Analysis of the giant genomes of Fritillaria (Liliaceae) indicates that a lack of DNA removal characterizes extreme expansions in genome size.

Laura J Kelly,Jaume Pellicer,Jiří Macas,Simon Renny‐Byfield,Ilia J Leitch,Richard A Nichols,Pavel Neumann,Michael F Fay,Martin A Lysak,Andrew R Leitch,Madeleine Berger,Peter D Day,Petr Novák

doi:10.1111/nph.13471

Abstract

Summary 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.

Highlights

Genome size may differ by > 40-fold between species of the same ploidy within a single genus of plants (Bennett & Leitch, 2012; Kelly et al, 2012)
In order to test the prediction that extreme genome size expansion occurs via the massive amplification of a few repeat families, we analysed two species of Fritillaria with similar monoploid genome sizes (1Cx-value = 2C value/ploidy level; Greilhuber et al, 2005), F. affinis (1Cx = 44.94 Gb) and F. imperialis (1Cx = 45.59 Gb; Table S1)
The scale of the difference is not sufficient to explain the contrast between the results we obtained in Fritillaria, where dozens of repeat families are required to have amplified in order to explain recent genome size expansion, and the scenario proposed previously whereby very large genomes derive from massive amplification of a small number of repeat families

Summary

Introduction

Genome size may differ by > 40-fold between species of the same ploidy within a single genus of plants (Bennett & Leitch, 2012; Kelly et al, 2012). The observation that a few families (Hawkins et al, 2006; Piegu et al, 2006), or even a single family (Neumann et al, 2006), of transposable elements (TEs) can dominate plant genomes and account for variation in genome size between closely related species has led to the suggestion that differences in the propensity for TE amplification play a primary role in governing genome size change (Grover & Wendel, 2010). At least some plant and animal species with large genomes appear to lose DNA more slowly than those with smaller genomes (Bensasson et al, 2001; Wicker & Keller, 2007; Hawkins et al, 2009; Hu et al, 2011; Sun et al, 2012a), indicating that differences in the rate of DNA removal may play an important role in determining genome size.

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Discussion

Conclusion