The power of “controllers”: Transposon-mediated duplicated genes evolve towards neofunctionalization

Huijing Ma; Mengxia Wang; Yong E. Zhang; Shengjun Tan

doi:10.1016/j.jgg.2023.04.003

Volume 50 Issue 7

Jul. 2023

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2023 > 50(7): 462-472

PDF( 1822 KB)

The power of “controllers”: Transposon-mediated duplicated genes evolve towards neofunctionalization

doi: 10.1016/j.jgg.2023.04.003

a. Key Laboratory of Zoological Systematics and Evolution&State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China;
b. University of Chinese Academy of Sciences, Beijing 100049, China;
c. CAS Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, Yunnan 650223, China;
d. Chinese Institute for Brain Research, Beijing 102206, China

Funds:

This work was supported by the Ministry of Agriculture and Rural Affairs of China, the National Key R&D Program of China (2019YFA0802600), the Chinese Academy of Sciences (ZDBS-LY-SM005, XDPB17) and the National Natural Science Foundation of China (31970565).

Received Date: 2022-12-22
Accepted Date: 2023-04-05
Rev Recd Date: 2023-04-04
Publish Date: 2023-07-28

Abstract

Abstract

Since the discovery of the first transposon by Dr. Barbara McClintock, the prevalence and diversity of transposable elements (TEs) have been gradually recognized. As fundamental genetic components, TEs drive organismal evolution not only by contributing functional sequences (e.g., regulatory elements or “controllers” as phrased by Dr. McClintock) but also by shuffling genomic sequences. In the latter respect, TE-mediated gene duplications have contributed to the origination of new genes and attracted extensive interest. In response to the development of this field, we herein attempt to provide an overview of TE-mediated duplication by focusing on common rules emerging across duplications generated by different TE types. Specifically, despite the huge divergence of transposition machinery across TEs, we identify three common features of various TE-mediated duplication mechanisms, including end bypass, template switching, and recurrent transposition. These three features lead to one common functional outcome, namely, TE-mediated duplicates tend to be subjected to exon shuffling and neofunctionalization. Therefore, the intrinsic properties of the mutational mechanism constrain the evolutionary trajectories of these duplicates. We finally discuss the future of this field including an in-depth characterization of both the duplication mechanisms and functions of TE-mediated duplicates.
- Transposable elements,
- Gene duplication,
- New gene origination,
- End bypass,
- Template switching,
- Exon shuffling,
- Neofunctionalization,
- Mutational constraint

FullText(HTML)

References(132)

References

[1]	Akiva, P., Toporik, A., Edelheit, S., Peretz, Y., Diber, A., Shemesh, R., Novik, A.,Sorek, R., 2006. Transcription-mediated gene fusion in the human genome. Genome Res. 16, 30-36.
[2]	Almeida, M.V., Vernaz, G., Putman, A.L.K.,Miska, E.A., 2022. Taming transposable elements in vertebrates: from epigenetic silencing to domestication. Trends Genet. 38, 529-553.
[3]	Babcock, M., Pavlicek, A., Spiteri, E., Kashork, C.D., Ioshikhes, I., Shaffer, L.G., Jurka, J.,Morrow, B.E., 2003. Shuffling of genes within low-copy repeats on 22q11 (LCR22) by Alu-mediated recombination events during evolution. Genome Res. 13, 2519-2532.
[4]	Bailey, J.A., Liu, G.,Eichler, E.E., 2003. An Alu transposition model for the origin and expansion of human segmental duplications. Am. J. Hum. Genet. 73, 823-834.
[5]	Barbaglia, A.M., Klusman, K.M., Higgins, J., Shaw, J.R., Hannah, L.C.,Lal, S.K., 2012. Gene capture by Helitron transposons reshuffles the transcriptome of maize. Genetics 190, 965-975.
[6]	Batcher, K., Dickinson, P., Maciejczyk, K., Brzeski, K., Rasouliha, S.H., Letko, A., Droegemueller, C., Leeb, T.,Bannasch, D., 2020. Multiple FGF4 retrocopies recently derived within canids. Genes 11, 839.
[7]	Batcher, K., Varney, S., York, D., Blacksmith, M., Kidd, J.M., Rebhun, R., Dickinson, P.,Bannasch, D., 2022. Recent, full-length gene retrocopies are common in canids. Genome Res. 32, 1602-1611.
[8]	Betran, E.,Long, M., 2001. Gene Fusion. e LS.
[9]	Brunner, S., Pea, G.,Rafalski, A., 2005. Origins, genetic organization and transcription of a family of non-autonomous helitron elements in maize. Plant J. 43, 799-810.
[10]	Buzdin, A., Gogvadze, E., Kovalskaya, E., Volchkov, P., Ustyugova, S., Illarionova, A., Fushan, A., Vinogradova, T.,Sverdlov, E., 2003. The human genome contains many types of chimeric retrogenes generated through in vivo RNA recombination. Nucleic Acids Res. 31, 4385-4390.
[11]	Buzdin, A., Ustyugova, S., Gogvadze, E., Vinogradova, T., Lebedev, Y.,Sverdlov, E., 2002. A new family of chimeric retrotranscripts formed by a full copy of U6 small nuclear RNA fused to the 3' terminus of L1. Genomics 80, 402-406.
[12]	Calatrava, V., Stephens, T.G., Gabr, A., Bhaya, D., Bhattacharya, D.,Grossman, A.R., 2022. Retrotransposition facilitated the establishment of a primary plastid in the thecate amoeba Paulinella. Proc. Natl. Acad. Sci. U. S. A. 119, e2121241119.
[13]	Carelli, F.N., Hayakawa, T., Go, Y., Imai, H., Warnefors, M.,Kaessmann, H., 2016. The life history of retrocopies illuminates the evolution of new mammalian genes. Genome Res. 26, 301-314.
[14]	Catoni, M., Jonesman, T., Cerruti, E.,Paszkowski, J., 2019. Mobilization of Pack-CACTA transposons in Arabidopsis suggests the mechanism of gene shuffling. Nucleic Acids Res. 47, 1311-1320.
[15]	Cerbin, S.,Jiang, N., 2018. Duplication of host genes by transposable elements. Curr. Opin. Genet. Dev. 49, 63-69.
[16]	Chan, Y.F., Marks, M.E., Jones, F.C., Villarreal, G., Jr., Shapiro, M.D., Brady, S.D., Southwick, A.M., Absher, D.M., Grimwood, J., Schmutz, J., et al., 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302-305.
[17]	Ciomborowska, J., Rosikiewicz, W., Szklarczyk, D., Makalowski, W.,Makalowska, I., 2013. "Orphan" retrogenes in the human genome. Mol. Biol. Evol. 30, 384-396.
[18]	Cosby, R.L., Chang, N.-C.,Feschotte, C., 2019. Host-transposon interactions: conflict, cooperation, and cooption. Genes Dev. 33, 1098-1116.
[19]	Cosby, R.L., Judd, J., Zhang, R., Zhong, A., Garry, N., Pritham, E.J.,Feschotte, C., 2021. Recurrent evolution of vertebrate transcription factors by transposase capture. Science 371, eabc6405.
[20]	Cost, G.J., Feng, Q.H., Jacquier, A.,Boeke, J.D., 2002. Human L1 element target-primed reverse transcription in vitro. EMBO J. 21, 5899-5910.
[21]	Delviks-Frankenberry, K., Galli, A., Nikolaitchik, O., Mens, H., Pathak, V.K.,Hu, W.-S., 2011. Mechanisms and factors that influence high frequency retroviral recombination. Viruses 3, 1650-1680.
[22]	Derr, L.K., Strathern, J.N.,Garfinkel, D.J., 1991. RNA-mediated recombination in Saccharomyces-cerevisiae. Cell 67, 355-364.
[23]	Dobzhansky, T., 1973. Nothing in biology makes sense except in the light of evolution. Am. Biol. Teach. 35, 125-129.
[24]	Dong, Y., Lu, X., Song, W., Shi, L., Zhang, M., Zhao, H., Jiao, Y.,Lai, J., 2011. Structural characterization of helitrons and their stepwise capturing of gene fragments in the maize genome. BMC Genomics 12, 1-11.
[25]	Dooner, H.K.,Weil, C.F., 2007. Give-and-take: interactions between DNA transposons and their host plant genomes. Curr. Opin. Genet. Dev. 17, 486-492.
[26]	Dooner, H.K.,Weil, C.F., 2013. Transposons and Gene Creation. Plant Transposons Genome Dynamics in Evolution pp, 143-164.
[27]	Eickbush, T.H., 1992. Transposing without ends - the non-LTR retrotransposable elements. New Biol. 4, 430-440.
[28]	Elrouby, N.,Bureau, T.E., 2010. Bs1, a new chimeric gene formed by retrotransposon-mediated exon shuffling in maize. Plant Physiol. 153, 1413-1424.
[29]	Emerson, J.J., Cardoso-Moreira, M., Borevitz, J.O.,Long, M., 2008. Natural selection shapes genome-wide patterns of copy-number polymorphism in Drosophila melanogaster. Science 320, 1629-1631.
[30]	Emerson, J.J., Kaessmann, H., Betran, E.,Long, M.Y., 2004. Extensive gene traffic on the mammalian X chromosome. Science 303, 537-540.
[31]	Fanning, T.G.,Singer, M.F., 1987. LINE-1 - a mammalian transposable element. Biochim. Biophys. Acta 910, 203-212.
[32]	Feng, Q.H., Moran, J.V., Kazazian, H.H.,Boeke, J.D., 1996. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87, 905-916.
[33]	Feschotte, C.,Wessler, S.R., 2001. Treasures in the attic: rolling circle transposons discovered in eukaryotic genomes. Proc. Natl. Acad. Sci. U. S. A. 98, 8923-8924.
[34]	Finnegan, D.J., 1989. Eukaryotic transposable elements and genome evolution. Trends Genet. 5, 103-107.
[35]	Fueyo, R., Judd, J., Feschotte, C.,Wysocka, J., 2022. Roles of transposable elements in the regulation of mammalian transcription. Nat. Rev. Mol. Cell Biol. 23, 481-497.
[36]	Gilbert, W., 1978. Why genes in pieces. Nature 271, 501-501.
[37]	Gloor, G.B., Nassif, N.A., Johnsonschlitz, D.M., Preston, C.R.,Engels, W.R., 1991. Targeted gene replacement in Drosophila via P-element-induced gap repair. Science 253, 1110-1117.
[38]	Goodier, J.L., Ostertag, E.M.,Kazazian, H.H., 2000. Transduction of 3'-flanking sequences is common in L1 retrotransposition. Hum. Mol. Genet. 9, 653-657.
[39]	Goodrich, D.W.,Duesberg, P.H., 1990. Retroviral recombination during reverse transcription. Proc. Natl. Acad. Sci. U. S. A. 87, 2052-2056.
[40]	Grabundzija, I., Hickman, A.B.,Dyda, F., 2018. Helraiser intermediates provide insight into the mechanism of eukaryotic replicative transposition. Nat. Commun. 9, 1278.
[41]	Grabundzija, I., Messing, S.A., Thomas, J., Cosby, R.L., Bilic, I., Miskey, C., Gogol-Doering, A., Kapitonov, V., Diem, T., Dalda, A., et al., 2016. A Helitron transposon reconstructed from bats reveals a novel mechanism of genome shuffling in eukaryotes. Nat. Commun. 7, 10716.
[42]	Gray, Y.H.M., 2000. It takes two transposons to tango - transposable-element-mediated chromosomal rearrangements. Trends Genet. 16, 461-468.
[43]	Hajjar, A.M.,Linial, M.L., 1993. A model system for nonhomologous recombination between retroviral and cellular RNA. J. Virol. 67, 3845-3853.
[44]	Han, M.-J., Shen, Y.-H., Xu, M.-S., Liang, H.-Y., Zhang, H.-H.,Zhang, Z., 2013. Identification and evolution of the silkworm Helitrons and their contribution to transcripts. DNA Res. 20, 471-484.
[45]	Hanada, K., Vallejo, V., Nobuta, K., Slotkin, R.K., Lisch, D., Meyers, B.C., Shiu, S.-H.,Jiang, N., 2009. The functional role of pack-MULEs in rice inferred from purifying selection and expression profile. Plant Cell 21, 25-38.
[46]	Hu, Y., Wu, X., Jin, G., Peng, J., Leng, R., Li, L., Gui, D., Fan, C.,Zhang, C., 2022. Rapid genome evolution and adaptation of Thlaspi arvense mediated by recurrent RNA-based and tandem gene duplications. Front. Plant Sci. 12, 772655.
[47]	Hwang, S.-Y., Jung, H., Mun, S., Lee, S., Park, K., Baek, S.C., Moon, H.C., Kim, H., Kim, B., Choi, Y., et al., 2021. L1 retrotransposons exploit RNA m(6)A modification as an evolutionary driving force. Nat. Commun. 12, 880.
[48]	Innan, H.,Kondrashov, F., 2010. The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11, 97-108.
[49]	Izsvak, Z., Stuwe, E., Fiedler, D., Katzer, A., Jeggo, P.,Ivics, Z., 2004. Healing the wounds inflicted by Sleeping Beauty transposition by double-strand break repair in mammalian somatic cells. Eur. J. Cell Biol. 83, 279-290.
[50]	Jamain, S., Girondot, M., Leroy, P., Clergue, M., Quach, H., Fellous, M.,Bourgeron, T., 2001. Transduction of the human gene FAM8A1 by endogenous retrovirus during primate evolution. Genomics 78, 38-45.
[51]	Jiang, N., Bao, Z.R., Zhang, X.Y., Eddy, S.R.,Wessler, S.R., 2004. Pack-MULE transposable elements mediate gene evolution in plants. Nature 431, 569-573.
[52]	Jiang, N., Gao, D., Xiao, H.,van der Knaap, E., 2009. Genome organization of the tomato sun locus and characterization of the unusual retrotransposon Rider. Plant J. 60, 181-193.
[53]	Kaessmann, H., 2009. Genetics. More than just a copy. Science 325, 958-959.
[54]	Kaessmann, H., Vinckenbosch, N.,Long, M., 2009. RNA-based gene duplication: mechanistic and evolutionary insights. Nat. Rev. Genet. 10, 19-31.
[55]	Kapitonov, V.V.,Jurka, J., 2007. Helitrons on a roll: eukaryotic rolling-circle transposons. Trends Genet. 23, 521-529.
[56]	Katju, V., 2012. In with the old, in with the new: the promiscuity of the duplication process engenders diverse pathways for novel gene creation. Int. J. Evol. Biol. 2012, 341932-341932.
[57]	Kazazian, H.H., 2004. Mobile elements: drivers of genome evolution. Science 303, 1626-1632.
[58]	Kazazian, H.H.,Moran, J.V., 1998. The impact of L1 retrotransposons on the human genome. Nat. Genet. 19, 19-24.
[59]	Kleckner, N., Chan, R.K., Tye, B.-K.,Botstein, D., 1975. Mutagenesis by insertion of a drug-resistance element carrying an inverted repetition. J. Mol. Biol. 97, 561-575.
[60]	Kojima, K.K., Bao, W., Kojima, N.F.,Kohany, O., 2023. Repbase 2022 Year in Review.
[61]	Kosek, D., Grabundzija, I., Lei, H., Bilic, I., Wang, H., Jin, Y., Peaslee, G.F., Hickman, A.B.,Dyda, F., 2021. The large bat Helitron DNA transposase forms a compact monomeric assembly that buries and protects its covalently bound 5'-transposon end. Mol. Cell 81, 4271-4286.
[62]	Kubiak, M.R.,Makalowska, I., 2017. Protein-coding genes' retrocopies and their functions. Viruses 9, 80.
[63]	Lal, S., Oetjens, M.,Hannah, L.C., 2009. Helitrons: enigmatic abductors and mobilizers of host genome sequences. Plant Sci. (Amsterdam, Neth.) 176, 181-186.
[64]	Lisch, D., 2005. Pack-MULEs: theft on a massive scale. Bioessays 27, 353-355.
[65]	Long, M., Betran, E., Thornton, K.,Wang, W., 2003. The origin of new genes: glimpses from the young and old. Nat. Rev. Genet. 4, 865-875.
[66]	Long, M., VanKuren, N.W., Chen, S.,Vibranovski, M.D., 2013. New gene evolution: little did we know. Annu. Rev. Genet. 47, 307-333.
[67]	Long, M.Y.,Langley, C.H., 1993. Natural-selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science 260, 91-95.
[68]	Luan, D.D., Korman, M.H., Jakubczak, J.L.,Eickbush, T.H., 1993. Reverse transcription of R2BM RNA is primed by a nick at the chromosomal target site - a mechanism for non-LTR retrotransposition. Cell 72, 595-605.
[69]	Lynch, M.,Conery, J.S., 2000. The evolutionary fate and consequences of duplicate genes. Science 290, 1151-1155.
[70]	Lynch, M.,Katju, V., 2004. The altered evolutionary trajectories of gene duplicates. Trends Genet. 20, 544-549.
[71]	Ma, C., Li, C., Ma, H., Yu, D., Zhang, Y., Zhang, D., Su, T., Wu, J., Wang, X., Zhang, L., et al., 2022. Pan-cancer surveys indicate cell cycle-related roles of primate-specific genes in tumors and embryonic cerebrum. Genome Biol. 23, 1-29.
[72]	Makalowski, W., Mitchell, G.A.,Labuda, D., 1994. Alu sequences in the coding regions of messenger-RNA - source of protein variability. Trends Genet. 10, 188-193.
[73]	Martin-Alonso, S., Frutos-Beltran, E.,Menendez-Arias, L., 2021. Reverse transcriptase: from transcriptomics to genome editing. Trends Biotechnol. 39, 194-210.
[74]	McClintock, B., 1948. Mutable loci in maize. Carnegie Inst. Wash. 47, 155-169.
[75]	McClintock, B., 1950. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. U. S. A. 36, 344-355.
[76]	McClintock, B., 1956. Controlling elements and the gene. Cold Spring Harb. Symp. Quant. Biol. 21, 197-216.
[77]	Moran, J.V., DeBerardinis, R.J.,Kazazian, H.H., 1999. Exon shuffling by L1 retrotransposition. Science 283, 1530-1534.
[78]	Moran, J.V., Holmes, S.E., Naas, T.P., DeBerardinis, R.J., Boeke, J.D.,Kazazian, H.H., 1996. High frequency retrotransposition in cultured mammalian cells. Cell 87, 917-927.
[79]	Moran, J.V., Zimmerly, S., Eskes, R., Kennell, J.C., Lambowitz, A.M., Butow, R.A.,Perlman, P.S., 1995. Mobile group-II introns of yeast mitochondrial-DNA are novel site-specific retroelements. Mol. Cell. Biol. 15, 2828-2838.
[80]	Morgante, M., Brunner, S., Pea, G., Fengler, K., Zuccolo, A.,Rafalski, A., 2005. Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat. Genet. 37, 997-1002.
[81]	Nei, M., 2007. The new mutation theory of phenotypic evolution. Proc. Natl. Acad. Sci. U. S. A. 104, 12235-12242.
[82]	Ohno, S., 1970. Evolution by Gene Duplication. London: George Alien & Unwin Ltd. Berlin, Heidelberg and New York: Springer-Verlag.
[83]	Pan, D.,Zhang, L., 2009. Burst of young retrogenes and independent retrogene formation in mammals. PLoS One 4, e5040.
[84]	Parker, H.G., VonHoldt, B.M., Quignon, P., Margulies, E.H., Shao, S., Mosher, D.S., Spady, T.C., Elkahloun, A., Cargill, M., Jones, P.G., et al., 2009. An expressed Fgf4 retrogene is associated with breed-defining chondrodysplasia in domestic dogs. Science 325, 995-998.
[85]	Paterson, A.H., Bowers, J.E., Bruggmann, R., Dubchak, I., Grimwood, J., Gundlach, H., Haberer, G., Hellsten, U., Mitros, T., Poliakov, A., et al., 2009. The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551-556.
[86]	Peng, H., Mirouze, M.,Bucher, E., 2022. Extrachromosomal circular DNA: a neglected nucleic acid molecule in plants. Curr. Opin. Plant Biol. 69, 102263.
[87]	Petrov, D.A., Lozovskaya, E.R.,Hartl, D.L., 1996. High intrinsic: rate of DNA loss in Drosophila. Nature 384, 346-349.
[88]	Pickeral, O.K., Makalowski, W., Boguski, M.S.,Boeke, J.D., 2000. Frequent human genomic DNA transduction driven by LINE-1 retrotransposition. Genome Res. 10, 411-415.
[89]	Pritham, E.J.,Feschotte, C., 2007. Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus. Proc. Natl. Acad. Sci. U. S. A. 104, 1895-1900.
[90]	Qian, W.,Zhang, J., 2008. Gene dosage and gene duplicability. Genetics 179, 2319-2324.
[91]	Rosenberg, S.M.,Queitsch, C., 2014. Combating evolution to fight disease. Science 343, 1088-1089.
[92]	Rosikiewicz, W., Kabza, M., Kosinski, J.G., Ciomborowska-Basheer, J., Kubiak, M.R.,Makalowska, I., 2017. RetrogeneDB-a database of plant and animal retrocopies. Database-the Journal of Biological Databases and Curation.
[93]	Rubin, G.M., Kidwell, M.G.,Bingham, P.M., 1982. The molecular basis of P-M hybrid dysgenesis: the nature of induced mutations. Cell 29, 987-994.
[94]	Sayah, D.M., Sokolskaja, E., Berthoux, L.,Luban, J., 2004. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430, 569-573.
[95]	Schacherer, J., Tourrette, Y., Souciet, J.L., Potier, S.,De Montigny, J., 2004. Recovery of a function involving gene duplication by retroposition in Saccharomyces cerevisiae. Genome Res. 14, 1291-1297.
[96]	Sulak, M., Fong, L., Mika, K., Chigurupati, S., Yon, L., Mongan, N.P., Emes, R.D.,Lynch, V.J., 2016. TP53 copy number expansion is associated with the evolution of increased body size and an enhanced DNA damage response in elephants. Elife 5, e11994.
[97]	Sun, C., Shepard, D.B., Chong, R.A., Arriaza, J.L., Hall, K., Castoe, T.A., Feschotte, C., Pollock, D.D.,Mueller, R.L., 2012. LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders. Genome Biol. Evol. 4, 168-183.
[98]	Tan, S., Cardoso-Moreira, M., Shi, W., Zhang, D., Huang, J., Mao, Y., Jia, H., Zhang, Y., Chen, C., Shao, Y., et al., 2016. LTR-mediated retroposition as a mechanism of RNA-based duplication in metazoans. Genome Res. 26, 1663-1675.
[99]	Tan, S., Ma, H., Wang, J., Wang, M., Wang, M., Yin, H., Zhang, Y., Zhang, X., Shen, J., Wang, D., et al., 2021. DNA transposons mediate duplications via transposition-independent and -dependent mechanisms in metazoans. Nat. Commun. 12, 4280.
[100]	Tempel, S., Nicolas, J., El Amrani, A.,Couee, I., 2007. Model-based identification of Helitrons results in a new classification of their families in Arabidopsis thaliana. Gene 403, 18-28.
[101]	Thomas, J., Phillips, C.D., Baker, R.J.,Pritham, E.J., 2014. Rolling-circle transposons catalyze genomic innovation in a mammalian lineage. Genome Biol. Evol. 6, 2595-2610.
[102]	Thomas, J.,Pritham, E.J., 2015. Helitrons, the eukaryotic rolling-circle transposable elements. Mobile DNA iii, 891-924.
[103]	Tsubota, S.I.,Huong, D.V., 1991. Capture of flanking DNA by a P-element in Drosophila-melanogaster - creation of a transposable element. Proc. Natl. Acad. Sci. U. S. A. 88, 693-697.
[104]	Vinckenbosch, N., Dupanloup, I.,Kaessmann, H., 2006. Evolutionary fate of retroposed gene copies in the human genome. Proc. Natl. Acad. Sci. U. S. A. 103, 3220-3225.
[105]	Wang, D., Yu, C., Zuo, T., Zhang, J., Weber, D.F.,Peterson, T., 2015. Alternative transposition generates new chimeric genes and segmental duplications at the maize p1 locus. Genetics 201, 925-935.
[106]	Wang, L., Tracy, L., Su, W., Yang, F., Feng, Y., Silverman, N.,Zhang, Z.Z.Z., 2022a. Retrotransposon activation during Drosophila metamorphosis conditions adult antiviral responses. Nat. Genet., 1-13.
[107]	Wang, W., Brunet, F.G., Nevo, E.,Long, M., 2002. Origin of sphinx, a young chimeric RNA gene in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 99, 4448-4453.
[108]	Wang, W., Zheng, H., Fan, C., Li, J., Shi, J., Cai, Z., Zhang, G., Liu, D., Zhang, J., Vang, S., et al., 2006. High rate of chimeric gene origination by retroposition in plant genomes. Plant Cell 18, 1791-1802.
[109]	Wang, X., Yan, X., Hu, Y., Qin, L., Wang, D., Jia, J.,Jiao, Y., 2022b. A recent burst of gene duplications in Triticeae. Plant Commun. 3, 100286.
[110]	Wei, W., Gilbert, N., Ooi, S.L., Lawler, J.F., Ostertag, E.M., Kazazian, H.H., Boeke, J.D.,Moran, J.V., 2001. Human L1 retrotransposition: cis preference versus trans complementation. Mol. Cell. Biol. 21, 1429-1439.
[111]	Wells, J.N.,Feschotte, C., 2020. A field guide to eukaryotic transposable elements. Annu. Rev. Genet. 54, 539-561.
[112]	Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J.L., Capy, P., Chalhoub, B., Flavell, A., Leroy, P., Morgante, M., Panaud, O., et al., 2007. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8, 973-982.
[113]	Wilhelm, M.,Wilhelm, F.X., 2001. Reverse transcription of retroviruses and LTR retrotransposons. Cell. Mol. Life Sci. 58, 1246-1262.
[114]	Witt, E., Benjamin, S., Svetec, N.,Zhao, L., 2019. Testis single-cell RNA-seq reveals the dynamics of de novo gene transcription and germline mutational bias in Drosophila. Elife 8, e47138.
[115]	Xia, S., Wang, Z., Zhang, H., Hu, K., Zhang, Z., Qin, M., Dun, X., Yi, B., Wen, J., Ma, C., et al., 2016. Altered transcription and neofunctionalization of duplicated genes rescue the harmful effects of a chimeric gene in Brassica napus. Plant Cell 28, 2060-2078.
[116]	Xiao, H., Jiang, N., Schaffner, E., Stockinger, E.J.,van der Knaap, E., 2008. A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319, 1527-1530.
[117]	Xie, K.T., Wang, G., Thompson, A.C., Wucherpfennig, J.I., Reimchen, T.E., MacColl, A.D.C., Schluter, D., Bell, M.A., Vasquez, K.M.,Kingsley, D.M., 2019. DNA fragility in the parallel evolution of pelvic reduction in stickleback fish. Science 363, 81-84.
[118]	Yang, L., Emerman, M., Malik, H.S.,McLaughlin, R.N.J.E., 2020. Retrocopying expands the functional repertoire of APOBEC3 antiviral proteins in primates. Elife 9, e58436.
[119]	Yang, L.X.,Bennetzen, J.L., 2009. Distribution, diversity, evolution, and survival of Helitrons in the maize genome. Proc. Natl. Acad. Sci. U. S. A. 106, 19922-19927.
[120]	Yang, S., Arguello, J.R., Li, X., Ding, Y., Zhou, Q., Chen, Y., Zhang, Y., Zhao, R., Brunet, F., Peng, L., et al., 2008. Repetitive element-mediated recombination as a mechanism for new gene origination in Drosophila. PLoS Genet. 4, e3.
[121]	Yant, S.R.,Kay, M.A., 2003. Nonhomologous-end-joining factors regulate DNA repair fidelity during Sleeping Beauty element transposition in mammalian cells. Mol. Cell. Biol. 23, 8505-8518.
[122]	Zhang, D., Leng, L., Chen, C., Huang, J., Zhang, Y., Yuan, H., Ma, C., Chen, H.,Zhang, Y.E., 2022. Dosage sensitivity and exon shuffling shape the landscape of polymorphic duplicates in Drosophila and humans. Nat. Ecol. Evol. 6, 273-287.
[123]	Zhang, J., Yang, H., Long, M., Li, L.,Dean, A.M., 2010. Evolution of enzymatic activities of testis-specific short-chain dehydrogenase/reductase in Drosophila. J. Mol. Evol. 71, 241-249.
[124]	Zhang, J.M., Dean, A.M., Brunet, F.,Long, M.Y., 2004a. Evolving protein functional diversity in new genes of Drosophila. Proc. Natl. Acad. Sci. U. S. A. 101, 16246-16250.
[125]	Zhang, J.Z., 2003. Evolution by gene duplication: an update. Trends Ecol. Evol. 18, 292-298.
[126]	Zhang, W.,Tautz, D., 2022. Tracing the origin and evolutionary fate of recent gene retrocopies in natural populations of the house mouse. Mol. Biol. Evol. 39, msab360.
[127]	Zhang, Y., Lu, S., Zhao, S., Zheng, X., Long, M.,Wei, L., 2009. Positive selection for the male functionality of a co-retroposed gene in the hominoids. BMC Evol. Biol. 9, 1-12.
[128]	Zhang, Z.L., Carriero, N.,Gerstein, M., 2004b. Comparative analysis of processed pseudogenes in the mouse and human genomes. Trends Genet. 20, 62-67.
[129]	Zhang, Z.L., Harrison, P.M., Liu, Y.,Gerstein, M., 2003. Millions of years of evolution preserved: a comprehensive catalog of the processed pseudogenes in the human genome. Genome Res. 13, 2541-2558.
[130]	Zhao, D., Ferguson, A.A.,Jiang, N., 2016. What makes up plant genomes: the vanishing line between transposable elements and genes. Biochim. Biophys. Acta - Gene Regul. Mech. 1859, 366-380.
[131]	Zhao, D., Hamilton, J.P., Vaillancourt, B., Zhang, W., Eizenga, G.C., Cui, Y., Jiang, J., Buell, C.R.,Jiang, N., 2018. The unique epigenetic features of Pack-MULEs and their impact on chromosomal base composition and expression spectrum. Nucleic Acids Res. 46, 2380-2397.
[132]	Zhou, Y.,Zhang, C., 2019. Evolutionary patterns of chimeric retrogenes in Oryza species. Sci. Rep. 9, 17733.