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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

Jia-Qi Chen Ming-Peng Zhang Xin-Kai Tong Jing-Quan Li Zhou Zhang Fei Huang Hui-Peng Du Meng Zhou Hua-Shui Ai Lu-Sheng Huang

Jia-Qi Chen, Ming-Peng Zhang, Xin-Kai Tong, Jing-Quan Li, Zhou Zhang, Fei Huang, Hui-Peng Du, Meng Zhou, Hua-Shui Ai, Lu-Sheng Huang. 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, 2022, 43(3): 423-441. doi: 10.24272/j.issn.2095-8137.2021.379
Citation: Jia-Qi Chen, Ming-Peng Zhang, Xin-Kai Tong, Jing-Quan Li, Zhou Zhang, Fei Huang, Hui-Peng Du, Meng Zhou, Hua-Shui Ai, Lu-Sheng Huang. 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, 2022, 43(3): 423-441. doi: 10.24272/j.issn.2095-8137.2021.379

内源性逆转录病毒序列在猪基因组中的搜寻及其在中西方猪品种中的拷贝数变异和序列多样性调查

doi: 10.24272/j.issn.2095-8137.2021.379

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

Funds: This study was supported by the National Swine Industry and Technology System of China (nycytx-009), and National Natural Science Foundation of China (31672383)
More Information
  • 摘要: 在猪-人异种移植中,猪内源性逆转录病毒(PERV)的传播风险备受关注。然而,PERV在猪基因组中的分布、它们在欧亚猪中的遗传变异以及它们的进化史尚不清楚。我们根据序列相似性在当前猪参考基因组(11.1版)中搜寻了PERV,检测到36个长的完整或接近完整的PERV(lcPERV)和23个短的不完整PERV(siPERV)。除了三种已知PERV(PERV-A、-B和-C),该研究还检测到四种新的PERV类型(PERV-JX1、-JX2、-JX3和-JX4)。进化分析表明,新发现的PERV更古老,PERV-B可能在50万年前经历了多样性骤降。通过分析63个高质量猪全基因组测序数据,我们发现中国猪的PERV拷贝数(32.0 ± 4.0)低于西方猪的(49.1 ± 6.5)。此外,中国猪的PERV序列多样性也低于西方猪。在这些lcPERV中,西方猪的PERV-A和-JX2显著高于中国猪。值得注意的是,巴马香猪的PERV拷贝数最低(27.8±5.1),其中一头巴马香猪没有PERV-C,且PERV拷贝数是最低的(23)。这表明巴马香猪更适合作为异种移植供体进行筛选或被修饰。此外,我们还鉴定了451个PERV插入多态性位点,其中86个是10个中国和西方猪品种所共有的。我们的研究发现为PERV的基因组分布、变异、进化和可能的生物学功能提供了系统的见解。
  • Figure  1.  Prediction pipeline of PERV types in an individual using the resequencing data based on the unique k-mers

    An example was given to determine whether the individual CNWB01 contained the PERV (PERV-JX1-17-41.4M). The result indicated CNWB01 had PERV-JX1-17-41.4M in its genome.

    Figure  2.  59 PERVs in the S. Scrofa reference genome

    A: The positions of PERVs in the reference genome. NW965: NW_018084965; NW136: NW_018085136; NW086: NW_018085086; NW255: NW_018085255; NW331: NW_018085331; NW293: NW_018085293; NW154: NW_018085154; NW193: NW_018085193; NW355: NW_018085355. siPERV: short incomplete PERV. B: Maximum-likelihood (ML) phylogenetic tree of 36 long complete or near-complete PERVs (lcPERVs) without LTR. In the tree, 3 complete PERVs (PERV-A: AY099323.1, PERV-B: AY099324.1, and PERV-C: KY352351.1) were included, and an MLV (MLV-J01998.1) was set as the outgroup. The color on the outer circle represents the detection rate of PERVs on the genome by 10 breeds (n=63). The bluer the color, the more pigs have this PERV copy, and the redder the color, the fewer pigs. C: Maximum-likelihood (ML) phylogenetic tree of 36 lcPERVs with LTRs. The color on the outer circle represents LTR types. D: ORF prediction of 62 PERVs and their LTRs. 59 PERVs were identified from the swine reference genome Build 11.1, and 3 complete PERVs (PERV-A: AY099323.1, PERV-B: AY099324.1, and PERV-C: KY352351.1) were downloaded from the NCBI Genbank database. ORFs of gag, pol, env were predicted in three forward reading frames. For example, gag1 means gag ORF predicted in forward frame 1; gag2 means gag ORF predicted in forward frame 2; gag3 means gag ORF predicted in forward frame 3. The sequences of pol-probe and env-probe were downloaded from the reference (Yang et al., 2015).

    Figure  3.  Evolutionary histories of 39 lcPERVs and their 5' LTRs

    The evolutionary tree of lcPERVs is on the left. Yellow triangle: PERV contains full gag, pol and env ORFs; Yellow circular: the pol ORF is complete but the other ORFs are incomplete. The phylogenetic tree was estimated using 40 ERV internal sequences (including 3 PERV reference sequences and one outgroup MLV) by BEAST. We set the divergence time between MLV and PERV-A-AY099323.1 to be 96 Ma with confidence intervals from 91 to 101 Ma same as the divergence time of pig and mice in TimeTree database. The LTR tree is on the right. 5’ LTRs of 39 lcPERVs were used, and 5' LTR of MLV was used as an outgroup. The divergence time was the same as above. PERV and its corresponding LTR are connected with a solid line.

    Figure  4.  Correlation between PERV copy number and LTR copy number measured by method 1 (mapping-to-genome method)

    The correlation between the copy number of PERV and LTR in ten pig breeds was shown in the scatter plot. The box plot at the top shows the difference of PERV copy number between Chinese and Western pig breeds, and the box plot at the right shows the difference of LTR copy number between Chinese and Western pig breeds. ***: P<0.0001.

    Figure  5.  PERV copy number and PERV types in 63 Chinese and Western pigs

    A: The percentage of different PERV types in 63 Chinese and Western pigs. B: Copy number difference of each PERV type between Chinese and Western pig breeds. ***: P<0.0001. C: Heatmap of PERVs with a significant difference in copy number between Chinese and Western pig breeds.

    Figure  6.  Differences in PERV sequence diversity, copy number of PERVs with transposable potentiality and TIPs between Chinese and Western pig breeds

    A: Sequence diversity of PERVs without LTRs in Eurasian pig breeds. The number of k-mer types in the reads aligned to PERVs without LTRs can reflect the sequence diversity of PERVs. The left venn diagram shows the numbers of specific k-mer types of PERVs not shared and common k-mer types of PERVs shared between all Chinese and Western pigs; the middle one shows the relation between Chinese and Western domestic pigs; the right one shows the relation between Chinese and Western wild boars. B: The percentage of PERVs with transposable potentiality in 63 Chinese and Western pigs. The above bar plot with pink background shows the percentage of seven PERVs with complete gag, pol, and env ORF in all Chinese (32) and Western (31) pigs. The bar plot below with green background shows the percentage of four PERVs with incomplete gene structure but with complete pol ORF in all Chinese and Western pigs. C: Total copy number of eleven PERVs with transposition potentialities in different pig breeds. D: PERV TIPs in ten Chinese and Western pig breeds. The left horizontal bar plot shows the total number of PERV TIPs in each pig breed. The top bar plot shows the number of PERV TIPs for each intersection. Only 86 all breed-common, 6 Chinese pig breed-common, 6 Western pig breed-common, and 150 breed-specific TIP loci are showed.

    Table  1.   Classification and descriptive statistics of all 59 PERVs in the Sus scrofa reference genome (assembly Build 11.1).

    No.Category1SubclassPERV nameChromosome / unplaced contigStrandPositionLength2Unique k-mer3Detection rate4
    1lcPERVPERV-APERV-A-1-132.0M1+132020281–1320283618 0812530.57
    2lcPERVPERV-APERV-A-1-262.2M1+262166347–2621752628 916350.38
    3lcPERVPERV-APERV-A-3-10.6M310660619–106695338 9156470.24
    4lcPERVPERV-APERV-A-5-92.1M592185133–921940508 9182260.56
    5lcPERVPERV-APERV-A-7-105.7M7+105710884–1057191938 3101190.17
    6lcPERVPERV-APERV-A-8-51.6M8+51570546–515794608 9154660.94
    7lcPERVPERV-APERV-A-12-28.2M12+28221374–282302878 914950.43
    8lcPERVPERV-APERV-A-13-142.0M13142030847–1420397598 9134511
    9lcPERVPERV-APERV-A-13-146.7M13146750532–1467595218 9905201
    10lcPERVPERV-APERV-A-15-66.8M1566864153–668730448 8925000.44
    11lcPERVPERV-APERV-A-17-3.7M173794010–38027098 7004111
    12lcPERVPERV-APERV-A-17-33.1M17+33062883–330718008 9189300.41
    13lcPERVPERV-AlikePERV-Alike-U965-14.7kbNW_018084965+14674–228278 1541 9330
    14lcPERVPERV-APERV-A-U136-0.5MNW_018085136563793–5727258 9331 2050.86
    15lcPERVPERV-APERV-A-X-73.7MX73752986–737619038 9185770.51
    16lcPERVPERV-APERV-A-Y-20.1MY20194782–202035728 7919830.46
    17lcPERVPERV-APERV-A-Y-21.8MY21867301–218760358 7359200.38
    18lcPERVPERV-APERV-A-Y-25.2MY+25245606–252539058 300110.63
    19lcPERVPERV-BPERV-B-3-51.1M351108601–511173608 7601970.86
    20lcPERVPERV-BPERV-B-4-45.5M445599494–456082528 7591320.62
    21lcPERVPERV-BPERV-B-8-15.3M8+15319428–153281878 7601770.76
    22lcPERVPERV-BPERV-B-9-138.8M9138895584–1389043408 757510.46
    23lcPERVPERV-BPERV-B-11-38.2M11+38201361–382101168 7563860.86
    24lcPERVPERV-BPERV-B-14-119.7M14+119667621–1196762998 6794860.46
    25lcPERVPERV-BPERV-B-15-110.9M15110958945–1109677828 8383740.44
    26lcPERVPERV-BPERV-B-16-59.6M16+59571885–595806468 7621410.44
    27lcPERVPERV-BPERV-B-U086-42.1kbNW_01808508642158–508768 7195640.81
    28lcPERVPERV-BPERV-B-U255-1.9kbNW_018085255+1949–107438 7952420.54
    29lcPERVPERV-BPERV-B-U331-13.8kbNW_018085331+13836–225978 762850.87
    30lcPERVPERV-CPERV-C-14-62.5M1462550397–625576457 2496520.78
    31lcPERVPERV-JX1PERV-JX1-7-21.2M7+21236160–212449768 8171 3871
    32lcPERVPERV-JX1PERV-JX1-17-41.4M1741467519–414761018 5831 3431
    33lcPERVPERV-JX1PERV-JX1-U293-0.8MNW_018085293+820148–8291929 0452 0151
    34lcPERVPERV-JX2PERV-JX2-X-71.4MX+71402222–714099127 6911 4720.49
    35lcPERVPERV-JX3PERV-JX3-3-17.8M3+17778858–177880869 2291 4601
    36lcPERVPERV-JX4PERV-JX4-2-76.6M276648002–766557887 7878591
    37siPERVPERV-AsPERV-A-6-10.4M6+10402614–104076575 044200.57
    38siPERVPERV-AsPERV-A-X-55.1MX+55079139–550832114 0731680.86
    39siPERVPERV-BsPERV-B-1-38.5M1+38459013–384650065 994610.48
    40siPERVPERV-BsPERV-B-X-112.8MX112842765–1128476574 8931080.76
    41siPERVPERV-CsPERV-C-5-29.4M5+29356367–293616385 2726390.78
    42siPERVPERV-CsPERV-C-11-29.1M1129084884–290903285 4456110.57
    43siPERVPERV-CsPERV-C-13-146.75M13146759522–1467649905 469190.56
    44siPERVPERV-CsPERV-C-13-146.76M13146764392–1467698585 467340
    45siPERVPERV-CsPERV-C-X-81.5MX81543240–815458992 6601780.56
    46siPERVPERV-AlikesPERV-Alike-U293-0.9MNW_018085293+909902–9140284 1277290
    47siPERVPERV-ClikesPERV-Clike-U154-3.2kbNW_018085154+3178–64833 3065050
    48siPERVPERV-ClikesPERV-Clike-U193-4.0kbNW_018085193+3949–72503 3022320.57
    49siPERVPERV-ClikesPERV-Clike-U355-19.3kbNW_018085355+19304–239384 6356040.81
    50siPERVPERV-ClikesPERV-Clike-Y-25.269MY25269797–252738274 031160.24
    51siPERVPERV-ClikesPERV-Clike-Y-25.29MY25299007–253020573 0510/
    52siPERVPERV-JX2likesPERV-JX2like-12-23.0M1222986893–229912204 3287041
    53siPERVPERV-JX3likesPERV-JX3like-15-116.3M15+116321677–11633478113 1051 2061
    54siPERVPERV-JX3likesPERV-JX3like-17-9.5M179536784–95415044 7218541
    55siPERVPERV-JX3likesPERV-JX3like-X-72.2MX+72244018–722491705 1539070.49
    56siPERVPERV-UCsPERV-UC1-9-63.2M963235598–632381362 5394050.63
    57siPERVPERV-UCsPERV-UC2-13-21.3M13+21308535–213107322 1984220.78
    58siPERVPERV-UCsPERV-UC3-Y-24.4MY+24407502–244111553 6546440.24
    59siPERVPERV-UCsPERV-UC4-Y-25.261MY+25261084–252647963 7137280.16
    1: LcPERV indicates long and complete or near-complete PERV; siPERV indicates short incomplete PERV. 2: The pol gene of sPERV-JX3like-15-116.3M was inserted by a 6 302 bp long sequence containing LINE1 transposon and (T)n simple repeat, which resulted in the length of the PERV increasing to 13 105 bp. 3: The number of unique k-mer (k=31) of PERV on pig reference genome. 4: The detection proportion of the PERV in the 63 Chinese and Western pigs; since the PERV sPERV-Clike-Y-25.29M has no unique k-mers, it cannot be detected in the tested pigs.
    下载: 导出CSV

    Table  2.   Average PERV and LTR copy numbers in ten pig breeds

    Pig breedAverage PERV copy No. (n, Method 1)Average PERV copy No. (n, Method 2)Average LTR copy No. (n, Method 1)Average LTR copy No. (n, Method 2)
    Western pigs49.1±6.548.2±6.3254.8±30.0204.7±26.7
    Duroc45.3±6.344.0±6.2224.5±18.2172.6±16.8
    European
    wild boar
    43.3±4.542.5±4.5234.0±10.6192.0±8.8
    Landrace55.6±4.054.6±4.0280.9±18.4230.4±16.1
    Large White46.1±5.045.7±4.2248.8±21.7197.0±15.0
    White Duroc51.9±4.150.7±4.0271.3±29.1219.1±23.0
    Chinese pigs32.0±4.032.0±4.2197.8±10.9160.4±13.6
    Bama Xiang27.8±5.128.5±5.4198.5±12.7164.0±13.6
    Chinese
    wild boar
    29.6±3.129.6±3.5189.9±12.4150.7±18.2
    Erhualian33.9±2.533.8±2.5196.5±12.6159.9±11.8
    Laiwu34.0±2.633.9±3.4202.0±7.3163.6±11.3
    Tibetian34.0±2.134.1±3.4202.4±4.6163.9±12.3
    P-value16.63×10-127.90×10-111.01×10-073.64×10-06
    1: P-value indicates the comparison result of PERV/LTR copy numbers between Chinese and Western pig breeds by student’s t-test. Number in bold indicates the minimum copy number detected by this method.
    下载: 导出CSV
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  • 收稿日期:  2022-03-05
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