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

Abstract

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 BioNumbers.hms.Harvard.edu; 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 Shutterstock.com.
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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.

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