seq data with the splicing analysis kit (Spanki). BMC Bioinformatics 14:320
Thanaraj TA, Clark F (2001) Human GC-AG alternative intron isoforms with weak donor sites show enhanced consensus at acceptor exon positions. Nucleic Acids Res 29:2581–2593
Thatcher SR, Zhou W, Leonard A et al (2014) Genome-wide analysis of alternative splicing in Zea mays: landscape and genetic regulation. Plant Cell 26:3472–3487
Thatcher SR, Danilevskaya ON, Meng X et al (2016) Genome-wide analysis of alternative splicing during development and drought stress in maize. Plant Physiol 170:586–599
Tilgner H, Nikolaou C, Althammer S, Sammeth M, Beato M, Valcarcel J, Guigo R (2009) Nucleosome positioning as a determinant of exon recognition. Nat Struct Mol Biol 16:996–1001
Underhill C, Qutob MS, Yee SP, Torchia J (2000) A novel nuclear receptor corepressor complex, N-CoR, contains components of the mammalian SWI/SNF complex and the corepressor KAP-1. J Biol Chem 275:40463–40470
Wang X, Hu L, Wang X, Li N, Xu C, Gong L, Liu B (2016) DNA methylation affects gene alternative splicing in plants: an example from rice. Mol Plant 9:305–307
Wi SJ, Kim SJ, Kim WT, Park KY (2014) Constitutive S-adenosylmethionine decarboxylase gene expression increases drought tolerance through inhibition of reactive oxygen species accumulation in Arabidopsis. Planta 239:979–988
Wilson PB, Estavillo GM, Field KJ et al (2009) The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. Plant J 58:299–317
Xing A, Williams ME, Bourett TM et al (2014) A pair of homoeolog ClpP5 genes underlies a virescent yellow-like mutant and its modifier in maize. Plant J 79:192–205
Xu ZY, Lee KH, Dong T et al (2012) A vacuolar beta-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24:2184–2199
Yu S, Waldholm J, Bohm S, Visa N (2014) Brahma regulates a specific trans-splicing event at the mod(mdg4) locus of Drosophila melanogaster. RNA Biol 11:134–145
Yu X, Jiang L, Wu R et al (2016) The core subunit of a chromatin-remodeling complex, ZmCHB101, plays essential roles in maize growth and development. Sci Rep 6:38504
Yu X, Meng X, Liu Y et al (2018) The chromatin remodeler ZmCHB101 impacts expression of osmotic stress-responsive genes in maize. Plant Mol Biol 97:451–465
Zhang G, Guo G, Hu X et al (2010) Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. Genome Res 20:646–654
Zraly CB, Dingwall AK (2012) The chromatin remodeling and mRNA splicing functions of the Brahma (SWI/SNF) complex are mediated by the SNR1/SNF5 regulatory subunit. Nucleic Acids Res 40:5975–5987
Acknowledgements
The authors would like to thank Dr. Shucai Wang for critical reading of the manuscript and helpful discussions.
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The research was supported by the National Natural Science Foundation of China (#31601311 to Z.-Y.X. and #31471565 to X.Q.), Natural Science Foundation of Jilin Province of China (#20180101233JC to Z.-Y.X.) and the Fundamental Research Fund for the Central Universities (#2412018BJ002 to Z.-Y.X.).
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Communicated by Inhwan Hwang.
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Yu, X., Meng, X., Liu, Y. et al. The chromatin remodeler ZmCHB101 impacts alternative splicing contexts in response to osmotic stress. Plant Cell Rep 38, 131–145 (2019). https://doi.org/10.1007/s00299-018-2354-x
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DOI: https://doi.org/10.1007/s00299-018-2354-x