Differential Genome Size and Repetitive DNA Evolution in Diploid Species of Melampodium sect. Melampodium (Asteraceae)

Abstract

Plant genomes vary greatly in composition and size mainly due to the diversity of repetitive DNAs and the inherent propensity for their amplification and removal from the host genome. Most studies addressing repeatome dynamics focus on model organisms, whereas few provide comprehensive investigations across the genomes of related taxa. Herein, we analyze the evolution of repeats of the 13 species in Melampodium sect. Melampodium, representing all but two of its diploid taxa, in a phylogenetic context. The investigated genomes range in size from 0.49 to 2.27 pg/1C (ca. 4.5-fold variation), despite having the same base chromosome number (x = 10) and very strong phylogenetic affinities. Phylogenetic analysis performed in BEAST and ancestral genome size reconstruction revealed mixed patterns of genome size increases and decreases across the group. High-throughput genome skimming and the RepeatExplorer pipeline were utilized to determine the repeat families responsible for the differences in observed genome sizes. Patterns of repeat evolution were found to be highly correlated with phylogenetic position, namely taxonomic series circumscription. Major differences found were in the abundances of the SIRE (Ty1-copia), Athila (Ty3-gypsy), and CACTA (DNA transposon) lineages. Additionally, several satellite DNA families were found to be highly group-specific, although their overall contribution to genome size variation was relatively small. Evolutionary changes in repetitive DNA composition and genome size were complex, with independent patterns of genome up- and downsizing throughout the evolution of the analyzed diploids. A model-based analysis of genome size and repetitive DNA composition revealed evidence for strong phylogenetic signal and differential evolutionary rates of major lineages of repeats in the diploid genomes.

Keywords: Bayesian analysis; Melampodium; ancestral state reconstruction; genome size; phylogenetics; repetitive DNA; tandem repeats; transposable elements.

FIGURE 1

Results of phylogenetic inference and ancestral genome size reconstruction in section Melampodium: (A) the maximum clade credibility tree from the BEAST analysis; Color vertical lines and letters next to species names indicate the taxonomic series the species belong to (C, series Cupulata, pink; G, series Glabribracteata, green; L, series Leucantha, blue; M, series Melampodium, yellow). (B) posterior distributions obtained from RevBayes analysis of ancestral genome size on important, well-supported nodes [annotated by color at nodes in (A)]; and (C) posterior distributions of commonly used tree transformation statistics (δ, κ, and λ) in BayesTraits. The light-blue bar at each node indicates uncertainty in the node height of the tree.

FIGURE 2

Normalized genome representation of the top clusters of five major repeat groups found in the genomes of species analyzed in the comparative analysis. Each of the four major repeat types (Ty1-copia-SIRE; Ty1-copia-others; Ty3-gypsy-all and DNA transposon) is represented by 15 top clusters whereas satellite DNA is represented by all 17 clusters. The repeats are hierarchically clustered along the horizontal axis so that repeats with similar distributions across species are grouped together. Genome size (1C value) for each species is indicated next to species name abbreviation (in brackets, gray) and the color vertical lines to the left of the species names indicate the taxonomic series the species belong to (series Cupulata, pink; series Glabribracteata, green; series Leucantha, blue; series Melampodium, yellow).

FIGURE 3

Sequence similarity profiles (distributions of the logarithm of Hs/Ho) for different repeat types: (A) DNA transposons; (B) Ty3-gypsy elements; (C) Ty1-copia SIRE elements; and (D) other Ty1-copia elements except for the SIRE lineage. For each read the Hs/Ho ratio was calculated using either hits to reads from species in the same series (dark gray) or hits to reads from all other species (light gray).

FIGURE 4

A comparison of satellite DNAs identified in the comparative analysis of all species analyzed in this study: (A) Dot-plot comparison of identified satellite DNA clusters (each represented by one contig) and (B) the contribution of reads from different species to each satellite DNA cluster. The area of red rectangles is proportional to the number of reads (abundance) contributed by each species. Color bars and capital letters above species names indicate the taxonomic series the species belong to (C, series Cupulata, pink; G, series Glabribracteata, green; L, series Leucantha, blue; M, series Melampodium, yellow).

FIGURE 5

Maximum a posteriori trees recovered from repeat-abundance based phylogenetic analysis with a single rate parameter and fixed root height of 1: (A) all repeats included with best model; (B) Ty1-copia elements only; (C) Ty3-gypsy elements only; and (D) satellite DNAs only. Color bars and capital letters next to species names indicate the taxonomic series the species belong to (C, series Cupulata, pink; G, series Glabribracteata, green; L, series Leucantha, blue; M, series Melampodium, yellow).