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The chromatin remodeler ZmCHB101 impacts expression of osmotic stress-responsive genes in maize

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The maize chromatin remodeler ZmCHB101 plays an essential role in the osmotic stress response. ZmCHB101 controls nucleosome densities around transcription start sites of essential stress-responsive genes.

Abstract

Drought and osmotic stresses are recurring conditions that severely constrain crop production. Evidence accumulated in the model plant Arabidopsis thaliana suggests that core components of SWI/SNF chromatin remodeling complexes play essential roles in abiotic stress responses. However, how maize SWI/SNF chromatin remodeling complexes function in osmotic and drought stress responses remains unknown. Here we show that ZmCHB101, a homolog of A. thaliana SWI3D in maize, plays essential roles in osmotic and dehydration stress responses. ZmCHB101-RNA interference (RNAi) transgenic plants displayed osmotic, salt and drought stress-sensitive phenotypes. Genome-wide RNA-sequencing analysis revealed that ZmCHB101 impacts the transcriptional expression landscape of osmotic stress-responsive genes. Intriguingly, ZmCHB101 controls nucleosome densities around transcription start sites of essential stress-responsive genes. Furthermore, we identified that ZmCHB101 associates with RNA polymerase II (RNAPII) in vivo and is a prerequisite for the proper occupancy of RNAPII on the proximal regions of transcription start sites of stress-response genes. Taken together, our findings suggest that ZmCHB101 affects gene expression by remodeling chromatin states and controls RNAPII occupancies in maize under osmotic stress.

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References

  • Archacki R et al (2009) Genetic analysis of functional redundancy of BRM ATPase and ATSWI3C subunits of Arabidopsis SWI/SNF chromatin remodelling complexes. Planta 229:1281–1292

    Article  PubMed  CAS  Google Scholar 

  • Becker PB, Horz W (2002) ATP-dependent nucleosome remodeling. Annu Rev Biochem 71:247–273

    Article  PubMed  CAS  Google Scholar 

  • Ben Rejeb K 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

    Article  PubMed  CAS  Google Scholar 

  • Bhatnagar-Mathur P et al (2007) Stress-inducible expression of AtDREB1A in transgenic peanut (Arachis hypogaea L.) increases transpiration efficiency under water-limiting conditions. Plant Cell Rep 26:2071–2082

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Buratowski S (2009) Progression through the RNA polymerase II CTD cycle. Mol Cell 36:541–546

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cairns BR (2005) Chromatin remodeling complexes: strength in diversity, precision through specialization. Curr Opin Genet Dev 15:185–190

    Article  PubMed  CAS  Google Scholar 

  • Chen J et al (2017) Genome-wide nucleosome occupancy and organization modulates the plasticity of gene transcriptional status in maize. Mol Plant 10:962–974

    Article  PubMed  CAS  Google Scholar 

  • Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78:273–304

    Article  PubMed  CAS  Google Scholar 

  • Cosma MP, Tanaka T, Nasmyth K (1999) Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter. Cell 97:299–311

    Article  PubMed  CAS  Google Scholar 

  • Davie JK, Kane CM (2000) Genetic interactions between TFIIS and the Swi-Snf chromatin-remodeling complex. Mol Cell Biol 20:5960–5973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Efroni I et al (2013) Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Dev Cell 24:438–445

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Egloff S, Murphy S (2008) Role of the C-terminal domain of RNA polymerase II in expression of small nuclear RNA genes. Biochem Soc Trans 36:537–539

    Article  PubMed  CAS  Google Scholar 

  • Euskirchen GM et al (2011) Diverse roles and interactions of the SWI/SNF chromatin remodeling complex revealed using global approaches. PLoS Genet 7:e1002008

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fincher JA, Vera DL, Hughes DD, McGinnis KM, Dennis JH, Bass HW (2013) Genome-wide prediction of nucleosome occupancy in maize reveals plant chromatin structural features at genes and other elements at multiple scales. Plant Physiol 162:1127–1141

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Frey FP, Urbany C, Huttel B, Reinhardt R, Stich B (2015) Genome-wide expression profiling and phenotypic evaluation of European maize inbreds at seedling stage in response to heat stress. BMC Genom 16:123

    Article  CAS  Google Scholar 

  • Fuglsang AT et al (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+ -ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617–1634

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gangaraju VK, Bartholomew B (2007) Mechanisms of ATP dependent chromatin remodeling. Mutat Res 618:3–17

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gonzalez-Guzman M et al (2012) Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. Plant Cell 24:2483–2496

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Grasser M, Grasser KD (2018) The plant RNA polymerase II elongation complex: a hub coordinating transcript elongation and mRNA processing. Transcription 9:117–122

    Article  PubMed  CAS  Google Scholar 

  • Hajheidari M, Koncz C, Eick D (2013) Emerging roles for RNA polymerase II CTD in Arabidopsis. Trends Plant Sci 18:633–643

    Article  PubMed  CAS  Google Scholar 

  • Han SK, Sang Y, Rodrigues A, Biol F, Wu MF, Rodriguez PL, Wagner D (2012) The SWI2/SNF2 chromatin remodeling ATPase BRAHMA represses abscisic acid responses in the absence of the stress stimulus in Arabidopsis. Plant Cell 24:4892–4906

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han SK, Wu MF, Cui S, Wagner D (2015) Roles and activities of chromatin remodeling ATPases in plants. Plant J 83:62–77

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jerzmanowski A (2007) SWI/SNF chromatin remodeling and linker histones in plants. Biochim Biophys Acta 1769:330–345

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69:91–105

    Article  PubMed  CAS  Google Scholar 

  • Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci USA 107:2355–2360

    Article  PubMed  Google Scholar 

  • Kolmos E, Chow BY, Pruneda-Paz JL, Kay SA (2014) HsfB2b-mediated repression of PRR7 directs abiotic stress responses of the circadian clock. Proc Natl Acad Sci USA 111:16172–16177

    Article  PubMed  CAS  Google Scholar 

  • Kulaeva OI, Hsieh FK, Chang HW, Luse DS, Studitsky VM (2013) Mechanism of transcription through a nucleosome by RNA polymerase II. Biochim Biophys Acta 1829:76–83

    Article  PubMed  CAS  Google Scholar 

  • Lai WKM, Pugh BF (2017) Understanding nucleosome dynamics and their links to gene expression and DNA replication. Nat Rev Mol Cell Biol 18(9):548–562

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lescot M et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li JF, Bush J, Xiong Y, Li L, McCormack M (2011) Large-scale protein-protein interaction analysis in Arabidopsis mesophyll protoplasts by split firefly luciferase complementation. PLoS ONE 6:e27364

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li C et al (2016) Concerted genomic targeting of H3K27 demethylase REF6 and chromatin-remodeling ATPase BRM in Arabidopsis. Nat Genet 48:687–693

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lomvardas S, Thanos D (2001) Nucleosome sliding via TBP DNA binding in vivo. Cell 106:685–696

    Article  PubMed  CAS  Google Scholar 

  • Makhloufi E et al (2014) Isolation and molecular characterization of ERF1, an ethylene response factor gene from durum wheat (Triticum turgidum L. subsp. durum), potentially involved in salt-stress responses. J Exp Bot 65:6359–6371

    Article  PubMed  CAS  Google Scholar 

  • Malone EA, Clark CD, Chiang A, Winston F (1991) Mutations in SPT16/CDC68 suppress cis- and trans-acting mutations that affect promoter function in Saccharomyces cerevisiae. Mol Cell Biol 11:5710–5717

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15

    Article  PubMed  CAS  Google Scholar 

  • Mattiello EM, Ruiz HA, Neves JC, Ventrella MC, Araujo WL (2015) Zinc deficiency affects physiological and anatomical characteristics in maize leaves. J Plant Physiol 183:138–143

    Article  PubMed  CAS  Google Scholar 

  • Mitra D, Parnell EJ, Landon JW, Yu Y, Stillman DJ (2006) SWI/SNF binding to the HO promoter requires histone acetylation and stimulates TATA-binding protein recruitment. Mol Cell Biol 26:4095–4110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mittal A, Gampala SS, Ritchie GL, Payton P, Burke JJ, Rock CD (2014) Related to ABA-Insensitive3(ABI3)/Viviparous1 and AtABI5 transcription factor coexpression in cotton enhances drought stress adaptation. Plant Biotechnol J 12:578–589

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mittler R et al (2006) Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett 580:6537–6542

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moshkin YM, Armstrong JA, Maeda RK, Tamkun JW, Verrijzer P, Kennison JA, Karch F (2002) Histone chaperone ASF1 cooperates with the Brahma chromatin-remodelling machinery. Genes Dev 16:2621–2626

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Narlikar GJ (2010) A proposal for kinetic proof reading by ISWI family chromatin remodeling motors. Curr Opin Chem Biol 14:660–665

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Narlikar GJ, Fan H-Y, Kingston RE (2002) Cooperation between complexes that regulate chromatin structure and transcription. Cell 108:475–487

    Article  PubMed  CAS  Google Scholar 

  • Natarajan K, Jackson BM, Zhou H, Winston F, Hinnebusch AG (1999) Transcriptional activation by Gcn4p involves independent interactions with the SWI/SNF complex and the SRB/mediator. Mol Cell 4:657–664

    Article  PubMed  CAS  Google Scholar 

  • Neely KE, Hassan AH, Wallberg AE, Steger DJ, Cairns BR, Wright AP, Workman JL (1999) Activation domain-mediated targeting of the SWI/SNF complex to promoters stimulates transcription from nucleosome arrays. Mol Cell 4:649–655

    Article  PubMed  CAS  Google Scholar 

  • Neely KE, Hassan AH, Brown CE, Howe L, Workman JL (2002) Transcription activator interactions with multiple SWI/SNF subunits. Mol Cell Biol 22:1615–1625

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Novillo F, Medina J, Salinas J (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA 104:21002–21007

    Article  PubMed  Google Scholar 

  • Papdi C, Perez-Salamo I, Joseph MP, Giuntoli B, Bogre L, Koncz C, Szabados L (2015) The low oxygen, oxidative and osmotic stress responses synergistically act through the ethylene response factor VII genes RAP2.12, RAP2.2 and RAP2.3. Plant J 82:772–784

    Article  PubMed  CAS  Google Scholar 

  • Peirats-Llobet M et al (2016) A direct link between abscisic acid sensing and the chromatin-remodeling ATPase BRAHMA via core ABA signaling pathway components. Mol Plant 9:136–147

    Article  PubMed  CAS  Google Scholar 

  • Peterson CL, Workman JL (2000) Promoter targeting and chromatin remodeling by the SWI/SNF complex. Curr Opin Genet Dev 10:187–192

    Article  PubMed  CAS  Google Scholar 

  • Prochasson P, Neely KE, Hassan AH, Li B, Workman JL (2003) Targeting activity is required for SWI/SNF function in vivo and is accomplished through two partially redundant activator-interaction domains. Mol Cell 12:983–990

    Article  PubMed  CAS  Google Scholar 

  • Proft M, Struhl K (2004) MAP kinase-mediated stress relief that precedes and regulates the timing of transcriptional induction. Cell 118:351–361

    Article  PubMed  CAS  Google Scholar 

  • Qiu H, Hu C, Yoon S, Natarajan K, Swanson MJ, Hinnebusch AG (2004) An array of coactivators is required for optimal recruitment of TATA binding protein and RNA polymerase II by promoter-bound Gcn4p. Mol Cell Biol 24:4104–4117

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rafati H, Parra M, Hakre S, Moshkin Y, Verdin E, Mahmoudi T (2011) Repressive LTR nucleosome positioning by the BAF complex is required for HIV latency. PLoS Biol 9:e1001206

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reja R, Vinayachandran V, Ghosh S, Pugh BF (2015) Molecular mechanisms of ribosomal protein gene coregulation. Genes Dev 29:1942–1954

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ren X et al (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63:417–429

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reyes JC (2014) The many faces of plant SWI/SNF complex. Mol Plant 7:454–458

    Article  PubMed  CAS  Google Scholar 

  • Ricardi MM, Gonzalez RM, Iusem ND (2010) Protocol: fine-tuning of a chromatin immunoprecipitation (ChIP) protocol in tomato. Plant Methods 6:11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saez A, Rodrigues A, Santiago J, Rubio S, Rodriguez PL (2008) HAB1-SWI3B interaction reveals a link between abscisic acid signaling and putative SWI/SNF chromatin-remodeling complexes in Arabidopsis. Plant Cell 20:2972–2988

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sarnowska EA et al (2013) DELLA-interacting SWI3C core subunit of switch/sucrose nonfermenting chromatin remodeling complex modulates gibberellin responses and hormonal cross talk in Arabidopsis. Plant Physiol 163:305–317

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sarnowska E et al (2016) The role of SWI/SNF chromatin remodeling complexes in hormone crosstalk. Trends Plant Sci 21:594–608

    Article  PubMed  CAS  Google Scholar 

  • Sarnowski TJ et al (2005) SWI3 subunits of putative SWI/SNF chromatin-remodeling complexes play distinct roles during Arabidopsis development. Plant Cell 17:2454–2472

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmidt R, Caldana C, Mueller-Roeber B, Schippers JHM (2014) The contribution of SERF1 to root-to-shoot signaling during salinity stress in rice. Plant Signal Behav 9:e27540

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sheen J (2001) Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol 127:1466–1475

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shen Y, Devic M, Lepiniec L, Zhou DX (2015) Chromodomain, Helicase and DNA-binding CHD1 protein, CHR5, are involved in establishing active chromatin state of seed maturation genes. Plant Biotechnol J 13:811–820

    Article  PubMed  CAS  Google Scholar 

  • Shivaswamy S, Bhinge A, Zhao Y, Jones S, Hirst M, Iyer VR (2008) Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol 6:e65

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sudarsanam P, Winston F (2000) The Swi/Snf family nucleosome-remodeling complexes and transcriptional control. Trends Genet 16:345–351

    Article  PubMed  CAS  Google Scholar 

  • Vera DL et al (2014) Differential nuclease sensitivity profiling of chromatin reveals biochemical footprints coupled to gene expression and functional DNA elements in maize. Plant Cell 26:3883–3893

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Walley JW, Rowe HC, Xiao Y, Chehab EW, Kliebenstein DJ, Wagner D, Dehesh K (2008) The chromatin remodeler SPLAYED regulates specific stress signaling pathways. PLoS Pathog 4:e1000237

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weber CM, Ramachandran S, Henikoff S (2014) Nucleosomes are context-specific, H2A.Z-modulated barriers to RNA polymerase. Mol Cell 53:819–830

    Article  PubMed  CAS  Google Scholar 

  • Wilson CJ, Chao DM, Imbalzano AN, Schnitzler GR, Kingston RE, Young RA (1996) RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling. Cell 84:235–244

    Article  PubMed  CAS  Google Scholar 

  • Xu ZY 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu ZY et al (2013) The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell 25:4708–4724

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang S et al (2015) The Arabidopsis SWI2/SNF2 chromatin remodeling ATPase BRAHMA targets directly to PINs and is required for root stem cell niche maintenance. Plant Cell 27:1670–1680

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yen K, Vinayachandran V, Batta K, Koerber RT, Pugh BF (2012) Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell 149:1461–1473

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572

    Article  PubMed  CAS  Google Scholar 

  • Yoshinaga SK, Peterson CL, Herskowitz I, Yamamoto KR (1992) Roles of SWI1, SWI2, and SWI3 proteins for transcriptional enhancement by steroid receptors. Science 258:1598–1604

    Article  PubMed  CAS  Google Scholar 

  • Yu Q, An L, Li W (2014) The CBL-CIPK network mediates different signaling pathways in plants. Plant Cell Rep 33:203–214

    Article  PubMed  CAS  Google Scholar 

  • Yu X et al (2016) The core subunit of a chromatin-remodeling complex, ZmCHB101, plays essential roles in maize growth and dvelopment. Sci Rep 6:38504

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yudkovsky N, Logie C, Hahn S, Peterson CL (1999) Recruitment of the SWI/SNF chromatin remodeling complex by transcriptional activators. Genes Dev 13:2369–2374

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (#31601311 to Z-YX, #31471565 and #31170259 to XQ, #31200231 to XZ), National Key Research and Development Program of China (#2016YFD0102003-2 to Z-YX), National Transgenic Maize Project (#2014ZX0800305B to JP) and Natural Science Foundation of Jilin Province of China (#20150101086JC to MZ and #20180101233JC to Z-YX) and the Fundamental Research Fund for the Central Universities (#2412018BJ002 to Z-YX).

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  1. Xiaoming Yu and Xinchao Meng have contributed equally to this study.

Authors and Affiliations

  1. Key Laboratory of Molecular Epigenetics of the Ministry of Education (MOE), Northeast Normal University, Changchun, People’s Republic of China

    Xiaoming Yu, Xinchao Meng, Yutong Liu, Ning Li, Ai Zhang, Tian-Jing Wang, Lili Jiang, Jinsong Pang, Shucai Wang, Bao Liu & Zheng-Yi Xu

  2. Department of Agronomy, Jilin Agricultural University, Changchun, People’s Republic of China

    Xinxin Zhao, Xin Qi & Meishan Zhang

  3. Department of Bioengineering, Jilin Agricultural Science and Technology College, Jilin, People’s Republic of China

    Xiaoming Yu

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  1. Xiaoming Yu
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Contributions

Z-YX and BL devised and supervised the project. XY, Z-YX and BL designed the experiments. XY, XM, YL, T-JW, NL, AZ and LJ performed experiments and analyzed the data. JP, XZ, XQ and MZ produced transgenic maize. XY, SW, Z-YX and BL wrote the manuscript.

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Correspondence to Bao Liu or Zheng-Yi Xu.

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Data generated in this study are deposited in the NCBI Sequence Read Archive (accession no. SRP068174).

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Yu, X., Meng, X., Liu, Y. et al. The chromatin remodeler ZmCHB101 impacts expression of osmotic stress-responsive genes in maize. Plant Mol Biol 97, 451–465 (2018). https://doi.org/10.1007/s11103-018-0751-8

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