Transposons in Eukaryotes (Part B): Genomic Consequences of Transposition


The present contribution focuses on the known consequences of active transposition for the individual (∼100 human disease‐causing retrotransposon insertions have been recorded) and subsequently on the effects of TEs on populations over time (evolution), particularly on the arguments on TEs as ‘selfish DNA’ versus the ‘pacemakers of evolution’ inference (among them the effects of Helitrons in maize, the acclaimed V(D)J/RAG1 transposon hypothesis and also putative cases of transposon domestications in the history of the angiosperms as well as plant and animal breeding). Basic problems involved in the TE domestication hypothesis are elucidated (chicken‐or‐egg dilemma, key point: ‘Is the host gene really derived from the TE, or did the TE capture the host gene?’). Moreover, a proposition for a synthesis of the different views is offered on the basis of the hierarchy of gene redundancies (the variable part) and the importance of loss‐of‐function mutations for regressive evolution, the origin of ecotypes and cultivated plants and animals. Last not least, open problems of TE research are addressed.

Key Concepts

  • TEs are causes of heritable and somatic diseases in humans and are also involved in the aging of mammalian tissues.
  • TEs display an immense detrimental potential by mutagenesis in individuals and populations.
  • The celebrated RAG1 transposon hypothesis is unproven, several scientific alternatives are available.
  • As there are no immediate phenotypic benefits of TE integrations in almost all cases described, there cannot be immediate selective advantages for the organisms harbouring them (evolution is not anticipatory).
  • TEs can spread even if they constitute a slight energetic burden for their hosts.
  • The enormous genetic differences in inbred maize lines (up to 75% noncolinearity mostly due to TEs; hundreds of complete genes and 10 000 gene fragments not shared, more than 1 000 000 SNPs, 30 000 indel polymorphisms) do not display correspondingly different phenotypes.
  • The C‐value paradox (even found in closely related species) cannot be explained by functional genetic advantages of the hosts thus affected.
  • The chicken‐or‐egg dilemma (which came first: the host gene or the more or less similar sequence in the TE?) raises doubts for the majority of the putative TE domestications supposed to be key events in evolution and breeding research.
  • The hypothesis that TEs belong to the most important factors in the origin of species in general and of higher systematic categories (baupläne) in particular is most probably false.
  • Nevertheless, losses‐of‐function mutations are important in regressive evolution, the origin of ecotypes, cultivated plants and animal husbandry. Gene inactivations by TEs have been assumed and in part already detected to be of particular relevance for these areas of research.
  • The documented segment of site‐specific positive TE (like LINE1 and Alu‐) functions in humans (and other organisms) could either be of primary origin (the deleterious effects due to new insertions thus being secondary) or in part belong to the category of substitutions of earlier gene functions perhaps comparable to the syncytin genes.

Keywords: transposable elements; retrotransposons; DNA transposons; selfish DNA; V(D)J/RAG1 transposon hypothesis; hierarchy of gene redundancies; neo‐Darwinism; regressive evolution; origin of ecotypes; origin of cultivated plants and animals

Figure 1. The first homeotic plant gene to be cloned and characterised was mutated by a TE which helped identify it. (a) A transposon was shown to be the cause of the homeotic deficiensglobifera mutant of Antirrhinum majus (the mutant is depicted below, the wild‐type flower form with active transposons revealed by variegation of colour is shown above) illustrating inter alia the strongly negative effects TEs can have on individual plant and flower development: the male sterile recessive deficiensglobifera mutant displays a second row of sepals in lieu of petals and fused carpals instead of stamens (wild‐type flower length ∼3 cm, mutant ∼1.5 cm). (b) The original def mutant used had already exhibited somatic and germinal instability often typical for active TEs, later identified to be due to the insertion of Tam7 (Transposon Antirrhinum majus 7; length 7 kb) providing the final proof for the identification of the corresponding defA‐1 gene: insertion was correlated with the mutant phenotype, reversion to wild type with the absence of the TE. In the F1 consisting of 45 000 plants between the def mutant and a line with wild‐type flower form carrying the active 7‐kb Tam1 element (sequenced and characterised before), 17 newly TE‐tagged candidates were isolated, several with different degrees of anomalies and dysmorphologies and some with the same extreme mutant phenotype as shown in the figure (for the details, see Sommer et al., ). Photos courtesy of Maret Kalda, Max Planck Institute for Plant Breeding Research.
Figure 2. Transposon compositions in diverse species illustrating the strongly different percentages of various TE classes and subclasses [LTR and non‐LTR retrotransposons as well as terminal inverted repeat (TIR) DNA TEs and the essentially distinct subclass of the non‐TIR rolling circle Helitron DNA transposons discovered in 2001] occupying various organisms (percentages according to Huang et al., , as well as; 2015; there further references). The TE ‘pacemaker hypothesis’ has to assume that not only different organisms have been created by essentially distinct transposons in divergent percentages and/or combinations of them but also that this could be true even for closely related species (e.g. in species of Lilium or bats; see, please, the text). However, apart from teratological features due to TE‐elicited losses of gene functions or ectopic gene expression usually disturbing/disrupting normal plant or animal development, there is no stringent (if any) correlation between intra‐ and interspecific genetic variation by TEs, SNPs, Indels and in several inbred maize lines even the presence/absence of hundreds of complete genes, on the one hand, and the morphological characters defining species, genera and higher systematic categories on the other. Figure 2 was prepared by computer graphics specialist Roland Slowig, Dietzenbach, Germany, in cooperation with Dr Wolf‐Ekkehard Loennig (2015). Photographs reproduced with permission from


Arendsee ZW , Li L and Wurtele ES (2014) Coming of age: orphan genes in plants. Trends in Plant Science 19 (11): 698–708.

Barbaglia AM , Klusman KM , Higgins J , et al. (2012) Gene capture by Helitron transposons reshuffles the transcriptome of maize. Genetics 190 (3): 965–975.

Becker H‐A and Lönnig W‐E (2001) Transposons: eukaryotic. In: eLS. John Wiley & Sons, Ltd. DOI: doi:10.1038/npg.els.0003876.

Bedada G (2014) Genomic Divergence in Differentially Adapted Wild and Domesticated Barley. PhD thesis.

Behe MJ (2006) Darwin's Black Box. The Biochemical Challenge to Evolution (2nd Edition with Answers to Critics). New York: The Free Press.

Behe MJ (2007) The Edge of Evolution. Testing the Limits of Darwinism. New York: The Free Press.

Bellone RR , Holl H , Setaluri V , et al. (2013) Evidence for a retroviral insertion in TRPM1 as the cause of congenital stationary night blindness and leopard complex spotting in the horse. PLoS One 8 (10): e78280.

Bergman CM and Bensasson D (2007) Recent LTR retrotransposition insertion contrasts with waves of non‐LTR insertion since speciation in Drosophila melanogaster . Proceedings of the National Academy of Sciences of the United States of America 104: 11340–11345.

Burt A and Trivers R (2006) Genes in Conflict. The Biology of Selfish Genetic Elements. Cambridge, MA: Belknap Press of Harvard University Press.

Chen S , Zhang YE and Long M (2010) New genes in Drosophila quickly become essential. Science 330 (6011): 1682–1685.

De Cecco M , Criscione SW , Peckham EJ , et al. (2013) Genomes of replicatively senescent cells undergo global epigenetic changes leading to gene silencing and activation of transposable elements. Aging Cell 12 (2): 247–256.

Dietrich FS , Voegeli S , Kuo S and Philippsen P (2013) Genomes of Ashbya fungi isolated from insects reveal four mating‐type loci, numerous translocations, lack of transposons, and distinct gene duplications. G3: Genes|Genomes|Genetics 3 (8): 1225–1239. DOI: 10.1534/g3.112.002881.

Doolittle WF and Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284 (5757): 601–603.

Dreyfus DH (2009) Paleo‐immunology: evidence consistent with insertion of a primordial herpes virus‐like element in the origins of acquired immunity. PLoS One 4 (6): e5778.

Erwin DH and Valentine JW (2013) The Cambrian Explosion: The Reconstruction of Animal Biodiversity. Greenwood Village, CO.: Roberts & Co.

Falchi R , Vendramin E , Zanon L , et al. (2013) Three distinct mutational mechanisms acting on a single gene underpin the origin of yellow flesh in peach. The Plant Journal 76 (2): 175–187.

Feyereisen R , Dermauw W and Van Leeuwen T (2015) Genotype to phenotype, the molecular and physiological dimensions of resistance in arthropods. Pesticide Biochemistry and Physiology. DOI: 10.1016/j.pestbp.2015.01.004.

Ffrench‐Constant R , Daborn P and Feyereisen R (2006) Resistance and the jumping gene. Bioessays 28 (1): 6–8.

Fischer MG and Suttle CA (2011) A virophage at the origin of large DNA transposons. Science 332 (6026): 231–234.

Giovannoni SJ , Tripp HJ , Givan S , et al. (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309 (5738): 1242–1245.

Goldschmidt RB (1948) Ecotype, ecospecies, and macroevolution. Experientia 4 (12): 465–472.

Han MJ , Shen YH , Xu MS , et al. (2013) Identification and evolution of the silkworm helitrons and their contribution to transcripts. DNA Research 20 (5): 471–484.

Hellen EH and Brookfield JF (2013) Alu elements in primates are preferentially lost from areas of high GC content. PeerJ 1: e78.

Hemmrich G , Miller DJ and Bosch TCG (2007) The evolution of immunity: a low‐life perspective. Trends in Immunology 26 (10): 449–454.

Hickey DA (1982) Selfish DNA: a sexually‐transmitted nuclear parasite. Genetics 101 (3–4): 519–531.

Huang CR , Burns KH and Boeke JD (2012) Active transposition in genomes. Annual Review of Genetics 46: 651–675.

Joly‐Lopez Z , Forczek E , Hoen DR , Juretic N and Bureau TE (2012) A gene family derived from transposable elements during early angiosperm evolution has reproductive fitness benefits in Arabidopsis thaliana. PLoS Genetics 8 (9): e1002931.

Jones RB , Song H , Xu Y , et al. (2013) LINE‐1 retrotransposable element DNA accumulates in HIV‐1‐infected cells. Journal of Virology 87 (24): 13307–13320.

Kaelin CB and Barsh GS (2012) Molecular genetics of coat colour, texture and length in the dog. In: Ostrander E and Ruvinski A (eds) The Genetics of the Dog, pp. 57–82. Oxforshire, UK: CABI.

Kapitonov VV and Jurka J (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biology 3 (6): e181.

Kennedy J , Flemer B , Jackson SA , et al. (2010) Marine metagenomics: new tools for the study and exploitation of marine microbial metabolism. Marine Drugs 8 (3): 608–628.

Kozeretska IA , Demydov SV and Ostapchenko LI (2011) Mobile genetic elements and cancer. From mutations to gene therapy. Experimental Oncology 33 (4): 198–205.

Krupovic M and Koonin EV (2015) Polintons: a hotbed of eukaryotic virus, transposon and plasmid evolution. Nature Reviews Microbiology 13 (2): 105–115.

Kunze R , Saedler H and Lönnig W‐E (1997) Plant transposable elements. In: Callow JA (ed) Advances in Botanical Research, vol. 27, pp. 331–470. San Diego: Academic Press.

Lai J , Li R , Xu X , et al. (2010) Genome‐wide patterns of genetic variation among elite maize inbred lines. Nature Genetics 42 (11): 1027–1030.

Lee SI and Kim NS (2014) Transposable elements and genome size variations in plants. Genomics & Informatics 12 (3): 87–97.

Lee SI , Park KC , Son JH , et al. (2013) Isolation and characterization of novel Ty1‐copia‐like retrotransposons from lily. Genome 56 (9): 495–503.

Leeton PRJ and Smyth DR (1993) An abundant LINE‐like element amplified in the genome of Lilium speciosum . Molecular & General Genetics 237: 97–104.

Light S , Basile W and Elofsson A (2014) Orphans and new gene origination, a structural and evolutionary perspective. Current Opinion in Structural Biology 26: 73–83.

Llaca V , Campbell M and Deschamps S (2011) Genome diversity in maize. Journal of Botany 2011: 1–10.

Lönnig WE (1982) Dominance, overdominance and epistasis in Pisum sativum L. Theoretical and Applied Genetics 63 (3): 255–264.

Lönnig W‐E (1986/1993) Artbegriff, Evolution und Schöpfung, –Köln (1. und 3. Auflage). Naturwissenschaftlicher Verlag.

Lönnig W‐E (2001) Natural selection. In: Craighead WE and Nemeroff CB (eds) The Corsini Encyclopedia of Psychology and Behavioral Sciences, Third edn, vol. 3, pp. 1008–1016. New York: John Wiley and Sons.

Lönnig W‐E (2005) Mutation breeding, evolution, and the law of recurrent variation. Recent Developments in Genetics and Breeding 2: 45–70.

Lönnig W‐E (2006) Mutations: the law of recurrent variation. In: Teixeira da Silva JA (ed) Floriculture, Ornamental and Plant Biotechnology, vol. I, pp. 601–607.

Lönnig W‐E (2012) Die Evolution der karnivoren Pflanzen: Was die Selektion nicht leisten kann ‐ das Beispiel Utricularia (Wasserschlauch) 3. Auflage. Münster: Verlagshaus Monsenstein und Vannerdat OHG.

Lönnig W‐E (2014) Unser Haushund: Eine Spitzmaus im Wolfspelz? Oder beweisen die Hunderassen, dass der Mernsch von Bakterien abstammt? Münster: Verlagshaus Monsenstein und Vannerdat OHG.

Lönnig WE and Saedler H (1997) Plant transposons: contributors to evolution? Gene 205 (1–2): 245–253.

Lönnig WE and Saedler H (2002) Chromosome rearrangements and transposable elements. Annual Review of Genetics 36: 389–410.

Mateo L , Ullastres A and Gonzalez J (2014) A transposable element insertion confers xenobiotic resistance in Drosophila. PLoS Genetics 10 (8): e1004560.

Maxwell PH (2014) Consequences of ongoing retrotransposition in mammalian genomes. Advances in Genomics and Genetics 4: 129–142.

McClintock B (1987) The Discovery and Characterization of Transposable Elements. The Collected Papers of Barbara McClintock. New York: Garland Publishing. DOI: 10.1016/0092-8674(88)90481-3.

McGaugh SE , Gross JB , Aken B , et al. (2014) The cavefish genome reveals candidate genes for eye loss. Nature communications 5: 5307. DOI: 10.1038/ncomms6307.

Meyer RS and Purugganan MD (2013) Evolution of crop species: genetics of domestication and diversification. Nature Reviews Genetics 14 (12): 840–852.

Moreira D and Lopez‐Garcia P (2009) Ten reasons to exclude viruses from the tree of life. Nature Reviews Microbiology 7 (4): 306–311.

Morgante M , Brunner S , Pea G , et al. (2005) Gene duplication and exon shuffling by helitron‐like transposons generate intraspecies diversity in maize. Nature Genetics 37 (9): 997–1002.

Naito K , Monden Y , Yasuda K , Saiato H and Okumoto Y (2014) mPing: the bursting transposon. Breeding Science 64 (2): 109–114.

Nei M (2013) Mutation‐Driven Evolution. Oxford: Oxford University Press.

Neuveglise C , Feldmann H , Bon E , Gaillardin C and Casaregola S (2002) Genomic evolution of the long terminal repeat retrotransposons in hemiascomycetous yeasts. Genome Research 14 (6): 930–943. DOI: 10.1101/gr.219202.

Oliver KR , McComb JA and Greene WK (2013) Transposable elements: powerful contributors to angiosperm evolution and diversity. Genome Biology and Evolution 5 (10): 1886–1901.

Orgel LE and Crick FH (1980) Selfish DNA: the ultimate parasite. Nature 284 (5757): 604–607.

Parker HG , VonHoldt BM , Quignon P , et al. (2009) An expressed fgf4 retrogene is associated with breed‐defining chondrodysplasia in domestic dogs. Science 325 (5943): 995–998.

Parker J , Tsagkogeorga G , Cotton JA , et al. (2013) Genome‐wide signatures of convergent evolution in echolocating mammals. Nature 502 (7470): 228–231.

Pereira V (2004) Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biology 5 (10): R79.

Rands CM , Meader S , Ponting CP and Lunter G (2014) 8.2% of the human genome is constrained: variation in rates of turnover across functional element classes in the human lineage. PLoS Genetics 10 (7): e1004525.

Redelsperger F , Cornelis G , Vernochet C , et al. (2014) Capture of syncytin‐Mar1, a fusogenic endogenous retroviral envelope gene involved in placentation in the Rodentia squirrel‐related clade. Journal of Virology 88 (14): 7915–7928.

ReMine WJ (1993) The Biotic Message. Saint Paul, MN: St. Paul Science.

Rocap G , Larimer FW , Lamerdin J , et al. (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424 (6952): 1042–1047.

Samson M , Libert F , Doranz BJ , et al. (1996) Resistance to HIV‐1 infection in caucasian individuals bearing mutant alleles of the CCR‐5 chemokine receptor gene. Nature 382 (6593): 722–725.

Schubert C (2015) Co‐opted viral gene in ancient mammals fuses placental cells. Biology of Reproduction 92 (1): 4.

Shapiro JA and von Sternberg R (2005) Why repetitive DNA is essential to genome function. Biological Reviews of the Cambridge Philosophical Society 80 (2): 227–250.

Sommer H , Beltran JP , Huiser P , et al. (1990) Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO Journal 9 (3): 605–613.

Starlinger P (1984) Transposition: Ein neuer Mechanismus zur Evolution. Rheinisch‐Westfälische Akademie der Wissenschaften Vorträge N 328: 7–33.

Starlinger P (1993) What do we still need to know about transposable element Ac? Gene 135 (1–2): 251–255.

Tang Z , Zhang HH , Huang K , et al. (2015) Repeated horizontal transfers of four DNA transposons in invertebrates and bats. Mobile DNA 6 (1): 3. DOI: 10.1186/s13100-014-0033-1.eCollection2015.

Tautz D , Neme R and Domazet‐Lošo T (2013) Evolutionary origin of orphan genes. In: eLS. John Wiley & Sons, Ltd. DOI: 10.1002/9780470015902.a0024601.

Thomas J , Phillips CD , Baker RJ and Pritham EJ (2014) Rolling‐circle transposons catalyze genomic innovation in a mammalian lineage. Genome Biology and Evolution 6 (10): 2595–2610.

Vaughn MW , Tanurd Ic M , Lippman Z , et al. (2007) Epigenetic natural variation in Arabidopsis thaliana . PLoS Biology 5 (7): e174.

Vendramin E , Pea G , Dondini L , et al. (2014) A unique mutation in a MYB gene cosegregates with the nectarine phenotype in peach. PLoS One 9 (3): e90574.

Vitte C , Fustier MA , Alix K and Tenaillon MI (2014) The bright side of transposons in crop evolution. Briefings in Functional Genomics 13 (4): 276–295.

Volff JN (2006) Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28 (9): 913–922.

Walters‐Conte KB , Johnson DL , Allard MW and Pecon‐Slattery J (2011) Carnivore‐specific SINEs (Can‐SINEs): distribution, evolution, and genomic impact. Journal of Heredity 102 (Suppl 1): S2–S10.

Wang Q and Dooner HK (2006) Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proceedings of the National Academy of Sciences of the United States of America 103 (47): 17644–17649.

Weill M , Lutfalla G , Mogensen K , et al. (2003) Comparative genomics: insecticide resistance in mosquito vectors. Nature 423 (6936): 136–137.

Wells J (2011) The Myth of Junk DNA. Seattle: Discovery Institute Press.

Werren JH (2011) Selfish genetic elements, genetic conflict, and evolutionary innovation. Proceedings of the National Academy of Sciences of the United States of America 108 (Suppl 2): 10863–10870.

Xiong W , He L , Lai J , Dooner HK and Du C (2014) HelitronScanner uncovers a large overlooked cache of Helitron transposons in many plant genomes. Proceedings of the National Academy of Sciences of the United States of America 111 (28): 10263–10268.

Further Reading

Belancio VP , Blask DE , Deiniger P , Hill SM and Jazwinski SM (2015) The aging clock and circadian control of metabolism and genome stability. Frontiers in Genetics 5: 455. DOI: 10.3389/fgene.2014.00455 eCollection 2014.

Roy NS , Choi J‐Y , Lee S‐I and Kim N‐S (2015) Marker utility of transposable elements for plant genetics, breeding and ecology: a review. Genes and Genomics 37 (2): 141–151.

Stapley J , Santure AW and Dennis SR (2015) Transposable elements as agents of rapid adaptation may explain the genetic paradox of invasive species. Molecular Ecology. DOI: 10.1111/mec.13013089. [Epub ahead of print].

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Lönnig, Wolf‐Ekkehard(Aug 2015) Transposons in Eukaryotes (Part B): Genomic Consequences of Transposition. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0026265]