A high-quality Buxus austro-yunnanensis (Buxales) genome provides new insights into karyotype evolution in early eudicots

Abstract

Background: Eudicots are the most diverse group of flowering plants that compromise five well-defined lineages: core eudicots, Ranunculales, Proteales, Trochodendrales, and Buxales. However, the phylogenetic relationships between these five lineages and their chromosomal evolutions remain unclear, and a lack of high-quality genome analyses for Buxales has hindered many efforts to address this knowledge gap.

Results: Here, we present a high-quality chromosome-level genome of Buxus austro-yunnanensis (Buxales). Our phylogenomic analyses revealed that Buxales and Trochodendrales are genetically similar and classified as sisters. Additionally, both are sisters to the core eudicots, while Ranunculales was found to be the first lineage to diverge from these groups. Incomplete lineage sorting and hybridization were identified as the main contributors to phylogenetic discordance (34.33%) between the lineages. In fact, B. austro-yunnanensis underwent only one whole-genome duplication event, and collinear gene phylogeny analyses suggested that separate independent polyploidizations occurred in the five eudicot lineages. Using representative genomes from these five lineages, we reconstructed the ancestral eudicot karyotype (AEK) and generated a nearly gapless karyotype projection for each eudicot species. Within core eudicots, we recovered one common chromosome fusion event in asterids and malvids, respectively. Further, we also found that the previously reported fused AEKs in Aquilegia (Ranunculales) and Vitis (core eudicots) have different fusion positions, which indicates that these two species have different karyotype evolution histories.

Conclusions: Based on our phylogenomic and karyotype evolution analyses, we revealed the likely relationships and evolutionary histories of early eudicots. Ultimately, our study expands genomic resources for early-diverging eudicots.

Keywords: Ancestral eudicot karyotype; Buxales; Eudicots; Karyotype evolution; Phylogenomic; Polyploidization.

Fig. 1

Features and phylogenetic analysis of the B. austro-yunnanensis genome. a Overview of the B. austro-yunnanensis genome. The outer layer of the circular, gray blocks represents the 14 chromosomes, and gaps within the chromosomes are shown in white. The various inner tracks represent the following genome features, calculated over 500 kb sliding windows: (I) gypsy density; (II) copia density; (III) LTR density; (IV) gene density; (V) LAI score; and (VI) GC content. b Phylogenetic tree of 28 species generated by coalescent analysis. Branch lengths represent divergence times. Posterior probabilities (PPs) and bootstrap support (BP) are indicated for each internal branch. Asterisks indicate 100 BP in concatenation analysis and 1.0 PP in coalescent analysis. Dots represent nodes with different topology. The nodal circles represent the gene tree variation calculated by the nodal recovery in the gene trees. c ILS. Nodes are colored by estimated theta values. d Gene tree estimation error. Nodes are colored by BP values that represent the percentage of nodes recovered from the simulation. e Hybridization. Nodes are colored by the Reticulation Index. Warmer colors indicate greater gene tree variation, higher ILS occurrence probabilities, higher gene tree estimation errors, and higher probabilities of hybridization in b, c, d, and e, respectively. Percentages of gene tree variation ascribed to ILS, estimation error, and gene flow are specified above the gray arrows

Fig. 2

WGD analyses. a The Ks distributions of intragenomic synteny blocks. b The proportion of collinear gene trees supporting independent polyploidization between each species pair. c Synteny blocks of the B. austro-yunnanensis genome

Fig. 3

Karyotype projection of five early-diverging eudicot species. The topology is the same as in Fig. 1 and the branch length represent the divergence time (see detail in Additional file 1: Fig. S9). Polyploidization events are indicated by red dots (duplication)

Fig. 4

Karyotype projection of 21 core eudicot species. The topology is the same as in Fig. 1 and the branch length represent the divergence time (see detail in Additional file 1: Fig. S9). Different background colors represent different lineages corresponding to Fig. 1: light purple represents Caryophyllales, light blue represents asterids, light pink represents rosid clades I and III, and light yellow represent rosid clade II. Polyploidization events are indicated by red dots (duplication) and blue stars (triplication). Shared fusion events are marked below the corresponding lineages

Fig. 5

Karyotype evolution of Aquilegia, Muscadinia, and Vitis. a Collinear gene dot plots and karyotype projections between Aquilegia and Vitis. The enlarged, inset part indicates that there is no sharing variation event between Aquilegia chr 5 and Vitis chr 7. b Possible karyotype evolution histories of Aquilegia, Vitis, and Muscadinia. Aco, Mro, and Vvi are the abbreviations for Aquilegia, Muscadinia, and Vitis, respectively. RTA and EEJ are the abbreviations for reciprocally translocated chromosome arms and end-end joining