{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T05:02:03Z","timestamp":1790053323905,"version":"4.0.1"},"reference-count":64,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2026,9,18]],"date-time":"2026-09-18T00:00:00Z","timestamp":1789689600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Natural Science Foundation of Jilin Province","award":["YDZJ202601ZYTS281"],"award-info":[{"award-number":["YDZJ202601ZYTS281"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>Populus simonii \u00d7 P. nigra is a valuable model for studying woody plant responses to saline-alkaline stress, however the molecular mechanisms underlying its adaptation remain poorly understood. Here, integrated transcriptomic and metabolomic analyses were used to examine the responses in leaves to low (50 mmol\/L) and high (200 mmol\/L) alkaline salt stress over 7 and 14 days. Physiological assessments revealed that high-concentration stress inhibited growth, induced oxidative damage, elevated malondialdehyde (MDA) content, enhanced antioxidant enzyme activity (SOD, POD, CAT), and promoted osmoregulatory compound accumulation (soluble sugars, proline, free amino acids). RNA sequencing revealed extensive transcriptional reprogramming, with more pronounced changes under higher stress and longer exposure. KEGG enrichment highlighted pathways such as plant hormone signal transduction starch\/sucrose metabolism, and flavonoid and phenylpropanoid biosynthesis. Metabolomic profiling detected 4257 metabolites, with notable increases in amino acids, organic acids, sugars, and flavonoids. Integrated analyses revealed coordinated regulation of genes and metabolites in phenylalanine, tyrosine, and tryptophan biosynthesis, as well as hormone signaling. Weighted gene co-expression network analysis (WGCNA) identified modules correlated with physiological traits, enriched in stress-responsive transcription factors (MYB, AP2\/ERF, NAC, WRKY) and metabolic pathways. Key genes in starch\/sucrose degradation, and raffinose metabolism were upregulated, whereas phenylpropanoid metabolism-related genes were suppressed. Collectively, these findings provide insight into the adaptive mechanisms of P. simonii \u00d7 P. nigra to saline-alkaline stress, highlighting regulatory genes and pathways that contribute to tolerance and offering potential targets for enhancing poplar resilience in alkaline salt environments.<\/jats:p>","DOI":"10.3390\/biology15181656","type":"journal-article","created":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T09:01:38Z","timestamp":1789981298000},"page":"1656","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Integrated Multi-Omics Exploration of the Molecular Mechanisms Underlying Differential Responses to Saline-Alkaline Stress in Leaves of Populus simonii \u00d7 P. nigra"],"prefix":"10.3390","volume":"15","author":[{"given":"Xue","family":"Leng","sequence":"first","affiliation":[{"name":"College of Agriculture, Jilin Agricultural Science and Technology College, Jilin 132101, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"funding-acquisition","vocabulary":"credit"}]},{"given":"Sisu","family":"Li","sequence":"additional","affiliation":[{"name":"College of Agriculture, Jilin Agricultural Science and Technology College, Jilin 132101, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0922-5954","authenticated-orcid":false,"given":"Jingli","family":"Yang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"software","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"}]},{"given":"Shicheng","family":"Zhao","sequence":"additional","affiliation":[{"name":"School of Pharmacy, Harbin University of Commerce, Harbin 150040, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"visualization","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9660-7127","authenticated-orcid":false,"given":"Jinhui","family":"Gao","sequence":"additional","affiliation":[{"name":"Heilongjiang Academy of Forestry Yichun Branch, Yichun 153000, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"visualization","vocabulary":"credit"}]},{"given":"Ke","family":"Ma","sequence":"additional","affiliation":[{"name":"Heilongjiang Academy of Forestry Yichun Branch, Yichun 153000, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"data-curation","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"}]},{"given":"Hanzeng","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Agriculture, Jilin Agricultural Science and Technology College, Jilin 132101, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"data-curation","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"}]}],"member":"1968","published-online":{"date-parts":[[2026,9,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1071\/FP12285","article-title":"The integration of activity in saline environments: Problems and perspectives","volume":"40","author":"Cheeseman","year":"2013","journal-title":"Funct. Plant Biol."},{"key":"ref_2","first-page":"1497","article-title":"Effects of alkali-stress on Aneurolepidium chinense and Helianthus annuus","volume":"16","author":"Yan","year":"2005","journal-title":"Ying Yong Sheng Tai Xue Bao"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1007\/s00425-024-04368-4","article-title":"Inroads into saline-alkaline stress response in plants: Unravelling morphological, physiological, biochemical, and molecular mechanisms","volume":"259","author":"Sharma","year":"2024","journal-title":"Planta"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1016\/j.devcel.2020.10.012","article-title":"Thriving under stress: How plants balance growth and the stress response","volume":"55","author":"Zhang","year":"2020","journal-title":"Dev. Cell"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Fang, S., Hou, X., and Liang, X. (2021). Response mechanisms of plants under saline-alkali stress. Front. Plant Sci., 12.","DOI":"10.3389\/fpls.2021.667458"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Sun, J., He, L., and Li, T. (2019). Response of seedling growth and physiology of Sorghum bicolor (L.) moench to saline-alkali stress. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0220340"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1918885","DOI":"10.1080\/15592324.2021.1918885","article-title":"Analysis of drought and salt-alkali tolerance in tobacco by overexpressing wrky39 gene from Populus trichocarpa","volume":"16","author":"Niu","year":"2021","journal-title":"Plant Signal. Behav."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Guo, R., Yang, Z., Li, F., Yan, C., Zhong, X., Liu, Q., Xia, X., Li, H., and Zhao, L. (2015). Comparative metabolic responses and adaptive strategies of wheat (Triticum aestivum) to salt and alkali stress. BMC Plant Biol., 15.","DOI":"10.1186\/s12870-015-0546-x"},{"key":"ref_9","first-page":"100017","article-title":"Mechanisms of plant responses and adaptation to soil salinity","volume":"1","author":"Zhao","year":"2020","journal-title":"Innovation"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Qu, D., Show, P., and Miao, X. (2021). Transcription factor chbzip1 from Alkaliphilic Microalgae Chlorella sp. Bld enhancing alkaline tolerance in transgenic Arabidopsis thaliana. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22052387"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Wang, J., Zhang, Y., Yan, X., and Guo, J. (2020). Physiological and transcriptomic analyses of yellow horn (Xanthoceras sorbifolia) provide important insights into salt and saline-alkali stress tolerance. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0244365"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Liu, W., Li, P., Wang, X., Zhang, Z., and Wang, Y. (2024). Functional identification of malus halliana mhbzip23 gene demonstrates that it enhances saline-alkali stress tolerance in Arabidopsis thaliana. Plants, 13.","DOI":"10.3390\/plants13131803"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Cao, Y., Song, H., and Zhang, L. (2022). New insight into plant saline-alkali tolerance mechanisms and application to breeding. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms232416048"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Sharma, A., Shahzad, B., Rehman, A., Bhardwaj, R., Landi, M., and Zheng, B. (2019). Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules, 24.","DOI":"10.3390\/molecules24132452"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Ninkuu, V., Aluko, O.O., Yan, J., Zeng, H., Liu, G., Zhao, J., Li, H., Chen, S., and Dakora, F.D. (2025). Phenylpropanoids metabolism: Recent insight into stress tolerance and plant development cues. Front. Plant Sci., 16.","DOI":"10.3389\/fpls.2025.1571825"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1111\/jipb.13054","article-title":"Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions","volume":"63","author":"Dong","year":"2021","journal-title":"J. Integr. Plant Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2543","DOI":"10.1099\/mic.0.28136-0","article-title":"The gene stla encodes a phenylalanine ammonia-lyase that is involved in the production of a stilbene antibiotic in Photorhabdus luminescens TT01","volume":"151","author":"Williams","year":"2005","journal-title":"Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1016\/S1360-1385(02)02290-2","article-title":"Impact of phyto-oxylipins in plant defense","volume":"7","author":"Blee","year":"2002","journal-title":"Trends Plant Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.plaphy.2010.01.024","article-title":"Analysis of expressed sequence tags from a NaHCO3-treated alkali-tolerant plant, Chloris virgata","volume":"48","author":"Nishiuchi","year":"2010","journal-title":"Plant Physiol. Biochem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"109048","DOI":"10.1016\/j.plaphy.2024.109048","article-title":"Multi-omics integrative analysis provided new insights into alkaline stress in alfalfa","volume":"215","author":"Li","year":"2024","journal-title":"Plant Physiol. Biochem."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1900","DOI":"10.1111\/tpj.16896","article-title":"Metabolomics and transcriptomics analysis revealed the response mechanism of alfalfa to combined cold and saline-alkali stress","volume":"119","author":"Liu","year":"2024","journal-title":"Plant J."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"5477","DOI":"10.1021\/acs.jafc.3c07139","article-title":"Integrated metabolomics and transcriptomics analyses highlight the flavonoid compounds response to alkaline salt stress in Glycyrrhiza uralensis leaves","volume":"72","author":"Lv","year":"2024","journal-title":"J. Agric. Food Chem."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"uhae243","DOI":"10.1093\/hr\/uhae243","article-title":"Saline-alkali stress affects the accumulation of proanthocyanidins and sesquiterpenoids via the MYB5-ANR\/TPS31 cascades in the rose petals","volume":"11","author":"Wang","year":"2024","journal-title":"Hortic. Res."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Liang, Y., Li, X., Lei, F., Yang, R., Bai, W., Yang, Q., and Zhang, D. (2024). Transcriptome profiles reveals scdreb10 from Syntrichia caninervis regulated phenylpropanoid biosynthesis and starch\/sucrose metabolism to enhance plant stress tolerance. Plants, 13.","DOI":"10.3390\/plants13020205"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Sengupta, S., Mukherjee, S., Basak, P., and Majumder, A.L. (2015). Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Front. Plant Sci., 6.","DOI":"10.3389\/fpls.2015.00656"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Elango, D., Rajendran, K., Van der Laan, L., Sebastiar, S., Raigne, J., Thaiparambil, N.A., El Haddad, N., Raja, B., Wang, W., and Ferela, A. (2022). Raffinose family oligosaccharides: Friend or foe for human and plant health?. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.829118"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Sanyal, R., Kumar, S., Pattanayak, A., Kar, A., and Bishi, S.K. (2023). Optimizing raffinose family oligosaccharides content in plants: A tightrope walk. Front. Plant Sci., 14.","DOI":"10.3389\/fpls.2023.1134754"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"32717","DOI":"10.1038\/srep32717","article-title":"Na2CO3-responsive mechanisms in halophyte Puccinellia tenuiflora roots revealed by physiological and proteomic analyses","volume":"6","author":"Zhao","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"153916","DOI":"10.1016\/j.jplph.2023.153916","article-title":"Mechanisms of plant saline-alkaline tolerance","volume":"281","author":"Rao","year":"2023","journal-title":"J. Plant Physiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"The Uniprot Consortium (2025). Uniprot: The universal protein knowledgebase in 2025. Nucleic Acids Res., 53, D609\u2013D617.","DOI":"10.1093\/nar\/gkae1010"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"D672","DOI":"10.1093\/nar\/gkae909","article-title":"KEGG: Biological systems database as a model of the real world","volume":"53","author":"Kanehisa","year":"2025","journal-title":"Nucleic Acids Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e70083","DOI":"10.1002\/pro.70083","article-title":"Mining the UniProtKB\/Swiss-Prot database for antimicrobial peptides","volume":"34","author":"Li","year":"2025","journal-title":"Protein Sci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"D523","DOI":"10.1093\/nar\/gkae997","article-title":"The Pfam protein families database: Embracing AI\/ML","volume":"53","author":"Andreeva","year":"2025","journal-title":"Nucleic Acids Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1038\/75556","article-title":"Gene ontology: Tool for the unification of biology","volume":"25","author":"Ashburner","year":"2000","journal-title":"Nat. Genet."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3292","DOI":"10.1038\/s41596-024-01020-z","article-title":"Using clusterprofiler to characterize multiomics data","volume":"19","author":"Xu","year":"2024","journal-title":"Nat. Protoc."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1016\/j.molp.2023.09.010","article-title":"Tbtools-II: A \u201cone for all, all for one\u201d bioinformatics platform for biological big-data mining","volume":"16","author":"Chen","year":"2023","journal-title":"Mol. Plant"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"4052","DOI":"10.1093\/jxb\/erae124","article-title":"Overexpressing GLUTAMINE SYNTHETASE 1;2 maintains carbon and nitrogen balance under high-ammonium conditions and results in increased tolerance to ammonium toxicity in hybrid poplar","volume":"75","author":"Leng","year":"2024","journal-title":"J. Exp. Bot."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Pettengill, E.A., Parmentier-Line, C., and Coleman, G.D. (2012). Evaluation of qPCR reference genes in two genotypes of Populus for use in photoperiod and low-temperature studies. BMC Res. Notes, 5.","DOI":"10.1186\/1756-0500-5-366"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1097\/00019606-200603000-00009","article-title":"Validation of the 2-deltadeltact calculation as an alternate method of data analysis for quantitative PCR of BCR-ABL P210 transcripts","volume":"15","author":"Arocho","year":"2006","journal-title":"Diagn. Mol. Pathol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"4731","DOI":"10.1093\/jxb\/err210","article-title":"Role of DREBs in regulation of abiotic stress responses in plants","volume":"62","author":"Lata","year":"2011","journal-title":"J. Exp. Bot."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1007\/s00299-023-02999-7","article-title":"Integration of light and ABA signaling pathways to combat drought stress in plants","volume":"42","author":"Mukherjee","year":"2023","journal-title":"Plant Cell Rep."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"894","DOI":"10.1111\/plb.13303","article-title":"Auxin and its role in plant development: Structure, signalling, regulation and response mechanisms","volume":"23","author":"Gomes","year":"2021","journal-title":"Plant Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1007\/978-1-0716-2867-6_19","article-title":"Microtubule reorganization during ABA-induced stomatal closure in Arabidopsis","volume":"2604","author":"Dou","year":"2023","journal-title":"Methods Mol. Biol."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Li, Q., Zhu, P., Yu, X., Xu, J., and Liu, G. (2024). Physiological and molecular mechanisms of rice tolerance to salt and drought stress: Advances and future directions. Int. J. Mol. Sci., 25.","DOI":"10.20944\/preprints202407.1678.v1"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"3470","DOI":"10.1105\/tpc.105.035659","article-title":"AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis","volume":"17","author":"Fujita","year":"2005","journal-title":"Plant Cell"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"108284","DOI":"10.1016\/j.plaphy.2023.108284","article-title":"Perspective of ethylene biology for abiotic stress acclimation in plants","volume":"210","author":"Khan","year":"2024","journal-title":"Plant Physiol. Biochem."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.plaphy.2019.12.019","article-title":"Genome-wide analysis of ethylene-response factor family in adzuki bean and functional determination of VaERF3 under saline-alkaline stress","volume":"147","author":"Li","year":"2020","journal-title":"Plant Physiol. Biochem."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1007\/s00425-016-2532-4","article-title":"Gserf6, an ethylene-responsive factor from Glycine soja, mediates the regulation of plant bicarbonate tolerance in Arabidopsis","volume":"244","author":"Yu","year":"2016","journal-title":"Planta"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1007\/s11103-017-0623-7","article-title":"A novel AP2\/ERF family transcription factor from Glycine soja, GsERF71, is a DNA binding protein that positively regulates alkaline stress tolerance in Arabidopsis","volume":"94","author":"Yu","year":"2017","journal-title":"Plant Mol. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2355","DOI":"10.1111\/nph.17323","article-title":"Metabolomics-driven gene mining and genetic improvement of tolerance to salt-induced osmotic stress in maize","volume":"230","author":"Liang","year":"2021","journal-title":"New Phytol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1091","DOI":"10.1111\/nph.15862","article-title":"Osmotic adjustment and energy limitations to plant growth in saline soil","volume":"225","author":"Munns","year":"2020","journal-title":"New Phytol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1563","DOI":"10.1007\/s00299-019-02467-1","article-title":"A maize stress-responsive Di19 transcription factor, ZmDi19-1, confers enhanced tolerance to salt in transgenic Arabidopsis","volume":"38","author":"Zhang","year":"2019","journal-title":"Plant Cell Rep."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1038\/s41438-019-0172-0","article-title":"Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline-alkali stress","volume":"6","author":"Jia","year":"2019","journal-title":"Hortic. Res."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1111\/tpj.15191","article-title":"The apple palmitoyltransferase MdPAT16 influences sugar content and salt tolerance via an mMdCBL1-MdCIPK13-MdSUT2.2 pathway","volume":"106","author":"Jiang","year":"2021","journal-title":"Plant J."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Hanin, M., Ebel, C., Ngom, M., Laplaze, L., and Masmoudi, K. (2016). New insights on plant salt tolerance mechanisms and their potential use for breeding. Front. Plant Sci., 7.","DOI":"10.3389\/fpls.2016.01787"},{"key":"ref_58","first-page":"701596","article-title":"Mechanism of salinity tolerance in plants: Physiological, biochemical, and molecular characterization","volume":"2014","author":"Gupta","year":"2014","journal-title":"Int. J. Genom."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"An, Y., Song, L., Liu, Y., Shu, Y., and Guo, C. (2016). De novo transcriptional analysis of alfalfa in response to saline-alkaline stress. Front. Plant Sci., 7.","DOI":"10.3389\/fpls.2016.00931"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Wang, X., Ajab, Z., Liu, C., Hu, S., Liu, J., and Guan, Q. (2020). Overexpression of transcription factor SlWRKY28 improved the tolerance of Populus davidiana \u00d7 P. Bolleana to alkaline salt stress. BMC Genet., 21.","DOI":"10.1186\/s12863-020-00904-9"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"e7817","DOI":"10.7717\/peerj.7817","article-title":"Genome-wide identification and expression analysis of the WRKY genes in sugar beet (Beta vulgaris L.) under alkaline stress","volume":"7","author":"Wu","year":"2019","journal-title":"PeerJ"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1139\/gen-2018-0132","article-title":"Functional activation of a novel R2R3-MYB protein gene, GmMYB68, confers salt-alkali resistance in soybean (Glycine max L.)","volume":"63","author":"He","year":"2020","journal-title":"Genome"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1016\/j.bbrc.2018.03.026","article-title":"Overexpression of a novel transcriptional repressor GmMYB3a negatively regulates salt-alkali tolerance and stress-related genes in soybean","volume":"498","author":"He","year":"2018","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Wang, L., Li, Z., Lu, M., and Wang, Y. (2017). ThNAC13, a NAC transcription factor from Tamarix hispida, confers salt and osmotic stress tolerance to transgenic Tamarix and Arabidopsis. Front. Plant Sci., 8.","DOI":"10.3389\/fpls.2017.00635"}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/18\/1656\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T04:13:53Z","timestamp":1790050433000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/18\/1656"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,18]]},"references-count":64,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2026,9]]}},"alternative-id":["biology15181656"],"URL":"https:\/\/doi.org\/10.3390\/biology15181656","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,18]]}}}