{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,20]],"date-time":"2026-08-20T05:23:33Z","timestamp":1787203413342,"version":"build-2736575974"},"reference-count":37,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T00:00:00Z","timestamp":1787011200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Background\/Objectives: Soybean (Glycine max) productivity is increasingly constrained by soil salinity. WIP transcription factors, a subfamily of C2H2-type zinc finger proteins, regulate cell division, differentiation, and tissue patterning in several plant species, but this gene family had not previously been systematically characterized in soybean or any other major legume crop. This study aimed to identify and characterize the GmWIP gene family genome-wide and evaluate its potential involvement in the soybean salt-stress response. Methods: Genome-wide identification of GmWIP genes was performed using sequence similarity and domain-based searches against the Wm82.gnm4.ann1 reference genome, followed by characterization of physicochemical properties, chromosomal distribution, phylogenetic relationships, gene duplication, conserved motifs, gene structure, and promoter cis-acting elements. Tissue-specific expression was examined using transcriptome data, and GmWIP responses to salt stress were profiled by RT-qPCR in roots, stems, and leaves of a salt-tolerant cultivar (HN531) and a salt-sensitive cultivar (HN563), alongside physiological measurements of oxidative stress and osmotic adjustment. Results: Thirty GmWIP genes were identified, with molecular weights from 26.90 to 57.52 kDa, distributed unevenly across 15 soybean chromosomes, with chromosomes 11, 12, and 13 forming a major hotspot (53.3% of the family). Duplication analysis detected 54 reconciled segmental duplicate gene pairs, all exhibiting Ka\/Ks values &lt; 1 (ranging from 0.0351 to 0.4471; mean 0.214), consistent with purifying selection acting on this gene set. GmWIP promoters were enriched for ABRE, MBS, and MeJA cis-acting elements. RT-qPCR showed genotype- and tissue-dependent differential expression under salt stress (e.g., up to 14.9-fold induction of GmWIP22 in HN531 stems), paralleled by superior proline accumulation (+45%), soluble sugars, and CAT activity (+38%) alongside reduced MDA accumulation in the tolerant cultivar. Conclusions: The GmWIP gene family has expanded substantially in soybean relative to previously characterized species and shows genotype-dependent transcriptional responses to salt stress, suggesting that specific GmWIP members are candidate regulators of salt tolerance and warrant further functional investigation.<\/jats:p>","DOI":"10.3390\/genes17080968","type":"journal-article","created":{"date-parts":[[2026,8,19]],"date-time":"2026-08-19T09:30:53Z","timestamp":1787131853000},"page":"968","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Genome-Wide Characterization of the WIP Transcription Factor Gene Family in Soybean and Physiological Responses to Salt Stress"],"prefix":"10.3390","volume":"17","author":[{"given":"Tianjiao","family":"Gao","sequence":"first","affiliation":[{"name":"Hinggan League Institute of Agricultural and Husbandry Sciences (Inner Mongolia Innovation Center of Biological Breeding Technology), Ulan Hot City 137400, China"},{"name":"Soybean Research Institute, Heilongjiang Academy of Agriculture Sciences, Harbin 150086, China"},{"name":"Resource Utilization and Plant Protection, College of Modern Agriculture and Ecological Environment, Heilongjiang University, Harbin 150080, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuping","family":"Yan","sequence":"additional","affiliation":[{"name":"Soybean Research Institute, Heilongjiang Academy of Agriculture Sciences, Harbin 150086, China"},{"name":"Resource Utilization and Plant Protection, College of Modern Agriculture and Ecological Environment, Heilongjiang University, Harbin 150080, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5003-9275","authenticated-orcid":false,"given":"Sobhi F.","family":"Lamlom","sequence":"additional","affiliation":[{"name":"Soybean Research Institute, Heilongjiang Academy of Agriculture Sciences, Harbin 150086, China"},{"name":"Plant Production Department, Faculty of Agriculture Saba Basha, Alexandria University, Alexandria 21531, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huilong","family":"Hong","sequence":"additional","affiliation":[{"name":"National Key Facility for Gene Resources and Genetic Improvement, Key Laboratory of Crop Germplasm Utilization, Ministry of Agriculture, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tiantian","family":"Huang","sequence":"additional","affiliation":[{"name":"Hinggan League Institute of Agricultural and Husbandry Sciences (Inner Mongolia Innovation Center of Biological Breeding Technology), Ulan Hot City 137400, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guoqing","family":"Li","sequence":"additional","affiliation":[{"name":"Hinggan League Institute of Agricultural and Husbandry Sciences (Inner Mongolia Innovation Center of Biological Breeding Technology), Ulan Hot City 137400, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Narentuya","family":"Chen","sequence":"additional","affiliation":[{"name":"Hinggan League Institute of Agricultural and Husbandry Sciences (Inner Mongolia Innovation Center of Biological Breeding Technology), Ulan Hot City 137400, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunlei","family":"Zhang","sequence":"additional","affiliation":[{"name":"Soybean Research Institute, Heilongjiang Academy of Agriculture Sciences, Harbin 150086, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-6846-3479","authenticated-orcid":false,"given":"Honglei","family":"Ren","sequence":"additional","affiliation":[{"name":"Soybean Research Institute, Heilongjiang Academy of Agriculture Sciences, Harbin 150086, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiang","family":"Qiu","sequence":"additional","affiliation":[{"name":"Soybean Research Institute, Jilin Academy of Agricultural Sciences (Northeast Agricultural Research Center of China), Changchun 130033, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lichun","family":"Huang","sequence":"additional","affiliation":[{"name":"Hinggan League Institute of Agricultural and Husbandry Sciences (Inner Mongolia Innovation Center of Biological Breeding Technology), Ulan Hot City 137400, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,8,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Liu, Q., Wang, Z., Xu, X., Zhang, H., and Li, C. (2015). Genome-wide analysis of C2H2 zinc-finger family transcription factors and their responses to abiotic stresses in poplar (Populus trichocarpa). PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0134753"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Ma, J., Zhang, X., Jiang, S., Fei, S., Kong, L., Pan, M., Ma, W., and Ren, W. (2026). The Structure, Classification, Functional Diversity and Regulatory Mechanism of Plant C2H2 Transcription Factors. Biology, 15.","DOI":"10.3390\/biology15060471"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Chang, X., Song, T., Ren, J., Wang, X., Zhou, J., Bu, Y., Chen, X., Wang, Y., Li, S., and Lei, X. (2025). Genome-wide identification of the WIP family in foxtail millet (Setaria italica) and functional analysis of SiWIP3 in inhibiting growth in transgenic Arabidopsis thaliana. BMC Genom., 26.","DOI":"10.1186\/s12864-025-12069-9"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1111\/nph.15175","article-title":"Gh WIP 2, a WIP zinc finger protein, suppresses cell expansion in Gerbera hybrida by mediating crosstalk between gibberellin, abscisic acid, and auxin","volume":"219","author":"Ren","year":"2018","journal-title":"New Phytol."},{"key":"ref_5","first-page":"925","article-title":"Seed plant-specific gene lineages involved in carpel development","volume":"34","author":"Pfannebecker","year":"2017","journal-title":"Mol. Biol. Evol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Diaz-Ramirez, D., Diaz-Garcia, U.S., Magdaleno-Garcia, G., Huep, G., Appelhagen, I., Sagasser, M., and Marsch-Martinez, N. (2022). Expression and functional analyses of the WIP gene family in Arabidopsis. Plants, 11.","DOI":"10.3390\/plants11152010"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1111\/tpj.15958","article-title":"DEFECTIVELY ORGANIZED TRIBUTARIES 5 is not required for leaf venation patterning in Arabidopsis thaliana","volume":"112","author":"Vlad","year":"2022","journal-title":"Plant J."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e70715","DOI":"10.1111\/tpj.70715","article-title":"The transcription factor NO TRANSMITTING TRACT\/WIP2 modulates cytokinin homeostasis in Arabidopsis","volume":"125","year":"2026","journal-title":"Plant J."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1038\/s42003-020-0969-2","article-title":"Integrative genome-wide analysis reveals the role of WIP proteins in inhibition of growth and development","volume":"3","author":"Roldan","year":"2020","journal-title":"Commun. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1007\/s00425-006-0351-8","article-title":"The INDEHISCENT protein regulates unequal cell divisions in Arabidopsis fruit","volume":"224","author":"Wu","year":"2006","journal-title":"Planta"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1111\/tpj.12617","article-title":"The NTT transcription factor promotes replum development in A rabidopsis fruits","volume":"80","author":"Ouwerkerk","year":"2014","journal-title":"Plant J."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1729","DOI":"10.1111\/ppl.13357","article-title":"A novel insight into transcriptional and epigenetic regulation underlying sex expression and flower development in melon (Cucumis melo L.)","volume":"173","author":"Aamir","year":"2021","journal-title":"Physiol. Plant."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2204","DOI":"10.1111\/nph.19242","article-title":"Genome evolution in plants and the origins of innovation","volume":"240","author":"Clark","year":"2023","journal-title":"New Phytol."},{"key":"ref_14","unstructured":"Singh, K., Gupta, S., Shivakumar, M., and Nataraj, V. (2025). Soybean [Glycine max (L.) Merr.] Breeding. Fundamentals of Legume Breeding: A Text for Students and Practitioners, Springer."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1007\/978-3-030-23400-3_12","article-title":"Soybean [Glycine max (L.) Merr.] breeding: History, improvement, production and future opportunities","volume":"Volume 7","author":"Anderson","year":"2019","journal-title":"Advances in Plant Breeding Strategies: Legumes"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Zhang, C., Lamlom, S.F., Hong, H., Huang, L., Yuan, R., Zhang, F., Xia, X., Wang, X., Zhao, K., and Liu, X. (2026). Integrative multi-trait phenotyping reveals coordinated root and antioxidant responses underlying drought tolerance in soybean. BMC Plant Biol., 26.","DOI":"10.1186\/s12870-026-08478-x"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"14702","DOI":"10.1038\/s41598-026-51413-1","article-title":"Integrating morphophysiological traits with salt-responsive gene expression uncovers cultivar-specific tolerance mechanisms in faba beans facing NaCl stress","volume":"16","author":"Lamlom","year":"2026","journal-title":"Sci. Rep."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"e13702","DOI":"10.1111\/ppl.13702","article-title":"Ion transporters and their regulatory signal transduction mechanisms for salinity tolerance in plants","volume":"174","author":"Joshi","year":"2022","journal-title":"Physiol. Plant."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2700909","DOI":"10.1080\/15592324.2026.2700909","article-title":"Salinity signaling networks in wheat: Crosstalk among Ca2+, ROS, phytohormones, and metabolic signals in salt adaptation","volume":"21","author":"Zamir","year":"2026","journal-title":"Plant Signal. Behav."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.plaphy.2020.08.042","article-title":"Salinity induced physiological and biochemical changes in plants: An omic approach towards salt stress tolerance","volume":"156","author":"Arif","year":"2020","journal-title":"Plant Physiol. Biochem."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Jan, R., Asaf, S., Numan, M., and Kyung-Min, K. (2021). Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy, 11.","DOI":"10.3390\/agronomy11050968"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Woodrow, P., Pontecorvo, G., Ciarmiello, L.F., Annunziata, M.G., Fuggi, A., and Carillo, P. (2011). Transcription factors and genes in abiotic stress. Crop Stress and Its Management: Perspectives and Strategies, Springer.","DOI":"10.1007\/978-94-007-2220-0_9"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"msae263","DOI":"10.1093\/molbev\/msae263","article-title":"MEGA12: Molecular evolutionary genetic analysis version 12 for adaptive and green computing","volume":"41","author":"Kumar","year":"2024","journal-title":"Mol. Biol. Evol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"W202","DOI":"10.1093\/nar\/gkp335","article-title":"MEME SUITE: Tools for motif discovery and searching","volume":"37","author":"Bailey","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"ref_25","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_26","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1093\/nar\/30.1.325","article-title":"PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences","volume":"30","author":"Lescot","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/0003-9861(68)90654-1","article-title":"Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation","volume":"125","author":"Heath","year":"1968","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1007\/BF00018060","article-title":"Rapid determination of free proline for water-stress studies","volume":"39","author":"Bates","year":"1973","journal-title":"Plant Soil"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1042\/bj0570508","article-title":"The estimation of carbohydrates in plant extracts by anthrone","volume":"57","author":"Yemm","year":"1954","journal-title":"Biochem. J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/S0076-6879(84)05016-3","article-title":"Catalase in vitro","volume":"Volume 105","author":"Aebi","year":"1984","journal-title":"Methods in Enzymology"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1550762918801071","DOI":"10.1177\/1550762918801071","article-title":"C2H2-type zinc finger proteins: Evolutionarily old and new partners of the nuclear hormone receptors","volume":"15","author":"Mackeh","year":"2018","journal-title":"Nucl. Recept. Signal."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e18455","DOI":"10.7717\/peerj.18455","article-title":"Genome-wide identification and expression analysis of C2H2 zinc finger proteins in Chinese jujube (Ziziphus jujuba Mill.) in different fruit development stages and under different levels of water stress","volume":"12","author":"Zhengwan","year":"2024","journal-title":"PeerJ"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Li, Y., Sun, A., Wu, Q., Zou, X., Chen, F., Cai, R., Xie, H., Zhang, M., and Guo, X. (2021). Comprehensive genomic survey, structural classification and expression analysis of C2H2-type zinc finger factor in wheat (Triticum aestivum L.). BMC Plant Biol., 21.","DOI":"10.1186\/s12870-021-03016-3"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1016\/j.cj.2025.02.003","article-title":"Brassica napus BnaWIP2 transcription factor promotes seed germination under salinity stress by repressing ABA biosynthesis and signaling","volume":"13","author":"He","year":"2025","journal-title":"Crop J."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1007\/s00299-026-03768-y","article-title":"MsWIP3 functions as a transcriptional regulator affecting alfalfa (Medicago sativa) response under saline-alkali stress","volume":"45","author":"Kexin","year":"2026","journal-title":"Plant Cell Rep."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1007\/s13562-021-00725-6","article-title":"Genome-wide analysis of tomato WIP family genes and their response to salt stress under glutathione treatment","volume":"31","author":"Zhou","year":"2022","journal-title":"J. Plant Biochem. Biotechnol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"e70638","DOI":"10.1111\/tpj.70638","article-title":"Insights into salt adaptation from comparative genomics of Scirpus mariqueter and a related freshwater species","volume":"124","author":"Qin","year":"2025","journal-title":"Plant J."}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/17\/8\/968\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,20]],"date-time":"2026-08-20T04:27:41Z","timestamp":1787200061000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/17\/8\/968"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,18]]},"references-count":37,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["genes17080968"],"URL":"https:\/\/doi.org\/10.3390\/genes17080968","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,18]]}}}