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Nuclear pore complex-mediated gene expression in Arabidopsis thaliana

  • JPR Symposium
  • New Aspects of Functional Plant Nuclear Architecture
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Abstract

Nuclear pore complexes (NPCs) are large multi-protein complexes that control bidirectional trafficking of macromolecules between the nucleus and cytoplasm. This trafficking is highly regulated and participates in a considerably broader range of cellular activities, including defense responses against pathogens in plants. Recently, NPC is emerging as a platform to physically associate the underlying chromatin with the nuclear periphery, thus regulating chromatin structure and gene expression. For instance, NPC components have been shown to promote the formation of specific genomics loops, which is linked to transcriptional memory for rapid reactivation of genes. With newly developed techniques and tools, our insight in this area has been substantially advanced. This review summarizes recent works on the molecular function of NPC machinery as hubs for transcriptional regulation and compares systems between plant and non-plant organisms.

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References

  • Ahmed S, Brickner DG, Light WH, Cajigas I, McDonough M, Froyshteter AB, Volpe T, Brickner JH (2010) DNA zip codes control an ancient mechanism for gene targeting to the nuclear periphery. Nat Cell Biol 12:111–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akhtar A, Gasser SM (2007) The nuclear envelope and transcriptional control. Nat Rev Genet 8:507–517

    Article  CAS  PubMed  Google Scholar 

  • Andika IB, Jamal A, Kondo H, Suzuki N (2017) SAGA complex mediates the transcriptional up-regulation of antiviral RNA silencing. Proc Natl Acad Sci USA 114:E3499–E3506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aramburu IV, Lemke EA (2017) Floppy but not sloppy: Interaction mechanism of FG-nucleoporins and nuclear transport receptors. Semin Cell Dev Biol 68:34–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bertrand C, Bergounioux C, Domenichini S, Delarue M, Zhou DX (2003) Arabidopsis histone acetyltransferase AtGCN5 regulates the floral meristem activity through the WUSCHEL/AGAMOUS pathway. J Biol Chem 278:28246–28251

    Article  CAS  PubMed  Google Scholar 

  • Bi X, Cheng YJ, Hu B, Ma X, Wu R, Wang JW, Liu C (2017) Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery. Genome Res 27:1162–1173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9:1573–1584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brickner DG, Randise-Hinchliff C, Lebrun Corbin M, Liang JM, Kim S, Sump B, D'Urso A, Kim SH, Satomura A, Schmit H, Coukos R, Hwang S, Watson R, Brickner JH (2019) The role of transcription factors and nuclear pore proteins in controlling the spatial organization of the yeast genome. Dev Cell 49(936–947):e934

    Google Scholar 

  • Brzezinka K, Altmann S, Czesnick H, Nicolas P, Gorka M, Benke E, Kabelitz T, Jahne F, Graf A, Kappel C, Baurle I (2016) Arabidopsis FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling. elife 5:e17061

    Article  PubMed  PubMed Central  Google Scholar 

  • Capelson M, Liang Y, Schulte R, Mair W, Wagner U, Hetzer MW (2010) Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140:372–383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng YT, Germain H, Wiermer M, Bi D, Xu F, Garcia AV, Wirthmueller L, Despres C, Parker JE, Zhang Y, Li X (2009) Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell 21:2503–2516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denning DP, Patel SS, Uversky V, Fink AL, Rexach M (2003) Disorder in the nuclear pore complex: the FG repeat regions of nucleoporins are natively unfolded. Proc Natl Acad Sci USA 100:2450–2455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devos D, Dokudovskaya S, Williams R, Alber F, Eswar N, Chait BT, Rout MP, Sali A (2006) Simple fold composition and modular architecture of the nuclear pore complex. Proc Natl Acad Sci USA 103:2172–2177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dogan ES, Liu C (2018) Three-dimensional chromatin packing and positioning of plant genomes. Nat Plants 4:521–529

    Article  CAS  PubMed  Google Scholar 

  • Feng CM, Qiu Y, Van Buskirk EK, Yang EJ, Chen M (2014) Light-regulated gene repositioning in Arabidopsis. Nat Commun 5:3027

    Article  PubMed  CAS  Google Scholar 

  • Fischer T, Strasser K, Racz A, Rodriguez-Navarro S, Oppizzi M, Ihrig P, Lechner J, Hurt E (2002) The mRNA export machinery requires the novel Sac3p-Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. EMBO J 21:5843–5852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiserova J, Kiseleva E, Goldberg MW (2009) Nuclear envelope and nuclear pore complex structure and organization in tobacco BY-2 cells. Plant J 59:243–255

    Article  CAS  PubMed  Google Scholar 

  • Garcia AV, Blanvillain-Baufume S, Huibers RP, Wiermer M, Li G, Gobbato E, Rietz S, Parker JE (2010) Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathog 6:e1000970

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garcia-Oliver E, Garcia-Molinero V, Rodriguez-Navarro S (2012) mRNA export and gene expression: the SAGA-TREX-2 connection. Biochim Biophys Acta 1819:555–565

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis–2001 status. Curr Opin Plant Biol 4:301–308

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Aguilera C, Tous C, Gomez-Gonzalez B, Huertas P, Luna R, Aguilera A (2008) The THP1-SAC3-SUS1-CDC31 complex works in transcription elongation-mRNA export preventing RNA-mediated genome instability. Mol Biol Cell 19:4310–4318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grossman E, Medalia O, Zwerger M (2012) Functional architecture of the nuclear pore complex. Annu Rev Biophys 41:557–584

    Article  CAS  PubMed  Google Scholar 

  • Gu Y, Zebell SG, Liang Z, Wang S, Kang BH, Dong X (2016) Nuclear pore permeabilization is a convergent signaling event in effector-triggered immunity. Cell 166:1526–1538.e1511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerreiro I, Kind J (2019) Spatial chromatin organization and gene regulation at the nuclear lamina. Curr Opin Genet Dev 55:19–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hale CJ, Potok ME, Lopez J, Do T, Liu A, Gallego-Bartolome J, Michaels SD, Jacobsen SE (2016) Identification of multiple proteins coupling transcriptional gene silencing to genome stability in Arabidopsis thaliana. PLoS Genet 12:e1006092

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hampoelz B, Andres-Pons A, Kastritis P, Beck M (2019) Structure and assembly of the nuclear pore complex. Annu Rev Biophys 48:515–536

    Article  CAS  PubMed  Google Scholar 

  • Hampsey M, Singh BN, Ansari A, Laine JP, Krishnamurthy S (2011) Control of eukaryotic gene expression: gene loops and transcriptional memory. Adv Enzyme Regul 51:118–125

    Article  CAS  PubMed  Google Scholar 

  • Helmlinger D, Tora L (2017) Sharing the SAGA. Trends Biochem Sci 42:850–861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jirage D, Zhou N, Cooper B, Clarke JD, Dong X, Glazebrook J (2001) Constitutive salicylic acid-dependent signaling in cpr1 and cpr6 mutants requires PAD4. Plant J 26:395–407

    Article  CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kohler A, Hurt E (2007) Exporting RNA from the nucleus to the cytoplasm. Nat Rev Mol Cell Biol 8:761–773

    Article  PubMed  CAS  Google Scholar 

  • Laine JP, Singh BN, Krishnamurthy S, Hampsey M (2009) A physiological role for gene loops in yeast. Genes Dev 23:2604–2609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li B, Meng X, Shan L, He P (2016) Transcriptional regulation of pattern-triggered immunity in plants. Cell Host Microbe 19:641–650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Q, Zheng J, Li S, Huang G, Skilling SJ, Wang L, Li L, Li M, Yuan L, Liu P (2017) Transporter-mediated nuclear entry of jasmonoyl-isoleucine is essential for jasmonate signaling. Mol Plant 10:695–708

    Article  CAS  PubMed  Google Scholar 

  • Light WH, Brickner DG, Brand VR, Brickner JH (2010) Interaction of a DNA zip code with the nuclear pore complex promotes H2A.Z incorporation and INO1 transcriptional memory. Mol Cell 40:112–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Wang C, Wang G, Becker C, Zaidem M, Weigel D (2016) Genome-wide analysis of chromatin packing in Arabidopsis thaliana at single-gene resolution. Genome Res 26:1057–1068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Cheng YJ, Wang JW, Weigel D (2017) Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis. Nat Plants 3:742–748

    Article  CAS  PubMed  Google Scholar 

  • Liu HC, Lamke J, Lin SY, Hung MJ, Liu KM, Charng YY, Baurle I (2018) Distinct heat shock factors and chromatin modifications mediate the organ-autonomous transcriptional memory of heat stress. Plant J 95:401–413

    Article  CAS  PubMed  Google Scholar 

  • Lott K, Cingolani G (2011) The importin beta binding domain as a master regulator of nucleocytoplasmic transport. Biochim Biophys Acta 1813:1578–1592

    Article  CAS  PubMed  Google Scholar 

  • Lu Q, Tang X, Tian G, Wang F, Liu K, Nguyen V, Kohalmi SE, Keller WA, Tsang EW, Harada JJ, Rothstein SJ, Cui Y (2010) Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. Plant J 61:259–270

    Article  CAS  PubMed  Google Scholar 

  • Meier I, Richards EJ, Evans DE (2017) Cell biology of the plant nucleus. Annu Rev Plant Biol 68:139–172

    Article  CAS  PubMed  Google Scholar 

  • Moraga F, Aquea F (2015) Composition of the SAGA complex in plants and its role in controlling gene expression in response to abiotic stresses. Front Plant Sci 6:865

    Article  PubMed  PubMed Central  Google Scholar 

  • Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    Article  CAS  PubMed  Google Scholar 

  • Palma K, Zhang Y, Li X (2005) An importin alpha homolog, MOS6, plays an important role in plant innate immunity. Curr Biol 15:1129–1135

    Article  CAS  PubMed  Google Scholar 

  • Pfab A, Bruckmann A, Nazet J, Merkl R, Grasser KD (2018) The adaptor protein ENY2 is a component of the deubiquitination module of the Arabidopsis SAGA transcriptional co-activator complex but not of the TREX-2 complex. J Mol Biol 430:1479–1494

    Article  CAS  PubMed  Google Scholar 

  • Raices M, D'Angelo MA (2012) Nuclear pore complex composition: a new regulator of tissue-specific and developmental functions. Nat Rev Mol Cell Biol 13:687–699

    Article  CAS  PubMed  Google Scholar 

  • Roberts K, Northcote DH (1970) Structure of the nuclear pore in higher plants. Nature 228:385–386

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Navarro S, Fischer T, Luo MJ, Antunez O, Brettschneider S, Lechner J, Perez-Ortin JE, Reed R, Hurt E (2004) Sus1, a functional component of the SAGA histone acetylase complex and the nuclear pore-associated mRNA export machinery. Cell 116:75–86

    Article  CAS  PubMed  Google Scholar 

  • Roth C, Wiermer M (2012) Nucleoporins Nup160 and Seh1 are required for disease resistance in Arabidopsis. Plant Signal Behav 7:1212–1214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid M, Arib G, Laemmli C, Nishikawa J, Durussel T, Laemmli UK (2006) Nup-PI: the nucleopore-promoter interaction of genes in yeast. Mol Cell 21:379–391

    Article  CAS  PubMed  Google Scholar 

  • Smith S, Galinha C, Desset S, Tolmie F, Evans D, Tatout C, Graumann K (2015) Marker gene tethering by nucleoporins affects gene expression in plants. Nucleus 6:471–478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava R, Rai KM, Pandey B, Singh SP, Sawant SV (2015) Spt-Ada-Gcn5-acetyltransferase (SAGA) complex in plants: genome wide identification, evolutionary conservation and functional determination. PLoS ONE 10:e0134709

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stockinger EJ, Mao Y, Regier MK, Triezenberg SJ, Thomashow MF (2001) Transcriptional adaptor and histone acetyltransferase proteins in Arabidopsis and their interactions with CBF1, a transcriptional activator involved in cold-regulated gene expression. Nucleic Acids Res 29:1524–1533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strambio-De-Castillia C, Niepel M, Rout MP (2010) The nuclear pore complex: bridging nuclear transport and gene regulation. Nat Rev Mol Cell Biol 11:490–501

    Article  CAS  PubMed  Google Scholar 

  • Takizawa T, Meaburn KJ, Misteli T (2008) The meaning of gene positioning. Cell 135:9–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Hara-Nishimura I (2011) Involvement of the nuclear pore complex in morphology of the plant nucleus. Nucleus 2:168–172

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Hara-Nishimura I (2013) The molecular architecture of the plant nuclear pore complex. J Exp Bot 64:823–832

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Hara-Nishimura I (2014) Functional insights of nucleocytoplasmic transport in plants. Front Plant Sci 5:118

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Fukao Y, Iwamoto M, Haraguchi T, Hara-Nishimura I (2010) Identification and characterization of nuclear pore complex components in Arabidopsis thaliana. Plant Cell 22:4084–4097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Goto C, Hara-Nishimura I (2015) Recent advances in understanding plant nuclear envelope proteins involved in nuclear morphology. J Exp Bot 66:1641–1647

    Article  CAS  PubMed  Google Scholar 

  • Tan-Wong SM, Wijayatilake HD, Proudfoot NJ (2009) Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes Dev 23:2610–2624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vlachonasios KE, Thomashow MF, Triezenberg SJ (2003) Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. Plant Cell 15:626–638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Gu Y, Zebell SG, Anderson LK, Wang W, Mohan R, Dong X (2014) A noncanonical role for the CKI-RB-E2F cell-cycle signaling pathway in plant effector-triggered immunity. Cell Host Microbe 16:787–794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiermer M, Germain H, Cheng YT, Garcia AV, Parker JE, Li X (2010) Nucleoporin MOS7/Nup88 contributes to plant immunity and nuclear accumulation of defense regulators. Nucleus 1:332–336

    Article  PubMed  PubMed Central  Google Scholar 

  • Wiermer M, Cheng YT, Imkampe J, Li M, Wang D, Lipka V, Li X (2012) Putative members of the Arabidopsis Nup107-160 nuclear pore sub-complex contribute to pathogen defense. Plant J 70:796–808

    Article  CAS  PubMed  Google Scholar 

  • Xu S, Zhang Z, Jing B, Gannon P, Ding J, Xu F, Li X, Zhang Y (2011) Transportin-SR is required for proper splicing of resistance genes and plant immunity. PLoS Genet 7:e1002159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, La H, Tang K, Miki D, Yang L, Wang B, Duan CG, Nie W, Wang X, Wang S, Pan Y, Tran EJ, An L, Zhang H, Zhu JK (2017) SAC3B, a central component of the mRNA export complex TREX-2, is required for prevention of epigenetic gene silencing in Arabidopsis. Nucleic Acids Res 45:181–197

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Li X (2005) A putative nucleoporin 96 Is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1, constitutive 1. Plant Cell 17:1306–1316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Goritschnig S, Dong X, Li X (2003) A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15:2636–2646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by Grants-in Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan (18K06283), and by the Human Frontier Science Program (RGP0009/2018 to KT) from the International Human Frontier Science Program Organization.

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  1. Department of Environmental and Life Sciences, University of Shizuoka, Shizuoka, 422-8526, Japan

    Kentaro Tamura

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Tamura, K. Nuclear pore complex-mediated gene expression in Arabidopsis thaliana. J Plant Res 133, 449–455 (2020). https://doi.org/10.1007/s10265-020-01177-0

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