Volume 40 Issue 4
Jul.  2019
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Article Contents
Yu Wang, Shan Gao, Yue Zhao, Chen Wei-Huang, Jun-Jie Shao, Wang Ni-Ni, Ming Li, Guang-Xian Zhou, Lei Wang, Wen-Jing Shen, Jing-Tao Xu, Wei-Dong Deng, Wen Wang, Yu-Lin Chen, Yu Jiang. Allele-specific expression and alternative splicing in horse×donkey and cattle×yak hybrids. Zoological Research, 2019, 40(4): 293-305. doi: 10.24272/j.issn.2095-8137.2019.042
Citation: Yu Wang, Shan Gao, Yue Zhao, Chen Wei-Huang, Jun-Jie Shao, Wang Ni-Ni, Ming Li, Guang-Xian Zhou, Lei Wang, Wen-Jing Shen, Jing-Tao Xu, Wei-Dong Deng, Wen Wang, Yu-Lin Chen, Yu Jiang. Allele-specific expression and alternative splicing in horse×donkey and cattle×yak hybrids. Zoological Research, 2019, 40(4): 293-305. doi: 10.24272/j.issn.2095-8137.2019.042

Allele-specific expression and alternative splicing in horse×donkey and cattle×yak hybrids

doi: 10.24272/j.issn.2095-8137.2019.042
Funds:  This work was supported by grants from the National Natural Science Foundation of China (31572381), National Thousand Youth Talents Plan of the International Science and Technology Cooperation Project of China (2013DFA31420), and Science and Technology Innovation Capability Promotion Program of the Science and Technology Department of Qinghai Province (2015-ZJ-712)
More Information
  • Corresponding author: Yu Jiang
  • Received Date: 2019-04-01
  • Publish Date: 2019-07-18
  • Divergence of gene expression and alternative splicing is a crucial driving force in the evolution of species; to date, however the molecular mechanism remains unclear. Hybrids of closely related species provide a suitable model to analyze allele-specific expression (ASE) and allele-specific alternative splicing (ASS). Analysis of ASE and ASS can uncover the differences in cis-regulatory elements between closely related species, while eliminating interference of trans-regulatory elements. Here, we provide a detailed characterization of ASE and ASS from 19 and 10 transcriptome datasets across five tissues from reciprocal-cross hybrids of horse×donkey (mule/hinny) and cattle×yak (dzo), respectively. Results showed that 4.8%–8.7% and 10.8%–16.7% of genes exhibited ASE and ASS, respectively. Notably, lncRNAs and pseudogenes were more likely to show ASE than protein-coding genes. In addition, genes showing ASE and ASS in mule/hinny were found to be involved in the regulation of muscle strength, whereas those of dzo were involved in high-altitude adaptation. In conclusion, our study demonstrated that exploration of genes showing ASE and ASS in hybrids of closely related species is feasible for species evolution research.
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  • [1]
    null Babbitt CC , Fedrigo O , Pfefferle AD , Boyle AP , Horvath JE , Furey TS , Wray GA . 2010. Both noncoding and protein-coding RNAs contribute to gene expression evolution in the Primate Brain. Genome Biology and Evolution, 2: 67–79.
    null Bellucci E , Bitocchi E , Ferrarini A , Benazzo A , Biagetti E , Klie S , Minio A , Rau D , Rodriguez M , Panziera A , Venturini L , Attene G , Albertini E , Jackson SA , Nanni L , Fernie AR , Nikoloski Z , Bertorelle G , Delledonne M , Papa R . 2014. Decreased nucleotide and expression diversity and modified coexpression patterns characterize domestication in the Common Bean. The Plant Cell, 26(5): 1901–1912.
    null Bolger AM , Lohse M , Usadel B . 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30(15): 2114–2120.
    null Brown JB , Boley N , Eisman R , May GE, Stoiber MH , Duff MO, Booth BW , Wen J , Park S , Suzuki AM , Wan KH , Yu C , Zhang D , Carlson JW , Cherbas L , Eads BD , Miller D , Mockaitis K , Roberts J , Davis CA , Frise E , Hammonds AS , Olson S , Shenker S , Sturgill D , Samsonova AA , Weiszmann R , Robinson G , Hernandez J , Andrews J , Bickel PJ , Carninci P , Cherbas P , Gingeras TR , Hoskins RA , Kaufman TC , Lai EC , Oliver B , Perrimon N , Graveley BR , Celniker SE . 2014. Diversity and dynamics of the Drosophila transcriptome. Nature, 512(7515): 393–399.
    null Crowley JJ , Zhabotynsky V , Sun W , Huang S , Pakatci IK , Kim Y , Wang JR , Morgan AP , Calaway JD , Aylor DL , Yun Z , Bell TA , Buus RJ , Calaway ME , Didion JP , Gooch TJ , Hansen SD , Robinson NN , Shaw GD , Spence JS , Quackenbush CR , Barrick CJ , Nonneman RJ , Kim K , Xenakis J , Xie Y , Valdar W , Lenarcic AB , Wang W , Welsh CE , Fu C , Zhang Z , Holt J , Guo Z , Threadgill DW , Tarantino LM , Miller DR , Zou F , Mcmillan L , Sullivan PF , De Villena FP . 2015. Analyses of allele-specific gene expression in highly divergent mouse crosses identifies pervasive allelic imbalance. Nature Genetics, 47: 353–360.
    null Eckersley-Maslin MA , Spector DL . 2014. Random monoallelic expression: regulating gene expression one allele at a time. Trends in Genetics, 30(6): 237–244.
    null Forrest ARR , Kawaji H , Rehli M , Baillie JK , de Hoon MJL , Haberle V , Lassmann T , Kulakovskiy IV , Lizio M , Itoh M , Andersson R , Mungall CJ , Meehan TF , Schmeier S , Bertin N , Jorgensen M , Dimont E , Arner E , Schmidl C , Schaefer U , Medvedeva YA , Plessy C , Vitezic M , Severin J , Semple C , Ishizu Y , Young RS , Francescatto M , Alam I , Albanese D , Altschuler GM , Arakawa T , Archer JA , Arner P , Babina M , Rennie S , Balwierz PJ , Beckhouse AG , Pradhan-Bhatt S , Blake JA , Blumenthal A , Bodega B , Bonetti A , Briggs J , Brombacher F , Burroughs AM , Califano A , Cannistraci CV , Carbajo D , Chen Y , Chierici M , Ciani Y , Clevers HC , Dalla E , Davis CA , Detmar M , Diehl AD , Dohi T , Drablos F , Edge AS , Edinger M , Ekwall K , Endoh M , Enomoto H , Fagiolini M , Fairbairn L , Fang H , Farach-Carson MC , Faulkner GJ , Favorov AV , Fisher ME , Frith MC , Fujita R , Fukuda S , Furlanello C , Furino M , Furusawa J , Geijtenbeek TB , Gibson AP , Gingeras T , Goldowitz D , Gough J , Guhl S , Guler R , Gustincich S , Ha TJ , Hamaguchi M , Hara M , Harbers M , Harshbarger J , Hasegawa A , Hasegawa Y , Hashimoto T , Herlyn M , Hitchens KJ , Ho SS , Hofmann OM , Hoof I , Hori F , Huminiecki L , Iida K , Ikawa T , Jankovic BR , Jia H , Joshi A , Jurman G , Kaczkowski B , Kai C , Kaida K , Kaiho A , Kajiyama K , Kanamori-Katayama M , Kasianov AS , Kasukawa T , Katayama S , Kato S , Kawaguchi S , Kawamoto H , Kawamura YI, Kawashima T , Kempfle JS , Kenna TJ , Kere J , Khachigian LM , Kitamura T , Klinken SP , Knox AJ , Kojima M , Kojima S , Kondo N , Koseki H , Koyasu S , Krampitz S , Kubosaki A , Kwon AT , Laros JF , Lee W , Lennartsson A , Li K , Lilje B , Lipovich L , Mackay-Sim A , Manabe R , Mar JC , Marchand B , Mathelier A , Mejhert N , Meynert A , Mizuno Y , de Lima MD , Morikawa H , Morimoto M , Moro K , Motakis E , Motohashi H , Mummery CL , Murata M , Nagao-Sato S , Nakachi Y , Nakahara F , Nakamura T , Nakamura Y , Nakazato K , van Nimwegen E , Ninomiya N , Nishiyori H , Noma S , Noma S , Noazaki T , Ogishima S , Ohkura N , Ohimiya H , Ohno H , Ohshima M , Okada-Hatakeyama M , Okazaki Y , Orlando V , Ovchinnikov DA , Pain A , Passier R , Patrikakis M , Persson H , Piazza S , Prendergast JG , Rackham OJ , Ramilowski JA , Rashid M , Ravasi T , Rizzu P , Roncador M , Roy S , Rye MB , Saijyo E , Sajantila A , Saka A , Sakaguchi S , Sakai M , Sato H , Savvi S , Saxena A , Schneider C , Schultes EA , Schulze-Tanzil GG , Schwegmann A , Sengstag T , Sheng G , Shimoji H , Shimoni Y , Shin JW , Simon C , Sugiyama D , Sugiyama T , Suzuki M , Suzuki N , Swoboda RK , Hoen PAC , Tagami M , Takahashi N , Takai J , Tanaka H , Tatsukawa H , Tatum Z , Thompson M , Toyodo H , Toyoda T , Valen E , van de Wetering M , van den Berg LM , Verado R , Vijayan D , Vorontsov IE , Wasserman WW , Watanabe S , Wells CA , Winteringham LN , Wolvetang E , Wood EJ , Yamaguchi Y , Yamamoto M , Yoneda M , Yonekura Y , Yoshida S , Zabierowski SE , Zhang PG , Zhao X , Zucchelli S , Summers KM , Suzuki H , Daub CO , Kawai J , Heutink P , Hide W , Freeman TC , Lenhard B , Bajic VB , Taylor MS , Makeev VJ , Sandelin A , Hume DA , Carninci P , Hayashizaki Y . 2014. A promoter-level mammalian expression atlas. Nature, 507(7493): 462–470.
    null Gamage N , Barnett A , Hempel N , Duggleby RG , Windmill KF , Martin JL , Mcmanus ME . 2006. Human sulfotransferases and their role in chemical metabolism. Toxicological Sciences, 90(1): 5–22.
    null Gao Q , Sun W , Ballegeer M , Libert C , Chen W . 2015. Predominant contribution of cis-regulatory divergence in the evolution of mouse alternative splicing. Molecular Systems Biology, 11(7): 816.
    null Ge RL , Cai Q , Shen YY , San A , Ma L , Zhang Y , Yi X , Chen Y , Yang L , Huang Y , He R , Hui Y , Hao M , Li Y , Wang B , Ou X , Xu J , Zhang Y , Wu K , Geng C , Zhou W , Zhou T , Irwin DM , Yang Y , Ying L , Bao H , Kim J , Larkin DM , Ma J , Lewin HA , Xing J , Platt RN , Ray DA , Auvil L , Capitanu B , Zhang X , Zhang G , Murphy RW , Wang J , Zhang YP , Wang J . 2013. Draft genome sequence of the Tibetan antelope. Nature Communications, 4: 1858.
    null Huitema LFA , Apschner A , Logister I , Spoorendonk KM , Bussmann J , Hammond CL , Schulte-Merker S . 2012. Entpd5 is essential for skeletal mineralization and regulates phosphate homeostasis in zebrafish. Proceedings of the National Academy of Sciences, 109(52): 21372–21377.
    null Johnsson P , Lipovich L , Grandér D , Morris KV . 2014. Evolutionary conservation of long non-coding RNAs; sequence, structure, function. Biochimica Biophysica Acta, 1840(3): 1063–1071.
    null Jordan IK , Mari?o-Ramírez L , Wolf YI, Koonin EV . 2004. Conservation and coevolution in the scale-free human gene coexpression network. Molecular Biology and Evolution, 21(11): 2058–2070.
    null Keane TM , Goodstadt L , Danecek P , White MA , Wong K , Yalcin B , Heger A , Agam A , Slater G , Goodson M , Furlotte NA, Eskin E , Nell?ker C , Whitley H , Cleak J , Janowitz D , Hernandez-Pliego P , Edwards A , Belgard TG , Oliver PL , Mcintyre RE , Bhomra A , Nicod J , Gan X , Yuan W , van der Weyden L , Steward CA , Bala S , Stalker J , Mott R , Durbin R , Jackson IJ , Czechanski A , Guerra-Assun??o JA , Donahue LR , Reinholdt LG , Payseur BA, Ponting CP , Birney E , Flint J , Adams DJ . 2011. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature, 477(7364): 289–294.
    null Kim D , Langmead B , Salzberg SL . 2015. HISAT: a fast spliced aligner with low memory requirements. Nature Methods, 12(4): 357–360.
    null Kwan T , Benovoy D , Dias C , Gurd S , Provencher C , Beaulieu P , Hudson TJ , Sladek R , Majewski J . 2008. Genome-wide analysis of transcript isoform variation in humans. Nature Genetics, 40(2): 225–231.
    null León-Novelo L , Gerken AR , Graze RM , Mcintyre LM , Marroni F . 2018. Direct testing for allele-specific expression differences between conditions. G 3, 8(2): g3–g300139.
    null Li H , Durbin R . 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14): 1754–1760.
    null Liao BY , Zhang J . 2006. Evolutionary conservation of expression profiles between human and mouse orthologous genes. Molecular Biology and Evolution, 23(3): 530–540.
    null Mira A , Pushker R . 2005. The silencing of pseudogenes. Molecular Biology and Evolution, 22(11): 2135–2138.
    null Orlando L , Ginolhac A , Zhang G , Froese D , Albrechtsen A , Stiller M , Schubert M , Cappellini E , Petersen B , Moltke I , Johnson PLF , Fumagalli M , Vilstrup JT , Raghavan M , Korneliussen T , Malaspinas A , Vogt J , Szklarczyk D , Kelstrup CD , Vinther J , Dolocan A , Stenderup J , Velazquez AMV , Cahill J , Rasmussen M , Wang X , Min J , Zazula GD , Seguin-Orlando A , Mortensen C , Magnussen K , Thompson JF , Weinstock J , Gregersen K , R?ed KH , Eisenmann V , Rubin CJ , Miller DC , Antczak DF , Bertelsen MF , Brunak S , Al-Rasheid KAS , Ryder O , Andersson L , Mundy J , Krogh A , Gilbert MTP , Kj?r K , Sicheritz-Ponten T , Jensen LJ , Olsen JV , Hofreiter M , Nielsen R , Shapiro B , Wang J , Willerslev E . 2013. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature, 499(7456): 74–78.
    null Pertea M , Kim D , Pertea GM , Leek JT , Salzberg SL . 2016. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nature Protocols, 11(9): 1650–1667.
    null Pinter SF , Colognori D , Beliveau BJ , Sadreyev RI , Payer B , Yildirim E , Wu CT , Lee JT . 2015. Allelic imbalance is a prevalent and Tissue-Specific Feature of the Mouse Transcriptome. Genetics, 200(2): 537–549.
    null Pollard KS , Salama SR , Lambert N , Lambot MA , Coppens S , Pedersen JS , Katzman S , King B , Onodera C , Siepel A , Kern AD , Dehay C , Igel H , Ares MJ , Vanderhaeghen P , Haussler D . 2006. An RNA gene expressed during cortical development evolved rapidly in humans. Nature, 443(7108): 167–172.
    null Prabhakar S , Visel A , Akiyama JA , Shoukry M , Lewis KD , Holt A , Plajzer-Frick I , Morrison H , Fitzpatrick DR , Afzal V , Pennacchio LA , Rubin EM , Noonan JP . 2008. Human-specific gain of function in a developmental enhancer. Science, 321(5894): 1346–1350.
    null Qiu Q , Zhang G , Ma T , Qian W , Wang J , Ye Z , Cao C , Hu Q , Kim J , Larkin DM , Auvil L , Capitanu B , Ma J , Lewin HA , Qian X , Lang Y , Zhou R , Wang L , Wang K , Xia J , Liao S , Pan S , Lu X , Hou H , Wang Y , Zang X , Yin Y , Ma H , Zhang J , Wang Z , Zhang Y , Zhang D , Yonezawa T , Hasegawa M , Zhong Y , Liu W , Zhang Y , Huang Z , Zhang S , Long R , Yang H , Wang J , Lenstra JA , Cooper DN , Wu Y , Wang J , Shi P , Wang J , Liu J . 2012. The yak genome and adaptation to life at high altitude. Nature Genetics, 44(8): 946–949.
    null Renaud G , Petersen B , Seguin-Orlando A , Bertelsen MF , Waller A , Newton R , Paillot R , Bryant N , Vaudin M , Librado P , Orlando L . 2018. Improved de novo genomic assembly for the domestic donkey. Science advances, 4(4): q392.
    null Shen S , Park JW , Lu Z , Lin L , Henry MD , Wu YN , Zhou Q , Xing Y . 2014. rMATS: Robust and flexible detection of differential alternative splicing from replicate RNA-Seq data. Proceedings of the National Academy of Sciences, 111(51): E5593–E5601.
    null Storer BE , Kim C . 1990. Exact properties of some exact test statistics for comparing two binomial proportions. Journal of the American Statistical Association, 85(409): 146–155.
    null Takada F , Woude DLV , Tong HQ , Thompson TG , Watkins SC , Kunkel LM , Beggs AH . 2001. Myozenin: an alpha-actinin- and gamma-filamin-binding protein of skeletal muscle Z lines. Proceedings of the National Academy of Sciences of the United States of America, 98(4): 1595–1600.
    null Tirosh I , Reikhav S , Levy AA , Barkai N . 2009. A yeast hybrid provides insight into the evolution of gene expression regulation. Science, 324(5927): 659–662.
    null Trapnell C , Pachter L , Salzberg SL . 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25(9): 1105–1111.
    null Villar D , Berthelot C , Aldridge S , Rayner TF , Lukk M , Pignatelli M , Park TJ , Deaville R , Erichsen JT , Jasinska AJ , Turner JMA , Bertelsen MF , Murchison EP , Flicek P , Odom DT . 2015. Enhancer evolution across 20 mammalian species. Cell, 160(3): 554–566.
    null Wang ET , Sandberg R , Luo S , Khrebtukova I , Zhang L , Mayr C , Kingsmore SF , Schroth GP , Burge CB . 2008. Alternative isoform regulation in human tissue transcriptomes. Nature, 456(7221): 470–476.
    null Wang X , Miller DC , Harman R , Antczak DF , Clark AG . 2013. Paternally expressed genes predominate in the placenta. Proceedings of the National Academy of Sciences of the United States of America, 110(26): 10705–10710.
    null Wood DLA , Nones K , Steptoe A , Christ A , Harliwong I , Newell F , Bruxner TJC , Miller D , Cloonan N , Grimmond SM . 2015. Recommendations for accurate resolution of gene and isoform Allele-Specific Expression in RNA-Seq Data. PLoS One, 10(5): e126911.
    null Zhang Z , Li J , Zhao XQ , Wang J , Wong GK , Yu J . 2006. KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics, Proteomics & Bioinformatics, 4(4): 259–263.
    null Zheng-Bradley X , Rung J , Parkinson H , Brazma A . 2010. Large scale comparison of global gene expression patterns in human and mouse. Genome Biology, 11(12): R124.
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