Transposable element proliferation and genome expansion are rare in contemporary sunflower hybrid populations despite widespread transcriptional activity of LTR retrotransposons

Abstract

Hybridization is a natural phenomenon that has been linked in several organismal groups to transposable element derepression and copy number amplification. A noteworthy example involves three diploid annual sunflower species from North America that have arisen via ancient hybridization between the same two parental taxa, Helianthus annuus and H. petiolaris. The genomes of the hybrid species have undergone large-scale increases in genome size attributable to long terminal repeat (LTR) retrotransposon proliferation. The parental species that gave rise to the hybrid taxa are widely distributed, often sympatric, and contemporary hybridization between them is common. Natural H. annuus × H. petiolaris hybrid populations likely served as source populations from which the hybrid species arose and, as such, represent excellent natural experiments for examining the potential role of hybridization in transposable element derepression and proliferation in this group. In the current report, we examine multiple H. annuus × H. petiolaris hybrid populations for evidence of genome expansion, LTR retrotransposon copy number increases, and LTR retrotransposon transcriptional activity. We demonstrate that genome expansion and LTR retrotransposon proliferation are rare in contemporary hybrid populations, despite independent proliferation events that took place in the genomes of the ancient hybrid species. Interestingly, LTR retrotransposon lineages that proliferated in the hybrid species genomes remain transcriptionally active in hybrid and nonhybrid genotypes across the entire sampling area. The finding of transcriptional activity but not copy number increases in hybrid genotypes suggests that proliferation and genome expansion in contemporary hybrid populations may be mitigated by posttranscriptional mechanisms of repression.

FIG. 1.

Estimates of nuclear DNA content (2C genome size) for individuals in natural Helianthus annuus × H. petiolaris hybrid populations (HP-x) and nearby stands of pure H. annuus and H. petiolaris. Data are shown for five different sampling locations (subpanels A–E). Lower case letters indicate results of Turkey–Kramer HSD post hoc tests. Number of individuals sampled: n = 129 for H. annuus, n = 130 for H. petiolaris, and n = 222 for individuals from hybrid populations.

FIG. 2.

Estimates of genome copy number abundance of Ty3/gypsy-like and Ty1/copia-like sequences for individuals in natural Helianthus annuus × H. petiolaris hybrid populations (HP-x) and nearby stands of pure H. annuus and H. petiolaris. Data are shown for five different sampling locations (subpanels A–E). Lower case letters indicate results of Turkey–Kramer HSD post hoc tests. Number of individuals sampled: n = 45 for H. annuus, n = 45 for H. petiolaris, and n = 79 for individuals from hybrid populations.

FIG. 3.

Genomic copy number estimates of Ty3/gypsy (A) and Ty1/copia (B) elements as a function of hybrid index score for 59 hybrid individuals from four different regional sampling locations. Hybrid index scores range from 0 (H. petiolaris-like) to 1 (Helianthus annuus-like). Individuals from the Barton Co. Kansas site were not included in this analysis (see Materials and Methods).

FIG. 4.

Transcriptional assays of Ty3/gypsy and Ty1/copia elements in Helianthus annuus, H. petiolaris, and hybrid individuals collected from five different regional sampling locations (subpanels A–E). Plus (+) and minus (–) signs indicate whether RT enzyme was provided or withheld from the RT-PCR reaction, respectively. Ann, H. annuus; Pet, H. petiolaris; Hyb, hybrid individual