Advertisement

Molecular Genetics and Genomics

, Volume 294, Issue 1, pp 121–133 | Cite as

Birth and death of Mx genes and the presence/absence of genes regulating Mx transcription are correlated with the diversity of anti-pathogenicity in vertebrate species

  • Furong Qi
  • Airong Yang
  • Sadaf Ambreen
  • Xue Bai
  • Yali HouEmail author
  • Xuemei LuEmail author
Original Article
  • 71 Downloads

Abstract

Gene duplication and amino acid substitution are two types of genetic innovations of antiviral genes in inhibiting the emerging pathogens in different species. Mx proteins are well known for inhibiting negative-stranded RNA viruses and have evolved a number of paralogs or orthologs, showing distinct antiviral activities or capacities within or between species. The presence of upstream genes in the signaling pathway(s) that activates Mx genes (upstream regulators of Mx gene) also exhibits variety across species. The association between the evolution of Mx gene and their upstream regulators and the various antiviral capacities in host species has not been investigated. Herein, we traced the evolution of Mx gene and profiled the gene birth/death events on each branch of the 64 chordate species. We provided additional support that the diversity in gene member and amino acid changes in the different clades is correlated to their various antiviral activities of the species. We identified amino acid substitutions that may lead to the functional divergence between Mx paralogs in rodents. Although the copy number of the Mx gene is conserved in birds, infection by influenza A virus (IAV) results in diverse morbidity rates in different avian species. The evidences of gene interaction in the IAV-induced pathway and the genome analysis performed in this study indicated that the existence of the upstream regulators of Mx gene exhibits variation among different species, particularly in birds. The variation is related to the differences in the expression of Mx genes, resulting in the antiviral specificity and morbidity rates in avian species. We conclude that the antiviral capacity in host species is associated with the variations in the gene number of the Mx gene family and the existence of upstream regulators of Mx gene as well.

Keywords

Influenza A virus Mx Regulatory genes Gene occurrence Antiviral activity 

Notes

Author contributions

XL, YH and FQ conceived and designed the experiments, FQ, AY and XB performed the data collection, FQ performed the data analysis, FQ, YH and XL wrote and revised the manuscript. SA revised the manuscript.

Funding

This study was funded by the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant number XDB13000000); the National Natural Science Foundation of China (Grant number 91531305, 31771416 and 31301963); Youth Innovation Promotion Association, Chinese Academy of Sciences; and CAS-TWAS President’s Fellowship for International PhD Students.

Compliance with ethical standards

Conflict of interest

Furong Qi declares that she has no conflict of interest. Airong Yang declares that she has no conflict of interest. Sadaf Ambreen declares that she has no conflict of interest. Xue Bai declares that she has no conflict of interest. Yali Hou declares that she has no conflict of interest. Xuemei Lu declares that she has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

438_2018_1490_MOESM1_ESM.tiff (1.2 mb)
Supplementary material 1 (TIFF 1195 KB)
438_2018_1490_MOESM2_ESM.tiff (406 kb)
Supplementary material 2 (TIFF 406 KB)
438_2018_1490_MOESM3_ESM.tiff (1.3 mb)
Supplementary material 3 (TIFF 1342 KB)
438_2018_1490_MOESM4_ESM.tiff (2.5 mb)
Supplementary material 4 (TIFF 2567 KB)
438_2018_1490_MOESM5_ESM.tiff (302 kb)
Supplementary material 5 (TIFF 301 KB)
438_2018_1490_MOESM6_ESM.tiff (1.3 mb)
Supplementary material 6 (TIFF 1378 KB)
438_2018_1490_MOESM7_ESM.docx (114 kb)
Supplementary material 7 (DOCX 114 KB)
438_2018_1490_MOESM8_ESM.xlsx (53 kb)
Supplementary material 8 (XLSX 52 KB)
438_2018_1490_MOESM9_ESM.xlsx (42 kb)
Supplementary material 9 (XLSX 41 KB)
438_2018_1490_MOESM10_ESM.xlsx (48 kb)
Supplementary material 10 (XLSX 48 KB)
438_2018_1490_MOESM11_ESM.xlsx (35 kb)
Supplementary material 11 (XLSX 35 KB)
438_2018_1490_MOESM12_ESM.xlsx (37 kb)
Supplementary material 12 (XLSX 36 KB)

References

  1. Abdul-Sater AA, Majoros A, Plumlee CR, Perry S, Gu A-D, Lee C, Shresta S, Decker T, Schindler C (2015) Different STAT transcription complexes drive early and delayed responses to type I IFNs. J Immunol 195:210–216Google Scholar
  2. Adzhubei I, Jordan DM, Sunyaev SR (2013) Predicting functional effect of human missense mutations using PolyPhen-2. Curr Protoc Hum Genet 76:7–20Google Scholar
  3. Anisimova M, Nielsen R, Yang Z (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229–1236Google Scholar
  4. Barber MRW, Aldridge JR, Webster RG, Magor KE (2010) Association of RIG-I with innate immunity of ducks to influenza. Proc Natl Acad Sci 107:5913–5918Google Scholar
  5. Bazzigher L, Schwarz A, Staeheli P (1993) No enhanced influenza virus resistance of murine and avian cells expressing cloned duck Mx protein. Virology 195:100–112Google Scholar
  6. Benfield CTO, Lyall JW, Kochs G, Tiley LS (2008) Asparagine 631 variants of the chicken Mx protein do not inhibit influenza virus replication in primary chicken embryo fibroblasts or in vitro Surrogate assays. J Virol 82:7533–7539Google Scholar
  7. Bernasconi D, Schultz U, Staeheli P (1995) The interferon-induced Mx protein of chickens lacks antiviral activity. J Interferon Cytokine Res 15:47–53Google Scholar
  8. Blanchet S, Thomas F, Loot G (2009) Reciprocal effects between host phenotype and pathogens: new insights from an old problem. Trends Parasitol 25:364–369Google Scholar
  9. Brawand D, Soumillon M, Necsulea A, Julien P, Csardi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M, Albert FW, Zeller U, Khaitovich P, Grutzner F, Bergmann S, Nielsen R, Paabo S, Kaessmann H (2011) The evolution of gene expression levels in mammalian organs. Nature 478:343–348Google Scholar
  10. Budzko L, Marcinkowska-Swojak M, Jackowiak P, Kozlowski P, Figlerowicz M (2016) Copy number variation of genes involved in the hepatitis C virus-human interactome. Sci Rep 6:31340Google Scholar
  11. Byrne AB, Weirauch MT, Wong V, Koeva M, Dixon SJ, Stuart JM, Roy PJ (2007) A global analysis of genetic interactions in Caenorhabditis elegans. J Biol 6:8Google Scholar
  12. Cagliani R, Sironi M (2013) Pathogen-driven selection in the human genome. Int J Evol Biol 2013:6Google Scholar
  13. Chang M, Collet B, Nie P, Lester K, Campbell S, Secombes CJ, Zou J (2011) Expression and functional characterization of the RIG-I-like receptors MDA5 and LGP2 in rainbow trout (Oncorhynchus mykiss). J Virol 85:8403–8412Google Scholar
  14. Cheon H, Holvey-Bates EG, Schoggins JW, Forster S, Hertzog P, Imanaka N, Rice CM, Jackson MW, Junk DJ, Stark GR (2013) IFNβ-dependent increases in STAT1, STAT2, and IRF9 mediate resistance to viruses and DNA damage. EMBO J 32:2751–2763Google Scholar
  15. Cornelissen JBWJ, Post J, Peeters B, Vervelde L, Rebel JMJ (2012) Differential innate responses of chickens and ducks to low-pathogenic avian influenza. Avian Pathol 41:519–529Google Scholar
  16. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JLY, Toufighi K, Mostafavi S, Prinz J, St. Onge RP, VanderSluis B, Makhnevych T, Vizeacoumar FJ, Alizadeh S, Bahr S, Brost RL, Chen Y, Cokol M, Deshpande R, Li Z, Lin Z-Y, Liang W, Marback M, Paw J, San Luis B-J, Shuteriqi E, Tong AHY, van Dyk N, Wallace IM, Whitney JA, Weirauch MT, Zhong G, Zhu H, Houry WA, Brudno M, Ragibizadeh S, Papp B, Pál C, Roth FP, Giaever G, Nislow C, Troyanskaya OG, Bussey H, Bader GD, Gingras A-C, Morris QD, Kim PM, Kaiser CA, Myers CL, Andrews BJ, Boone C (2010) The genetic landscape of a cell. Science 327:425–431Google Scholar
  17. de Almeida ERD, Reiche EMV, Kallaur AP, Flauzino T, Watanabe MAE (2013) The roles of genetic polymorphisms and human immunodeficiency virus infection in lipid metabolism. Biomed Res Int 2013:15Google Scholar
  18. Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3:e314Google Scholar
  19. Fang L-Z, Zhao L, Wen H-L, Zhang Z-T, Liu J-W, He S-T, Xue Z-F, Ma D-Q, Zhang X-S, Zhang Y, Yu X-j (2015) Reservoir host expansion of hantavirus, China. Emerging Infect Dis 21:170–171Google Scholar
  20. Frese M, Kochs G, Feldmann H, Hertkorn C, Haller O (1996) Inhibition of bunyaviruses, phleboviruses, and hantaviruses by human MxA protein. J Virol 70:915–923Google Scholar
  21. Gao S, von der Malsburg A, Dick A, Faelber K, Schroder GF, Haller O, Kochs G, Daumke O (2011) Structure of myxovirus resistance protein a reveals intra- and intermolecular domain interactions required for the antiviral function. Immunity 35:514–525Google Scholar
  22. Glasauer SMK, Neuhauss SCF (2014) Whole-genome duplication in teleost fishes and its evolutionary consequences. Mol Genet Genom 289:1045–1060Google Scholar
  23. Goodman M, Czelusniak J, Moore GW, Romero-Herrera AE, Matsuda G (1979) Fitting the gene lineage into its species lineage, a parsimony strategy illustrated by cladograms constructed from globin sequences. Syst Zool 28:132–163Google Scholar
  24. Goujon C, Moncorge O, Bauby H, Doyle T, Ward CC, Schaller T, Hue S, Barclay WS, Schulz R, Malim MH (2013) Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 502:559–562Google Scholar
  25. Haller O, Staeheli P, Schwemmle M, Kochs G (2015) Mx GTPases: dynamin-like antiviral machines of innate immunity. Trends Microbiol 23:154–163Google Scholar
  26. Hatesuer B, Hoang HTT, Riese P, Trittel S, Gerhauser I, Elbahesh H, Geffers R, Wilk E, Schughart K (2017) Deletion of irf3 and rf7 genes in mice results in altered interferon pathway activation and granulocyte-dominated inflammatory responses to influenza A infection. J Innate Immun 9:145–161Google Scholar
  27. Heaton NS, Langlois RA, Sachs D, Lim JK, Palese P, tenOever BR (2014) Long-term survival of influenza virus infected club cells drives immunopathology. J Exp Med 211:1707–1714Google Scholar
  28. Henikoff S, Henikoff JG (1992) Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 89:10915–10919Google Scholar
  29. Herenda D, Chambers PG, Ettriqui A, Seneviratna P, da Silva TJP (2000) Manual on meat inspection for developing countries, Chap 7. FAO, RomeGoogle Scholar
  30. Hinshaw JE (2000) Dynamin and its role in membrane fission. Annu Rev Cell Dev Biol 16:483–519Google Scholar
  31. Holzinger D, Jorns C, Stertz S, Boisson-Dupuis S, Thimme R, Weidmann M, Casanova J-L, Haller O, Kochs G (2007) Induction of MxA gene expression by influenza A virus requires type I or type III interferon signaling. J Virol 81:7776–7785Google Scholar
  32. Horisberger MA (1992) Virus-specific effects of recombinant porcine interferon-γ and the induction of Mx proteins in pig cells. J Interferon Res 12:439–444Google Scholar
  33. Hu J, Mo Y, Wang X, Gu M, Hu Z, Zhong L, Wu Q, Hao X, Hu S, Liu W, Liu H, Liu X, Liu X (2015) PA-X decreases the pathogenicity of highly pathogenic H5N1 influenza A virus in avian species by inhibiting virus replication and host response. J Virol 89:4126–4142Google Scholar
  34. Huang B, Qi ZT, Xu Z, Nie P (2010) Global characterization of interferon regulatory factor (IRF) genes in vertebrates: glimpse of the diversification in evolution. BMC Immunol 11:22Google Scholar
  35. Hughes AL, Friedman R (2008) Genome size reduction in the chicken has involved massive loss of ancestral protein-coding genes. Mol Biol Evol 25:2681–2688Google Scholar
  36. Jin KH, Yoshimatsu K, Takada A, Ogino M, Asano A, Arikawa J, Watanabe T (2001) Mouse Mx2 protein inhibits hantavirus but not influenza virus replication. Arch Virol 146:41–49Google Scholar
  37. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden T (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5Google Scholar
  38. Kaessmann H (2010) Origins, evolution, and phenotypic impact of new genes. Genome Res 20:1313–1326Google Scholar
  39. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh C-S, Reis e Sousa C, Matsuura Y, Fujita T, Akira S (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101–105Google Scholar
  40. Kaufman J, Milne S, Göbel TWF, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923Google Scholar
  41. Ko J-H, Jin H-K, Asano A, Takada A, Ninomiya A, Kida H, Hokiyama H, Ohara M, Tsuzuki M, Nishibori M, Mizutani M, Watanabe T (2002) Polymorphisms and the differential antiviral activity of the chicken Mx gene. Genome Res 12:595–601Google Scholar
  42. Kuchipudi SV, Dunham SP, Chang K-C (2015) DNA microarray global gene expression analysis of influenza virus-infected chicken and duck cells. Genom Data 4:60–64Google Scholar
  43. Lage K, Karlberg EO, Storling ZM, Olason PI, Pedersen AG, Rigina O, Hinsby AM, Tumer Z, Pociot F, Tommerup N, Moreau Y, Brunak S (2007) A human phenome–interactome network of protein complexes implicated in genetic disorders. Nat Biotech 25:309–316Google Scholar
  44. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Meth 9:357–359Google Scholar
  45. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948Google Scholar
  46. Lee I, Ambaru B, Thakkar P, Marcotte EM, Rhee SY (2010a) Rational association of genes with traits using a genome-scale gene network for Arabidopsis thaliana. Nat Biotech 28:149–156Google Scholar
  47. Lee SMY, Chan RWY, Gardy JL, Lo C-k, Sihoe ADL, Kang SSR, Cheung TKW, Guan Y, Chan MCW, Hancock REW, Peiris MJS (2010b) Systems-level comparison of host responses induced by pandemic and seasonal influenza A H1N1 viruses in primary human type I-like alveolar epithelial cells in vitro. Respir Res 11:147Google Scholar
  48. Lee I, Seo Y-S, Coltrane D, Hwang S, Oh T, Marcotte EM, Ronald PC (2011) Genetic dissection of the biotic stress response using a genome-scale gene network for rice. Proc Natl Acad Sci 108:18548–18553Google Scholar
  49. Lefèvre T, Lebarbenchon C, Gauthier-Clerc M, Missé D, Poulin R, Thomas F (2009) The ecological significance of manipulative parasites. Trends Ecol Evol 24:41–48Google Scholar
  50. Lehner B (2013) Genotype to phenotype: lessons from model organisms for human genetics. Nat Rev Genet 14:168–178Google Scholar
  51. Li G, Zhang J, Sun Y, Wang H, Wang Y (2009a) The evolutionarily dynamic IFN-inducible GTPase proteins play conserved immune functions in vertebrates and cephalochordates. Mol Biol Evol 26:1619–1630Google Scholar
  52. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S (2009b) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079Google Scholar
  53. Li Y, Zhou H, Wen Z, Wu S, Huang C, Jia G, Chen H, Jin M (2011) Transcription analysis on response of swine lung to H1N1 swine influenza virus. BMC Genom 12:398Google Scholar
  54. Loo Y-M, Fornek J, Crochet N, Bajwa G, Perwitasari O, Martinez-Sobrido L, Akira S, Gill MA, García-Sastre A, Katze MG, Gale M (2008) Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 82:335–345Google Scholar
  55. Lu L, Chen Y, Wang Z, Li X, Chen W, Tao Z, Shen J, Tian Y, Wang D, Li G, Chen L, Chen F, Fang D, Yu L, Sun Y, Ma Y, Li J, Wang J (2015) The goose genome sequence leads to insights into the evolution of waterfowl and susceptibility to fatty liver. Genome Biol 16:89Google Scholar
  56. Mansour SMG, ElBakrey RM, Ali H, Knudsen DEB, Eid AAM (2014) Natural infection with highly pathogenic avian influenza virus H5N1 in domestic pigeons (Columba livia) in Egypt. Avian Pathol 43:319–324Google Scholar
  57. McCormack WT, Tjoelker LW, Thompson CB (1991) Avian B-cell development: generation of an immunoglobulin repertoire by gene conversion. Annu Rev Immunol 9:219–241Google Scholar
  58. Mitchell PS, Patzina C, Emerman M, Haller O, Malik Harmit S, Kochs G (2012) Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe 12:598–604Google Scholar
  59. Mitchell PS, Young JM, Emerman M, Malik HS (2015) Evolutionary analyses suggest a function of MxB immunity proteins beyond lentivirus restriction. PLoS Pathog 11:e1005304Google Scholar
  60. Nakatani Y, Takeda H, Kohara Y, Morishita S (2007) Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res 17:1254–1265Google Scholar
  61. Nakhaei P, Genin P, Civas A, Hiscott J (2009) RIG-I-like receptors: sensing and responding to RNA virus infection. Semin Immunol 21:215–222Google Scholar
  62. Page RDM (1994) Maps between trees and cladistic analysis of historical associations among genes, organisms, and areas. Syst Biol 43:58–77Google Scholar
  63. Pavlovic J, Zürcher T, Haller O, Staeheli P (1990) Resistance to influenza virus and vesicular stomatitis virus conferred by expression of human MxA protein. J Virol 64:3370–3375Google Scholar
  64. Pavlovic J, Haller O, Staeheli P (1992) Human and mouse Mx proteins inhibit different steps of the influenza virus multiplication cycle. J Virol 66:2564–2569Google Scholar
  65. Perkins LEL, Swayne DE (2003) Varied pathogenicity of a Hong Kong-origin H5N1 avian influenza virus in four passerine species and budgerigars. Vet Pathol 40:14–24Google Scholar
  66. Phillips PC (2008) Epistasis—the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9:855–867Google Scholar
  67. Prelich G (2012) Gene overexpression: uses, mechanisms, and interpretation. Genetics 190:841–854Google Scholar
  68. Reemers SS, Groot Koerkamp MJ, Holstege FC, van Eden W, Vervelde L (2009) Cellular host transcriptional responses to influenza A virus in chicken tracheal organ cultures differ from responses in in vivo infected trachea. Vet Immunol Immunopathol 132:91–100Google Scholar
  69. Reubold TF, Faelber K, Plattner N, Posor Y, Ketel K, Curth U, Schlegel J, Anand R, Manstein DJ, Noé F, Haucke V, Daumke O, Eschenburg S (2015) Crystal structure of the dynamin tetramer. Nature 525:404Google Scholar
  70. Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, Nakao K, Nakaya T, Katsuki M, Noguchi S, Tanaka N, Taniguchi T (2000) Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-α/β gene induction. Immunity 13:539–548Google Scholar
  71. Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538Google Scholar
  72. Schneider WM, Chevillotte MD, Rice CM (2014) Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol 32:513–545Google Scholar
  73. Schoggins JW, Rice CM (2011) Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 1:519–525Google Scholar
  74. Schusser B, Reuter A, von der Malsburg A, Penski N, Weigend S, Kaspers B, Staeheli P, Hartle S (2011) Mx is dispensable for interferon-mediated resistance of chicken cells against influenza A virus. J Virol 85:8307–8315Google Scholar
  75. Shapira SD, Gat-Viks I, Shum BOV, Dricot A, Degrace MM, Liguo W, Gupta PB, Hao T, Silver SJ, Root DE, Hill DE, Regev A, Hacohen N (2009) A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell 139:1255–1267Google Scholar
  76. Sottoriva A, Spiteri I, Piccirillo SGM, Touloumis A, Collins VP, Marioni JC, Curtis C, Watts C, Tavaré S (2013) Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci USA 110:4009–4014Google Scholar
  77. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313Google Scholar
  78. Taubenberger JK, Kash JC (2010) Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7:440–451Google Scholar
  79. Torgerson DG, Singh RS (2004) Rapid evolution through gene duplication and subfunctionalization of the testes-specific α4 proteasome subunits in drosophila. Genetics 168:1421–1432Google Scholar
  80. Tumpey TM, Szretter KJ, Van Hoeven N, Katz JM, Kochs G, Haller O, García-Sastre A, Staeheli P (2007) The Mx1 gene protects mice against the pandemic 1918 and highly lethal human H5N1 influenza viruses. J Virol 81:10818–10821Google Scholar
  81. Verhelst J, Hulpiau P, Saelens X (2013) Mx proteins: antiviral gatekeepers that restrain the uninvited. Microbiol Mol Biol Rev 77:551–566Google Scholar
  82. Wei L, Cui J, Song Y, Zhang S, Han F, Yuan R, Gong L, Jiao P, Liao M (2014) Duck MDA5 functions in innate immunity against H5N1 highly pathogenic avian influenza virus infections. Vet Res 45:66Google Scholar
  83. Woo GH, Bae YC, Jean YH, Bak EJ, Kim MJ, Hwang EK, Joo YS (2011) Comparative histopathological characteristics of highly pathogenic avian influenza (HPAI) in chickens and domestic ducks in 2008 Korea. Histol Histopathol 26:167–175Google Scholar
  84. Xu W, Shao Q, Zang Y, Guo Q, Zhang Y, Li Z (2015) Pigeon RIG-I function in innate immunity against H9N2 IAV and IBDV. Viruses 7:4131–4151Google Scholar
  85. Yan Q, Yang H, Yang D, Zhao B, Ouyang Z, Liu Z, Fan N, Ouyang H, Gu W, Lai L (2014) Production of transgenic pigs over-expressing the antiviral gene Mx. Cell Regen 3:11Google Scholar
  86. Yan Y, Yang N, Cheng HH, Song J, Qu L (2015) Genome-wide identification of copy number variations between two chicken lines that differ in genetic resistance to Marek’s disease. BMC Genom 16:843Google Scholar
  87. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591Google Scholar
  88. Zhang G, Li B, Li C, Gilbert MTP, Jarvis ED, Wang J (2014a) Comparative genomic data of the avian phylogenomics project. GigaScience 3:26Google Scholar
  89. Zhang G, Li C, Li Q, Li B, Larkin DM, Lee C, Storz JF, Antunes A, Greenwold MJ, Meredith RW, Ödeen A, Cui J, Zhou Q, Xu L, Pan H, Wang Z, Jin L, Zhang P, Hu H, Yang W, Hu J, Xiao J, Yang Z, Liu Y, Xie Q, Yu H, Lian J, Wen P, Zhang F, Li H, Zeng Y, Xiong Z, Liu S, Zhou L, Huang Z, An N, Wang J, Zheng Q, Xiong Y, Wang G, Wang B, Wang J, Fan Y, da Fonseca RR, Alfaro-Núñez A, Schubert M, Orlando L, Mourier T, Howard JT, Ganapathy G, Pfenning A, Whitney O, Rivas MV, Hara E, Smith J, Farré M, Narayan J, Slavov G, Romanov MN, Borges R, Machado JP, Khan I, Springer MS, Gatesy J, Hoffmann FG, Opazo JC, Håstad O, Sawyer RH, Kim H, Kim K-W, Kim HJ, Cho S, Li N, Huang Y, Bruford MW, Zhan X, Dixon A, Bertelsen MF, Derryberry E, Warren W, Wilson RK, Li S, Ray DA, Green RE, O’Brien SJ, Griffin D, Johnson WE, Haussler D, Ryder OA, Willerslev E, Graves GR, Alström P, Fjeldså J, Mindell DP, Edwards SV, Braun EL, Rahbek C, Burt DW, Houde P, Zhang Y, Yang H, Wang J, Consortium AG, Jarvis ED, Gilbert MTP, Wang J (2014b) Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346:1311–1320Google Scholar
  90. Zhou P, Zhai S, Zhou X, Lin P, Jiang T, Hu X, Jiang Y, Wu B, Zhang Q, Xu X, Li J-p, Liu B (2011) Molecular characterization of transcriptome-wide interactions between highly pathogenic porcine reproductive and respiratory syndrome virus and porcine alveolar macrophages in vivo. Int J Biol Sci 7:947–959Google Scholar
  91. Zou J, Chang M, Nie P, Secombes CJ (2009) Origin and evolution of the RIG-I like RNA helicase gene family. BMC Evol Biol 9:85Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Genomics and Precision Medicine, Beijing Institute of GenomicsChinese Academy of SciencesBeijingPeople’s Republic of China
  2. 2.CAS Center for Excellence in Animal Evolution and GeneticsChinese Academy of SciencesKunmingPeople’s Republic of China
  3. 3.University of Chinese Academy of SciencesBeijingPeople’s Republic of China

Personalised recommendations