Arabidopsis nucleoporin NUP96 mediates plant salt tolerance by modulating the transcription of salt-responsive genes

doi:10.1007/s00425-023-04312-y

. 2023 Dec 31;259(2):34.

doi: 10.1007/s00425-023-04312-y.

Arabidopsis nucleoporin NUP96 mediates plant salt tolerance by modulating the transcription of salt-responsive genes

Xiaomin Yang^#¹, Chengcheng Ji^#¹, Xinxin Liu^#¹, Zhaoxin Wei¹, Qiuying Pang², Aiqin Zhang³

Affiliations

¹ Key Laboratory of Saline-Alkali Vegetation Ecology Restoration, Ministry of Education, College of Life Sciences, Northeast Forestry University, Harbin, 150040, China.
² Key Laboratory of Saline-Alkali Vegetation Ecology Restoration, Ministry of Education, College of Life Sciences, Northeast Forestry University, Harbin, 150040, China. qiuying@nefu.edu.cn.
³ Key Laboratory of Saline-Alkali Vegetation Ecology Restoration, Ministry of Education, College of Life Sciences, Northeast Forestry University, Harbin, 150040, China. aiqinaegean@nefu.edu.cn.

^# Contributed equally.

PMID: 38160450
DOI: 10.1007/s00425-023-04312-y

Arabidopsis nucleoporin NUP96 mediates plant salt tolerance by modulating the transcription of salt-responsive genes

Xiaomin Yang et al. Planta. 2023.

. 2023 Dec 31;259(2):34.

doi: 10.1007/s00425-023-04312-y.

Authors

Xiaomin Yang^#¹, Chengcheng Ji^#¹, Xinxin Liu^#¹, Zhaoxin Wei¹, Qiuying Pang², Aiqin Zhang³

Affiliations

¹ Key Laboratory of Saline-Alkali Vegetation Ecology Restoration, Ministry of Education, College of Life Sciences, Northeast Forestry University, Harbin, 150040, China.
² Key Laboratory of Saline-Alkali Vegetation Ecology Restoration, Ministry of Education, College of Life Sciences, Northeast Forestry University, Harbin, 150040, China. qiuying@nefu.edu.cn.
³ Key Laboratory of Saline-Alkali Vegetation Ecology Restoration, Ministry of Education, College of Life Sciences, Northeast Forestry University, Harbin, 150040, China. aiqinaegean@nefu.edu.cn.

^# Contributed equally.

PMID: 38160450
DOI: 10.1007/s00425-023-04312-y

Abstract

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. 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.

Keywords: ATAP2; Nuclear pore complex; Nucleocytoplasmic transport; Nucleoporin 96 (NUP96); Salt stress.

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References

1. 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 - DOI - PubMed
1. 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 - DOI - PubMed - PMC
1. 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 - DOI - PubMed
1. 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 - DOI - PubMed - PMC
1. 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 - DOI - PubMed - PMC

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[1] 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 - DOI - PubMed

[2] 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 - DOI - PubMed

[3] 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 - DOI - PubMed - PMC

[4] 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 - DOI - PubMed - PMC

[5] 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 - DOI - PubMed

[6] 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 - DOI - PubMed

[7] 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 - DOI - PubMed - PMC

[8] 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 - DOI - PubMed - PMC

[9] 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 - DOI - PubMed - PMC

[10] 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 - DOI - PubMed - PMC

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Arabidopsis nucleoporin NUP96 mediates plant salt tolerance by modulating the transcription of salt-responsive genes

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Arabidopsis nucleoporin NUP96 mediates plant salt tolerance by modulating the transcription of salt-responsive genes

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