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Comprehensive annotation of the Chinese tree shrew genome by large-scale RNA sequencing and long-read isoform sequencing

Mao-Sen Ye Jin-Yan Zhang Dan-Dan Yu Min Xu Ling Xu Long-Bao Lv Qi-Yun Zhu Yu Fan Yong-Gang Yao

Mao-Sen Ye, Jin-Yan Zhang, Dan-Dan Yu, Min Xu, Ling Xu, Long-Bao Lv, Qi-Yun Zhu, Yu Fan, Yong-Gang Yao. Comprehensive annotation of the Chinese tree shrew genome by large-scale RNA sequencing and long-read isoform sequencing. Zoological Research, 2021, 42(6): 692-709. doi: 10.24272/j.issn.2095-8137.2021.272
Citation: Mao-Sen Ye, Jin-Yan Zhang, Dan-Dan Yu, Min Xu, Ling Xu, Long-Bao Lv, Qi-Yun Zhu, Yu Fan, Yong-Gang Yao. Comprehensive annotation of the Chinese tree shrew genome by large-scale RNA sequencing and long-read isoform sequencing. Zoological Research, 2021, 42(6): 692-709. doi: 10.24272/j.issn.2095-8137.2021.272

使用大规模二代转录组以及三代转录组数据集优化树鼩基因组注释

doi: 10.24272/j.issn.2095-8137.2021.272

Comprehensive annotation of the Chinese tree shrew genome by large-scale RNA sequencing and long-read isoform sequencing

Funds: This study was supported by the National Natural Science Foundation of China (U1902215 to Y.G.Y. and 31970542 to Y.F.), Chinese Academy of Sciences (Light of West China Program xbzg-zdsys-201909 to Y.G.Y.), and Yunnan Province (202001AS070023 and 2018FB046 to D.D.Y. and 202002AA100007 to Y.G.Y.)
More Information
  • 摘要: 树鼩(Tupaia belangeri chinensis)在多个生物医学研究领域逐渐成为重要的实验动物。对树鼩参考基因组,包括mRNA以及长链非编码RNA (Long non-coding RNA, lncRNA)在内更加完整的注释,对树鼩动物模型的创建至关重要。在该研究中,我们收集了234个高质量的二代转录组(RNA sequencing, RNA-seq)数据集以及两个三代转录组(Long-read isoform sequencing, ISO-seq)数据集,来提高改善已报道的树鼩染色体级别参考基因组的注释质量。我们总共获得了3 514个新注释的编码基因和50 576个新注释的lncRNA基因。基于新的注释信息,我们鉴定了mRNA和lncRNA的组织特异性表达模式与组织特异性可变剪切模式,并对11种哺乳动物中基因的同源情况进行了分析。我们鉴定出144个树鼩特异性扩张的基因家族,包括白介素6(Interleukin 6, IL6)和STT3寡糖基转移酶复合物催化亚基B(STT3 oligosaccharyltransferase complex catalytic subunit B, STT3B),都在树鼩基因组中发生了扩张。我们还比较了四个物种(人类、猕猴、树鼩和小鼠)的组织表达模式与通路相关基因的表达模式,发现相比于小鼠,树鼩的组织表达模式与灵长类动物更为接近。值得注意的是,在该研究中新注释出的富嘌呤元件结合蛋白A(Purine rich element binding protein A, PURA)和STT3B基因家族,在病毒感染过程中呈现显著的差异表达。更新版本的树鼩基因组注释信息(KIZ version 3: TS_3.0)已经发布在http://www.treeshrewdb.org。该注释信息有望为树鼩基础生物学和医学生物学模型等研究提供关键的参考信息。
    #Authors contributed equally to this work
  • Figure  1.  Reference-guided transcriptome assembly of tree shrew TS_3.0 genome annotation

    A: Integrative pipeline for tree shrew genome annotation using publicly available and newly generated transcriptome datasets. B, C: Number of RNA-seq datasets of virus-infected tissues/cells (B) and normal tissues (C) analyzed in this study. D, E: Mapping ratio of RNA-seq data of virus-infected tissues/cells (D) and normal tissues (E) relative to reference tree shrew genome TS_2.0 (Fan et al., 2019). Sample information in (D) is listed in Supplementary Table S1.

    Figure  2.  Characteristics of tree shrew TS_3.0 transcripts

    A: Expression level of mRNAs is greater than that of lncRNAs at gene and transcript levels. B: mRNA transcripts have a higher number of exons than lncRNA transcripts. C: Average length of mRNA transcripts is longer than that of lncRNA transcripts. Density plot was drawn based on kernel density and statistical analysis was performed with Wilcoxon rank-sum test. D: Tree shrew lncRNAs exert cis-regulatory function on expression of proximal mRNAs. Close, mRNA and lncRNA pairs neighboring each other on pseudochromosome of tree shrew. Random, randomly selected mRNA and lncRNA pairs distant from each other in the genome. E: Percentages of alternative splicing events in reference genome annotations of tree shrew (TS_3.0), mouse (GRCm39), and human (GRCh38.p13). SE, skipped exon; A5, alternative 5’ splice site; A3, alternative 3’ splice site; MXE, mutually exclusive exons; RI, retained intron. F: Expression level of newly annotated coding genes is lower than that of previously annotated genes at gene and transcript levels. G: BUSCO evaluation of different tree shrew genome annotations showing that current version (TS_3.0) is superior. H: Pathway enrichment analysis of newly annotated genes showing enrichment in 11 pathways (Padjust<0.05). Values in A, B and F are presented as a boxplot, and statistical analyses were performed by Wilcoxon rank-sum test.

    Figure  3.  Tissue expression and alternative splicing profiles of tree shrew TS_3.0 transcripts

    A: Tissue expression profiles of mRNAs and lncRNAs annotated in TS_3.0 at gene level (left panel) and transcript level (right panel). UMAP_1, UMAP dimension 1; UMAP_2, UMAP dimension 2. Detailed information on RNA-seq datasets of 13 tree shrew tissues is listed in Supplementary Tables S1, S2. B: Expression correlation matrix among different tree shrew tissues based on expression levels of mRNAs and lncRNAs. C: Tissue-specific expression patterns of mRNAs and lncRNAs at gene level (left) and transcript level (right). D: Comparison of PSI across 13 tree shrew tissues. P-value was calculated based on Dunn test and adjusted by Benjamini-Hochberg method. *: Padjust<0.05; ***: Padjust<0.0005. Different colors indicate different Padjust values in triangle map. E: UMAP was constructed based on PSI of each gene in 13 tree shrew tissues.

    Figure  4.  Orthologous relationships and gene family size changes among different species

    A: Phylogenetic tree of 11 mammals using orthogroups. Numbers on tree branches refer to numbers of gene family expansion (+red) and contraction (-blue), respectively. B: Maximum-likelihood (ML) trees of IL6 gene family. Coding sequence of the longest transcript for each gene in each species was used to construct ML tree. Values on tree branches refer to support of 1 000 bootstraps. The tree shrew IL6 gene family had 13 copies, labeled in red in the tree. C: Locations of 13 tree shrew IL6 gene copies on pseudochromosome 6 (chr6). D: ML trees of STT3B gene family and STT3A. Tree shrew STT3B gene family had 39 copies. E: Locations of 39 tree shrew STT3B gene copies on 15 pseudochromosomes and one unplaced contig. Pseudochromosomes and unplaced contig were defined in reference tree shrew genome TS_2.0 (Fan et al., 2019). F: Pathway enrichment of genes from tree shrew-specific gene families with significant expansion.

    Figure  5.  Expression similarities among different species

    A: Tissue expression similarities among humans, rhesus monkeys, tree shrews, and mice. Expression patterns in five tree shrew tissues more closely resembled that of primates than that of mice. B: Comparisons of protein sequence identity of genes in KEGG pathways between tree shrews and humans and between mice and humans. C: Expression patterns of genes in brain-related pathways in tree shrews, rhesus monkeys, humans, and mice. Brain-related pathways included “Alzheimer’s disease”, “Parkinson disease”, “Neuroactive ligand-receptor interaction”, “Pathways of neurodegeneration-multiple diseases”, and “Axon guidance”.

    Figure  6.  Changes in expression of genes in virus-infected tree shrew tissues and cells

    A: Changes in newly annotated genes upon viral infection. HBV, hepatitis B virus; NDV, Newcastle disease virus; EMCV, encephalomyocarditis virus; HSV-1, herpes simplex virus type 1; SeV Sendai virus; ZIKA, Zika virus. Genes were identified as differentially expressed genes (DEGs) upon virus infection if Padjust<0.05 and |log2 fold-change|>1. B: Plot of DEGs upon virus infection. PURA and IFI35 were dysregulated in cells and tissues infected with different viruses. Horizontal bar on left represents number of DEGs in each RNA-seq dataset. Dots and lines represent subsets of DEGs. Vertical histogram represents number of DEGs in each subset. C: Changes in expression of 19 gene copies of STT3B gene family upon SeV infection. Results are mean±standard deviation (SD). *: Padjust<0.05; **: Padjust<0.005; ***, Padjust<0.0005. Padjust values were calculated using DESeq2.

    Table  1.   Comparisons of five tree shrew genome annotations

    ParametersTupChi_1.0 (NCBI)TupaiaBaseTS_1.0TS_2.0TS_3.0
    Coding genes
    Total number of coding genes23 52719 23022 12123 56827 082
    Transcript per coding gene1.591112.17
    Annotated coding genes23 53712 61220 22520 81125 127
    Average mRNA length48 10433 71240 11441 239
    Average CDS length1 6821 4191 4041 5271 684
    Average exon number8.347.687.548.869.32
    Average exon length229185186172181
    Average intron length6 0033 411493749074 863
    Complete BUSCOs
    (Eukaryota 255 genes)
    216
    (84.7%)
    195
    (76.5%)
    221 (86.7%)235
    (92.2%)
    250
    (98.0%)
    Complete BUSCOs
    (Mammalia 9 224 genes)
    7 884
    (85.5%)
    6 080
    (65.9%)
    7 568
    (82.0%)
    7 519
    (81.5%)
    8 559
    (92.8%)
    Non-coding genes
    Total number of lncRNA genes3 71856 401
    Transcripts per lncRNA gene5 1792.05
    Average lncRNA length914823
    Average exon number3.543.06
    Average intron length17 6144 658
    Tree shrew genome annotations TS_1.0 (Fan et al., 2013), TS_2.0 (Fan et al., 2019), and TS_3.0 (this study) were established in our studies. Tupchi_1.0, NCBI tree shrew annotation (https://www.ncbi.nlm.nih.gov/assembly/GCF_000334495.1/). TupaiaBase was reported by (Sanada et al., 2019). BUSCO: Benchmarking with Universal Single-Copy Orthologs. –: Not available.
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  • 收稿日期:  2021-09-02
  • 录用日期:  2021-09-23
  • 网络出版日期:  2021-09-26
  • 刊出日期:  2021-11-18

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