Volume 45 Issue 1
Jan.  2024
Turn off MathJax
Article Contents
Tao Jiang, Zhi-Min Zhou, Zi-Qi Ling, Qing Zhang, Zhong-Zi Wu, Jia-Wen Yang, Si-Yu Yang, Bin Yang, Lu-Sheng Huang. Pig H3K4me3, H3K27ac, and gene expression profiles reveal reproductive tissue-specific activity of transposable elements. Zoological Research, 2024, 45(1): 138-151. doi: 10.24272/j.issn.2095-8137.2023.060
Citation: Tao Jiang, Zhi-Min Zhou, Zi-Qi Ling, Qing Zhang, Zhong-Zi Wu, Jia-Wen Yang, Si-Yu Yang, Bin Yang, Lu-Sheng Huang. Pig H3K4me3, H3K27ac, and gene expression profiles reveal reproductive tissue-specific activity of transposable elements. Zoological Research, 2024, 45(1): 138-151. doi: 10.24272/j.issn.2095-8137.2023.060

Pig H3K4me3, H3K27ac, and gene expression profiles reveal reproductive tissue-specific activity of transposable elements

doi: 10.24272/j.issn.2095-8137.2023.060
All epigenomic sequence data used in this study were submitted to the China National GeneBank DataBase (CNGBdb) with accession code: CNP0001696 (https://db.cngb.org/search/project/CNP0001696/), Genome Sequence Archive (GSA) database (https://ngdc.cncb.ac.cn/gsa/) under accession number CRA013785, Science Data Bank (doi:10.57760/sciencedb.j00139.00086) and NCBI under BioProjectID PRJNA1049515.
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
L.S.H. designed and supervised this study and revised the manuscript. B.Y. wrote and revised the manuscript and supervised the data analysis; T.J. and Z.M.Z. performed the experiments, analyzed the data, and wrote the manuscript; Z.Q.L., Q.Z., Z.Z.W., J.W.Y., and S.Y.Y. performed the experiments. All authors read and approved the final version of the manuscript.
#Authors contributed equally to this work
Funds:  This work was supported by the National Natural Science Foundation of China (32160781)
More Information
  • Regulatory sequences and transposable elements (TEs) account for a large proportion of the genomic sequences of species; however, their roles in gene transcription, especially tissue-specific expression, remain largely unknown. Pigs serve as an excellent animal model for studying genomic sequence biology due to the extensive diversity among their wild and domesticated populations. Here, we conducted an integrated analysis using H3K27ac ChIP-seq, H3K4me3 ChIP-seq, and RNA-seq data from 10 different tissues of seven fetuses and eight closely related adult pigs. We aimed to annotate the regulatory elements and TEs to elucidate their associations with histone modifications and mRNA expression across different tissues and developmental stages. Based on correlation analysis between mRNA expression and H3K27ac and H3K4me3 peak activity, results indicated that H3K27ac exhibited stronger associations with gene expression than H3K4me3. Furthermore, 1.45% of TEs overlapped with either the H3K27ac or H3K4me3 peaks, with the majority displaying tissue-specific activity. Notably, a TE subfamily (LTR4C_SS), containing binding motifs for SIX1 and SIX4, showed specific enrichment in the H3K27ac peaks of the adult and fetal ovaries. RNA-seq analysis also revealed widespread expression of TEs in the exons or promoters of genes, including 4 688 TE-containing transcripts with distinct development stage-specific and tissue-specific expression. Of note, 1 967 TE-containing transcripts were enriched in the testes. We identified a long terminal repeat (LTR), MLT1F1, acting as a testis-specific alternative promoter in SRPK2 (a cell cycle-related protein kinase) in our pig dataset. This element was also conserved in humans and mice, suggesting either an ancient integration of TEs in genes specifically expressed in the testes or parallel evolutionary patterns. Collectively, our findings demonstrate that TEs are deeply embedded in the genome and exhibit important tissue-specific biological functions, particularly in the reproductive organs.
  • All epigenomic sequence data used in this study were submitted to the China National GeneBank DataBase (CNGBdb) with accession code: CNP0001696 (https://db.cngb.org/search/project/CNP0001696/), Genome Sequence Archive (GSA) database (https://ngdc.cncb.ac.cn/gsa/) under accession number CRA013785, Science Data Bank (doi:10.57760/sciencedb.j00139.00086) and NCBI under BioProjectID PRJNA1049515.
    Supplementary data to this article can be found online.
    The authors declare that they have no competing interests.
    L.S.H. designed and supervised this study and revised the manuscript. B.Y. wrote and revised the manuscript and supervised the data analysis; T.J. and Z.M.Z. performed the experiments, analyzed the data, and wrote the manuscript; Z.Q.L., Q.Z., Z.Z.W., J.W.Y., and S.Y.Y. performed the experiments. All authors read and approved the final version of the manuscript.
    #Authors contributed equally to this work
  • loading
  • [1]
    Abuín JM, Pichel JC, Pena TF, et al. 2015. BigBWA: approaching the Burrows-Wheeler aligner to Big Data technologies. Bioinformatics, 31(24): 4003−4005. doi: 10.1093/bioinformatics/btv506
    [2]
    Ardeljan D, Taylor MS, Ting DT, et al. 2017. The human long interspersed element-1 retrotransposon: an emerging biomarker of neoplasia. Clinical Chemistry, 63(4): 816−822. doi: 10.1373/clinchem.2016.257444
    [3]
    Ayarpadikannan S, Kim HS. 2014. The impact of transposable elements in genome evolution and genetic instability and their implications in various diseases. Genomics & Informatics, 12(3): 98−104.
    [4]
    Bailey TL, Johnson J, Grant CE, et al. 2015. The MEME suite. Nucleic Acids Research, 43(W1): W39−W49. doi: 10.1093/nar/gkv416
    [5]
    Barski A, Cuddapah S, Cui KR, et al. 2007. High-resolution profiling of histone methylations in the human genome. Cell, 129(4): 823−837. doi: 10.1016/j.cell.2007.05.009
    [6]
    Behbakht K, Qamar L, Aldridge CS, et al. 2007. Six1 overexpression in ovarian carcinoma causes resistance to TRAIL-mediated apoptosis and is associated with poor survival. Cancer Research, 67(7): 3036−3042. doi: 10.1158/0008-5472.CAN-06-3755
    [7]
    Bernstein BE, Kamal M, Lindblad-Toh K, et al. 2005. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell, 120(2): 169−181. doi: 10.1016/j.cell.2005.01.001
    [8]
    Bhalla N. 2020. Meiosis: is spermatogenesis stress an opportunity for evolutionary innovation?. Current Biology, 30(24): R1471−R1473. doi: 10.1016/j.cub.2020.10.042
    [9]
    Biémont C. 2010. A brief history of the status of transposable elements: from junk DNA to major players in evolution. Genetics, 186(4): 1085−1093. doi: 10.1534/genetics.110.124180
    [10]
    Bourque G, Burns KH, Gehring M, et al. 2018. Ten things you should know about transposable elements. Genome Biology, 19(1): 199. doi: 10.1186/s13059-018-1577-z
    [11]
    Castañeda J, Genzor P, Bortvin A. 2011. piRNAs, transposon silencing, and germline genome integrity. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 714(1-2): 95−104. doi: 10.1016/j.mrfmmm.2011.05.002
    [12]
    Chang NC, Rovira Q, Wells J, et al. 2022. Zebrafish transposable elements show extensive diversification in age, genomic distribution, and developmental expression. Genome Research, 32(7): 1408−1423. doi: 10.1101/gr.275655.121
    [13]
    Chen JQ, Zhang MP, Tong XK, et al. 2022. Scan of the endogenous retrovirus sequences across the swine genome and survey of their copy number variation and sequence diversity among various Chinese and Western pig breeds. Zoological Research, 43(3): 423−441. doi: 10.24272/j.issn.2095-8137.2021.379
    [14]
    Chuong EB, Elde NC, Feschotte C. 2016. Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science, 351(6277): 1083−1087. doi: 10.1126/science.aad5497
    [15]
    Chuong EB, Elde NC, Feschotte C. 2017. Regulatory activities of transposable elements: from conflicts to benefits. Nature Reviews Genetics, 18(2): 71−86. doi: 10.1038/nrg.2016.139
    [16]
    Colonna Romano N, Fanti L. 2022. Transposable elements: major players in shaping genomic and evolutionary patterns. Cells, 11(6): 1048. doi: 10.3390/cells11061048
    [17]
    Cornelis G, Funk M, Vernochet C, et al. 2017. An endogenous retroviral envelope syncytin and its cognate receptor identified in the viviparous placental Mabuya lizard. Proceedings of the National Academy of Sciences of the United States of America, 114(51): E10991−E11000.
    [18]
    Cosby RL, Chang NC, Feschotte C. 2019. Host-transposon interactions: conflict, cooperation, and cooption. Genes & Development, 33(17-18): 1098−1116.
    [19]
    Creyghton MP, Cheng AW, Welstead GG, et al. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proceedings of the National Academy of Sciences of the United States of America, 107(50): 21931−21936.
    [20]
    Delaneau O, Zazhytska M, Borel C, et al. 2019. Chromatin three-dimensional interactions mediate genetic effects on gene expression. Science, 364(6439): eaat8266. doi: 10.1126/science.aat8266
    [21]
    Dobin A, Davis CA, Schlesinger F, et al. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics, 29(1): 15−21. doi: 10.1093/bioinformatics/bts635
    [22]
    Duttke SHC, Lacadie SA, Ibrahim MM, et al. 2015. Human promoters are intrinsically directional. Molecular Cell, 57(4): 674−684. doi: 10.1016/j.molcel.2014.12.029
    [23]
    Fedoroff NV. 2012. Presidential address. Transposable elements, epigenetics, and genome evolution. Science, 338(6108): 758−767. doi: 10.1126/science.338.6108.758
    [24]
    Ferguson L, Agoulnik AI. 2013. Testicular cancer and cryptorchidism. Frontiers in Endocrinology, 4: 32.
    [25]
    Fletcher J, Hu M, Berman Y, et al. 2005. Multicystic dysplastic kidney and variable phenotype in a family with a novel deletion mutation of PAX2. Journal of the American Society of Nephrology, 16(9): 2754–2761.
    [26]
    Fueyo R, Judd J, Feschotte C, et al. 2022. Roles of transposable elements in the regulation of mammalian transcription. Nature Reviews Molecular Cell Biology, 23(7): 481−497. doi: 10.1038/s41580-022-00457-y
    [27]
    Gardner EJ, Prigmore E, Gallone G, et al. 2019. Contribution of retrotransposition to developmental disorders. Nature Communications, 10(1): 4630. doi: 10.1038/s41467-019-12520-y
    [28]
    Giannakouros T, Nikolakaki E, Mylonis I, et al. 2011. Serine-arginine protein kinases: a small protein kinase family with a large cellular presence. The FEBS Journal, 278(4): 570−586. doi: 10.1111/j.1742-4658.2010.07987.x
    [29]
    Grant CE, Bailey TL, Noble WS. 2011. FIMO: scanning for occurrences of a given motif. Bioinformatics, 27(7): 1017−1018. doi: 10.1093/bioinformatics/btr064
    [30]
    Heinz S, Benner C, Spann N, et al. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Molecular Cell, 38(4): 576−589. doi: 10.1016/j.molcel.2010.05.004
    [31]
    Holley CL, Topkara VK. 2011. An introduction to small non-coding RNAs: miRNA and snoRNA. Cardiovascular Drugs and Therapy, 25(2): 151−159. doi: 10.1007/s10557-011-6290-z
    [32]
    Howe FS, Fischl H, Murray SC, et al. 2017. Is H3K4me3 instructive for transcription activation?. BioEssays, 39(1): 1−12.
    [33]
    Hughes AL, Kelley JR, Klose RJ. 2020. Understanding the interplay between CpG island-associated gene promoters and H3K4 methylation. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, 1863(8): 194567.
    [34]
    Jacques PÉ, Jeyakani J, Bourque G. 2013. The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genetics, 9(5): e1003504. doi: 10.1371/journal.pgen.1003504
    [35]
    Jin Y, Tam OH, Paniagua E, et al. 2015. TEtranscripts: a package for including transposable elements in differential expression analysis of RNA-seq datasets. Bioinformatics, 31(22): 3593−3599. doi: 10.1093/bioinformatics/btv422
    [36]
    Joly-Lopez Z, Bureau TE. 2018. Exaptation of transposable element coding sequences. Current Opinion in Genetics & Development, 49: 34−42.
    [37]
    Judd J, Sanderson H, Feschotte C. 2021. Evolution of mouse circadian enhancers from transposable elements. Genome Biology, 22(1): 193. doi: 10.1186/s13059-021-02409-9
    [38]
    Kaessmann H. 2010. Origins, evolution, and phenotypic impact of new genes. Genome Research, 20(10): 1313−1326. doi: 10.1101/gr.101386.109
    [39]
    Kapusta A, Kronenberg Z, Lynch VJ, et al. 2013. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genetics, 9(4): e1003470. doi: 10.1371/journal.pgen.1003470
    [40]
    Karlić R, Chung HR, Lasserre J, et al. 2010. Histone modification levels are predictive for gene expression. Proceedings of the National Academy of Sciences of the United States of America, 107(7): 2926−2931.
    [41]
    Kern C, Wang Y, Xu XQ, et al. 2021. Functional annotations of three domestic animal genomes provide vital resources for comparative and agricultural research. Nature Communications, 12(1): 1821. doi: 10.1038/s41467-021-22100-8
    [42]
    Kirk EP, Sunde M, Costa MW, et al. 2007. Mutations in cardiac T-box factor gene TBX20 are associated with diverse cardiac pathologies, including defects of septation and valvulogenesis and cardiomyopathy. The American Journal of Human Genetics, 81(2): 280−291. doi: 10.1086/519530
    [43]
    Kryuchkova-Mostacci N, Robinson-Rechavi M. 2017. A benchmark of gene expression tissue-specificity metrics. Briefings in Bioinformatics, 18(2): 205−214.
    [44]
    Kunarso G, Chia NY, Jeyakani J, et al. 2010. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nature Genetics, 42(7): 631−634. doi: 10.1038/ng.600
    [45]
    Kurhanewicz NA, Dinwiddie D, Bush ZD, et al. 2020. Elevated temperatures cause transposon-associated DNA damage in C. elegans spermatocytes. Current Biology, 30(24): 5007−5017.e4. doi: 10.1016/j.cub.2020.09.050
    [46]
    Lee HJ, Hou YR, Maeng JH, et al. 2022. Epigenomic analysis reveals prevalent contribution of transposable elements to cis-regulatory elements, tissue-specific expression, and alternative promoters in zebrafish. Genome Research, 32(7): 1424−1436. doi: 10.1101/gr.276052.121
    [47]
    Li DR, Ai YW, Guo J, et al. 2020. Casein kinase 1G2 suppresses necroptosis-promoted testis aging by inhibiting receptor-interacting kinase 3. eLife, 9: e61564. doi: 10.7554/eLife.61564
    [48]
    Li H, Handsaker B, Wysoker A, et al. 2009. The sequence alignment/map format and SAMtools. Bioinformatics, 25(16): 2078−2079. doi: 10.1093/bioinformatics/btp352
    [49]
    Liao Y, Smyth GK, Shi W. 2014. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30(7): 923−930. doi: 10.1093/bioinformatics/btt656
    [50]
    Liu JX, Liu Z, Zhang XZ, et al. 2019. Bioinformatic exploration of OLFML2B overexpression in gastric cancer base on multiple analyzing tools. BMC Cancer, 19(1): 227. doi: 10.1186/s12885-019-5406-x
    [51]
    Liu M, Qiu YL, Jin T, et al. 2018. Meta-analysis of microarray datasets identify several chromosome segregation-related cancer/testis genes potentially contributing to anaplastic thyroid carcinoma. PeerJ, 6: e5822. doi: 10.7717/peerj.5822
    [52]
    Lunney JK, Van Goor A, Walker KE, et al. 2021. Importance of the pig as a human biomedical model. Science Translational Medicine, 13(621): eabd5758. doi: 10.1126/scitranslmed.abd5758
    [53]
    Miao BP, Fu SH, Lyu C, et al. 2020. Tissue-specific usage of transposable element-derived promoters in mouse development. Genome Biology, 21(1): 255. doi: 10.1186/s13059-020-02164-3
    [54]
    Modzelewski AJ, Shao WQ, Chen JQ, et al. 2021. A mouse-specific retrotransposon drives a conserved Cdk2ap1 isoform essential for development. Cell, 184(22): 5541−5558.e22. doi: 10.1016/j.cell.2021.09.021
    [55]
    Naville M, Warren IA, Haftek-Terreau Z, et al. 2016. Not so bad after all: retroviruses and long terminal repeat retrotransposons as a source of new genes in vertebrates. Clinical Microbiology and Infection, 22(4): 312−323. doi: 10.1016/j.cmi.2016.02.001
    [56]
    Niknafs YS, Pandian B, Iyer HK, et al. 2017. TACO produces robust multisample transcriptome assemblies from RNA-seq. Nature Methods, 14(1): 68−70. doi: 10.1038/nmeth.4078
    [57]
    Pan ZY, Yao YL, Yin HW, et al. 2021. Pig genome functional annotation enhances the biological interpretation of complex traits and human disease. Nature Communications, 12(1): 5848. doi: 10.1038/s41467-021-26153-7
    [58]
    Pekowska A, Benoukraf T, Zacarias-Cabeza J, et al. 2011. H3K4 tri-methylation provides an epigenetic signature of active enhancers. The EMBO Journal, 30(20): 4198−4210. doi: 10.1038/emboj.2011.295
    [59]
    Pertea M, Pertea GM, Antonescu CM, et al. 2015. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology, 33(3): 290−295. doi: 10.1038/nbt.3122
    [60]
    Qian L, Mohapatra B, Akasaka T, et al. 2008. Transcription factor neuromancer/TBX20 is required for cardiac function in Drosophila with implications for human heart disease. Proceedings of the National Academy of Sciences of the United States of America, 105(50): 19833−19838.
    [61]
    Quinlan AR. 2014. BEDTools: the swiss-army tool for genome feature analysis. Current Protocols Bioinformatics, 47: 11.12.1−11.12.34.
    [62]
    Ramírez F, Dündar F, Diehl S, et al. 2014. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Research, 42(W1): W187−W191. doi: 10.1093/nar/gku365
    [63]
    Rebollo R, Romanish MT, Mager DL. 2012. Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annual Review of Genetics, 46: 21−42. doi: 10.1146/annurev-genet-110711-155621
    [64]
    Reik W, Dean W, Walter J. 2001. Epigenetic reprogramming in mammalian development. Science, 293(5532): 1089−1093. doi: 10.1126/science.1063443
    [65]
    Roth SY, Denu JM, Allis CD. 2001. Histone acetyltransferases. Annual Review of Biochemistry, 70: 81−120. doi: 10.1146/annurev.biochem.70.1.81
    [66]
    Safran M, Dalah I, Alexander J, et al. 2010. GeneCards Version 3: the human gene integrator. Database, 2010: baq020.
    [67]
    Senft AD, Macfarlan TS. 2021. Transposable elements shape the evolution of mammalian development. Nature Reviews Genetics, 22(11): 691−711. doi: 10.1038/s41576-021-00385-1
    [68]
    Slotkin RK, Martienssen R. 2007. Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics, 8(4): 272−285. doi: 10.1038/nrg2072
    [69]
    Sundaram V, Choudhary MNK, Pehrsson E, et al. 2017. Functional cis-regulatory modules encoded by mouse-specific endogenous retrovirus. Nature Communications, 8(1): 14550. doi: 10.1038/ncomms14550
    [70]
    Sundaram V, Wysocka J. 2020. Transposable elements as a potent source of diverse cis-regulatory sequences in mammalian genomes. Philosophical Transactions of the Royal Society B:Biological Sciences, 375(1795): 20190347. doi: 10.1098/rstb.2019.0347
    [71]
    Tarailo-Graovac M, Chen NS. 2009. Using RepeatMasker to identify repetitive elements in genomic sequences. Current Protocols in Bioinformatics,doi: 10.1002/0471250953.bi0410s25.
    [72]
    Ting CN, Rosenberg MP, Snow CM, et al. 1992. Endogenous retroviral sequences are required for tissue-specific expression of a human salivary amylase gene. Genes & Development, 6(8): 1457−1465.
    [73]
    Topaloğlu U, Akbalik ME, Sağsöz H. 2021. Immunolocalization of some HOX proteins in immature and mature feline testes. Anatomia, Histologia, Embryologia, 50(4): 726−735. doi: 10.1111/ahe.12716
    [74]
    Utomo ARH, Nikitin AY, Lee WH. 1999. Temporal, spatial, and cell type-specific control of Cre-mediated DNA recombination in transgenic mice. Nature Biotechnology, 17(11): 1091−1096. doi: 10.1038/15073
    [75]
    Wu YQ, Zhao H, Li YJ, et al. 2020. Genome-wide identification of imprinted genes in pigs and their different imprinting status compared with other mammals. Zoological Research, 41(6): 721−725. doi: 10.24272/j.issn.2095-8137.2020.072
    [76]
    Xian H, Xian Y, Liu LL, et al. 2015. Expression of β-nerve growth factor and homeobox A10 in experimental cryptorchidism treated with exogenous nerve growth factor. Molecular Medicine Reports, 11(4): 2875−2881. doi: 10.3892/mmr.2014.3005
    [77]
    Yang Y, Adeola AC, Xie HB, et al. 2018. Genomic and transcriptomic analyses reveal selection of genes for puberty in Bama Xiang pigs. Zoological Research, 39(6): 424−430. doi: 10.24272/j.issn.2095-8137.2018.068
    [78]
    Zhan JF, Li JB, Wu YR, et al. 2021. Chromatin-associated protein sugp2 involved in mRNA alternative splicing during mouse spermatogenesis. Frontiers in Veterinary Science, 8: 754021. doi: 10.3389/fvets.2021.754021
    [79]
    Zhang LK, Ma HD, Guo M, et al. 2022a. Dynamic transcriptional atlas of male germ cells during porcine puberty. Zoological Research, 43(4): 600−603. doi: 10.24272/j.issn.2095-8137.2022.037
    [80]
    Zhang Q, Li J, Zhang YF, et al. 2022b. Whole-genome sequence-based association study for immune cells in an eight-breed pig heterogeneous population. Journal of Genetics and Genomics, 49(11): 1068−1071. doi: 10.1016/j.jgg.2021.09.003
    [81]
    Zhang Y, Liu T, Meyer CA, et al. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biology, 9(9): R137. doi: 10.1186/gb-2008-9-9-r137
    [82]
    Zhang Y, Zhao B, Roy S, et al. 2016. microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti. Proceedings of the National Academy of Sciences of the United States of America, 113(33): E4828–E4836.
    [83]
    Zhao YX, Hou Y, Xu YY, et al. 2021. A compendium and comparative epigenomics analysis of cis-regulatory elements in the pig genome. Nature Communications, 12(1): 2217. doi: 10.1038/s41467-021-22448-x
    [84]
    Zhong LP, Zheng M, Huang YZ, et al. 2023. An atlas of expression quantitative trait loci of microRNAs in longissimus muscle of eight-way crossbred pigs. Journal of Genetics and Genomics, 50(6): 398−409. doi: 10.1016/j.jgg.2023.02.007
    [85]
    Zhu YL, Zhou ZM, Huang T, et al. 2022. Mapping and analysis of a spatiotemporal H3K27ac and gene expression spectrum in pigs. Science China Life Sciences, 65(8): 1517−1534. doi: 10.1007/s11427-021-2034-5
  • ZR-2023-060-Supplementary Materials.zip
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(6)

    Article Metrics

    Article views (896) PDF downloads(168) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return