Generic placeholder image

Current Genomics

Editor-in-Chief

ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

Opinion Article

The Role of Sequence Duplication in Transcriptional Regulation and Genome Evolution

Author(s): Luis M. Vaschetto* and Natalia Ortiz

Volume 20, Issue 6, 2019

Page: [405 - 408] Pages: 4

DOI: 10.2174/1389202920666190320140721

Price: $65

Open Access Journals Promotions 2
conference banner
Abstract

Sequence duplication is nowadays recognized as an important mechanism that underlies the evolution of eukaryote genomes, being indeed one of the most powerful strategies for the generation of adaptive diversity by modulating transcriptional activity. The evolutionary novelties simultaneously associated with sequence duplication and differential gene expression can be collectively referred to as duplication-mediated transcriptional regulation. In the last years, evidence has emerged supporting the idea that sequence duplication and functionalization represent important evolutionary strategies acting at the genome level, and both coding and non-coding sequences have been found to be targets of such events. Moreover, it has been proposed that deleterious effects of sequence duplication might be potentially silenced by endogenous cell machinery (i.e., RNA interference, epigenetic repressive marks, etc). Along these lines, our aim is to highlight the role of sequence duplication on transcriptional activity and the importance of both in genome evolution.

Keywords: Sequence duplication, genome evolution, transcriptional regulation, gene duplication, transposable elements, gene expression.

Graphical Abstract
[1]
Tang, M.; Chen, Z.; Grover, C.E.; Wang, Y.; Li, S.; Liu, G.; Ma, Z.; Wendel, J.F.; Hua, J. Rapid evolutionary divergence of Gossypium barbadense and G. hirsutum mitochondrial genomes. BMC Genomics, 2015, 16(1), 770.
[http://dx.doi.org/10.1186/s12864-015-1988-0] [PMID: 26459858]
[2]
Hermansen, R.A.; Hvidsten, T.R.; Sandve, S.R.; Liberles, D.A. Extracting functional trends from whole genome duplication events using comparative genomics. Biol. Proced. Online, 2016, 18(1), 11.
[http://dx.doi.org/10.1186/s12575-016-0041-2] [PMID: 27168732]
[3]
McElroy, K.E.; Denton, R.D.; Sharbrough, J.; Bankers, L.; Neiman, M.; Lisle Gibbs, H. Genome expression balance in a triploid trihybrid vertebrate. Genome Biol. Evol., 2017, 9(4), 968-980.
[http://dx.doi.org/10.1093/gbe/evx059] [PMID: 28369297]
[4]
Bittel, D.C.; Kibiryeva, N.; Dasouki, M.; Knoll, J.H.; Butler, M.G.A.A. 9-year-old male with a duplication of chromosome 3p25.3p26.2: Clinical report and gene expression analysis. Am. J. Med. Genet. A., 2006, 140(6), 573-579.
[http://dx.doi.org/10.1002/ajmg.a.31132] [PMID: 16470700]
[5]
Andersson, D.I.; Jerlström-Hultqvist, J.; Näsvall, J. Evolution of new functions de novo and from preexisting genes. Cold Spring Harb. Perspect. Biol., 2015, 7(6)a017996
[http://dx.doi.org/10.1101/cshperspect.a017996] [PMID: 26032716]
[6]
Espinosa-Cantú, A.; Ascencio, D.; Barona-Gómez, F.; DeLuna, A. Gene duplication and the evolution of moonlighting proteins. Front. Genet., 2015, 6, 227.
[http://dx.doi.org/10.3389/fgene.2015.00227] [PMID: 26217376]
[7]
Bianconi, M.E.; Dunning, L.T.; Moreno-Villena, J.J.; Osborne, C.P.; Christin, P.A. Gene duplication and dosage effects during the early emergence of C4 photosynthesis in the grass genus Alloteropsis. J. Exp. Bot., 2018, 69(8), 1967-1980.
[http://dx.doi.org/10.1093/jxb/ery029] [PMID: 29394370]
[8]
Leite, D.J.; Ninova, M.; Hilbrant, M.; Arif, S.; Griffiths-Jones, S.; Ronshaugen, M.; McGregor, A.P. Pervasive microRNA duplication in Chelicerates: Insights from the embryonic microRNA repertoire of the spider Parasteatoda tepidariorum. Genome Biol. Evol., 2016, 8(7), 2133-2144.
[http://dx.doi.org/10.1093/gbe/evw143] [PMID: 27324919]
[9]
Luo, J.; Wang, Y.; Yuan, J.; Zhao, Z.; Lu, J. MicroRNA duplication accelerates the recruitment of new targets during vertebrate evolution. RNA, 2018, 24(6), 787-802.
[http://dx.doi.org/10.1261/rna.062752.117] [PMID: 29511046]
[10]
Innan, H.; Kondrashov, F. The evolution of gene duplications: Classifying and distinguishing between models. Nat. Rev. Genet., 2010, 11(2), 97-108.
[http://dx.doi.org/10.1038/nrg2689] [PMID: 20051986]
[11]
Lan, X.; Pritchard, J.K. Coregulation of tandem duplicate genes slows evolution of subfunctionalization in mammals. Science, 2016, 352(6288), 1009-1013.
[http://dx.doi.org/10.1126/science.aad8411] [PMID: 27199432]
[12]
Guschanski, K.; Warnefors, M.; Kaessmann, H. The evolution of duplicate gene expression in mammalian organs. Genome Res., 2017, 27(9), 1461-1474.
[http://dx.doi.org/10.1101/gr.215566.116] [PMID: 28743766]
[13]
Gao, D.; Ko, D.C.; Tian, X.; Yang, G.; Wang, L. Expression divergence of duplicate genes in the protein kinase superfamily in Pacific oyster. Evol. Bioinform. Online, 2015, 11(Suppl. 1), 57-65.
[http://dx.doi.org/10.4137/EBO.S30230] [PMID: 26417197]
[14]
Chen, F.; Capecchi, M.R. Paralogous mouse Hox genes, Hoxa9, Hoxb9, and Hoxd9, function together to control development of the mammary gland in response to pregnancy. Proc. Natl. Acad. Sci. USA, 1999, 96(2), 541-546.
[http://dx.doi.org/10.1073/pnas.96.2.541] [PMID: 9892669]
[15]
Brena, C.; Chipman, A.D.; Minelli, A.; Akam, M. Expression of trunk Hox genes in the centipede Strigamia maritima: Sense and anti-sense transcripts. Evol. Dev., 2006, 8(3), 252-265.
[http://dx.doi.org/10.1111/j.1525-142X.2006.00096.x] [PMID: 16686636]
[16]
Lemons, D.; McGinnis, W. Genomic evolution of Hox gene clusters. Science, 2006, 313(5795), 1918-1922.
[http://dx.doi.org/10.1126/science.1132040] [PMID: 17008523]
[17]
Hrycaj, S.M.; Dye, B.R.; Baker, N.C.; Larsen, B.M.; Burke, A.C.; Spence, J.R.; Wellik, D.M. Hox5 genes regulate the Wnt2/2b-Bmp4-signaling axis during lung development. Cell Rep., 2015, 12(6), 903-912.
[http://dx.doi.org/10.1016/j.celrep.2015.07.020] [PMID: 26235626]
[18]
Ptaschinski, C.; Hrycaj, S.M.; Schaller, M.A.; Wellik, D.M.; Lukacs, N.W. Hox5 paralogous genes modulate Th2 cell function during chronic allergic inflammation via regulation of Gata3. J. Immunol., 2017, 199(2), 501-509.
[http://dx.doi.org/10.4049/jimmunol.1601826] [PMID: 28576978]
[19]
Schwager, E.E.; Sharma, P.P.; Clarke, T.; Leite, D.J.; Wierschin, T.; Pechmann, M.; Akiyama-Oda, Y.; Esposito, L.; Bechsgaard, J.; Bilde, T.; Buffry, A.D.; Chao, H.; Dinh, H.; Doddapaneni, H.; Dugan, S.; Eibner, C.; Extavour, C.G.; Funch, P.; Garb, J.; Gonzalez, L.B.; Gonzalez, V.L.; Griffiths-Jones, S.; Han, Y.; Hayashi, C.; Hilbrant, M.; Hughes, D.S.T.; Janssen, R.; Lee, S.L.; Maeso, I.; Murali, S.C.; Muzny, D.M.; Nunes da Fonseca, R.; Paese, C.L.B.; Qu, J.; Ronshaugen, M.; Schomburg, C.; Schönauer, A.; Stollewerk, A.; Torres-Oliva, M.; Turetzek, N.; Vanthournout, B.; Werren, J.H.; Wolff, C.; Worley, K.C.; Bucher, G.; Gibbs, R.A.; Coddington, J.; Oda, H.; Stanke, M.; Ayoub, N.A.; Prpic, N.M.; Flot, J.F.; Posnien, N.; Richards, S.; McGregor, A.P. The house spider genome reveals an ancient whole-genome duplication during arachnid evolution. BMC Biol., 2017, 15(1), 62.
[http://dx.doi.org/10.1186/s12915-017-0399-x] [PMID: 28756775]
[20]
Sharma, P.P.; Schwager, E.E.; Extavour, C.G.; Wheeler, W.C. Hox gene duplications correlate with posterior heteronomy in scorpions. Proc. R. Soc. Lond. B Biol. Sci., 2014.
[http://dx.doi.org/10.1098/rspb.2014.0661]
[21]
Turetzek, N.; Pechmann, M.; Schomburg, C.; Schneider, J.; Prpic, N.M. Neofunctionalization of a duplicate dachshund gene underlies the evolution of a novel leg segment in arachnids. Mol. Biol. Evol., 2016, 33(1), 109-121.
[http://dx.doi.org/10.1093/molbev/msv200] [PMID: 26443673]
[22]
Barthélémy, R.M.; Grino, M.; Pontarotti, P.; Casanova, J.P.; Faure, E. The differential expression of ribosomal 18S RNA paralog genes from the chaetognath Spadella cephaloptera. Cell. Mol. Biol. Lett., 2007, 12(4), 573-583.
[http://dx.doi.org/10.2478/s11658-007-0026-x] [PMID: 17588220]
[23]
Barthélémy, R.M.; Grino, M.; Pontarotti, P.; Casanova, J.P.; Faure, E. A possible relationship between the phylogenetic branch lengths and the chaetognath rRNA paralog gene functionalities: Ubiquitous, tissue-specific or pseudogenes. In: Evolutionary Biology from Concept to Application; Springer: Berlin, Heidelberg, 2008; pp. 155-164.
[http://dx.doi.org/10.1007/978-3-540-78993-2_9]
[24]
Elbarbary, R.A.; Lucas, B.A.; Maquat, L.E. Retrotransposons as regulators of gene expression. Science, 2016, 351(6274), 7247.
[http://dx.doi.org/10.1126/science.aac7247] [PMID: 26912865]
[25]
Chuong, E.B.; Elde, N.C.; Feschotte, C. Regulatory activities of transposable elements: From conflicts to benefits. Nat. Rev. Genet., 2017, 18(2), 71-86.
[http://dx.doi.org/10.1038/nrg.2016.139] [PMID: 27867194]
[26]
Trizzino, M.; Kapusta, A.; Brown, C.D. Transposable elements generate regulatory novelty in a tissue-specific fashion. BMC Genomics, 2018, 19(1), 468.
[http://dx.doi.org/10.1186/s12864-018-4850-3] [PMID: 29914366]
[27]
Wang, K.; Huang, G.; Zhu, Y. Transposable elements play an important role during cotton genome evolution and fiber cell development. Sci. China Life Sci., 2016, 59(2), 112-121.
[http://dx.doi.org/10.1007/s11427-015-4928-y] [PMID: 26687725]
[28]
Macías, F.; Afonso-Lehmann, R.; López, M.C.; Gómez, I.; Thomas, M.C. Biology of Trypanosoma cruzi retrotransposons: From an enzymatic to a structural point of view. Curr. Genomics, 2018, 19(2), 110-118.
[http://dx.doi.org/10.2174/1389202918666170815150738] [PMID: 29491739]
[29]
González, J.; Petrov, D.A. The adaptive role of transposable elements in the Drosophila genome. Gene, 2009, 448(2), 124-133.
[http://dx.doi.org/10.1016/j.gene.2009.06.008] [PMID: 19555747]
[30]
Boutanaev, A.M.; Osbourn, A.E. Multigenome analysis implicates miniature inverted-repeat transposable elements (MITEs) in metabolic diversification in eudicots. Proc. Natl. Acad. Sci. USA, 2018, 115(28), E6650-E6658.
[http://dx.doi.org/10.1073/pnas.1721318115] [PMID: 29941591]
[31]
Vaschetto, L.M. Miniature Inverted-repeat Transposable Elements (MITEs) and their effects on the regulation of major genes in cereal grass genomes. Mol. Breed., 2016, 36(3), 1-4.
[http://dx.doi.org/10.1007/s11032-016-0440-8]
[32]
Feschotte, C.; Swamy, L.; Wessler, S.R. Genome-wide analysis of mariner-like transposable elements in rice reveals complex relationships with stowaway miniature inverted repeat transposable elements (MITEs). Genetics, 2003, 163(2), 747-758.
[PMID: 12618411]
[33]
Yang, G.; Nagel, D.H.; Feschotte, C.; Hancock, C.N.; Wessler, S.R. Tuned for transposition: Molecular determinants underlying the hyperactivity of a stowaway MITE. Science, 2009, 325(5946), 1391-1394.
[http://dx.doi.org/10.1126/science.1175688] [PMID: 19745152]
[34]
Zeng, L.; Pederson, S.M.; Cao, D.; Qu, Z.; Hu, Z.; Adelson, D.L.; Wei, C. Genome-wide analysis of the association of transposable elements with gene regulation suggests that alu elements have the largest overall regulatory impact. J. Comput. Biol., 2018, 25(6), 551-562.
[http://dx.doi.org/10.1089/cmb.2017.0228] [PMID: 29708779]
[35]
Scarpato, M.; Angelini, C.; Cocca, E.; Pallotta, M.M.; Morescalchi, M.A.; Capriglione, T. Short interspersed DNA elements and miRNAs: A novel hidden gene regulation layer in zebrafish? Chromosome Res., 2015, 23(3), 533-544.
[http://dx.doi.org/10.1007/s10577-015-9484-6] [PMID: 26363800]
[36]
Luchetti, A.; Plazzi, F.; Mantovani, B. Evolution of two short interspersed elements in callorhinchus milii (Chondrichthyes, Holocephali) and related elements in sharks and the coelacanth. Genome Biol. Evol., 2017, 9(6)
[http://dx.doi.org/10.1093/gbe/evx094] [PMID: 28505260]
[37]
Kojima, K.K.; Fujiwara, H. Cross-genome screening of novel sequence-specific non-LTR retrotransposons: Various multicopy RNA genes and microsatellites are selected as targets. Mol. Biol. Evol., 2004, 21(2), 207-217.
[http://dx.doi.org/10.1093/molbev/msg235] [PMID: 12949131]
[38]
Kojima, K.K.; Fujiwara, H. Long-term inheritance of the 28S rDNA-specific retrotransposon R2. Mol. Biol. Evol., 2005, 22(11), 2157-2165.
[http://dx.doi.org/10.1093/molbev/msi210] [PMID: 16014872]
[39]
Gladyshev, E.A.; Arkhipova, I.R. Rotifer rDNA-specific R9 retrotransposable elements generate an exceptionally long target site duplication upon insertion. Gene, 2009, 448(2), 145-150.
[http://dx.doi.org/10.1016/j.gene.2009.08.016] [PMID: 19744548]
[40]
Roiha, H.; Miller, J.R.; Woods, L.C.; Glover, D.M. Arrangements and rearrangements of sequences flanking the two types of rDNA insertion in D. melanogaster. Nature, 1981, 290(5809), 749-753.
[http://dx.doi.org/10.1038/290749a0] [PMID: 6783966]
[41]
Fujiwara, H.; Ogura, T.; Takada, N.; Miyajima, N.; Ishikawa, H.; Maekawa, H. Introns and their flanking sequences of Bombyx mori rDNA. Nucleic Acids Res., 1984, 12(17), 6861-6869.
[http://dx.doi.org/10.1093/nar/12.17.6861] [PMID: 6091041]
[42]
Luchetti, A.; Mingazzini, V.; Mantovani, B. 28S junctions and chimeric elements of the rDNA targeting non-LTR retrotransposon R2 in crustacean living fossils (Branchiopoda, Notostraca). Genomics, 2012, 100(1), 51-56.
[http://dx.doi.org/10.1016/j.ygeno.2012.04.005] [PMID: 22564473]
[43]
Kapitonov, V.V.; Jurka, J. R2 non-LTR retrotransposons in the bird genome. Repbase Rep., 2009, 9, 1329.
[44]
Eickbush, D.G.; Eickbush, T.H. R2 retrotransposons encode a self-cleaving ribozyme for processing from an rRNA cotranscript. Mol. Cell. Biol., 2010, 30(13), 3142-3150.
[http://dx.doi.org/10.1128/MCB.00300-10] [PMID: 20421411]
[45]
Eickbush, D.G.; Ye, J.; Zhang, X.; Burke, W.D.; Eickbush, T.H. Epigenetic regulation of retrotransposons within the nucleolus of Drosophila. Mol. Cell. Biol., 2008, 28(20), 6452-6461.
[http://dx.doi.org/10.1128/MCB.01015-08] [PMID: 18678644]
[46]
Eickbush, T.H.; Eickbush, D.G. Integration, regulation, and long-term stability of R2 retrotransposons. Microbiol. Spectr., 2015, 3(2), MDNA3-0011-2014.
[47]
Ay, F.; Bunnik, E.M.; Varoquaux, N.; Bol, S.M.; Prudhomme, J.; Vert, J-P.; Noble, W.S.; Le Roch, K.G. Three-dimensional modeling of the P. falciparum genome during the erythrocytic cycle reveals a strong connection between genome architecture and gene expression. Genome Res., 2014, 24(6), 974-988.
[http://dx.doi.org/10.1101/gr.169417.113] [PMID: 24671853]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy