Abstract
Populus euphratica Oliv. response to salinity stress has been mainly studied at a whole-plant level. However, many genes associated with salinity tolerance are constitutively expressed or show strong organ-or tissue-specific, and the relationship between reactive oxygen species (ROS) and the antioxidant system has been rarely investigated. In present work, the effects of salinity treatments (0, 50, 100, 150, and 200 mM NaCl) on cell ultrastructure, ROS, antioxidant enzymes, and relevant gene expressions were investigated to get an overview of salinity stress response of P. euphratica micro-shoots under in vitro conditions. Antioxidant enzymes such as superoxide dismutase (SOD) and ascorbate peroxidase (APX), etc., were activated in the presence of low and moderate salt stress (≤ 150 mM NaCl). Regulation of ROS levels and the cellular redox equilibrium, as well as an increase in glutathione (GSH) and ascorbic acid (AsA) content, were also recorded at 150 mM NaCl. PeCu/ZnSOD upregulation occurred 12 h before PeAPX2 upregulation at 100 mM NaCl. The enzymes SOD, APX, CAT, and POD were inhibited by high salinity stress (200 mM NaCl), whereas the level of H2O2 was significantly increased. PeCu/ZnSOD expression increased after 12 h, whereas PeAPX2 expression increased after 36–72 h at 200 mM NaCl. This resulted in a burst of O2.− and H2O2, which accelerated membrane lipid peroxidation, significantly reduced chlorophyll content, and eventually led to chlorosis and cellular damage. In this study, the bigger contributing markers to salt tolerance were AsA, APX, CAT, and SOD. Our results indicated the coordinated alterations between enzymatic, ROS and gene expressions facilitated the resistance to salinity in P. euphratica micro-shoots under moderate salinity.
Key message
The micro-shoots of P. euphratica could endure 150 mM NaCl stress. The coordinated changes in PeCu/ZnSOD and PeAPX2 expression and antioxidative enzymes facilitated in vitro Populus euphratica resistance to salinity stress.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Asrara H, Hussaina T, Qasima M, Nielsen BL, Gul B, Khan MA (2020) Salt induced modulations in antioxidative defense system of Desmostachya bipinnata Hina. Plant Physiol Biochem 147:113–124. https://doi.org/10.1016/j.plaphy.2019.12.012
Bartwall A, Arora S (2017) Drought, stress-induced enzyme activity and mdar and apx gene expression in tolerant and susceptible genotypes of Eleusine coracana (L.). In Vitro Cell Dev Biol Plant 53:41–49. https://doi.org/10.1007/s11627-016-9787-0
Bernardi R, Nali C, Ginestri P, Pugliesi C, Lorenzini G, Durante M (2004) Antioxidant enzyme isoforms on gels in two poplar clones differing in sensitivity after exposure to ozone. Biol Plant 48(1):41–48. https://doi.org/10.1023/b:biop.0000024273.35976.cb
Bernstein N, Shoresh M, Xu Y, Huang BR (2010) Involvement of the plant antioxidative response in the differential growth sensitivity to salinity of leaves vs roots during cell development. Free Radic Biol Med 49:1161–1171. https://doi.org/10.1016/j.freeradbiomed.2010.06.032
Bradford MM (1976) Arapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Cao K, Yu J, Xu D, Ai K, Bao E, Zou Z (2018) Exposure to lower red to far-red light ratios improve tomato tolerance to salt stress. BMC Plant Biol 18:92. https://doi.org/10.1186/s12870-018-1310-9
Caverzan A, Passaia GSB, Ribeiro CW, Lazzarotto F, Margis PM (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35:1011–1019. https://doi.org/10.1590/s1415-47572012000600016
Chen Y, Lin FZ, Yang H, Yue L, Hu F, Wang JL, Cao FL (2014) Effect of varying NaCl doses on flavonoid production in suspension cells of Ginkgo biloba L.: relationship to chlorophyll fluorescence, ion homeostasis, antioxidant system and ultrastructure. Acta Physiol Plant 36:3173–3187
Chen Y, Yuan BL, Wei ZH, Chen X, Chen YQ, Qiu NF (2018) The ion homeostasis and ROS scavenging responses in ‘NL895’ poplar plantlet organs under in vitro salinity stress. In Vitro Cell Dev Biol-Plant 54:318–331. https://doi.org/10.1007/s11627-018-9896-z
Chourasia KN, More SJ, Kumar A, Kumar D, Singh B, Bhardwaj V, Kumar A, Das SK, Singh RK, Zinta G (2022) Salinity responses and tolerance mechanisms in underground vegetable crops: an integrative review. Planta 255:68. https://doi.org/10.1007/s00425-022-03845-y
Chrysargyris A, Michailidi E, Tzortzakis N (2018) Physiological and biochemical responses of Lavandula angustifolia to salinity under mineral foliar application. Front Plant Sci 9:489. https://doi.org/10.3389/fpls.2018.00489
Cipriano R, Martins JPR, Conde LT, Moreira SW, Clairvil E, de Souza Braga PC, Gontijo ABPL, Falqueto AR (2021) Anatomical, physiological, and biochemical modulations of silicon in Aechmea blanchetiana (Bromeliaceae) cultivated in vitro in response to cadmium. Plant Cell Tissue Organ Cult 147:271–285. https://doi.org/10.1007/s11240-021-02122-2
Czarnocka W, Karpiński S (2018) Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses. Free Radic Biol Med 122:4–20. https://doi.org/10.1016/j.freeradbiomed.2018.01.011
Dale JW, Schantz MV, Klena JD (2003) From genes to genomes. Concepts and applications of DNA technology. https://doi.org/10.1046/j.1364-3703.2003.00149.x
de Freitas PAF, de Carvalho HH, Costa JH, de Souza MR, da Cruz Saraiva KD, De Oliveira FDB, Coelho DG, Prisco JT, Gomes-Filho E (2019) Salt acclimation in sorghum plants by exogenous proline: physiological and biochemical changes and regulation of proline metabolism. Plant Cell Rep 38:403–416. https://doi.org/10.1007/s00299-019-02382-5
Ding M, Hou P, Shen X, Wang M, Deng S, Sun J, **ao F, Wang R, Zhou X, Lu C (2010) Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant Mol Biol 73:251–269. https://doi.org/10.1007/s11103-010-9612-9
Dlamini P (2021) Drought stress tolerance mechanisms and breeding effort in sugarcane: a review of progress and constraints in South Africa. Plant Stress 2:1–17. https://doi.org/10.1016/j.stress.2021.100027
Galeano E, Vasconcelos TS, Ramiro DA, Martin VFD, Carre H (2014) Identification and validation of quantitative real-time reverse transcription PCR reference genes for gene expression analysis in teak (Tectona grandis L.f.). BMC Res Notes 7:464. https://doi.org/10.1016/j.plaphy.2016.07.022
Gu RS, Fonseca S, Puskas LG, Hackler JRL, Zvara Á, Dudits D, Pais MS (2004) Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiol 24:265–276. https://doi.org/10.1093/treephys/24.3.265
Guan Q, Liao X, He M, Li X, Wang Z, Ma H, Yu S, Liu S (2017) Tolerance analysis of chloroplast OsCu/Zn-SOD overexpressing rice under NaCl and NaHCO3 stress. PLoS ONE 12(10):e0186052. https://doi.org/10.1371/journal.pone.0186052
Haider MS, Sudisha J, Pervaiz T, Zhao YX, Khan N, Fang JG (2019) Physiological and transcriptional variations inducing complex adaptive mechanisms in grapevine by salt stress. Environ Exp Bot 162:455–467. https://doi.org/10.1016/j.envexpbot.2019.03.022
Han YS, Wang SJ, Zhao N, Deng SR, Zhao CJ, Li NF, Sun J, Zhao R, Yi HL, Shen X, Chen SL (2016) Exogenous abscisic acid alleviates cadmium toxicity by restricting Cd2+ influx in Populus euphratica cells. Plant Growth Regul 35:827–837. https://doi.org/10.1007/s00344-016-9585-2
He F, Li HG, Wang JJ, Su Y, Wang HL, Feng CH, Yang Y, Niu MX, Liu C, Yin W, **a X (2019) PeSTZ1, a C2H2-type zinc finger transcription factor from Populus euphratica, enhances freezing tolerance through modulation of ROS scavenging by directly regulating PeAPX2. Plant Biotechnol J 17:2169–2183. https://doi.org/10.1111/pbi.13130
Hu LP, **ang LX, Zhang L, Zhou X, Zou Z (2014) The photoprotective role of spermidine in tomato seedlings under salinity-alkalinity stress. PLoS ONE 9:e110855. https://doi.org/10.1371/journal.pone.0110855
Huang H, Wang H, Tong Y, Wang YH (2020) Insights into the superoxide dismutase gene family and its roles in Dendrobium catenatum under abiotic stresses. Plants 9:1452. https://doi.org/10.3390/plants9111452
Kaya C, Ashraf M, Alyemeni MN, Parvaiz Ahmad P (2020) The role of endogenous nitric oxide in salicylic acid-induced up-regulation of ascorbate-glutathione cycle involved in salinity tolerance of pepper (Capsicum annuum L.) plants. Plant Physiol Biochem 147:10–20. https://doi.org/10.1016/j.plaphy.2019.11.040
Kim BM, Lee JW, Seo JS, Shin KH, Rhee JS, Lee JS (2015) Modulated expression and enzymatic activity of the monogonont rotifer Brachionus koreanus Cu/ Zn- and Mn- superoxide dismutase (SOD) in response to environmental biocides. Chemosphere 120:470–478. https://doi.org/10.1016/j.chemosphere.2014.08.042
Li C, Qin S, Bao LH, Guo ZZ, Zhao LF (2020) Identification and functional prediction of circRNAs in Populus Euphratica Oliv. heteromorphic leaves. Genomics 112:92–98. https://doi.org/10.1016/j.ygeno.2019.01.013
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592
Liu L, Liu D, Wang ZY, Zou CL, Bin Wang B, Zhang H, Gai ZJ, Zhang PF, Wang YB, Li CF (2020) Exogenous allantoin improves the salt tolerance of sugar beet by increasing putrescine metabolism and antioxidant activities. Plant Physiol Biochem 154:699–713. https://doi.org/10.1016/j.plaphy.2020.06.034
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lu W, Duanmu H, Qiao Y, ** X, Yu Y, Yu L, Chen C (2020) Genome-wide identification and characterization of the soybean SOD family during alkaline stress. PeerJ 8:e8457. https://doi.org/10.7717/peerj.8457
Lu Y, Zeng FJ, Li XY, Zhang B (2021) Physiological changes of three woody plants exposed to progressive salt stress. Photosynthetica 59(1):171–184. https://doi.org/10.32615/ps.2021.007
Ma T, Wang K, Hu Q, ** Z, Wan D, Wang Q, Feng J, Jiang D, Ahani H, Abbott RJ, Lascoux M, Nevo E, Liu J (2018) Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex. Proc Natl Acad Sci USA 115:E236–E243. https://doi.org/10.1073/pnas.1713288114
Markad VL, Gaupale TC, Bhargava KKM, Ghole VS (2015) Biomarker responses in the earthworm Dichogaster curgensis exposed to fly ash polluted soils. Ecotoxicol Environ Saf 118:62–70. https://doi.org/10.1016/j.ecoenv.2015.04.011
Miao L, Clair DKS (2009) Regulation of superoxide dismutase genes: implication in diseases. Free Radic Biol Med 47:344–356
Mishra P, Bhoomika K, Dubey RS (2013) Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings. Protoplasma 250:3–19. https://doi.org/10.1007/s00709-011-0365-3
Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19. https://doi.org/10.1016/j.tplants.2016.08.002
Mo YL, Wang YQ, Yang RP, Zheng JX, Liu CM, Li H, Ma JX, Zhang Y, Wei CH, Zhang X (2016) Regulation of plant growth, photosynthesis, antioxidation and osmosis by an arbuscular mycorrhizal fungus in watermelon seedlings under well-watered and drought conditions. Front Plant Sci 7:644. https://doi.org/10.3389/fpls.2016.00644
Mohammadi F, Reza KH, Mansouri M (2019) Effects of salt stress on physio-biochemical characters and gene expressions in halophyte grass Leptochloa fusca (L.) Kunth. Acta Physiol Plantarum 41:143. https://doi.org/10.1007/s11738-019-2935-5
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nabi RBS, Tayade R, Hussain A, Krishnanand P, Kulkarnic KP, Imran OM, Mun BG, Yun BW (2019) Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress. Environ Exp Bot 161:120–133. https://doi.org/10.1016/j.envexpbot.2019.02.003
Naeem M, Hasitha W, Liu HB, Liu D, Rashid A, Ejaz AW, Xu L, Zhou WJ (2012) 5-Aminolevulinic acid alleviates the salinity-induced changes in Brassica napus as revealed by the ultrastructural study of chloroplast. Plant Physiol Biochem 57:84–92. https://doi.org/10.1016/j.plaphy.2012.05.018
Omoto E, Haruto N, Mitsutaka T, Hiroshi M (2013) Localization of reactive oxygen species and change of antioxidant capacities in mesophyll and bundle sheath chloroplasts of maize under salinity. Physiol Plantarum 149:1–12. https://doi.org/10.1111/ppl.12017
Ottow EA, Polle A, Brosché M, Kangasjärvi J, Dibrov P, Zörb C, Teichmann T (2005) Molecular characterization of PeNhaD1: the first member of the NhaD Na+/H+ antiporter family of plant origin. Plant Mol Biol 58:75–88. https://doi.org/10.1007/s11103-005-4525-8
Panda A, Rangani J, Parida AK (2019) Cross talk between ROS homeostasis and antioxidative machinery contributes to salt tolerance of the xero-halophyte Haloxylon salicornicum. Environ Exp Bot 166:1–19. https://doi.org/10.1016/j.envexpbot.2019.103799
Parida AK, Veerabathini SK, Kumari A, Agarwal PK (2016) Physiological, anatomical and metabolic implications of salt tolerance in the halophyte Salvadora persica under hydroponic culture condition. Front Plant Sci 7:1–18. https://doi.org/10.3389/fpls.2016.00351
Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265. https://doi.org/10.1007/s00299-005-0972-6
Qiao W, Li C, Fan LM (2013) Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses. Environ Exp Bot 100:83–93. https://doi.org/10.1016/j.envexpbot.2013.12.014
Raia MK, Kalia RK, Singh R, Gangola MP, Dhawan AK (2011) Develo** stress tolerant plants through in vitro selection—an overview of the recent progress. Environ Exp Bot 71:89–98. https://doi.org/10.1016/j.envexpbot.2010.10.021
Rangani J, Parida AK, Panda A, Kumari A (2016) Coordinated changes in antioxidative enzymes protect the photosynthetic machinery from salinity induced oxidative damage and confer salt tolerance in an extreme halophyte Salvadora persica L. Front Plant Sci 7:50. https://doi.org/10.3389/fpls.2016.00050
Rangani J, Panda A, Patel M, Kumar A (2018) Regulation of ROS through proficient modulations of antioxidative defense system maintains the structural and functional integrity of photosynthetic apparatus and confers drought tolerance in the facultative halophyte Salvadora persica L. Photochem Photochem Photobiol B 189:214–233. https://doi.org/10.1016/j.jphotobiol.2018.10.021
Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 37:1059–1073. https://doi.org/10.1111/pce.12199
Rossatto T, Do Amaral MN, Benitez LC, Vighi IL, Braga EJB, de Magalhaes J, Ariano M, Colares Maia MA, de Silva Pinto L (2017) Gene expression and activity of antioxidant enzymes in rice plants, cv. BRS AG, under saline stress. Physiol Mol Biol Plants 23:865–875. https://doi.org/10.1007/s12298-017-0467-2
Sami A, Shah FA, Abdullah M, Zhou X, Yan Y, Zhu Z, Zhou K (2020) Melatonin mitigates cadmium and aluminium toxicity through modulation of antioxidant potential in Brassica napus L. Plant Biol 22:679–690. https://doi.org/10.1111/plb.13093
Shafi A, Chauhan R, Gill T, Swarnkar MK, Sreenivasulu Y, Kumar S, Kumar N, Shankar R, Ahuja PS, Singh AK (2015) Expression of SOD and APX genes positively regulates secondary cell wall biosynthesis and promotes plant growth and yield in Arabidopsis under salt stress. Plant Mol Biol 87:615–631. https://doi.org/10.1007/s11103-015-0301-6
Shafi A, Gill T, Zahoor I, Ahuja PS, Sreenivasulu SSK (2019) Ectopic expression of SOD and APX genes in Arabidopsis alters metabolic pools and genes related to secondary cell wall cellulose biosynthesis and improve salt tolerance. Mol Biol Rep 46:1985–2002. https://doi.org/10.1007/s11033-019-04648-3
Singh P, Pandey SS, Dubey BK, Raj R, Barnawal D, Chandran A, Rahman L (2021) Salt and drought stress tolerance with increased biomass in transgenic Pelargonium graveolens through heterologous expression of ACC deaminase gene from Achromobacter xylosoxidans. Plant Cell Tissue Organ Cult 147:297–311. https://doi.org/10.1007/s11240-021-02124-0
Song ZH, Ni XB, Yao J, Wang F (2021) Progress in studying heteromorphic leaves in Populus euphratica: leaf morphology, anatomical structure, development regulation and their ecological adaptation to arid environments. Plant Signal Behav 16(4):e1870842. https://doi.org/10.1080/15592324.2020.1870842
Snyman SJ, Mhlanga P, Watt MP (2016) Rapid screening of sugarcane Plantlets for in vitro mannitol-induced stress. Sugar Tech 18:437–440
Su YT, Bai XT, Yang WL, Wang WW, Chen ZY, Ma JC, Ma T (2018) Single-base-resolution methylomes of Populus euphratica reveal the association between DNA methylation and salt stress. Tree Genet Genom 14:86. https://doi.org/10.1007/s11295-018-1298-1
Sun J, Wang M, Ding M, Deng S, Liu M, Lu C, Zhou X, Shen X, Zheng X, Zhang Z, Song J, Hu Z, Xu Y, Chen S (2010) H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. Plant Cell Environ 33:943–958. https://doi.org/10.1111/j.1365-3040.2010.02118.x
Takagi H, Yamada S (2013) Roles of enzymes in anti-oxidative response system on three species of chnopodiaceous halophytes under NaCl-stress condition. Soil Sci Plant Nutr 59:603–611. https://doi.org/10.1080/00380768.2013.809600
Watanabe S, Kojima K, Ide Y, Sasaki S (2000) Effects of saline and osmotic stress on proline and sugar accumulation in Populus euphratica in vitro. Plant Cell Tissue Organ Cult 63:199–206. https://doi.org/10.1023/A:1010619503680
**e YH, Chen HB, Zheng SY, Zhang XL, Mu SN (2018) Molecular characterization of cu/Zn SOD gene in Asian clam Corbicula fluminea and mRNA expression and enzymatic activity modulation induced by metals. Gene 663:189–195. https://doi.org/10.1016/j.gene.2018.04.044
Yalcinkaya T, Uzilday B, Ozgur R, Turkana I, Manob J (2019) Lipid peroxidation-derived reactive carbonyl species (RCS): Their interaction with ROS and cellular redox during environmental stresses. Environ Exp Bot 165:139–149. https://doi.org/10.1016/j.envexpbot.2019.06.004
Yao YN, Sun YF, Feng Q, Zhang X, Gao YF, Ou YB, Yang F, **e W, de Dios VR, Ma JB, Yousefi M (2021) Acclimation to nitrogen × salt stress in Populus bolleana mediated by potassium/sodium balance. Ind Crops Prod 170:113789. https://doi.org/10.1016/j.indcrop.2021.113789
Ye L, Zhao X, Bao E, Cao K, Zou Z (2019a) Effects of arbuscular mycorrhizal fungi on watermelon growth, elemental uptake, antioxidant, and photosystem II activities and stress-response gene expressions under salinity-alkalinity stresses. Front Plant Sci 10:863. https://doi.org/10.3389/fpls.2019.00863
Ye ZQ, Wang JM, Wang WJ, Zhang TH, Li JW (2019b) Effects of root phenotypic changes on the deep rooting of Populus euphratica seedlings under drought stresses. Peer J Life Environ 7:e6513. https://doi.org/10.7717/peerj.6513
Yoon SK, Park EJ, Choi YI, Bae EK, Kim JH, Park SY, Kang KS, Lee HS (2014) Response to drought and salt stress in leaves of poplar (Populus alba×Populus glandulosa): Expression profiling by oligonucleotide microarray analysis. Plant Physiol Biochem 84:158–168. https://doi.org/10.1016/j.plaphy.2014.09.008
Yu L, Ma JC, Niu ZJ, Bai X, Lei W, Shao X, Chen N, Zhou F, Wan D (2017) Tissue-specific transcriptome analysis reveals multiple responses to salt stress in Populus euphratica seedlings. Genes 8:372. https://doi.org/10.3390/genes8120372
Yuan XH, Wu JY, Yang XJ, Teng WJ (2012) Assessment of salt tolerance of ornamental grasses at germination stage and seedling stage based on LC50. Chin J Grassland 34(06):1673–5021 (in Chinese)
Zelm EV, Zhang YX, Christa T (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71:403–433. https://doi.org/10.1146/annurev-arplant-050718-100005
Zhao Q, Zhou LJ, Liu JC, Cao ZZ, Du XX, Huang FD, Pan G, Cheng FM (2018) Involvement of CAT in the detoxification of HT-induced ROS burst in rice anther and its relation to pollen fertility. Plant Cell Res. https://doi.org/10.1007/s00299-018-2264-y
Zhao H, Niu Y, Dong H, Jia Y, Wang Y (2021) Characterization of the function of two S1Fa-like family genes from Populus trichocarpa. Front Plant Sci 12:753099. https://doi.org/10.3389/fpls.2021.753099
Funding
This work was funded by the National Natural Science Foundation of China (Grant No. 31770674), and the National Key Research and Development Program of China (Grant No. 2017YFD0601301), the Program for Priority Academic Program Development of Jiangsu Province of China (PAPD); the Jiangsu province Natural Science Foundation of China (BK2012818). The Project of Undergraduate Innovation of Nan**g Forestry University (2019NFUSPITP1071).
Author information
Authors and Affiliations
Contributions
KF, JL, YC, YL performed most of the experiments, prepared and wrote the manuscript. YH and XL performed original draft preparation. KF, SZ, LC analyzed the data. Funding acquisition and project administration was carried out by YC. All the authors read and approved the final version of the paper.
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest declared by the authors.
Additional information
Communicated by Paloma Moncaleán.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Feng, K., Lu, J., Chen, Y. et al. The coordinated alterations in antioxidative enzymes, PeCu/ZnSOD and PeAPX2 expression facilitated in vitro Populus euphratica resistance to salinity stress. Plant Cell Tiss Organ Cult 150, 399–416 (2022). https://doi.org/10.1007/s11240-022-02292-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-022-02292-7