{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,31]],"date-time":"2025-10-31T01:44:48Z","timestamp":1761875088193,"version":"build-2065373602"},"reference-count":56,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2025,10,30]],"date-time":"2025-10-30T00:00:00Z","timestamp":1761782400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Science and Technology Planning Project of Guangdong Province, China","award":["2023B1212060047"],"award-info":[{"award-number":["2023B1212060047"]}]},{"name":"Higher Education Teaching Reform Program of Guangdong Province"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Background\/Objectives: Long non-coding RNA (lncRNA) was structurally similar to mRNAs, yet they could not be translated into proteins. While an increasing number of reports have systematically identified and described lncRNA in model species, information about non-model species remains scarce. Sea cucumber Holothuria leucospilota could be used for both medicinal and food purposes, which have high economic value, gradually attracting the attention of researchers. Methods: In this research, we constructed lncRNA library and compared the difference in lncRNA expression profiles between testis and ovary of sea cucumber H. leucospilota. To elucidate the molecular interactions between lncRNA and mRNA, we computationally predicted potential complementary binding sites through analysis of both cis- and trans-acting antisense mechanisms. Subsequent Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses demonstrated that the identified target genes are potentially involved in the regulatory pathways governing gonad development. Results: Quantitative reverse transcription PCR analysis showed that MSTRG.32831.1-sox9 and MSTRG.57315.1-mthfr exhibited a high expression pattern in testis; while MSTRG.11041.1-mafa and MSTRG.11074.1-macf1 showed a high expression pattern in the ovary. Conclusions: Deciphering lncRNA\u2013mRNA expression patterns may uncover fundamental principles governing reproductive regulation in marine invertebrates. This discovery not only deepens understanding in this field but also provides valuable comparative insights for developmental biology.<\/jats:p>","DOI":"10.3390\/genes16111293","type":"journal-article","created":{"date-parts":[[2025,10,31]],"date-time":"2025-10-31T01:23:59Z","timestamp":1761873839000},"page":"1293","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Gonadal Transcriptome Analysis Reveals the lncRNA\u2013mRNA Pair in Sea Cucumber Holothuria leucospilota"],"prefix":"10.3390","volume":"16","author":[{"given":"Jing","family":"Zhang","sequence":"first","affiliation":[{"name":"School of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou 510006, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0003-9245-0964","authenticated-orcid":false,"given":"Jingwei","family":"Yu","sequence":"additional","affiliation":[{"name":"School of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou 510006, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0789-4938","authenticated-orcid":false,"given":"Yang","family":"Zhang","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Applied Marine Biology, Guangzhou 510301, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Meiyao","family":"Su","sequence":"additional","affiliation":[{"name":"School of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou 510006, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,10,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Zhang, S., Shao, Y., and Li, C. (2021). Characterization of Host lncRNAs in Response to Vibrio splendidus Infection and Function as Efficient miRNA Sponges in Sea Cucumber. Front. Immunol., 12.","DOI":"10.3389\/fimmu.2021.792040"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1038\/nsmb.1806","article-title":"Pol II and its Associated Epigenetic Marks Are Present at Pol III-Transcribed Noncoding RNA Genes","volume":"17","author":"Barski","year":"2010","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1038\/349038a0","article-title":"A Gene from the Region of the Human X Inactivation Centre Is Expressed Exclusively from the Inactive X Chromosome","volume":"349","author":"Brown","year":"1991","journal-title":"Nature"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Li, Y., Zhai, H., Tong, L., Wang, C., Xie, Z., and Zheng, K. (2023). LncRNA Functional Screening in Organismal Development. Noncoding RNA, 9.","DOI":"10.3390\/ncrna9040036"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"365","DOI":"10.2217\/epi-2021-0414","article-title":"The significance of studying functional lncRNA in mouse spermatogenesis","volume":"14","author":"Tang","year":"2022","journal-title":"Epigenomics"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1007\/978-94-017-7417-8_5","article-title":"Non-coding RNA in Ovarian Development and Disease","volume":"886","author":"Fitzgerald","year":"2016","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Mao, H., Chen, L., Bao, R., Weng, S., Wang, M., Xu, N., Qi, L., and Wang, J. (2022). Mechanisms of Oogenesis-Related Long Non-coding RNAs in Porcine Ovaries Treated With Recombinant Pig Follicle-Stimulating Hormone. Front. Vet. Sci., 8.","DOI":"10.3389\/fvets.2021.838703"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1016\/j.fsi.2021.12.014","article-title":"Full-length transcriptome sequencing of Heliocidaris crassispina using PacBio single-molecule real-time sequencing","volume":"120","author":"Huang","year":"2022","journal-title":"Fish Shellfish Immunol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"dsae020","DOI":"10.1093\/dnares\/dsae020","article-title":"Chromosome-level genome assembly and annotation of the black sea urchin Arbacia lixula (Linnaeus, 1758)","volume":"31","author":"Carreras","year":"2024","journal-title":"DNA Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1007\/s12192-021-01207-3","article-title":"Novel lncRNA lncRNA001074 participates in the low salinity-induced response in the sea cucumber Apostichopus japonicus by targeting the let-7\/NKA\u03b1 axis","volume":"26","author":"Shang","year":"2021","journal-title":"Cell Stress Chaperones"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1007\/s10126-016-9711-y","article-title":"Long Non-Coding RNAs (lncRNAs) of Sea Cucumber: Large-Scale Prediction, Expression Profiling, Non-Coding Network Construction, and lncRNA-microRNA-Gene Interaction Analysis of lncRNAs in Apostichopus japonicus and Holothuria glaberrima During LPS Challenge and Radial Organ Complex Regeneration","volume":"18","author":"Mu","year":"2016","journal-title":"Mar. Biotechnol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Chen, X., Han, W., Yang, R., Zhu, X., Li, S., Wang, Y., Sun, X., Li, Y., Bao, L., and Zhang, L. (2024). Transcriptome Analysis Reveals the lncRNA-mRNA Co-expression Network Regulating the Aestivation of Sea Cucumber. Mar. Biotechnol., 27.","DOI":"10.1007\/s10126-024-10388-8"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"136045","DOI":"10.1016\/j.scitotenv.2019.136045","article-title":"The regulation mechanism of lncRNAs and mRNAs in sea cucumbers under global climate changes: Defense against thermal and hypoxic stresses","volume":"709","author":"Huo","year":"2020","journal-title":"Sci. Total Environ."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1016\/j.fsi.2022.04.040","article-title":"Dynamic N6-methyladenosine modification of lncRNA modulated by METTL3 during bacterial disease development in an echinoderm","volume":"124","author":"Zhang","year":"2022","journal-title":"Fish Shellfish Immunol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1007\/s10126-018-9798-4","article-title":"Gonad Transcriptome Analysis of the Pacific Oyster Crassostrea gigas Identifies Potential Genes Regulating the Sex Determination and Differentiation Process","volume":"20","author":"Yue","year":"2018","journal-title":"Mar. Biotechnol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Chieu, H.D., Turner, L., Smith, M.K., Wang, T., Nocillado, J., Palma, P., Suwansa-Ard, S., Elizur, A., and Cummins, S.F. (2019). Aquaculture Breeding Enhancement: Maturation and Spawning in Sea Cucumbers Using a Recombinant Relaxin-Like Gonad-Stimulating Peptide. Front. Genet., 10.","DOI":"10.3389\/fgene.2019.00077"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Percie du Sert, N., Hurst, V., Ahluwalia, A., Alam, S., Avey, M.T., Baker, M., Browne, W.J., Clark, A., Cuthill, I.C., and Dirnagl, U. (2020). The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol., 18.","DOI":"10.1371\/journal.pbio.3000410"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"i884","DOI":"10.1093\/bioinformatics\/bty560","article-title":"fastp: An ultra-fast all-in-one FASTQ preprocessor","volume":"34","author":"Chen","year":"2018","journal-title":"Bioinformatics"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with Bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1650","DOI":"10.1038\/nprot.2016.095","article-title":"Transcript-level expression. analysis of RNA-seq experiments with HISAT, StringTie and Ballgown","volume":"11","author":"Pertea","year":"2016","journal-title":"Nat. Protoc."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1038\/nprot.2012.016","article-title":"Differential gene and tran- script expression analysis of RNA-seq experiments with TopHat and Cufflinks","volume":"7","author":"Trapnell","year":"2012","journal-title":"Nat. Protoc."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Anders, S., and Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biol., 11.","DOI":"10.1186\/gb-2010-11-10-r106"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e121","DOI":"10.1093\/nar\/gkt263","article-title":"Challenges in homology. search: HMMER3 and convergent evolution of coiled-coil regions","volume":"41","author":"Mistry","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"D279","DOI":"10.1093\/nar\/gkv1344","article-title":"The Pfam protein families database: Towards a more sustainable future","volume":"44","author":"Finn","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"W345","DOI":"10.1093\/nar\/gkm391","article-title":"CPC: Assess. the protein-coding potential of transcripts using sequence features and support vector machine","volume":"35","author":"Kong","year":"2007","journal-title":"Nucleic Acids Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e166","DOI":"10.1093\/nar\/gkt646","article-title":"Utilizing sequence intrinsic composition to classify protein- coding and long non-coding transcripts","volume":"41","author":"Sun","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"I275","DOI":"10.1093\/bioinformatics\/btr209","article-title":"PhyloCSF: A comparative genomics method to. distinguish protein coding and non-coding regions","volume":"27","author":"Lin","year":"2011","journal-title":"Bioinformatics"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1038\/nbt.3122","article-title":"StringTie enables improved reconstruction of a transcriptome from RNA-seq reads","volume":"33","author":"Pertea","year":"2015","journal-title":"Nat. Biotechnol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Li, B., and Dewey, C.N. (2011). RSEM: Accurate transcript quantification from RNA-Seq. data with or without a reference genome. BMC Bioinformatics, 12.","DOI":"10.1186\/1471-2105-12-323"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Wu, X., Chen, T., Huo, D., Yu, Z., Ruan, Y., Cheng, C., Jiang, X., and Ren, C. (2020). Transcriptomic. analysis of sea cucumber (Holothuria leucospilota) coelomocytes revealed the echinoderm cytokine response during immune challenge. BMC Genom., 21.","DOI":"10.1186\/s12864-020-6698-6"},{"key":"ref_31","first-page":"3119","article-title":"Principal component analysis and cluster analysis of inorganic elements in sea cucumber Apostichopus japonicus","volume":"31","author":"Liu","year":"2011","journal-title":"Guang Pu Xue Yu Guang Pu Fen Xi"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Sun, J., Wang, H., Zhan, Y., Zhao, T., Li, C., Cheng, C., Wang, Z., Zou, A., and Chang, Y. (2024). Identification of Key Genes Correlated with Economic Trait Superiorities and Their SNP Screening Through Transcriptome Comparisons, WGCNA and Pearson Correlation Coefficient in the Sea Cucumber Apostichopus japonicus. Mar. Biotechnol., 27.","DOI":"10.1007\/s10126-024-10384-y"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"121514","DOI":"10.1016\/j.envpol.2023.121514","article-title":"Perfluoroalkyl substances (PFASs) in aquatic products from the Yellow-Bohai Sea coasts, China: Concentrations and profiles across species and regions","volume":"327","author":"Guo","year":"2023","journal-title":"Environ. Pollut."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"432","DOI":"10.4103\/1735-5362.268204","article-title":"Phytochemical analysis of Holothuria leucospilota, a sea cucumber from Persian Gulf","volume":"14","author":"Shushizadeh","year":"2019","journal-title":"Res. Pharm. Sci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"163219","DOI":"10.1016\/j.scitotenv.2023.163219","article-title":"Abundance of microplastic in different coastal areas using Phragmatopoma caudata (Kroyer in Morch, 1863) (Polychaeta: Sabelariidae) as an indicator","volume":"880","author":"Schuab","year":"2023","journal-title":"Sci. Total Environ."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1016\/j.gene.2016.06.051","article-title":"Pm-miR-133 hosting in one potential. lncRNA regulates RhoA expression in pearl oyster Pinctada martensii","volume":"591","author":"Zheng","year":"2016","journal-title":"Gene"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Thepsuwan, T., Rungrassamee, W., Sangket, U., Whankaew, S., and Sathapondecha, P. (2021). Long. non-coding RNA profile in banana shrimp, Fenneropenaeus merguiensis and the potential role of lncPV13 in vitellogenesis. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol., 261.","DOI":"10.1016\/j.cbpa.2021.111045"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Yu, Y., Zhang, M., Wang, D., Xiang, Z., Zhao, Z., Cui, W., Ye, S., Fazhan, H., Waiho, K., and Ikhwanuddin, M. (2024). Whole transcriptome RNA sequencing provides novel insights into the molecular dynamics of ovarian development in mud crab, Scylla paramamosain after mating. Comp. Biochem. Physiol. Part D Genom. Proteom., 51.","DOI":"10.1016\/j.cbd.2024.101247"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1007\/s10126-017-9784-2","article-title":"Comparative Transcriptome Analysis Provides Insights into Differentially Expressed Genes and Long Non-Coding RNAs between Ovary and Testis of the Mud Crab (Scylla paramamosain)","volume":"20","author":"Yang","year":"2018","journal-title":"Mar. Biotechnol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Yu, H., Zhao, X., and Li, Q. (2016). Genome-wide identification and characterization of long intergenic noncoding RNAs and their potential association with larval development in the Pacific oyster. Sci. Rep., 6.","DOI":"10.1038\/srep20796"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Li, Z., Liu, X., Tang, X., and Yang, Y. (2025). Analysis of gonadal transcriptome reveals core long non-coding RNA-mRNA regulatory network in sea cucumber Apostichopus japonicus. Comp. Biochem. Physiol. Part D Genom. Proteom., 54.","DOI":"10.1016\/j.cbd.2024.101396"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1016\/j.csbj.2025.03.047","article-title":"LncRNA-miRNA interplay regulate intestinal regeneration in the sea cucumber Apostichopus japonicus","volume":"27","author":"Su","year":"2025","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Ge, L., Wei, Y., Ye, Z., Jiang, Z., Liu, Y., Wang, Y., Xu, X., Wang, J., Yang, J., and Sun, L. (2025). Non-coding RNA regulatory networks underlying intestinal degradation in Apostichopus japonicus under starvation stress: Insights from transcriptome analysis. Int. J. Biol. Macromol., 307.","DOI":"10.1016\/j.ijbiomac.2025.142069"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1016\/j.gde.2017.07.009","article-title":"Cis- and trans-acting lncRNAs in pluripotency and reprogramming","volume":"46","author":"Yan","year":"2017","journal-title":"Curr. Opin. Genet. Dev."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1038\/s41576-019-0184-5","article-title":"Regulation of gene expression by cis-acting long non-coding RNAs","volume":"21","author":"Gil","year":"2020","journal-title":"Nat. Rev. Genet."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Zhang, S., Zhang, L., Ru, X., Ding, K., and Feng, Q. (2021). Transcriptome analysis of gender-biased CYP genes in gonads of the sea cucumber Apostichopus japonicus. Comp. Biochem. Physiol. Part D Genom. Proteom., 38.","DOI":"10.1016\/j.cbd.2021.100790"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.cbpa.2009.09.002","article-title":"Molecular characterization of the major yolk protein of the Japanese common sea cucumber (Apostichopus japonicus) and its expression profile during ovarian development","volume":"155","author":"Fujiwara","year":"2010","journal-title":"Comp. Biochem. Physiol. A Mol. Integr. Physiol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Thongbuakaew, T., Suwansa-Ard, S., Chaiyamoon, A., Cummins, S.F., and Sobhon, P. (2021). Sex. steroids and steroidogenesis-related genes in the sea cucumber, Holothuria scabra and their potential role in gonad maturation. Sci. Rep., 11.","DOI":"10.1038\/s41598-021-81917-x"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Liu, B.Z., Cong, J.J., Su, W.Y., Hao, Z.L., Sun, Z.H., and Chang, Y.Q. (2023). Identification and functional analysis of Dmrt1 gene and the SoxE gene in the sexual development of sea cucumber, Apostichopus japonicus. Front. Genet., 14.","DOI":"10.3389\/fgene.2023.1097825"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Dolmatov, I.Y., Kalacheva, N.V., Tkacheva, E.S., Shulga, A.P., Zavalnaya, E.G., Shamshurina, E.V., Girich, A.S., Boyko, A.V., and Eliseikina, M.G. (2021). Expression of Piwi, MMP, TIMP, and Sox during Gut Regeneration in Holothurian Eupentacta fraudatrix (Holothuroidea, Dendrochirotida). Genes, 12.","DOI":"10.3390\/genes12081292"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1007\/s00335-011-9351-5","article-title":"Targeted insertion of two Mthfr promoters in mice reveals temporal- and tissue-specific regulation","volume":"22","author":"Pickell","year":"2011","journal-title":"Mamm. Genome"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Han, X., Wang, B., Jin, D., Liu, K., Wang, H., Chen, L., and Zu, Y. (2021). Precise Dose of Folic Acid Supplementation Is Essential for Embryonic Heart Development in Zebrafish. Biology, 11.","DOI":"10.3390\/biology11010028"},{"key":"ref_53","first-page":"470","article-title":"Single-cell transcriptomic analysis deciphers heterogenous cancer stem-like cells in colorectal cancer and their organ-specific metastasis","volume":"73","author":"Li","year":"2024","journal-title":"Gut"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"770","DOI":"10.1016\/j.rvsc.2011.11.003","article-title":"cDNA cloning and. mRNA expression of canine pancreatic and duodenum homeobox 1 (Pdx-1)","volume":"93","author":"Takemitsu","year":"2012","journal-title":"Res. Vet. Sci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1091\/mbc.E20-09-0607","article-title":"Rab14\/MACF2 complex regulates endosomal targeting during cytokinesis","volume":"32","author":"Peterman","year":"2021","journal-title":"Mol. Biol. Cell"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/S0169-328X(02)00394-7","article-title":"Expression of the mouse Macf2 gene during inner ear development","volume":"105","author":"Leonova","year":"2002","journal-title":"Brain Res. Mol. Brain Res."}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/16\/11\/1293\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,31]],"date-time":"2025-10-31T01:37:36Z","timestamp":1761874656000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/16\/11\/1293"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,30]]},"references-count":56,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2025,11]]}},"alternative-id":["genes16111293"],"URL":"https:\/\/doi.org\/10.3390\/genes16111293","relation":{},"ISSN":["2073-4425"],"issn-type":[{"type":"electronic","value":"2073-4425"}],"subject":[],"published":{"date-parts":[[2025,10,30]]}}}