S-nitrosylation coordination enhances high salt tolerance in <italic style="font-style: italic">Ulva prolifera</italic>

Dongren ZHANG; Xiuwen YANG; Jingwei DONG; Hongyan HE; Aurang ZEB; Ruyi SONG; Bing HAN; Songdong SHEN

doi:10.1007/s00343-025-4163-8

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S-nitrosylation coordination enhances high salt tolerance in Ulva prolifera

Biology | Updated：2025-10-16

- S-nitrosylation coordination enhances high salt tolerance in Ulva prolifera
- Journal of Oceanology and Limnology Vol. 43, Issue 5, Pages: 1553-1566(2025)
- Affiliations：
  
  School of Basic Medical Sciences, Soochow University, Suzhou 215101, China
- Author bio：
  
  shensongdong@suda.edu.cn
- Funds：
- DOI：10.1007/s00343-025-4163-8
  CLC：
- Received：05 January 2024，
  
  Accepted：13 May 2024，
  
  Online First：01 November 2024，
  
  Published：01 September 2025
- Accepted：
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ZHANG Dongren,YANG Xiuwen,DONG Jingwei,et al.S-nitrosylation coordination enhances high salt tolerance in Ulva prolifera[J].Journal of Oceanology and Limnology,2025,43(05):1553-1566.
DOI：

ZHANG Dongren,YANG Xiuwen,DONG Jingwei,et al.S-nitrosylation coordination enhances high salt tolerance in Ulva prolifera[J].Journal of Oceanology and Limnology,2025,43(05):1553-1566. DOI： 10.1007/s00343-025-4163-8.

摘要

Abstract

Ulva prolifera

the primary causative species of green tide

has garnered significant attention due to its robust growth and reproductive capacity under high salt stress. However

there has been relatively little research on the regulation of high salt stress in this species. In this study

we observed that high salt stress suppressed the growth of

prolifera

and leading to the nitric oxide (NO) accumulation

along with increased gene expression levels and enzyme activity of S-nitrosoglutathione reductase (GSNOR). Treatment with GSNOR inhibitor resulted in elevated NO levels under high salt stress

accompanied by reduced activity of antioxidant enzymes and decreased glutathione (GSH) accumulation

making

prolifera

more sensitive to high salt stress. Conversely

NO scavenger treatment not only reduced NO levels

but also weakened the high salt stress tolerance of

prolifera

. Furthermore

using tandem mass tags (TMT) switch analysis and mass spectrometry

we observed a significant increase in S-nitrosylated protein levels in

prolifera

under high salt stress

with further augmentation upon GSNOR inhibitor treatment. We also found high salt stress induced S-nitrosylation (SNO) of glutathione reductase (GR)

which is negati

vely regulated by GSNOR

resulting in increased GR activity. Our results show that under short-term high salt stress

the elevated expression level of GSNOR avoided excessive accumulation of NO

and a certain amount of NO enhanced the activity of antioxidant enzymes through SNO modification

which improve the high salt stress tolerance of

prolifera

whereas under long-term high salt stress

excessive NO was toxic to

prolifera

关键词

Keywords

references

Arnon D I . 1949 . Copper enzymes in isolated chloroplasts. polyphenoloxidase in Beta vulgaris . Plant Physiology , 24 ( 1 ): 1 - 15 , https://doi.org/10.1104/pp.24.1.1 https://doi.org/10.1104/pp.24.1.1 .

Astier J , Gross I , Durner J . 2018 . Nitric oxide production in plants: an update . Journal of Experimental Botany , 69 ( 14 ): 3401 - 3411 , https://doi.org/10.1093/jxb/erx420 https://doi.org/10.1093/jxb/erx420 .

Astier J , Rossi J , Chatelain P et al . 2021 . Nitric oxide production and signalling in algae . Journal of Experimental Botany , 72 ( 3 ): 781 - 792 , https://doi.org/10.1093/jxb/eraa421 https://doi.org/10.1093/jxb/eraa421 .

Chen P , Yang W X , Wen M X et al . 2021 . Hydrogen sulfide alleviates salinity stress in Cyclocarya paliurus by maintaining chlorophyll fluorescence and regulating nitric oxide level and antioxidant capacity . Plant Physiology and Biochemistry , 167 : 738 - 747 , https://doi.org/10.1016/j.plaphy.2021.09.004 https://doi.org/10.1016/j.plaphy.2021.09.004 .

Chen X D , Tian D G , Kong X X et al . 2016 . The role of nitric oxide signalling in response to salt stress in Chlamydomonas reinhardtii . Planta , 244 ( 3 ): 651 - 669 , https://doi.org/10.1007/s00425-016-2528-0 https://doi.org/10.1007/s00425-016-2528-0 .

Cox J , Hein M Y , Luber C A et al . 2014 . Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ . Molecular Cellular Proteomics , 13 ( 9 ): 2513 - 2526 , https://doi.org/10.1074/mcp.M113.031591 https://doi.org/10.1074/mcp.M113.031591 .

Cui J J , Shi J T , Zhang J H et al . 2018 . Rapid expansion of Ulva blooms in the Yellow Sea, China through sexual reproduction and vegetative growth . Marine Pollution Bulletin , 130 : 223 - 228 , https://doi.org/10.1016/j.marpolbul.2018.03.036 https://doi.org/10.1016/j.marpolbul.2018.03.036 .

Dan A , Hiraoka M , Ohno M et al . 2002 . Observations on the effect of salinity and photon fluence rate on the induction of sporulation and rhizoid formation in the green alga Enteromorpha prolifera (Müller) J. Agardh (Chlorophyta, Ulvales) . Fisheries Science , 68 ( 6 ): 1182 - 1188 , https://doi.org/10.1046/j.1444-2906.2002.00553.x https://doi.org/10.1046/j.1444-2906.2002.00553.x .

De Clerck O , Kao S M , Bogaert K A et al . 2018 . Insights into the evolution of multicellularity from the sea lettuce genome . Current Biology , 28 ( 18 ): 2921 - 2933.E5 , https://doi.org/10.1016/j.cub.2018.08.015 https://doi.org/10.1016/j.cub.2018.08.015 .

Estevez M S , Puntarulo S . 2005 . Nitric oxide generation upon growth of Antarctic Chlorella sp. cells . Physiologia Plantarum , 125 ( 2 ): 192 - 201 , https://doi.org/10.1111/j.1399-3054.2005.00561.x https://doi.org/10.1111/j.1399-3054.2005.00561.x .

Feng J , Wang C , Chen Q G et al . 2013 . S -nitrosylation of phosphotransfer proteins represses cytokinin signaling. Nature Communications , 4 : 1529 , https://doi.org/10.1038/ncomms2541 https://doi.org/10.1038/ncomms2541 .

Gao S , Shen S D , Wang G C et al . 2011 . PSI-driven cyclic electron flow allow s intertidal macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions . Plant and Cell Physiology , 52 ( 5 ): 885 - 893 , https://doi.org/10.1093/pcp/pcr038 https://doi.org/10.1093/pcp/pcr038 .

Ghaderiardakani F , Langhans L , Kurbel V B et al . 2022 . Metabolite profiling reveals insights into the species-dependent cold stress response of the green seaweed holobiont Ulva (Chlorophyta). Environmental and Experimental Botany , 200 : 104913 , https://doi.org/10.1016/j.envexpbot.2022.104913 https://doi.org/10.1016/j.envexpbot.2022.104913 .

Ghaderiardakani F , Quartino M L , Wichard T . 2020 . Microbiome-dependent adaptation of seaweeds under environmental stresses: a perspective. Frontiers in Marine Science , 7 : 575228 , https://doi.org/10.3389/fmars.2020.575228 https://doi.org/10.3389/fmars.2020.575228 .

He H Y , Yang J J , He Y et al . 2024 . Proliferating cell nuclear antigen of Ulva prolifera is involved in the response to temperature stress . Journal of Oceanology and Limnology , 42 ( 4 ): 1227 - 1241 , https://doi.org/10.1007/s00343-023-3170-x https://doi.org/10.1007/s00343-023-3170-x .

He Y L , Hu C Y , Wang Y H et al . 2018 . The metabolic survival strategy of marine macroalga Ulva prolifera under temperature stress . Journal of Applied Phycology , 30 ( 6 ): 3611 - 3621 , https://doi.org/10.1007/s10811-018-1493-3 https://doi.org/10.1007/s10811-018-1493-3 .

He Y , Shen S D , Yu D C et al . 2021 . The Ulva prolifera genome reveals the mechanism of green tides . Journal of Oceanology and Limnology , 39 ( 4 ): 1458 - 1470 , https://doi.org/10.1007/s00343-020-0212-5 https://doi.org/10.1007/s00343-020-0212-5 .

Hess D T , Matsumoto A , Kim S O et al . 2005 . Protein S -nitrosylation: purview and parameters . Nature Reviews Molecular Cell Biology , 6 ( 2 ): 150 - 166 , https://doi.org/10.1038/nrm1569 https://doi.org/10.1038/nrm1569 .

Hmani I , Ghaderiardakani F , Ktari L et al . 2024 . High-temperature stress induces bacteria-specific adverse and reversible effects on Ulva (Chlorophyta) growth and its chemosphere in a reductionist model system . Botanica Marina , 67 ( 2 ): 131 - 138 , https://doi.org/10.1515/bot-2023-0053 https://doi.org/10.1515/bot-2023-0053 .

Hu J L , Huang X H , Chen L C et al . 2015 . Site-specific nitrosoproteomic identification of endogenously S -nitrosylated proteins in Arabidopsis . Plant Physiology , 167 ( 4 ): 1731 - 1746 , https://doi.org/10.1104/pp.15.00026 https://doi.org/10.1104/pp.15.00026 .

Huan L , Xie X J , Zheng Z B et al . 2014 . Positive correlation between PSI response and oxidative pentose phosphate pathway activity during salt stress in an intertidal macroalga . Plant and Cell Physiology , 55 ( 8 ): 1395 - 1403 , https://doi.org/10.1093/pcp/pcu063 https://doi.org/10.1093/pcp/pcu063 .

Keesing J K , Liu D Y , Fearns P et al . 2011 . Inter- and intra-annual patterns of Ulva prolifera green tides in the Yellow Sea during 2007-2009, their origin and relationship to the expansion of coastal seaweed aquaculture in China . Marine Pollution Bulletin , 62 ( 6 ): 1169 - 1182 , https://doi.org/10.1016/j.marpolbul.2011.03.040 https://doi.org/10.1016/j.marpolbul.2011.03.040 .

Lamotte O , Bertoldo J B , Besson-Bard A et al . 2015 . Protein S-nitrosylation: specificity and identification strategies in plants. Frontiers in Chemistry , 2 : 114 , https://doi.org/10.3389/fchem.2014.00114 https://doi.org/10.3389/fchem.2014.00114 .

Li B H , Sun C L , Lin X Y et al . 2021 . The emerging role of GSNOR in oxidative stress regulation . Trends in Plant Science , 26 ( 2 ): 156 - 168 , https://doi.org/10.1016/j.tplants.2020.09.004 https://doi.org/10.1016/j.tplants.2020.09.004 .

Lin A P , Shen S D , Wang J W et al . 2008 . Reproduction diversity of Enteromorpha prolifera . Journal of Integrative Plant Biology , 50 ( 5 ): 622 - 629 , https://doi.org/10.1111/j.1744-7909.2008.00647.x https://doi.org/10.1111/j.1744-7909.2008.00647.x .

Lin A P , Wang C , Qiao H J et al . 2009 . Study on the photosynthetic performances of Enteromorpha prolifera collected from the surface and bottom of the sea of Qingdao sea area . Chinese Science Bulletin , 54 ( 3 ): 399 - 404 , https://doi.org/10.1007/s11434-009-0025-6 https://doi.org/10.1007/s11434-009-0025-6 .

Liu R , Zhu T , Chen X et al . 2022 . GSNOR regulates ganoderic acid content in Ganoderma lucidum under heat stress through S-nitrosylation of catalase . Communications Biology , 5 ( 32 ), https://doi.org/10.1038/s42003-021-02988-0.

Livak K J , Schmittgen T D . 2001 . Analysis of relative gene expression data using real-time quantitative PCR and the 2 ΔΔ C t method . Methods , 25 ( 4 ): 402 - 408 , https://doi.org/10.1006/meth.2001.1262 https://doi.org/10.1006/meth.2001.1262 .

Luber C A , Cox J , Lauterbach H et al . 2010 . Quantitative proteomics reveals subset-specific viral recognition in dendritic cells . Immunity , 32 ( 2 ): 279 - 289 , https://doi.org/10.1016/j.immuni.2010.01.013 https://doi.org/10.1016/j.immuni.2010.01.013 .

Mioto P T , Rodríguez-Ruiz M , Mot A C et al . 2017 . Alternative fluorimetric-based method to detect and compare total S -nitrosothiols in plants . Nitric Oxide , 68 : 7 - 13 , https://doi.org/10.1016/j.niox.2017.03.001 https://doi.org/10.1016/j.niox.2017.03.001 .

Morisse S , Zaffagnini M , Gao X H et al . 2014 . Insight into Protein S-nitrosylation in Chlamydomonas reinhardtii . Antioxidants Redox Signaling , 21 ( 9 ): 1271 - 1284 , https://doi.org/10.1089/ars.2013.5632 https://doi.org/10.1089/ars.2013.5632 .

Mur L A J , Mandon J , Persijn S et al . 2013 . Nitric oxide in plants: an assessment of the current state of knowledge . AoB Plants , 5 : pls 052 , https://doi.org/10.1093/aobpla/pls052 https://doi.org/10.1093/aobpla/pls052 .

Pan C L , Li X , Yao S C et al . 2021 . S -nitrosated proteomic analysis reveals the regulatory roles of protein S -nitrosation and S -nitrosoglutathione reductase during Al-induced PCD in peanut root tips. Plant Science , 308 : 110931 , https://doi.org/10.1016/j.plantsci.2021.110931 https://doi.org/10.1016/j.plantsci.2021.110931 .

Qiu C , Sun J H , Wang Y et al . 2019 . First nitrosoproteomic profiling deciphers the cysteine S-nitrosylation involved in multiple metabolic pathways of tea leaves . Scientific Reports , 9 ( 1 ): 17525 , https://doi.org/10.1038/s41598-019-54077-2 https://doi.org/10.1038/s41598-019-54077-2 .

Qu Z G , Li Y Q , Li W H et al . 2024 . Global profiling of protein S-palmitoylation in the second-generation merozoites of Eimeria tenella . Parasitology Research , 123 ( 4 ): 190 , https://doi.org/10.1007/s00436-024-08204-2 https://doi.org/10.1007/s00436-024-08204-2 .

Saini S , Sharma P , Singh P et al . 2023 . Nitric oxide: an emerging warrior of plant physiology under abiotic stress . Nitric Oxide , 140 - 141 : 58 - 76 , https://doi.org/10.1016/j.niox.2023.10.001 https://doi.org/10.1016/j.niox.2023.10.001 .

Schwanhäusser B , Busse D , Li N et al . 2013 . Correction: corrigendum: global quantification of mammalian gene expression control , Nature , 495 ( 7439 ): 126 - 127 , https://doi.org/10.1038/nature11848 https://doi.org/10.1038/nature11848 .

Sun X C , Wasley J W F , Qiu J et al . 2011 . Discovery of S -nitrosoglutathione reductase inhibitors: potential agents for the treatment of asthma and other inflammatory diseases . ACS Medicinal Chemistry Letters , 2 ( 5 ): 402 - 406 , https://doi.org/10.1021/ml200045s https://doi.org/10.1021/ml200045s .

Sun Y Q , Liu J L , Xia J et al . 2022 . Research development on resource utilization of green tide algae from the Southern Yellow Sea . Energy Reports , 8 ( 4 ): 295 - 303 , https://doi.org/10.1016/j.egyr.2022.01.168 https://doi.org/10.1016/j.egyr.2022.01.168 .

Thompson S E M , Callow M E , Callow J A . 2009 . The effects of nitric oxide in settlement and adhesion of zoospores of the green alga Ulva . Biofouling , 26 ( 2 ): 167 - 178 , https://doi.org/10.1080/08927010903402420 https://doi.org/10.1080/08927010903402420 .

Wang C L , Wei L J , Zhang J et al . 2023 . Nitric oxide enhances salt tolerance in tomato seedlings by regulating endogenous S -nitrosylation levels . Journal of Plant Growth Regulation , 42 ( 1 ): 275 - 293 , https://doi.org/10.1007/s00344-021-10546-5 https://doi.org/10.1007/s00344-021-10546-5 .

Wang H , Wang G C , Gu W . H . 2020 . Macroalgal blooms caused by marine nutrient changes resulting from human activities. Journal of Applied Ecology , 57 ( 4 ): 766 - 776 , https://doi.org/10.1111/1365-2664.13587 https://doi.org/10.1111/1365-2664.13587 .

Wei L J , Zhang J , Wei S H et al . 2022 . Nitric oxide alleviates salt stress through protein S -nitrosylation and transcriptional regulation in tomato seedlings . Planta , 256 ( 6 ): 101 , https://doi.org/10.1007/s00425-022-04015-w https://doi.org/10.1007/s00425-022-04015-w .

Wichard T . 2023 . From model organism to application: bacteria-induced growth and development of the green seaweed Ulva and the potential of microbe leveraging in algal aquaculture . Seminars in Cell Developmental Biology , 134 : 69 - 78 , https://doi.org/10.1016/j.semcdb.2022.04.007 https://doi.org/10.1016/j.semcdb.2022.04.007 .

Wiśniewski J R , Zougman A , Nagaraj N et al . 2009 . Universal sample preparation method for proteome analysis . Nature Methods , 6 ( 5 ): 359 - 362 , https://doi.org/10.1038/nmeth.1322 https://doi.org/10.1038/nmeth.1322 .

Xiao J , Zhang X H , Gao C L et al . 2016 . Effect of temperature, salinity and irradiance on growth and photosynthesis of Ulva prolifera . Acta Oceanologica Sinica , 35 ( 10 ): 114 - 121 , https://doi.org/10.1007/s13131-016-0891-0 https://doi.org/10.1007/s13131-016-0891-0 .

Yang J J , Yu D C , Ma Y F et al . 2019 . Antioxidative defense response of Ulva prolifera under high or low-temperature stimulus. Algal Research , 44 : 101703 , https://doi.org/10.1016/j.algal.2019.101703 https://doi.org/10.1016/j.algal.2019.101703 .

Zhai J L , Liang Y L , Zeng S L et al . 2023 . Overexp ression of tomato glutathione reductase ( SlGR ) in transgenic tobacco enhances salt tolerance involving the S -nitrosylation of GR . Plant Physiology and Biochemistry , 196 : 497 - 506 , https://doi.org/10.1016/j.plaphy.2023.02.010 https://doi.org/10.1016/j.plaphy.2023.02.010 .

Zhang X , Du H , Shi Q H et al . 2022 . Loss of GSNOR increases abiotic stress sensitivity via regulating MAPK - ethylene cascade signaling in Solanum lycopersicum L. Environmental and Experimental Botany , 199 : 104872 , https://doi.org/10.1016/j.envexpbot.2022.104872 https://doi.org/10.1016/j.envexpbot.2022.104872 .

Zhang Y Y , He P M , Li H M et al . 2019 . Ulva prolifera green-tide outbreaks and their environmental impact in the Yellow Sea, China . National Science Review , 6 ( 4 ): 825 - 838 , https://doi.org/10.1093/nsr/nwz026 https://doi.org/10.1093/nsr/nwz026 .

Zheng Z B , Gao S , Wang G C . 2019 . High salt stress in the upper part of floating mats of Ulva prolifera , a species that causes green tides, enhances non-photochemical quenching . Journal of Phycology , 55 ( 5 ): 1041 - 1049 , https://doi.org/10.1111/jpy.12881 https://doi.org/10.1111/jpy.12881 .

Zhou S , Jia L X , Chu H Y et al . 2016 . Arabidopsis CaM1 and CaM4 promote nitric oxide production and salt resistance by inhibiting S -nitrosoglutathione reductase via direct binding . PLOS Genetics , 12 ( 9 ): e 1006255 , https://doi.org/10.1371/journal.pgen.1006255 https://doi.org/10.1371/journal.pgen.1006255 .

Zhuo J T , Wang H , Du Y F et al . 2023 . Transcriptomic analysis of Ulva prolifera in response to salt stress . Water , 15 ( 1 ): 63 , https://doi.org/10.3390/w15010063 https://doi.org/10.3390/w15010063 .

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Related Author

Jingwei DONG

Hongyan HE

Aurang ZEB

Ruyi SONG

Bing HAN

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Related Institution

Key Laboratory of Space Ocean Remote Sensing and Application, Ministry of Natural Resources (MNR)

National Satellite Ocean Application Service

Qingdao Ecological and Environment Monitoring Center of Shandong Province

College of Oceanography and Space Informatics, China University of Petroleum (East China)

Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao)

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S-nitrosylation coordination enhances high salt tolerance in Ulva prolifera

DOI：10.1007/s00343-025-4163-8

摘要

Abstract

关键词

Keywords

references