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The chromosome-level genome for Toxicodendron vernicifluum provides crucial insights into Anacardiaceae evolution and urushiol biosynthesis

ABSTRACT: Summary The lacquer tree (Toxicodendron vernicifluum (Stokes) F.A. Barkley) is an important tree with economic, industrial, and medicinal values. Here, we generated the reference genome of T. vernicifluum at the chromosome level with 491.93 Mb in size, in which 98.26% of the assembled contigs were anchored onto 15 pseudochromosomes with the scaffold N50 of 32.97 Mb. Comparative genomic analysis revealed the gene families related to urushiol biosynthesis were expanded, contributing to the ecological fitness and biological adaptability of the lacquer tree. We combined multi-omics data to identify genes that encode key enzymes in the T. vernicifluum urushiol and lignin biosynthetic pathways. Furthermore, the unique active metabolites, such as butin and fisetin, in cultivar lacquers were identified by metabolism profiling. Our work would provide crucial insights into metabolite synthesis such as urushiol and lignin, meanwhile offer a basis for further exploration of the cultivation and breeding of T. vernicifluum and other Anacardiaceae members. Graphical abstract Highlights • We provide the first chromosome-level genome for Toxicodendron vernicifluum• We explore the phylogenetic position of lacquer tree• We identify genes involved in the urushiol and lignin biosynthetic pathways• Analysis of the unique active metabolites in cultivar lacquers by LC-MS/MS is reported Genetics; Evolutionary biology; Plant biology; Omics

SUBMITTER: Bai G

PROVIDER: S-EPMC9207680 | biostudies-literature | 2022 Jun

REPOSITORIES: biostudies-literature

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Project description:Species' phylogeographic patterns reflect the interplay between landscape features, climatic forces, and evolutionary processes. Here, we used two chloroplast DNA (cpDNA) markers (trnL and trnL-F) to explore the role of stepped geomorphology in shaping the phylogeographic structure of Toxicodendron vernicifluum, an economically important tree species widely distributed in East Asia. The range-wide pattern of sequence variation was analyzed based on a dataset including 357 individuals from China, together with published sequences of 92 individuals mainly from Japan and South Korea. We identified five chloroplast haplotypes based on seven substitutions across the 717-bp alignment. A clear east-west phylogeographic break was recovered according to the stepped landforms of mainland China. The wild trees of the western clade were found to be geographically restricted to the "middle step", which is characterized by high mountains and plateaus, while those of the eastern clade were confined to the "low step", which is mainly made up of hills and plains. The two major clades were estimated to have diverged during the Early Pleistocene, suggesting that the cool glacial climate may have caused the ancestral population to retreat to at least two glacial refugia, leading to allopatric divergence in response to long-term geographic isolation. Migration vector analyses based on the outputs of ecological niche models (ENMs) supported a gradual range expansion since the Last Interglacial. Mountain ranges in western China and the East China Sea land bridge were inferred to be dispersal corridors in the western and eastern distributions of T. vernicifluum, respectively. Overall, our study provides solid evidence for the role of stepped geomorphology in shaping the phylogeographic patterns of T. vernicifluum. The resulting east-west genetic discontinuities could persist for a long time, and could occur at a much larger scale than previously reported, extending from subtropical (e.g., the Xuefeng Mountain) to warm-temperate China (e.g., the Taihang Mountain).

Project description:This work tested antioxidant, anti-lung cancer, and antibacterial activities by in vitro, in vivo, and computational experiments for the metabolites extracted from the bark, seed, and stem of Toxicodendron vernicifluum. The results showed that all the extracts significantly scavenged 1,2-diphenyl-1-picrylhydrazyl (DPPH) in a dose-dependent manner. But, the total phenol content (TPC) ranged from 2.12 to 89.25% and total flavonoids content (TFC) ranged from 1.02 to 15.62% in the extracts. The methanolic bark extract (MBE) exhibited higher DPPH scavenging activity than the other extracts, probably due to the higher content of the TPC and TFC present in it. Among the extracts, only the MBE showed anti-lung cancer activity at an acceptable level with a therapeutic index value (22.26) against human lung carcinoma. This was due to the cancer cell death in A549 induced by MBE through reactive oxygen species (ROS) generation, apoptosis, and cell arrest in G1 phase and inhibition of anti-pro-apoptotic protein survivin. Among the extracts, MBE showed significantly higher antibacterial activity as evident through the higher zone of inhibition 13 ± 0.5 mm against methycilin resistant strain of Staphylococcus aureus (MRSA), Salmonila enteria subp. enterica, and P. aeruginosa, 11 ± 0.3 mm against E. coli and 10 ± 0.2 mm against B. cereus. The MBE also showed an excellent antibacterial activity with lower minimal inhibitory concentration (MIC). Particularly, the MBE showed more significant antibacterial activity in MRSA. The in vivo antibacterial activity of the MBE was further tested in C. elegans model. The treatment of the MRSA induced cell disruption, damage and increased mortality of C. elegans as compared to the untreated and MBE treated C. elegans with normal OP50 diet. Moreover, the MBE treatment enhanced the survival of the MRSA infected C. elegans. The compounds, such as 2,3,3-trimethyl-Octane and benzoic from the MBE, metabolized the novel bacterial topoisomerases inhibitor (NBTI) and MRSA related protein (PBP2a). Overall the T. vernicifluum is potentially bioactive as evident by antioxidant, anti-lung cancer, and antibacterial assays. Further studies were targeted on the purification of the novel compounds for the clinical evaluation.

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The chromosome-level genome for Toxicodendron vernicifluum provides crucial insights into Anacardiaceae evolution and urushiol biosynthesis

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