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The nucleoporin NUP160 and NUP96 regulate nucleocytoplasmic export of mRNAs and participate in ethylene signaling and response in Arabidopsis

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Abstract

Key message

Arabidopsis nucleoporin involved in the regulation of ethylene signaling via controlling of nucleocytoplasmic transport of mRNAs.

Abstract

The two-way transport of mRNAs between the nucleus and cytoplasm are controlled by the nuclear pore complex (NPC). In higher plants, the NPC contains at least 30 nucleoporins. The Arabidopsis nucleoporins are involved in various biological processes such as pathogen interaction, nodulation, cold response, flowering, and hormone signaling. However, little is known about the regulatory functions of the nucleoporin NUP160 and NUP96 in ethylene signaling pathway. In the present study, we provided data showing that the Arabidopsis nucleoporin NUP160 and NUP96 participate in ethylene signaling-related mRNAs nucleocytoplasmic transport. The Arabidopsis nucleoporin mutants (nup160, nup96-1, nup96-2) exhibited enhanced ethylene sensitivity. Nuclear qRT-PCR analysis and poly(A)-mRNA in situ hybridization showed that the nucleoporin mutants affected the nucleocytoplasmic transport of all the examined mRNAs, including the ethylene signaling-related mRNAs such as ETR2, ERS1, ERS2, EIN4, CTR1, EIN2, and EIN3. Transcriptome analysis of the nucleoporin mutants provided clues suggesting that the nucleoporin NUP160 and NUP96 may participate in ethylene signaling via various molecular mechanisms. These observations significantly advance our understanding of the regulatory mechanisms of nucleoporin proteins in ethylene signaling and ethylene response.

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All the data are provided in Supplementary s1–s5.

References

  • Bleecker AB, Estelle MA, Somerville C, Kende H (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241(4869):1086–1089

    Article  CAS  PubMed  Google Scholar 

  • Boch J, Verbsky ML, Robertson TL, Larkin JC, Kunkel BN (1998) Analysis of resistance gene-mediated defense responses in Arabidopsis thaliana plants carrying a mutation in CPR5. Mol Plant Microbe Interact 11:1196–1206

    Article  CAS  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(9):1573–1584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262(5133):539–544

    Article  CAS  PubMed  Google Scholar 

  • Chen YF, Randlett MD, Findell JL, Schaller GE (2002) Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J Biol Chem 277(22):19861–19866

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Sui X, Ma B, Li Y, Li N, Qiao L, Yu Y, Dong CH (2022) Arabidopsis CPR5 plays a role in regulating nucleocytoplasmic transport of mRNAs in ethylene signaling pathway. Plant Cell Rep 41(4):1075–1085

    Article  CAS  PubMed  Google Scholar 

  • Dong CH, Xia GX, Hong Y, Ramachandran S, Kost B, Chua NH (2001) ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion and organ growth in Arabidopsis. Plant Cell 13(6):1333–1346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong CH, Hu X, Tang W, Zheng X, Kim YS, Lee BH, Zhu JK (2006) A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Mol Cell Biol 26(24):9533–9543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong CH, Rivarola M, Resnick JS, Maggin BD, Chang C (2008) Subcellular co-localization of Arabidopsis RTE1 and ETR1 supports a regulatory role for RTE1 in ETR1 ethylene signaling. Plant J 53(2):275–286

    Article  CAS  PubMed  Google Scholar 

  • Dong CH, Jang M, Scharein B, Malach A, Rivarola M, Liesch J, Groth G, Hwang I, Chang C (2010) Molecular association of the Arabidopsis ETR1 ethylene receptor and a regulator of ethylene signaling, RTE1. J Biol Chem 285(52):40706–40713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubois M, Van den Broeck L, Inze D (2018) The pivotal role of ethylene in plant growth. Trends Plant Sci 23(4):311–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ehrnsberger HF, Grasser M, Grasser KD (2019a) Nucleocytosolic mRNA transport in plants: export factors and their influence on growth and development. J Exp Bot 70(15):3757–3763

    Article  CAS  PubMed  Google Scholar 

  • Ehrnsberger HF, Pfaff C, Hachani I, Flores-Tornero M, Sørensen BB, Längst G, Sprunck S, Grasser M, Grasser KD (2019b) The UAP56-Interacting export factors UIEF1 and UIEF2 function in mRNA export. Plant Physiol 179(4):1525–1536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Germain H, Qu N, Cheng YT, Lee E, Huang Y, Dong OX, Gannon P, Huang S, Ding P, Li Y, Sack F, Zhang Y, Li X (2010) MOS11: a new component in the mRNA export pathway. PLoS Genet 6(12):e1001250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong Z, Dong CH, Lee H, Zhu J, Xiong L, Gong D, Stevenson B, Zhu J-K (2005) A DEAD Box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 17(1):256–267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Görlich D, Kutay U (1999) Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 15:607–660

    Article  PubMed  Google Scholar 

  • Gu YN, Zebell SG, Liang ZZ, Wang S, Kang BH, Dong XN (2016) Nuclear pore permeabilization is a convergent signaling event in effector-triggered immunity. Cell 166(6):1526–1538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guzmán P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2(6):513–523

    PubMed  PubMed Central  Google Scholar 

  • Hall AE, Bleecker AB (2003) Analysis of combinatorial loss-of-function mutants in the Arabidopsis ethylene receptors reveals that the ers1 etr1 double mutant has severe developmental defects that are EIN2 dependent. Plant Cell 15(9):2032–2041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94(2):261–271

    Article  CAS  PubMed  Google Scholar 

  • Hua J, Chang C, Sun Q, Meyerowitz EM (1995) Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269(5231):1712–1714

    Article  CAS  PubMed  Google Scholar 

  • Hua J, Sakai H, Nourizadeh S, Chen QG, Bleecker AB, Ecker JR, Meyerowitz EM (1998) EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant Cell 10(8):1321–1332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacob Y, Mongkolsiriwatana C, Veley KM, Kim SY, Michaels SD (2007) The nuclear pore protein AtTPR is required for RNA homeostasis, flowering time, and auxin signaling. Plant Physiol 144(3):1383–1390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Xu C, Wen CK (2010) Genetic and transformation studies reveal negative regulation of ERS1 ethylene receptor signaling in Arabidopsis. BMC Plant Biol 10:60

    Article  PubMed  PubMed Central  Google Scholar 

  • Lyons R, Iwase A, Gänsewig T, Sherstnev A, Duc C, Barton GJ, Hanada K, Higuchi-Takeuchi M, Matsui M, Sugimoto K, Kazan K, Simpson GG, Shirasu K (2013) The RNA-binding protein FPA regulates flg22-triggered defense responses and transcription factor activity by alternative polyadenylation. Sci Rep 3:2866

    Article  PubMed  PubMed Central  Google Scholar 

  • Meier I, Brkljacic J (2009) The nuclear pore and plant development. Curr Opin Plant Biol 12(1):87–95

    Article  CAS  PubMed  Google Scholar 

  • Naranjo MA, Forment J, Roldán M, Serrano R, Vicente O (2006) Overexpression of Arabidopsis thaliana LTL1, a salt-induced gene encoding a GDSL-motif lipase, increases salt tolerance in yeast and transgenic plants. Plant Cell Environ 29(10):1890–1900

    Article  CAS  PubMed  Google Scholar 

  • Parry G, Ward S, Cernac A, Dharmasiri S, Estelle M (2006) The Arabidopsis SUPPRESSOR OF AUXIN RESISTANCE proteins are nucleoporins with an important role in hormone signaling and development. Plant Cell 18(7):1590–1603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfaff C, Ehrnsberger HF, Flores-Tornero M, Sørensen BB, Schubert T, Längst G, Griesenbeck J, Sprunck S, Grasser M, Grasser KD (2018) ALY RNA-binding proteins are required for nucleocytosolic mRNA transport and modulate plant growth and development. Plant Physiol 177(1):226–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu X, Hall BP, Gao Z, Schaller GE (2007) A strong constitutive ethylene-response phenotype conferred on Arabidopsis plants containing null mutations in the ethylene receptors ETR1 and ERS1. BMC Plant Biol 7:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Resnick J, Wen C, Shockey J, Chang C (2006) REVERSION-TO-ETHYLENE SENSITIVITY1, a conserved gene that regulates ethylene receptor function in Arabidopsis. Proc Natl Acad Sci USA 103(20):7917–7922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Resnick JS, Rivarola M, Chang C (2008) Involvement of RTE1 in conformational changes promoting ETR1 ethylene receptor signaling in Arabidopsis. Plant J 56(3):423–431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, Chait BT (2000) The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 148(4):635–651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rudzka M, Hyjek-Skladanowska M, Wroblewska-Ankiewicz P, Majewska K, Golebiewski M, Sikora M, Smolinski DJ, Kolowerzo-Lubnau A (2022) Functional nuclear retention of pre-mRNA involving Cajal bodies during meiotic prophase in European larch (Larix decidua). Plant Cell 34(6):2404–2423

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakai H, Hua J, Chen QG, Chang C, Medrano LJ, Bleecker AB, Meyerowitz EM (1998) ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. Proc Natl Acad Sci USA 95(10):5812–5817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaller GE, Bleecker AB (1995) Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science 270(5243):1809–1811

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Zhang X, Xu ZY, Li L, Zhang C, Schläppi M, Xu ZQ (2011) Influence of EARLI1-like genes on flowering time and lignin synthesis of Arabidopsis thaliana. Plant Biol (stuttg) 13(5):731–739

    Article  CAS  PubMed  Google Scholar 

  • Shi J, Drummond BJ, Wang H, Archibald RL, Habben JE (2016) Maize and Arabidopsis ARGOS proteins interact with ethylene receptor signaling complex, supporting a regulatory role for ARGOS in ethylene signal transduction. Plant Physiol 171(4):2783–2797

    Article  CAS  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(12):4084–4097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogel MO, Gomez-Perez D, Probst N, Dietz KJ (2012) Combinatorial signal integration by APETALA2/Ethylene Response Factor (ERF)-transcription factors and the involvement of AP2-2 in starvation response. Int J Mol Sci 13(5):5933–5951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Wang L, Qiao L, Chen J, Pappa MB, Pei H, Zhang T, Chang C, Dong CH (2017) Arabidopsis CPR5 regulates ethylene signaling via molecular association with the ETR1 receptor. J Integr Plant Biol 59(11):810–824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson RL, Kim H, Bakshi A, Binder BM (2014) The ethylene receptors ETHYLENE RESPONSE1 and ETHYLENE RESPONSE2 have contrasting roles in seed germination of Arabidopsis during salt stress. Plant Physiol 165(3):1353–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu XM, Rose A, Muthuswamy S, Jeong SY, Venkatakrishnan S, Zhao Q, Meier I (2007) NUCLEAR PORE ANCHOR, the Arabidopsis homolog of Tpr/Mlp1/Mlp2/megator, is involved in mRNA export and SUMO homeostasis and affects diverse aspects of plant development. Plant Cell 19(5):1537–1548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Q, Rout MP, Akey CW (1998) Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol Cell 1(2):223–234

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Qiao L, Chen J, Rong Y, Zhao Y, Cui X, Xu J, Hou X, Dong CH (2020) Arabidopsis REM16 acts as a B3 domain transcription factor to promote flowering time via directly binding to the promoters of SOC1 and FT. Plant J 103(4):1386–1398

    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(4):1306–1316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Hong Y, Huang L, Li D, Song F (2016) Arabidopsis AtERF014 acts as a dual regulator that differentially modulates immunity against Pseudomonas syringae pv. tomato and Botrytis cinerea. Sci Rep 6:30251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng F, Cui X, Rivarola M, Gao T, Chang C, Dong CH (2017) Molecular association of Arabidopsis RTH with its homolog RTE1 in regulating ethylene signaling. J Exp Bot 68(11):2821–2832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Liu Q, Xie F, Wen C-K (2007) RTE1 is a Golgi-Associated and ETR1-dependent negative regulator of ethylene responses. Plant Physiol 145(1):75–86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the Experimental Center of Qingdao Agricultural University for confocal microscopy support (Leica TCS SP5). This work was supported by National Natural Science Foundation of China (#31870255; #31370322); and Natural Science Foundation of Shandong Province (#ZR2021MC020) to Y.Y.

Funding

This study was supported by National Natural Science Foundation of China (#31870255; #31370322); and Natural Science Foundation of Shandong Province (#ZR2021MC020) to Y.Y.

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YN conducted the experiments of ethylene sensitivity and transcriptome analysis, YL examined the mutant phenotype and ethylene responses, BM did qRT-PCR and DAPI staining imaging, XS performed the experiments of nuclear qRT-PCR, JC did in situ examination of mRNAs and part of nuclear qRT-PCR, ML did data analysis, YY worked on the manuscript revision, and CHD designed the experiments and wrote the manuscript.

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Correspondence to Chun-Hai Dong.

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Communicated by Xian Sheng Zhang.

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Nie, Y., Li, Y., Liu, M. et al. The nucleoporin NUP160 and NUP96 regulate nucleocytoplasmic export of mRNAs and participate in ethylene signaling and response in Arabidopsis. Plant Cell Rep 42, 549–559 (2023). https://doi.org/10.1007/s00299-022-02976-6

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