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
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
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
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
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
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
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
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
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
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
Dubois M, Van den Broeck L, Inze D (2018) The pivotal role of ethylene in plant growth. Trends Plant Sci 23(4):311–323
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
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
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
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
Görlich D, Kutay U (1999) Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 15:607–660
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
Guzmán P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2(6):513–523
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
Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94(2):261–271
Hua J, Chang C, Sun Q, Meyerowitz EM (1995) Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269(5231):1712–1714
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
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
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
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
Meier I, Brkljacic J (2009) The nuclear pore and plant development. Curr Opin Plant Biol 12(1):87–95
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
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
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
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
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
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
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
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
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
Schaller GE, Bleecker AB (1995) Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science 270(5243):1809–1811
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
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
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
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
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
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
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
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
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
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
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
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
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
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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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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DOI: https://doi.org/10.1007/s00299-022-02976-6