Abstract
Main conclusion
Physiological and molecular tests show that NUP96 plays an important role in the plant response to salt stress, resulting from the reprogramming of transcriptomic profiles, which are likely to be mediated by the influence on the nuclear/cytosol shuttling of the key regulators of salt tolerance.
Abstract
As a key component of the nuclear pore complex (NPC), nucleoporin 96 (NUP96) is critical for modulating plant development and interactions with environmental factors, but whether NUP96 is involved in the salt response is still unknown. Here, we analyzed the role of Arabidopsis NUP96 under salt stress. The loss-of-function mutant nup96 exhibited salt sensitivity in terms of rosette growth and root elongation, and showed attenuated capacity in maintaining ion and ROS homeostasis, which could be compensated for by the overexpression of NUP96. RNA sequencing revealed that many salt-responsive genes were misregulated after NUP96 mutation, and especially NUP96 is required for the expression of a large portion of salt-induced genes. This is likely correlated with the activity in facilitating nuclear/cytosol transport of the underlying regulators in salt tolerance such as the transcription factor ATAP2, targeted by eight downregulated genes in nup96 under salt stress. Our results illustrate that NUP96 plays an important role in the salt response, probably by regulating the nucleocytoplasmic shuttling of key mRNAs or proteins associated with plant salt responsiveness.
This is a preview of subscription content, log in via an institution to check access.
Data availability
The data that support the findings of this study are available in supplementary datasets and from the corresponding author Aiqin Zhang upon reasonable request.
Abbreviations
- COR :
-
Cold regulated gene
- DEG:
-
Differentially expressed gene
- MDA:
-
Malondialdehyde
- NPC:
-
Nuclear pore complex
- NUP:
-
Nucleoporin
- RD :
-
Responsive to dehydration gene
References
Chang YN, Wang ZJ, Ren ZY, Wang CH, Wang PC, Zhu JK, Li X, Duan CG (2022) NUCLEAR PORE ANCHOR and EARLY IN SHORT DAYS 4 negatively regulate abscisic acid signaling by inhibiting Snf1-related protein kinase2 activity and stability in Arabidopsis. J Integr Plant Biol 64(11):2060–2074. https://doi.org/10.1111/jipb.13349
Cheng YT, Germain H, Wiermer M, Bi DL, Xu F, Garcia AV, Wirthmueller L, Despres C, Parker JE, Zhang YL, 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(8):2503–2516. https://doi.org/10.1105/tpc.108.064519
Cheng ZY, Zhang XM, Huang PH, Huang GW, Zhu JL, Chen FL, Miao YC, Liu LY, Yong F, Wang X (2020) Nup96 and HOS1 are mutually stabilized and gate CONSTANS protein level, conferring long-day photoperiodic flowering regulation in Arabidopsis. Plant Cell 32(2):374–391. https://doi.org/10.1105/tpc.19.00661
Deinlein U, Stephan AB, Horie T, Luo W, Xu GH, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379. https://doi.org/10.1016/j.tplants.2014.02.001
Dong CH, Agarwal M, Zhang YY, Xie Q, Zhu JK (2006a) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Natl Acad Sci USA 103(21):8281–8286. https://doi.org/10.1073/pnas.0602874103
Dong CH, Hu XY, Tang WP, Zheng XW, Kim YS, Lee BH, Zhu JK (2006b) 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. https://doi.org/10.1128/MCB.01063-06
Ferrandez-Ayela A, Alonso-Peral MM, Sanchez-Garcia AB, Micol-Ponce R, Perez-Perez JM, Micol JL (2013) Arabidopsis TRANSCURVATA1 encodes NUP58, a component of the nucleopore central channel. PLoS ONE 8(6):e67661. https://doi.org/10.1371/journal.pone.0067661
Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124(4):1854–1865. https://doi.org/10.1104/pp.124.4.1854
Gu Y, Zebell SG, Liang Z, Wang S, Kang BH, Dong XN (2016) Nuclear pore permeabilization is a convergent signaling event in effector-triggered immunity. Cell 166(6):1526-1538.e11. https://doi.org/10.1016/j.cell.2016.07.042
Hampoelz B, Andres-Pons A, Kastritis P, Beck M (2019) Structure and assembly of the nuclear pore complex. Annu Rev Biophys 48:515–536. https://doi.org/10.1146/annurev-biophys-052118-115308
Harel A, Orjalo AV, Vincent T, Lachish-Zalait A, Vasu S, Shah S, Zimmerman E, Elbaum M, Forbes DJ (2003) Removal of a single pore subcomplex results in vertebrate nuclei devoid of nuclear pores. Mol Cell 11(4):853–864. https://doi.org/10.1016/s1097-2765(03)00116-3
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. https://doi.org/10.1104/pp.107.100735
Jung JH, Park JH, Lee S, To TK, Kim JM, Seki M (2013) The cold signaling attenuator HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 activates FLOWERING LOCUS C transcription via chromatin remodeling under short-term cold stress in Arabidopsis. Plant Cell 25(11):4378–4390. https://doi.org/10.1105/tpc.113.118364
Lee K, Seo PJ (2015) The E3 ubiquitin ligase HOS1 is involved in ethylene regulation of leaf expansion in Arabidopsis. Plant Signal Behav 10(3):e1003755. https://doi.org/10.1080/15592324.2014.1003755
Luo Y, Wang Z, Ji H, Fang H, Wang S, Tian L, Li X (2013) An Arabidopsis homolog of importin β1 is required for ABA response and drought tolerance. Plant J 75(3):377–389. https://doi.org/10.1111/tpj.12207
Meier I, Brkljacic J (2009) The nuclear pore and plant development. Curr Opin Plant Biol 12(1):87–95. https://doi.org/10.1016/j.pbi.2008.09.001
Nam H, Han S, Lee S, Nam H, Lim H, Lee G, Cho HS, Dang TVT, Choi S, Lee MM, Hwang I (2023) CPR5-mediated nucleo-cytoplasmic localization of IAA12 and IAA19 controls lateral root development during abiotic stress. Proc Natl Acad Sci USA 120(3):e2209781120. https://doi.org/10.1073/pnas.2209781120
Nie Y, Li Y, Liu M, Ma B, Sui X, Chen J, Yu Y, Dong CH (2023) The nucleoporin NUP160 and NUP96 regulate nucleocytoplasmic export of mRNAs and participate in ethylene signaling and response in Arabidopsis. Plant Cell Rep 42(3):549–559. https://doi.org/10.1007/s00299-022-02976-6
Pang Q, Zhang A, Zang W, Wei L, Yan X (2016) Integrated proteomics and metabolomics for dissecting the mechanism of global responses to salt and alkali stress in Suaeda corniculate. Plant Soil 402:379–394. https://doi.org/10.1007/s11104-015-2774-0
Parry G (2015) The plant nuclear envelope and regulation of gene expression. J Exp Bot 66(6):1673–1685. https://doi.org/10.1093/jxb/erv023
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. https://doi.org/10.1105/tpc.106.041566
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(11):687–699. https://doi.org/10.1038/nrm3461
Sekulska-Nalewajko J, Goclawski J, Chojak-Kozniewska J, Kuzniak E (2016) Automated image analysis for quantification of reactive oxygen species in plant leaves. Method 109:114–122. https://doi.org/10.1016/j.ymeth.2016.05.018
Van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71:403–433. https://doi.org/10.1146/annurev-arplant-050718-100005
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(6):787–794. https://doi.org/10.1016/j.chom.2014.10.005
Weis K (2003) Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell 112(4):441–451. https://doi.org/10.1016/s0092-8674(03)00082-5
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(5):796–808. https://doi.org/10.1111/j.1365-313X.2012.04928.x
Xu XM, Meier I (2008) The nuclear pore comes to the fore. Trends Plant Sci 13(1):20–27. https://doi.org/10.1016/j.tplants
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(6):e1002159. https://doi.org/10.1371/journal.pgen
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. https://doi.org/10.1105/tpc104.029926
Zhang A, Zang W, Zhang X, Ma Y, Yan X, Pang Q (2016) Global proteomic mapping of alkali stress regulated molecular networks in Helianthus tuberosus L. Plant Soil 409:175–202. https://doi.org/10.1007/s11104-016-2945-7
Zhang A, Han D, Wang Y, Mu H, Zhang T, Yan X, Pang Q (2018) Transcriptomic and proteomic feature of salt stress-regulated network in Jerusalem artichoke (Helianthus tuberosus L.) root based on de novo assembly sequencing analysis. Planta 247(3):715–732. https://doi.org/10.1007/s00425-017-2818-1
Zhang A, Wang S, Kim J, Yan J, Yan X, Pang Q, Hua J (2020) Nuclear pore complex components have temperature-influenced roles in plant growth and immunity. Plant Cell Environ 43(6):1452–1466. https://doi.org/10.1111/pce.13741
Zhu Y, Wang B, Tang K, Hsu CC, Xie S, Du H, Yang Y, Tao WA, Zhu JK (2017) An Arabidopsis nucleoporin NUP85 modulates plant responses to ABA and salt stress. PLoS Genet 13(12):e1007124. https://doi.org/10.1371/journal.pgen.1007124
Acknowledgements
This work was supported by the National Natural Science Foundation of China (No. 32100298 and No. 32070350) and the Excellent Youth Project of Natural Science Foundation of Heilongjiang Province (YQ2021C001).
Author information
Authors and Affiliations
Contributions
AQZ and QYP designed the experiments and supervised the research. XMY, CCJ, XXL and ZXW performed the experiments and analyzed the data. XMY and AQZ wrote the manuscript with contributions from other authors.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
425_2023_4312_MOESM1_ESM.docx
Supplementary file1 Table S1 Primers used for real-time qRT-PCR. Table S2 Primers used for gene cloning. Table S3 The mis-regulated salt responsive genes in nup96 which are targeted by ATAP2 transcription factor (DOCX 20 KB)
425_2023_4312_MOESM3_ESM.pptx
Supplementary file3 Fig. S1 The growth phenotype of nup96 mutant under control and salt stress. a Rosette leaf of Arabidopsis nup96-1 and nup96-2 mutants. b Phenotypes of four-week-old nup96 mutants grown in soil (three-week under normal condition, followed by 7 days NaCl treatment). c Quantifications of rosette fresh weight. d The rate of cotyledon greening. f-g Biochemical properties were determined after 24 h, 72 h and 7 days of salt treatment: Relative water content (e, RWC), MDA content (f), Na+ and K+ (g) content in nup96 mutant under salt stress. Error bars represent ±SD from three biological repeats. Different letters above the bars indicate significant differences among samples (one-way ANOVA/Duncan P < 0.05). Fig. S2 Effects of salt stress on root length of NUP96 complementation lines. a NUP96 expression in complementation lines. b The growth phenotype of complementation lines under salt stress. c The quantitative analysis of root length. Error bars represent ±SD from 15 seedlings. The significant differences between Col-0 and OE lines were analyzed by one-way ANOVA/Duncan (P < 0.05). ns, not significant. Fig. S3 Analysis of differentially expressed genes in wild type and nup96 mutant response to salt. a, b Up-regulated genes and down-regulated genes in nup96 mutant under normal condition. GO enrichment analysis of differentially expressed genes in nup96 mutant under normal condition. c, d Up-regulated genes and down-regulated genes in wild type under salt stress and GO enrichment analysis. e, f Up-regulated genes and down-regulated genes in wild type and nup96 mutant under salt stress and GO enrichment analysis. Fig. S4 Analysis of salt-responsive genes expressed in nup96 mutant. a, d Overlap of DEGs between up-regulated genes and down-regulated genes in wild type or nup96 mutant under salt stress. b, e The number of differentially expressed genes and GO enrichment analysis. c, f The number of differentially expressed genes and KEGG enrichment analysis (PPTX 42842 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yang, X., Ji, C., Liu, X. et al. Arabidopsis nucleoporin NUP96 mediates plant salt tolerance by modulating the transcription of salt-responsive genes. Planta 259, 34 (2024). https://doi.org/10.1007/s00425-023-04312-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04312-y