Genome size variation at constant chromosome number is not correlated with repetitive DNA dynamism in Anacyclus (Asteraceae)

Abstract

Background and aims: Changes in the amount of repetitive DNA (dispersed and tandem repeats) are considered the main contributors to genome size variation across plant species in the absence of polyploidy. However, the study of repeatome dynamism in groups showing contrasting genomic features and complex evolutionary histories is needed to determine whether other processes underlying genome size variation may have been overlooked. The main aim here was to elucidate which mechanism best explains genome size evolution in Anacyclus (Asteraceae).

Methods: Using data from Illumina sequencing, we analysed the repetitive DNA in all species of Anacyclus, a genus with a reticulate evolutionary history, which displays significant genome size and karyotype diversity albeit presenting a stable chromosome number.

Key results: By reconstructing ancestral genome size values, we inferred independent episodes of genome size expansions and contractions during the evolution of the genus. However, analysis of the repeatome revealed a similar DNA repeat composition across species, both qualitative and quantitative. Using comparative methods to study repeatome dynamics in the genus, we found no evidence for repeat activity causing genome size variation among species.

Conclusions: Our results, combined with previous cytogenetic data, suggest that genome size differences in Anacyclus are probably related to chromosome rearrangements involving losses or gains of chromosome fragments, possibly associated with homoploid hybridization. These could represent balanced rearrangements that do not disrupt gene dosage in merged genomes, for example via chromosome segment exchanges.

Keywords: Anacyclus; Heliocauta atlantica; chromosome number; comparative genomics; genome size; homoploid hybridization; repetitive DNA; reticulate evolution; transposable elements (TEs).

Fig. 1.

Genome size evolution and comparative repeat composition of Anacyclus species. (A) Phylogenetic tree of Anacyclus species (from Oberprieler, 2004) with colour gradients along the tree branches indicating inferred genome size changes. (B) Species-specific genomic abundance of the ten largest clusters – sorted by their size in Anacyclus. Rectangles are coloured according to the type of repetitive element and their size is proportional to the total length of individual repeats on each species (acronyms as in Table 1).

Fig. 2.

Repeat composition of Anacyclus species and Heliocauta atlantica (acronyms as in Table 1). The abundances (percentage of repeatome) are detailed by type of repeat.

Fig. 3.

Pairwise scatterplots of the number of reads from each sister Anacyclus species in repeat clusters from the comparative analysis (acronyms as in Table 1). The slope of the dotted line is equal to the ratio of the genome sizes between the two species (i.e. repeats along the abline are found in the same genomic proportions in species compared).

Fig. 4.

Relative number of mapped Illumina reads on sets of reverse-transcriptase species-specific domains belonging to the most abundant transposon lineages of Anacyclus at three different stringency parameters (acronyms as in Table 1).

Fig. 5.

Evolutionary relationships among Anacyclus species based on repeatome information. (A) Neighbor-Net network inferred from rDNA sequences. (B) Filtered supernetwork summarizing a random selection of 10 000 bootstrap trees from the maximum parsimony analysis based on cluster abundances of the most abundant repeats in Anacyclus. (C) Filtered supernetwork summarizing neighbor-joining trees obtained from the interspecific sequence similarity matrices of the most abundant repeats in Anacyclus.

Fig. 6.

Scheme representing hypothetical recombination events between homologous chromosomes derived from distinct genomes (i.e. from homoploid hybridization) leading to chromosome arm exchanges, which would result in different genome sizes. The colours represent the distinct genomic origin of chromosomes and chromosome arms. Arrows indicate the direction of the recombination events and dash lines show the hypothetical chromosome segments that are exchanged.