In our series on top ten genomes, one candidate represented extremely large genomes. Extremely large genomes are unusual, and it is not unreasonable to ponder how they ended up being so large. A new paper offers insight (h/t:Detlef Weigel @plantevolution).
Plants exhibit an extraordinary range of genome sizes, varying by > 2000-fold between the smallest and largest recorded values. In the absence of polyploidy, changes in the amount of repetitive DNA (transposable elements and tandem repeats) are primarily responsible for genome size differences between species. However, there is ongoing debate regarding the relative importance of amplification of repetitive DNA versus its deletion in governing genome size.
Using data from 454 sequencing, we analysed the most repetitive fraction of some of the largest known genomes for diploid plant species, from members of Fritillaria.
We revealed that genomic expansion has not resulted from the recent massive amplification of just a handful of repeat families, as shown in species with smaller genomes. Instead, the bulk of these immense genomes is composed of highly heterogeneous, relatively low-abundance repeat-derived DNA, supporting a scenario where amplified repeats continually accumulate due to infrequent DNA removal.
Our results indicate that a lack of deletion and low turnover of repetitive DNA are major contributors to the evolution of extremely large genomes and show that their size cannot simply be accounted for by the activity of a small number of high-abundance repeat families.
From the conclusion section -
Our results from Fritillaria demonstrate that extreme cases of genomic expansion can take place via the accumulation of highly heterogeneous, relatively low-abundance, repeat-derived DNA and indicate that a lack of deletion and low turnover of repetitive DNA play major roles in genome size evolution. These findings will have important consequences for understanding the content and evolution of plant genomes. Very large genomes may clearly still contain highly amplified repeat families that individually have a substantial impact on genome size, such as is shown here with the high- abundance tandem repeat in F. affinis (Fig. 2). However, the overall picture we have revealed, both from analysis of genomic Fritillaria data and from S/L data from diverse plant species, is not one of genomes growing principally by the activity of a few repeat families as had previously been suggested. Whether very large plant genomes (> 20 Gb) exist where significant genome expansion results solely from the amplification of one or two repeat families remains to be seen. Irrespective of this, our results, as well as those from some gymnosperm and animal species, indicate that such a mode of evolution is not a general feature of extreme genome size expansions. The universality of the patterns we have revealed awaits testing with data from further species with giant genomes, such as those found in the Melanthiaceae (Pellicer et al., 2014) or Viscum (Zonneveld, 2010).
Repetitive DNA can be removed from the genome via homologous and illegitimate recombination (Fedoroff, 2012); the importance of recombination-based processes in DNA removal is suggested by the greater estimated rate of DNA deletion in genomic regions with high recombination rates compared with those undergoing less recombination (Nam & Ellegren, 2012). A recent theory presented by Fedoroff (2012) provides a plausible mechanism by which recombination frequency, and hence DNA removal rate, might be constrained. Most repetitive elements in plant genomes are highly methylated and contained within recombinationally inert heterochromatin (Fedoroff, 2012; Henderson, 2012). It is proposed that epigenetic mechanisms, which control the formation of heterochromatin, evolved to prevent deleterious effects of unconstrained recombination (Fedoroff, 2012); if unsuppressed, the presence of multiple TE copies would be expected to stimulate large numbers of ectopic recombination events (Bennetzen & Wang, 2014). Consequently, efficient epigenetic regulation of repetitive elements may actually prevent their removal, as they become locked into tracts of the genome that cannot be accessed by the recombination machinery (Fedoroff, 2012). If this theory holds true, plant species with large genomes may accumulate more repetitive DNA because of the rapid action of epigenetic mechanisms subsequent to amplification, whereas epigenetic silencing is predicted to reach completion more slowly in species with smaller genomes, providing a window of opportunity for removal of repetitive DNA via recombination before heterochromatinization is achieved. This argument runs counter to the suggestion that epigenetic silencing of repetitive DNA may be less effective in species with large genomes, thus allowing TEs to proliferate more easily (Kelly & Leitch, 2011). Although epigenetic mechanisms involved in regulating activity of repetitive elements have been examined in limited taxa, there is evidence that they may be less efficient in the larger genome of Arabidopsis lyrata (1C = 245 Mb; Lysak et al., 2009) than in the smaller genome of A. thaliana (Hollister et al., 2011). However, initial evidence on the function of epigenetic mechanisms in F. imperialis indicates that this species shows all the signatures that are usually associated with strict epigenetic regulation of repetitive DNA in small genomes (Becher et al., 2014). Nevertheless, irrespective of whether greater efficiency of epigenetic control has a role in stimulating genome size expansion, our results provide clear evidence that a key factor in the evolution of very large genomes is a lack of DNA removal leading to ongoing accumulation and low turnover of repetitive and repeat-derived sequences.
Readers may note that another plant genome was included in the top ten list for being ‘too small’, or rather with hardly any junk DNA. It would be interesting to check what genome evolution process made that happen.