Genome Size Evolution: Small Transposons with Large Consequences
2019; Elsevier BV; Volume: 29; Issue: 7 Linguagem: Inglês
10.1016/j.cub.2019.02.032
ISSN1879-0445
Autores Tópico(s)Legume Nitrogen Fixing Symbiosis
ResumoTransposable elements (TEs) heavily influence genome size variation between organisms. A new study on larvacean tunicates now shows that even non-autonomous TEs — small TEs that parasitize the enzymatic machinery of large, autonomous TEs — can have a large impact on genome size. Transposable elements (TEs) heavily influence genome size variation between organisms. A new study on larvacean tunicates now shows that even non-autonomous TEs — small TEs that parasitize the enzymatic machinery of large, autonomous TEs — can have a large impact on genome size. Genome sizes vary massively across the tree of life. Among animals, extreme genome sizes range from ∼0.02 Gb in a nematode to ∼130 Gb in a lungfish [1Gregory T.R. Animal Genome Size Database.http://www.genomesize.comDate: 2017Google Scholar, 2Doležel J. Bartoš J. Voglmayr H. Greilhuber J. Nuclear DNA content and genome size of trout and human.Cytometry A. 2003; 51A: 127-128Google Scholar]. This >6,600-fold genome size variance in animals alone has been puzzling researchers for decades. Genome size does not simply reflect the number of genes or organismal complexity, but instead strongly correlates with the abundance of transposable elements (TEs) in animals and other eukaryotes [3Elliott T.A. Gregory T.R. What's in a genome? The C-value enigma and the evolution of eukaryotic genome content.Philos. Trans. R. Soc. B. 2015; 370: 20140331Crossref PubMed Scopus (143) Google Scholar]. How much of genome size variation between organisms results from adaptive versus non-adaptive processes has been debated elsewhere [4Petrov D.A. Evolution of genome size: new approaches to an old problem.Trends Genet. 2001; 17: 23-28Abstract Full Text Full Text PDF PubMed Scopus (332) Google Scholar, 5Cavalier-Smith T. Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion.Ann. Bot. 2005; 95: 147-175Crossref PubMed Scopus (280) Google Scholar], but in the light of population genetics, at least a large aspect of genome size variation can be attributed to non-adaptive processes [6Lynch M. Conery J.S. The origins of genome complexity.Science. 2003; 302: 1401-1404Crossref PubMed Scopus (1160) Google Scholar, 7Lynch M. The frailty of adaptive hypotheses for the origins of organismal complexity.Proc. Natl. Acad. Sci. USA. 2007; 104: 8597-8604Crossref PubMed Scopus (505) Google Scholar]. Just like their organismal hosts, TEs come in many shapes and flavors [8Feschotte C. Jiang N. Wessler S.R. Plant transposable elements: where genetics meets genomics.Nat. Rev. Genet. 2002; 3: 329Crossref PubMed Scopus (735) Google Scholar]. TEs are selfish genetic elements that propagate via a cut-and-paste (DNA transposons) or copy-and-paste mechanism (retrotransposons). Transposition involves one or several proteins encoded by the TEs themselves (Figure 1) — at least a transposase protein in DNA transposons and a reverse transcriptase protein in retrotransposons. However, some TEs lack their own coding capacity — they are ‘non-autonomous’ and instead rely on proteins encoded by other (‘autonomous’) TEs. Considering that TEs propagate as parasites of their hosts, non-autonomous TEs in principle are ‘parasites of parasites’. They exist in all major groups of TEs (Figure 1), can be of diminutive size ( 32-Gb genomes of salamanders are heavily enriched in autonomous LTR retrotransposons which are each 6–16 kb in size [11Nowoshilow S. Schloissnig S. Fei J.-F. Dahl A. Pang A.W.C. Pippel M. Winkler S. Hastie A.R. Young G. Roscito J.G. et al.The axolotl genome and the evolution of key tissue formation regulators.Nature. 2018; 554: 50Crossref PubMed Scopus (280) Google Scholar].Figure 2Transposable elements are drivers of genome size evolution.Show full caption(A) Direct genome expansion through retrotransposition of autonomous TEs. The example shows a long interspersed element (LINE). (B) Indirect genome expansion through retrotransposition of non-autonomous TEs after hijacking the enzymatic machinery of autonomous TEs. The example shows a short interspersed element (SINE). (C) Schematic illustration of genome expansion via a SINE, which might ultimately lead to the interruption of the mobilizing LINE. Dashed lines indicate SINE insertion events in the expanded genome (below) relative to the pre-expansion situation (above). RNP, ribonucleoprotein. LINE/SINE poly(A) tails are not shown for simplicity.View Large Image Figure ViewerDownload Hi-res image Download (PPT) (A) Direct genome expansion through retrotransposition of autonomous TEs. The example shows a long interspersed element (LINE). (B) Indirect genome expansion through retrotransposition of non-autonomous TEs after hijacking the enzymatic machinery of autonomous TEs. The example shows a short interspersed element (SINE). (C) Schematic illustration of genome expansion via a SINE, which might ultimately lead to the interruption of the mobilizing LINE. Dashed lines indicate SINE insertion events in the expanded genome (below) relative to the pre-expansion situation (above). RNP, ribonucleoprotein. LINE/SINE poly(A) tails are not shown for simplicity. In a new study in this issue of Current Biology, Naville et al. [12Naville M. Henriet S. Warren I. Sumic S. Reeve M. Volff J.-N. Chourrout D. Massive changes of genome size driven by expansions of non-autonomous transposable elements.Curr. Biol. 2019; 29: 1161-1168Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar] report an alternative route to genome size expansion — one through small, non-autonomous TEs (Figure 2B,C). The authors studied larvacean tunicates, a group of planktonic, tadpole-resembling invertebrates that is very closely related to vertebrates [13Delsuc F. Brinkmann H. Chourrout D. Philippe H. Tunicates and not cephalochordates are the closest living relatives of vertebrates.Nature. 2006; 439: 965Crossref PubMed Scopus (1210) Google Scholar]. These tunicates have genome sizes of 72–874 Mb that may appear rather small compared to many vertebrates, but this notably corresponds to 12-fold variation in genome size across relatively short evolutionary timescales. Naville et al. [12Naville M. Henriet S. Warren I. Sumic S. Reeve M. Volff J.-N. Chourrout D. Massive changes of genome size driven by expansions of non-autonomous transposable elements.Curr. Biol. 2019; 29: 1161-1168Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar] analyzed in detail the genomes of seven larvacean tunicates for repetitive elements using various de novo prediction and homology-based methods. This approach should identify both known as well as novel families of TEs in each sampled genome. The authors further estimated the relative age of TE accumulation for each genome to decide whether the genome size differences are due to TE expansion in larger genomes or instead a lack of TE accumulation in smaller genomes. The data suggest that larger species have larger genomes, which in turn have larger densities of TEs resulting from recent bursts of (retro)transposition. Interestingly, while Naville et al. [12Naville M. Henriet S. Warren I. Sumic S. Reeve M. Volff J.-N. Chourrout D. Massive changes of genome size driven by expansions of non-autonomous transposable elements.Curr. Biol. 2019; 29: 1161-1168Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar] detected low numbers of autonomous TEs in all genomes, the authors found that a diversity of non-autonomous TE families makes up large genome proportions. SINEs alone account for 83% of the genome size variation. All of the identified non-autonomous TE families appear to be species-specific, i.e., they are each present in only one of the sampled genomes. This further indicates that the genome size differences result from differential TE accumulation on relatively recent evolutionary timescales. The authors note, however, that it is difficult to establish which autonomous TE families mobilized their non-autonomous parasites due to little shared sequence homology between them (cf. Figure 1). The results of Naville et al. [12Naville M. Henriet S. Warren I. Sumic S. Reeve M. Volff J.-N. Chourrout D. Massive changes of genome size driven by expansions of non-autonomous transposable elements.Curr. Biol. 2019; 29: 1161-1168Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar] are counterintuitive for two reasons. As mentioned above, non-autonomous TEs are much shorter than their autonomous counterparts and, more importantly, depend on parasitizing their enzymatic machinery. A continuous expansion of non-autonomous TEs should thus either coincide with a comparable expansion of the corresponding autonomous TEs, or happen strongly at the expense of the autonomous TEs, ultimately leading to the extinction of the latter through mutations (Figure 2C). Such an extinction would obviously stop the expansion of non-autonomous TEs and likewise lead to their extinction. Genomes thus usually have a mix of significant copy numbers of non-autonomous and autonomous TEs. Take, for example, our own human genome, arguably one of the best-studied animal genomes. SINEs are by far the most numerous group of TEs (>1.5 million copies) but make up only 13% of the genome, while less numerous autonomous TEs account for nearly 30% of the genome [14Lander E.S. Linton L.M. Birren B. Nusbaum C. Zody M.C. Baldwin J. Devon K. Dewar K. Doyle M. Fitzhugh W. et al.Initial sequencing and analysis of the human genome.Nature. 2001; 409: 860-921Crossref PubMed Scopus (17726) Google Scholar]. Why are larvacean tunicates so different in this regard? One may speculate about these findings in the light of population genetics. Larvacean tunicates likely have very large population sizes due to their marine planktonic life style, which might allow active autonomous TEs to persist at very low frequencies in the population. These low frequencies might still be sufficient for TE protein production and mobilization of non-autonomous TEs in significant numbers. Under this scenario, it seems counterintuitive that newly inserted small TEs would drift to fixation in such large numbers that they lead to genome expansion. However, it is plausible that new insertions of small TEs are less deleterious than those of large autonomous ones, and might thus more easily accumulate. This would be especially the case in large populations with a high efficacy of selection against deleterious mutations [15Wolf J.B.W. Ellegren H. Making sense of genomic islands of differentiation in light of speciation.Nat. Rev. Genet. 2017; 18: 87-100Crossref PubMed Scopus (237) Google Scholar]. It is also important to keep in mind that genome size is the net result of gain and loss of DNA [16Petrov D.A. Sangster T.A. Johnston J.S. Hartl D.L. Shaw K.L. Evidence for DNA loss as a determinant of genome size.Science. 2000; 287: 1060-1062Crossref PubMed Scopus (265) Google Scholar]. In organisms such as birds and mammals with relatively low genome size variation, the rate of TE accumulation covaries with the rate of deletions in an ‘accordion’-like process [17Kapusta A. Suh A. Feschotte C. Dynamics of genome size evolution in birds and mammals.Proc. Natl. Acad. Sci. USA. 2017; 114: E1460-E1469Crossref PubMed Scopus (187) Google Scholar]. It remains to be seen whether the extensive genome size variation in larvacean tunicates arises only from differential TE accumulation or additionally from differential covariation with DNA deletion rates. Future studies on larvacean tunicates will hopefully elucidate these open questions by sequencing additional species and looking at population-level variation of genome sizes. In summary, it now emerges that not only large TEs can have a significant impact on genome size, but also small, non-autonomous TEs through continuous hijacking of proteins from autonomous TEs. This phenomenon further adds to the diverse ways that TEs shape the genomes of their hosts [18Bourque G. Burns K.H. Gehring M. Gorbunova V. Seluanov A. Hammell M. Imbeault M. Izsvák Z. Levin H.L. Macfarlan T.S. et al.Ten things you should know about transposable elements.Genome Biol. 2018; 19: 199Crossref PubMed Scopus (407) Google Scholar]. One may wonder, however, whether larvacean tunicates are an exceptional case of genome size expansion through non-autonomous TEs. Maybe more such cases will be unearthed once we dive deeper into the genomes of other understudied organisms. Massive Changes of Genome Size Driven by Expansions of Non-autonomous Transposable ElementsNaville et al.Current BiologyMarch 14, 2019In BriefThe causes of genome size variation and their relation with life traits are poorly understood. Naville, Henriet, et al. show that, in tunicate larvaceans, close relatives of vertebrates, multiplications of non-autonomous transposable elements were the main drive of remarkable genome expansions. Full-Text PDF Open Archive
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