Power and Weakness of Repetition – Evaluating the Phylogenetic Signal From Repeatomes in the Family Rosaceae With Two Case Studies From Genera Prone to Polyploidy and Hybridization (Rosa and Fragaria)

Abstract

Plant genomes consist, to a considerable extent, of non-coding repetitive DNA. Several studies showed that phylogenetic signals can be extracted from such repeatome data by using among-species dissimilarities from the RepeatExplorer2 pipeline as distance measures. Here, we advanced this approach by adjusting the read input for comparative clustering indirectly proportional to genome size and by summarizing all clusters into a main distance matrix subjected to Neighbor Joining algorithms and Principal Coordinate Analyses. Thus, our multivariate statistical method works as a “repeatomic fingerprint,” and we proved its power and limitations by exemplarily applying it to the family Rosaceae at intrafamilial and, in the genera Fragaria and Rosa, at the intrageneric level. Since both taxa are prone to hybridization events, we wanted to show whether repeatome data are suitable to unravel the origin of natural and synthetic hybrids. In addition, we compared the results based on complete repeatomes with those from ribosomal DNA clusters only, because they represent one of the most widely used barcoding markers. Our results demonstrated that repeatome data contained a clear phylogenetic signal supporting the current subfamilial classification within Rosaceae. Accordingly, the well-accepted major evolutionary lineages within Fragaria were distinguished, and hybrids showed intermediate positions between parental species in data sets retrieved from both complete repeatomes and rDNA clusters. Within the taxonomically more complicated and particularly frequently hybridizing genus Rosa, we detected rather weak phylogenetic signals but surprisingly found a geographic pattern at a population scale. In sum, our method revealed promising results at larger taxonomic scales as well as within taxa with manageable levels of reticulation, but success remained rather taxon specific. Since repeatomes can be technically easy and comparably inexpensively retrieved even from samples of rather poor DNA quality, our phylogenomic method serves as a valuable alternative when high-quality genomes are unavailable, for example, in the case of old museum specimens.

Evolutionary Dynamics of the Repeatome Explains Contrasting Differences in Genome Sizes and Hybrid and Polyploid Origins of Grass Loliinae Lineages

“…In agreement with previous studies from other angiosperms (Dodsworth et al, 2015;McCann et al, 2018McCann et al, , 2020Vitales et al, 2020b;Herklotz et al, 2021), the different amounts of shared repeats retrieved from comparative RE2 analyses of Loliinae have been shown to contain phylogenetic information at different systematic levels across the four Loliinae evolutionary groups. All evolutionary analyses have confirmed their ability to recover deep-to-shallow evolutionary relationships that were highly or relatively consistent with those based on the 35S rDNA and the plastome and combined data sets, respectively (Tables 1, 4, Figures 4, 5, Supplementary Tables 3, 4, and Supplementary Figures 1, 3).…”

“…Several studies have demonstrated that similarity-based clustering of low coverage genome sequencing reads, which confidentially represent 0.50-0.01× of the total haploid genome coverage, is proportional to the genomic abundance and longitude of the corresponding repeat-types (Macas et al, 2015;Pellicer et al, 2018) and could therefore be used to quantify them. The utility of the Repeat Explorer 2 bioinformatics tools for the quantification and annotation of repeats in plants (Novák et al, 2020) has been implemented by phylogenetic and distance-based network methods and by multivariate statistical methods that have corroborated the phylogenetic signal of the repeatome in various groups of angiosperm (Vitales et al, 2020a,b;Herklotz et al, 2021). It has also been supplemented by 5S rDNA graphbased clustering methods which have successfully corroborated the identity of the ancestral progenitor genomes of several polyploid plants (Garcia et al, 2020;Vozárová et al, 2021).…”

Repeat turnover meets stable chromosomes: repetitive DNA sequences mark speciation and gene pool boundaries in sugar beet and wild beets

“…It is often observed that genomic repeat profiles contain a phylogenetic signal (Dodsworth et al ., 2015; McCann et al ., 2020; Vitales et al ., 2020b; Herklotz et al ., 2021). In the case of Beta and Patellifolia species, this is only partly true: Overall, the repeatomes enable to separate the beet species into genera and sections.…”

Repeat turnover meets stable chromosomes: repetitive DNA sequences mark speciation and gene pool boundaries in sugar beet and wild beets

“…It is often observed that genomic repeat profiles contain a phylogenetic signal (Dodsworth et al., 2015; Herklotz et al., 2021; McCann et al., 2020; Vitales, Garcia, & Dodsworth, 2020). In the case of Beta and Patellifolia species, this is only partly true: Overall, the repeatomes enable to separate the beet species into genera and sections.…”