Complete organelle genomes of Korean fir, Abies koreana and phylogenomics of the gymnosperm genus Abies using nuclear and cytoplasmic DNA sequence data

Abstract

Abies koreana E.H.Wilson is an endangered evergreen coniferous tree that is native to high altitudes in South Korea and susceptible to the effects of climate change. Hybridization and reticulate evolution have been reported in the genus; therefore, multigene datasets from nuclear and cytoplasmic genomes are needed to better understand its evolutionary history. Using the Illumina NovaSeq 6000 and Oxford Nanopore Technologies (ONT) PromethION platforms, we generated complete mitochondrial (1,174,803 bp) and plastid (121,341 bp) genomes from A. koreana. The mitochondrial genome is highly dynamic, transitioning from cis- to trans-splicing and breaking conserved gene clusters. In the plastome, the ONT reads revealed two structural conformations of A. koreana. The short inverted repeats (1186 bp) of the A. koreana plastome are associated with different structural types. Transcriptomic sequencing revealed 1356 sites of C-to-U RNA editing in the 41 mitochondrial genes. Using A. koreana as a reference, we additionally produced nuclear and organelle genomic sequences from eight Abies species and generated multiple datasets for maximum likelihood and network analyses. Three sections (Balsamea, Momi, and Pseudopicea) were well grouped in the nuclear phylogeny, but the phylogenomic relationships showed conflicting signals in the mitochondrial and plastid genomes, indicating a complicated evolutionary history that may have included introgressive hybridization. The obtained data illustrate that phylogenomic analyses based on sequences from differently inherited organelle genomes have resulted in conflicting trees. Organelle capture, organelle genome recombination, and incomplete lineage sorting in an ancestral heteroplasmic individual can contribute to phylogenomic discordance. We provide strong support for the relationships within Abies and new insights into the phylogenomic complexity of this genus.

Figure 1

Circle map of the mitochondrial genome of Abies koreana. Genes on the inside and outside the map are transcribed in the clockwise and counterclockwise directions, respectively.

Figure 2

Distribution of repetitive DNA in Abies koreana organelle genomes. Within the circular maps, black lines represent the locations of pairs of repeats, with crossing lines denoting reverse repeats. In the inner and outer circles, the black boxes denote the locations of the mitochondrial genes. (a). mitochondrial genome. (b) plastid genome.

Figure 3

Plastid genome of Abies koreana. (a) Circle map of the A form. Genes on the inside and outside the map are transcribed in the clockwise and counterclockwise directions, respectively. (b) Formation of two isoforms. Intermolecular recombination across inverted repeats (blue). ONT reads were aligned to the plastid genome of A. koreana. The gray parts of the ONT reads indicate that those regions are identical to the parts of the reference genome. The dark blue, green, orange, and yellow parts of the ONT reads could not be aligned with the reference regions, which are corresponding regions. The four single-copy genomic regions surrounding the IR are shown with numbers and colors.

Figure 4

Phylogenetic relationships among the analyzed Abies species. Cladograms based on plastid (a–d), mitochondrial (e–g), and nuclear (h) sequences. Maximum likelihood bootstrap support values are shown above the branches on each cladogram.

Figure 5

Phylogenomic trees of the nuclear single-copy genes inferred with ASTRAL-III and IQ-TREE2. Local posterior probability and maximum likelihood bootstrap support values are shown above the branches on each phylogram.

Figure 6

Phylogenetic relationships among the 25 Abies species based on whole plastid genomes. Maximum likelihood bootstrap support values > 50% are shown above the branches on each cladogram.