Genomics of homoploid hybrid speciation: diversity and transcriptional activity of long terminal repeat retrotransposons in hybrid sunflowers

Abstract

Hybridization is thought to play an important role in plant evolution by introducing novel genetic combinations and promoting genome restructuring. However, surprisingly little is known about the impact of hybridization on transposable element (TE) proliferation and the genomic response to TE activity. In this paper, we first review the mechanisms by which homoploid hybrid species may arise in nature. We then present hybrid sunflowers as a case study to examine transcriptional activity of long terminal repeat retrotransposons in the annual sunflowers Helianthus annuus, Helianthus petiolaris and their homoploid hybrid derivatives (H. paradoxus, H. anomalus and H. deserticola) using high-throughput transcriptome sequencing technologies (RNAseq). Sampling homoploid hybrid sunflower taxa revealed abundant variation in TE transcript accumulation. In addition, genetic diversity for several candidate genes hypothesized to regulate TE activity was characterized. Specifically, we highlight one candidate chromatin remodelling factor gene with a direct role in repressing TE activity in a hybrid species. This paper shows that TE amplification in hybrid lineages is more idiosyncratic than previously believed and provides a first step towards identifying the mechanisms responsible for regulating and repressing TE expansions.

Keywords: Helianthus; RNAseq; genome evolution; hybridization; transposable elements.

Figure 1.

Phylogenetic network based on a random subset of 11 522 high-quality SNPs genotyped for all individuals.

Figure 2.

Abundance of transcript reads from individual samples aligned to putative transposable element sequences classified as (a) Gypsy-like, (b) Copia-like or (c) Other elements. Sample groups (‘species’) are arrayed along the x-axes, with each point representing an individual sample. y-Axes indicate transcript estimates normalized by library size. ANOVA revealed significant differences among species per sample groups (Gypsy: F = 6.2, p-value = 1.7 × 10⁻⁴; Copia: F = 7.8, p-value = 2.0 × 10⁻⁵, Other elements: F = 7.7, p-value = 2.2 × 10⁻⁵). Within a given element class, species per sample groups labelled with the same letter (A, B, C) do not significantly differ (pairwise t-test, p-value > 0.05).

Figure 3.

Correlation between aggregate Gypsy and Copia transcript abundance. Dots are coloured according to whether they belong to the turquoise, blue or grey (unassigned) modules according to WGCNA. Grey area represents genes that had a correlation coefficient above |0.4| and were labelled as TE regulator genes in subsequent analyses.

Figure 4.

Boxplot of F_ST values for the subset of TE regulator genes against all other genes for the parental species pairs (H. annuus versus H. petiolaris) and their hybrids (H. anomalus, H. deserticola, H. paradoxus).

Figure 5.

Boxplot of genetic diversity (π) values for the subset of TE regulator genes against all other genes for the parental species (H. annuus and H. petiolaris) and their hybrids (H. anomalus, H. deserticola, H. paradoxus).

Figure 6.

Barplot of the estimated proportion of amino acid substitutions driven to fixation by positive selection (alpha) for the subset of TE regulator genes against all other genes for the parental species pairs (H. annuus versus H. petiolaris) and their hybrids (H. anomalus, H. deserticola, H. paradoxus).

Figure 7.

Example of a candidate gene. (a) BLAST and Gene Ontology annotation; (b) correlation between gene and TE Expression (aggregate Gypsy elements) and (c) genetic divergence (fixed or polymorphic synonymous and non-synonymous sites).