{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,11]],"date-time":"2026-08-11T12:36:56Z","timestamp":1786451816759,"version":"build-2736575974"},"reference-count":47,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T00:00:00Z","timestamp":1786060800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Jilin Provincial Science and Technology Development","award":["20250602061RC"],"award-info":[{"award-number":["20250602061RC"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Int. J. Mol. Sci.","IJMS"],"abstract":"<jats:p>Plant lipid transfer proteins (LTPs) are key components in defense against biotic and abiotic stresses, yet their functional diversity in Panax ginseng remains unclear. This study aimed to characterize LTP and evaluate its role in stress tolerance. The gene was identified from ginseng transcriptome data and analyzed using bioinformatics tools to determine its structural and physicochemical properties. Panax ginseng lipid transfer protein (PgLTP) was then heterologously expressed in Arabidopsis thaliana (A. thaliana). Transgenic lines were evaluated under fungal infection, drought, and salt stress conditions. Physiological and molecular responses, including reactive oxygen species(ROS) accumulation, malondialdehyde (MDA) content, proline levels, electrolyte leakage, and stomatal behavior under abscisic acid (ABA) treatment, were assessed. Bioinformatic analysis indicated that PgLTP encodes a small protein of approximately 12 kDa containing ten conserved cysteine residues, four \u03b1-helices, a signal peptide, and a transmembrane region, suggesting structural divergence from typical LTPs. Functional assays showed that transgenic plants exhibited significantly reduced disease indices under Fusarium oxysporum (F. oxysporum) and Cylindrocarpon destructans (C. destructans) infection. Under drought and salinity stress, transgenic lines demonstrated higher germination and survival rates, enhanced proline accumulation, reduced oxidative damage, and lower electrolyte leakage compared with the wild type. Additionally, PgLTP exhibited enhanced ABA-responsive stomatal closure, which was associated with reduced water loss. These findings indicate that PgLTP contributes to plant tolerance against both biotic and abiotic stresses, which is associated with changes in redox status, osmotic adjustment capacity, and stomatal responses.<\/jats:p>","DOI":"10.3390\/ijms27167094","type":"journal-article","created":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T16:00:43Z","timestamp":1786118443000},"page":"7094","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Bioinformatic Characterization and Functional Analysis of a Lipid Transfer Protein from Panax ginseng Involved in Biotic and Abiotic Stress Responses"],"prefix":"10.3390","volume":"27","author":[{"ORCID":"https:\/\/orcid.org\/0009-0005-9275-1120","authenticated-orcid":false,"given":"Tianxia","family":"Sun","sequence":"first","affiliation":[{"name":"Jilin Ginseng Academy, Changchun University of Chinese Medicine, Changchun 130117, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhimei","family":"Liu","sequence":"additional","affiliation":[{"name":"Jilin Ginseng Academy, Changchun University of Chinese Medicine, Changchun 130117, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingbin","family":"Liu","sequence":"additional","affiliation":[{"name":"Jilin Ginseng Academy, Changchun University of Chinese Medicine, Changchun 130117, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heng","family":"Li","sequence":"additional","affiliation":[{"name":"Jilin Ginseng Academy, Changchun University of Chinese Medicine, Changchun 130117, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miao","family":"Zhang","sequence":"additional","affiliation":[{"name":"Jilin Ginseng Academy, Changchun University of Chinese Medicine, Changchun 130117, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ge","family":"Hui","sequence":"additional","affiliation":[{"name":"Jilin Ginseng Academy, Changchun University of Chinese Medicine, Changchun 130117, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu","family":"Zhao","sequence":"additional","affiliation":[{"name":"Jilin Ginseng Academy, Changchun University of Chinese Medicine, Changchun 130117, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,8,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/s40011-022-01387-7","article-title":"Biomolecules regulating defense mechanism in plants","volume":"93","author":"Chowdhary","year":"2023","journal-title":"Proc. Natl. Acad. Sci. India Sect. B Biol. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"376","DOI":"10.2174\/1389203722666210125122827","article-title":"Mechanisms of plant defense under pathogen stress: A review","volume":"22","author":"Sood","year":"2021","journal-title":"Curr. Protein Pept. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Arya, G.C., Sarkar, S., Manasherova, E., Aharoni, A., and Cohen, H. (2021). The plant cuticle: An ancient guardian barrier set against long-standing rivals. Front. Plant Sci., 12.","DOI":"10.3389\/fpls.2021.663165"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.aac.2023.01.003","article-title":"Peptides, new tools for plant protection in eco-agriculture","volume":"2","author":"Zhang","year":"2023","journal-title":"Adv. Agrochem."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Apostolova, E.L. (2023). Molecular mechanisms of plant defense against abiotic stress. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms241210339"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"5492","DOI":"10.1039\/D3FO01119D","article-title":"Plant antimicrobial peptides: A comprehensive review of their classification, production, mode of action, functions, applications, and challenges","volume":"14","author":"Zou","year":"2023","journal-title":"Food Funct."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"170531","DOI":"10.1016\/j.peptides.2021.170531","article-title":"Biotechnological applications of versatile plant lipid transfer proteins (LTPs)","volume":"140","author":"Maximiano","year":"2021","journal-title":"Peptides"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1007\/s00425-016-2585-4","article-title":"Lipid transfer proteins: Classification, nomenclature, structure, and function","volume":"244","author":"Salminen","year":"2016","journal-title":"Planta"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Santos-Silva, C.A.D., da Silva, M.J., de Freitas, C.D.T., de Oliveira, J.T.A., and de Sales, M.P. (2023). From gene to transcript and peptide: A deep overview on non-specific lipid transfer proteins (nsLTPs). Antibiotics, 12.","DOI":"10.3390\/antibiotics12050939"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.plaphy.2021.12.026","article-title":"Plant non-specific lipid transfer proteins: An overview","volume":"171","author":"Missaoui","year":"2022","journal-title":"Plant Physiol. Biochem."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e491","DOI":"10.1002\/pld3.491","article-title":"Identification of potato Lipid transfer protein gene family and expression verification of drought genes StLTP1and StLTP7","volume":"7","author":"Wang","year":"2023","journal-title":"Plant Direct"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Zhang, Y., Wang, L., Liu, Y., Zhang, Q., Wei, Q., and Zhang, W. (2023). Plants\u2019 response to abiotic stress: Mechanisms and strategies. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms241310915"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Amador, V.C., dos Santos, I.S., Marques, J.P.C., and Franco, O.L. (2021). Lipid Transfer Proteins (LTPs)\u2014Structure, Diversity and Roles beyond Antimicrobial Activity. Antibiotics, 10.","DOI":"10.3390\/antibiotics10111281"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Fu, J., Gao, J., Liang, Z., and Yang, D. (2020). PDI-regulated disulfide bond formation in protein folding and biomolecular assembly. Molecules, 26.","DOI":"10.3390\/molecules26010171"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.biotechadv.2004.09.004","article-title":"The importance of disulfide bridging","volume":"23","author":"Swaisgood","year":"2005","journal-title":"Biotechnol. Adv."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"135219","DOI":"10.1016\/j.ijbiomac.2024.135219","article-title":"SlLTPg1, a tomato lipid transfer protein, positively regulates in response to biotic stresses","volume":"279","author":"Liu","year":"2024","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/s11240-023-02445-2","article-title":"Lipid transfer proteins: Structure, classification and prospects of genetic engineering for improved disease resistance in plants","volume":"153","author":"Iqbal","year":"2023","journal-title":"Plant Cell Tissue Organ Cult."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1093\/mp\/ssr019","article-title":"Evolutionary history of the non-specific lipid transfer proteins","volume":"4","author":"Edstam","year":"2011","journal-title":"Mol. Plant"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1093\/protein\/12.2.85","article-title":"Twilight zone of protein sequence alignments","volume":"12","author":"Burkhard","year":"1999","journal-title":"Protein Eng."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1093\/sysbio\/42.2.182","article-title":"An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis","volume":"42","author":"Hillis","year":"1993","journal-title":"Syst. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1080\/106351500750049761","article-title":"Improved bootstrap confidence limits in large-scale phylogenies, with an example from neo-astragalus (Leguminosae)","volume":"49","author":"Sanderson","year":"2000","journal-title":"Syst. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1046\/j.1365-313X.1994.6060849.x","article-title":"The promoter of the barley aleurone-specific gene encoding a putative 7 kDa lipid transfer protein confers aleurone cell-specific expression in transgenic rice","volume":"6","author":"Kalla","year":"1994","journal-title":"Plant J."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1006\/jcrs.2000.0315","article-title":"Mini review: Structure, biological and technological functions of lipid transfer proteins and indolines, the major lipid binding proteins from cereal kernels","volume":"32","author":"Douliez","year":"2000","journal-title":"J. Cereal Sci."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Boutrot, F., Chantret, N., and Gautier, M.F. (2008). Genome-wide analysis of the rice and arabidopsis non-specific lipid transfer protein (nsltp) gene families and identification of wheat nsltp genes by est data mining. BMC Genom., 9.","DOI":"10.1186\/1471-2164-9-86"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"130811","DOI":"10.1016\/j.ijbiomac.2024.130811","article-title":"Characterization of type1 lipid transfer protein from Citrus sinensis: Unraveling its potential as an antimicrobial and insecticidal agent","volume":"265","author":"Rode","year":"2024","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Ku\u017aniak, E., and Gajewska, E. (2024). Lipids and lipid-mediated signaling in plant pathogen interactions. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25137255"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Duan, M., Wang, Y., Zhang, L., Li, Z., Zhang, S., Guo, Y., Zhang, X., and Huang, S. (2024). The ectopic expression of the mpdir1(t)gene enhances the response of plants from Arabidopsis thaliana to biotic stress by regulating the defense genes and antioxidant flavonoids. Plants, 13.","DOI":"10.3390\/plants13192692"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Xue, Y., Zhang, L., Li, Z., Zhang, S., Guo, Y., Zhang, X., and Huang, S. (2022). Genome-wide identification and expression analysis of nsLTP gene family in rapeseed (Brassica napus) reveals their critical roles in biotic and abiotic stress responses. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23158372"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"7610","DOI":"10.1038\/s41598-024-57376-5","article-title":"Genome-wide identification and evolutionary analysis of the AP2\/EREBP, COX and LTP genes in Zea mays L. under drought stress","volume":"14","author":"Maghraby","year":"2024","journal-title":"Sci. Rep."},{"key":"ref_30","first-page":"211","article-title":"Bioinformatic analysis and expression pattern of LTP family genes in Populus davidiana \u00d7 P. alba var. pyramidalis","volume":"42","author":"Shi","year":"2022","journal-title":"Bull. Bot. Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"125007","DOI":"10.1016\/j.ijbiomac.2023.125007","article-title":"NtLTP1.38, a plasma membrane-localized protein, mediates lipid metabolism and salt tolerance in Nicotiana tabacum","volume":"242","author":"Yang","year":"2023","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Vafina, G., Mukhtarova, L., Burganov, A., Kuzmina, E., Kuznetsov, V., and Kuznetsov, V.V. (2024). The long-distance transport of jasmonates in salt-treated pea plants and involvement of lipid transfer proteins in the process. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25137486"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.plaphy.2022.01.002","article-title":"Systematic analysis of the non-specific lipid transfer protein gene family in Nicotiana tabacum reveal its potential roles in stress responses","volume":"172","author":"Yang","year":"2022","journal-title":"Plant Physiol. Biochem."},{"key":"ref_34","first-page":"96","article-title":"Expression analysis of lipid transfer protein gene in wheat (Triticum aestivum) under drought stress","volume":"9","author":"Nikaeen","year":"2020","journal-title":"Iran. J. Genet. Plant Breed."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"114683","DOI":"10.1016\/j.indcrop.2022.114683","article-title":"Poplar glycosylphosphatidylinositol-anchored lipid transfer proteins respond to osmotic stress by regulating fatty acid biosynthesis","volume":"179","author":"Wei","year":"2022","journal-title":"Ind. Crops Prod."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"102096","DOI":"10.1016\/j.pmpp.2023.102096","article-title":"The wheat lipid transfer protein (TdLTP2) mitigates biotic and abiotic stress damages in transgenic Arabidopsis thaliana plants","volume":"127","author":"Missaoui","year":"2023","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"111899","DOI":"10.1016\/j.postharvbio.2022.111899","article-title":"Slltpg3, a non-specific lipid transfer protein, acts on the cuticle synthetic pathway to delay water loss and softening of tomato fruit","volume":"188","author":"Wang","year":"2022","journal-title":"Postharvest Biol. Technol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1285","DOI":"10.1093\/jxb\/erae473","article-title":"Lipid transfer protein VAS inhibits the hypersensitive response via reactive oxygen species signaling in Nicotiana benthamiana","volume":"76","author":"Koyama","year":"2025","journal-title":"J. Exp. Bot."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1111\/mpp.13007","article-title":"A nonspecific lipid transfer protein, StLTP10, mediates resistance to Phytophthora infestans in potato","volume":"22","author":"Wang","year":"2020","journal-title":"Mol. Plant Pathol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Duo, J., Zhang, L., Li, Z., Zhang, S., Guo, Y., Zhang, X., and Huang, S. (2021). Genome-wide identification and expression profile under abiotic stress of the barley non-specific lipid transfer protein gene family and its qingke orthologues. BMC Genom., 22.","DOI":"10.1186\/s12864-021-07958-8"},{"key":"ref_41","unstructured":"Choudhary, A. (2023). Mechanism of Salinity Tolerance in Elite Wheat (Triticum aestivum L.) Germplasm. [Ph.D. Thesis, Punjab Agricultural University]."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1038\/nprot.2006.83","article-title":"The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: Twenty-something years on","volume":"1","author":"Chomczynski","year":"2006","journal-title":"Nat. Protoc."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"102294","DOI":"10.1016\/j.pmpp.2024.102294","article-title":"Overexpression of the Panax ginseng CyP gene enhances abiotic and biotic stress tolerance in transgenic Arabidopsis","volume":"133","author":"Sun","year":"2024","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_44","unstructured":"Fang, Z. (1998). Research Methods for Plant Diseases, China Agriculture Press. [3rd ed.]."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"16203","DOI":"10.1038\/nplants.2016.203","article-title":"ROS accumulation and antiviral defence control by microrna528 in rice","volume":"3","author":"Wu","year":"2017","journal-title":"Nat. Plants"},{"key":"ref_46","first-page":"288","article-title":"Separation and identification of malonaldehyde in plant tissue","volume":"28","author":"Changcheng","year":"1992","journal-title":"Plant Physiol. Commun."},{"key":"ref_47","unstructured":"Korth, L.M., Ritchie, P.E., and Tatham, B.D. (2015). Signal Transduction, Academic Press. [2nd ed.]."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/27\/16\/7094\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,11]],"date-time":"2026-08-11T11:52:21Z","timestamp":1786449141000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/27\/16\/7094"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,7]]},"references-count":47,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["ijms27167094"],"URL":"https:\/\/doi.org\/10.3390\/ijms27167094","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,7]]}}}