Evolution of Transcriptomes in Early-Generation Hybrids of the Apomictic Ranunculus auricomus Complex (Ranunculaceae)

Abstract

Hybridisation in plants may cause a shift from sexual to asexual seed formation (apomixis). Indeed, natural apomictic plants are usually hybrids, but it is still unclear how hybridisation could trigger the shift to apomixis. The genome evolution of older apomictic lineages is influenced by diverse processes such as polyploidy, mutation accumulation, and allelic sequence divergence. To disentangle the effects of hybridisation from these other factors, we analysed the transcriptomes of flowering buds from artificially produced, diploid F2 hybrids of the Ranunculus auricomus complex. The hybrids exhibited unreduced embryo sac formation (apospory) as one important component of apomixis, whereas their parental species were sexual. We revealed 2915 annotated single-copy genes that were mostly under purifying selection according to dN/dS ratios. However, pairwise comparisons revealed, after rigorous filtering, 79 genes under diversifying selection between hybrids and parents, whereby gene annotation assigned ten of them to reproductive processes. Four genes belong to the meiosis-sporogenesis phase (ASY1, APC1, MSP1, and XRI1) and represent, according to literature records, candidate genes for apospory. We conclude that hybridisation could combine novel (or existing) mutations in key developmental genes in certain hybrid lineages, and establish (together with altered gene expression profiles, as observed in other studies) a heritable regulatory mechanism for aposporous development.

Keywords: angiosperms; apospory; dN/dS ratios; hybrids; meiosis; sporogenesis.

Figure 1

Summary of Benchmarking Universal Single-Copy Orthologues (BUSCO) analysis results for the assembled transcriptomes of the five studied individuals against the Viridiplantae BUSCO dataset. Total number of analysed BUSCOs: 425. Complete BUSCOS (C) [=Complete and single-copy BUSCOs (S) + Complete and duplicated BUSCOs (D)], Fragmented BUSCOs (F), Missing BUSCOs (M).

Figure 2

Violin plot depicting average dN/dS ratios across putative single-copy loci over all samples as inferred by Nej–Gojobori algorithm using Bioperl.

Figure 3

Pie chart of genes involved in reproduction and inferred to be under diversifying selection in the F2 hybrids compared to the parental samples. “Onset” means genes involved in onset of reproductive process.