Genome sequencing of three Polyscias species reveals common features in terpene synthase gene family evolution in these species

Abstract

The genus Polyscias, part of the Araliaceae family, is known for its significant ornamental and medicinal value, as well as its rich variety of metabolites. These plants are primarily found in tropical regions, particularly in Southeast Asia and the Pacific islands. The diverse geographical environments have led to the emergence of many unique and endangered species, although there is limited genomic information available about them. In this study, we generated high-quality reference genomes for three endangered species: two that are endemic to Hawai'i, Polyscias cf. bisattenuata and Polyscias lallanii, and one more widespread species, Polyscias macgillivrayi. We identified a total of 51,083, 60,881, and 29,060 genes in these three species, respectively. Whole-genome duplication analysis indicated that all three species underwent a common duplication event. By examining the phylogenetic and structural characteristics of the terpene synthase gene family in these species and closely related species, we identified several gene clusters that play crucial roles in metabolite synthesis. A variety of mono- and sesquiterpenoids were detected, with several of these compounds having been validated in previous studies. Our findings provide a foundation for further genetic and biochemical investigations of Polyscias, which may aid in the conservation of these endangered species.

FIGURE 1

Evolutionary and annotation analyses of Polyscias cf. bisattenuata, Polyscias lallanii, and Polyscias macgillivrayi. (A) Inferred phylogenetic tree. Gene family expansions are indicated in green, and gene family comparisons are indicated in red. (B) Gene family analysis results. (C) Distributions of synonymous substitutions per synonymous site (Ks) of one‐to‐one orthologs identified among Po. cf. bisattenuata, Po. lallanii, Po. macgillivrayi, Aralia elata, Daucus carota, Eleutherococcus senticosus, Theobroma cacao, and Vitis vinifera. (D) Venn diagram of the gene families of the five species (Po. cf. bisattenuata, Po. lallanii, Po. macgillivrayi, Panax ginseng, and Arabidopsis thaliana).

FIGURE 2

Phylogenetic analysis of 107 candidate terpene synthase (TPS) genes with 231 TPS genes from other genomes (Aubourg et al., ; Tai et al., ; Thibaud‐Nissen et al., ; Tables S18 and S19).

FIGURE 3

Phylogenetic relationship, gene structure, and conserved motif analyses. (A) Phylogenetic analysis of the terpene synthase (TPS) genes in Polyscias cf. bisattenuata (Pbis), Polyscias lallanii (Plal), Polyscias macgillivrayi (Pmac), and Polyscias ginseng (GWHPBEIL). Members of different subfamilies are marked with different background colors. (B) Functional motif compositions of the TPS genes. The 10 motifs are represented by rectangular boxes of different colors. (C) The conserved functional domains of PF001397 and PF03936 in the TPS gene are represented by dark turquoise and light blue, respectively. (D) Intron‒exon organization of the TPS gene. The introns and exons are represented by the broken line and gray boxes, respectively. (E) The number and functional classification of cis‐acting elements in each TPS gene. (F) Distribution of 57 identified cis‐acting elements in each TPS gene. The elements are represented by boxes of different colors.

FIGURE 4

Evolution of terpene synthase (TPS) genes and biosynthesis pathways. (A, B) Synteny of the Polyscias cf. bisattenuata, Polyscias lallanii, and Polyscias macgillivrayi genes in the TPS‐b gene cluster. (C) Synteny of the Po. cf. bisattenuata, Po. lallanii, and Po. macgillivrayi genes in the TPS‐a gene cluster. (D) Terpene biosynthesis gene clusters (BGCs) in Po. macgillivrayi and gene synteny with Po. cf. bisattenuata and Po. lallanii.

FIGURE 5

Expression profiles of genes encoding enzymes involved in canonical terpenoid biosynthesis pathways. Abbreviations for enzymes in each catalytic step are shown in red, and their full names are listed in Table S20.