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Communication

The Identification of SQS/SQE/OSC Gene Families in Regulating the Biosynthesis of Triterpenes in Potentilla anserina

by
Yangmiao Jiao
1,2,
Xu Li
1,
Xueshuang Huang
1,2,
Fan Liu
1,
Zaiqi Zhang
1,* and
Liang Cao
1,*
1
Hunan Provincial Key Laboratory of Dong Medicine, Ethnic Medicine Research Center, Hunan University of Medicine, Huaihua 418000, China
2
Hunan Provincial Key Laboratory for Synthetic Biology of Traditional Chinese Medicine, School of Pharmacy, Hunan University of Medicine, Huaihua 418000, China
*
Authors to whom correspondence should be addressed.
Molecules 2023, 28(6), 2782; https://doi.org/10.3390/molecules28062782
Submission received: 8 February 2023 / Revised: 14 March 2023 / Accepted: 15 March 2023 / Published: 20 March 2023
(This article belongs to the Section Natural Products Chemistry)
Browse Figures
Versions Notes

Abstract

:
The tuberous roots of Potentilla anserina (Pan) are an edible and medicinal resource in Qinghai–Tibetan Plateau, China. The triterpenoids from tuberous roots have shown promising anti-cancer, hepatoprotective, and anti-inflammatory properties. In this study, we carried out phylogenetic analysis of squalene synthases (SQSs), squalene epoxidases (SQEs), and oxidosqualene cyclases (OSCs) in the pathway of triterpenes. In total, 6, 26, and 20 genes of SQSs, SQEs, and OSCs were retrieved from the genome of Pan, respectively. Moreover, 6 SQSs and 25 SQEs genes expressed in two sub-genomes (A and B) of Pan. SQSs were not expanded after whole-genome duplication (WGD), and the duplicated genes were detected in SQEs. Twenty OSCs were divided into two clades of cycloartenol synthases (CASs) and β-amyrin synthases (β-ASs) by a phylogenetic tree, characterized with gene duplication and evolutionary divergence. We speculated that β-ASs and CASs may participate in triterpenes synthesis. The data presented act as valuable references for future studies on the triterpene synthetic pathway of Pan.

1. Introduction

Triterpenes are one of the largest groups of secondary metabolites from natural origins with various skeletons; many deployed promising anti-cancer and anti-oxidant activity and are used widely in the pharmaceutical industry, such as ursolic acid, oleanolic acid, and ginsenoside [1,2]. Triterpenoids discovered from plants are commonly generated in the pathway of farnesyl pyrophosphate (FPP). squalene synthases (SQSs) catalyze FPP to squalene, and squalene is then oxidized by squalene epoxidases (SQEs) to 2,3-oxidosqualene, which is further converted into different triterpene skeletons by different members of oxidosqualene cyclases (OSCs) (Figure S1). Triterpene scaffolds are further oxidized or glycosylated into different structures of triterpenoids by various cytochrome P450 monooxygenases (CYP450) and UDP glucosyltransferases or cellulose synthase-like M-subfamilies [3]. In previous studies, 121 triterpenes skeletons have been summarized according to different conformation and ring numbers, among which 51 skeletons have been experimentally characterized as products of OSCs [4]. Interestingly, 24 skeletons not reported from nature sources were generated by OSCs in heterologous expressions [4]. Protosteryl and dammarenyl cations were parents of many triterpene skeletal types. Protosteryl cation with chair–boat–chair (CBC) conformation was further catalyzed by the OSCs of cycloartenol synthases (CASs), lanosterol synthases (LASs), and cucurbitadienol synthases (CDSs) to form products of cycloartenol, lanosterol, and cucurbitadienol, respectively, which are associated with the tetracyclic triterpene skeleton (6-6-6-5). While dammarenyl cation derived from the chair–chair–chair (CCC) conformation was the parent for classes of pentacyclic triterpenes, such as α-amyrin (6-6-6-6-6), β-amyrin (6-6-6-6-6), and lupeol (6-6-6-6-5), which were catalyzed by OSCs of α-amyrin synthases (α-ASs), β-amyrin synthases (β-ASs), and lupeol synthases (LUSs), respectively [5,6]. The stabilization of intermediate cations, steric hindrance, and the conformation of active center amino acid residues are primary factors affecting triterpene formation. OSCs in plants are encoded by polygenic families, and LASs, LUSs, and β-ASs may be differentiated and evolved from CASs [5,6]. The lengths of most exons of OSCs are conservative, but the lengths of exons 4, 7, and 9 show diversity [7]. Taking advantage of abundant genome resources to explore the key enzymes in the synthetic pathway of natural products and conducting research on the biosynthesis of bioactive small compounds can benefit the modern healthcare system [8].
Tuberous roots of Potentilla anserina (Pan), also named silverweed cinquefoil roots, served as important food and medicine sources for Tibetans in the Qinghai–Tibetan Plateau, China, over thousands of years. It is an important source of starch and bioactive compounds of triterpenoids and flavonoids [9,10,11,12]. Interestingly, all triterpenoids reported from Pan were pentacyclic triterpenes, including oleanane, ursane, and lupine types [9,13,14], which displayed outstanding hepatoprotective and anti-inflammatory effects [9,13]. The structure–activity relationships disclosed that 3α-OH, 19β-CH3, 20α-CH3, 20β-CH3, 21α-OH, and 30-OH groups in the structure of triterpenoid or saponins could strengthen the hepatoprotective and anti-inflammatory activities [13]. Many medicinal plants in the genus of Potentilla have been used in traditional Chinese and ethnic medicine. For example, the whole plants of P. chinensis Ser. and P. discolor Bge. were recorded in the Chinese pharmacopeia [14,15]. Studying the triterpene synthesis pathway in Pan is of great significance.
Pan and P. micrantha (Pmi) are two species in the genus of Potentilla with genomes that have recently been reported. Both species have a close genetic relationship to the woodland strawberry Fragaria vesca (Fve). The genome of Pan contains 14 chromosomes, diverged from that of Pmi 28.52 million years ago (Mya). Furthermore, Pan has undergone a recent whole-genome duplication (WGD) to ensure tetraploidization. The sub-genome structures of Pan are characterized with the A sub-genome, which is larger than the B sub-genome and phylogenetically closer to the genome of Pmi. In general, the A sub-genome had higher homoeologous gene expression in the tuberous root [16]. Fifty-one percent of genes of Pan and Pmi are in a ratio of 2:1, based on the collinearity analysis of 26,032 genes [16]. In this study, we analyzed SQSs, SQEs, and OSCs involved in the biosynthesis of triterpenes in Pan and revealed function and evolutionary relationships via comparative genomic studies, which could facilitate research on bioactive triterpenes in Pan.

2. Results

2.1. The Identification and Characterization of SQS/SQE/OSC Gene Families in Pan

In this study, from the genomic data of Pan, we retrieved 6, 26, and 20 genes for SQSs, SQEs, and OSCs, respectively (Figure 1A and Table S2). Six copies of SQSs were obtained by searching the genomic data of Pan with the Protein family database (Pfam, ID PF00494), while zero copies were derived from Homolog-based prediction (HBP). For SQEs, 25 copies of SQES were acquired using Pfam (ID PF08491) for searching, while 24 were obtained by HBP; among them, 23 were intersected, 1 new copy (Pan3G00107-1) was annotated by HBP, and 2 were refined with incomplete annotation (Pan8G00699-1 and Pan3G00106-1) (Figure 1D, Table S2). For OSCs, 18 and 19 copies were obtained via the Pfam database (IDs PF13249 and PF13243) and the HBP method, respectively, with 16 copies intersected. Pan11G02732 and Pan11G02733 mapped by Pfam were merged to Pan11G02732-1 by HBP (Figure 1D). Pan12G01400 (annotated) and Pan12G01401 (not acquired by Pfam) were merged to Pan12G01400-1 by the HBP method; moreover, the HBP method refined two genes (Pan7G00839-1 and Pan12G01259-1) and screened out one new copy (Pan11G02694-1) of OSCs (Table S2).
According to the Conserved Domain Database (CDD), we obtained the domains of SQSs/SQEs/OSCs (Figure 1C). The amino acid lengths of predicted products from SQSs, SQEs, and OSCs ranged from 318 bp to 627 bp, 215 bp to 420 bp, and 619 bp to 778 bp, respectively, and the isoelectric point ranged from 7.11 to 9.32, 5.01 to 8.84, and 5.73 to 7.61, respectively. Subcellular localization revealed that SQSs were located in organelle membranes and chloroplasts, products of SQEs located in endomembrane system, and organelle membranes, while proteins coded by OSCs were mainly located in plasma membranes and the nucleus (Table S2). In total, 6 SQSs genes and 25 SQEs genes were detected with different expression levels in root and tuberous root, respectively, and 8 OSCs genes were expressed in root and tuberous root (Figure 1B).

2.2. The Chromosomal Locations and Collinearity Analysis of SQSs/SQEs/OSCs

The genome of Pan contains 14 chromosomes, which underwent a tetraploidization in 6.4 Mya. The A sub-genome (A1–A7, from Chr1 to Chr13, odd numbers) and B sub-genome (B1–B7, from Chr2 to Chr14, even numbers) showed good collinearity [16]. SQSs were symmetrically distributed on two sub-genomes. SQEs were scattered on seven chromosomes such as Chr1 and Chr2, and the number of products located on the B sub-genome was larger than that of the A sub-genome, and there were tandem-duplicated genes on Chr2, Chr3, Chr4, Chr7, and Chr8. OSCs were concentrated and distributed on Chr7, Chr11, and Chr12 with tandem-duplicated genes, with the A sub-genome containing more copies (Figure 2).

2.3. The Phylogenetic Analysis of SQSs/SQEs

We constructed a phylogenetic tree of SQSs and SQEs of Pan, Fve, and Rosa rugosa (Rru) (Figure 3, Table S3). Orthologous genes showed good collinearity, i.e., in SQSs, the Pan:Fve:Rru ratio was 6:3:2, and FvH1g27480, Rru4g3473, Pan1G02399, and Pan2G00231 were distributed on a phylogenetic tree branch. FvH3g45220, Pan5G03590, and Pan6G03976 were grouped together, and FvH6g38780, Pan11G02890, and Pan12G01154 were grouped together. In SQEs, the Pan:Fve:Rru ratio was 26:10:20, and Pan was found to have many tandem-duplicated genes, such as in Chr3 (Pan3G00105 and Pan3G00304) and Chr4 (Pan4G03465 and Pan4G03385) in clade I (Figure 3). Meanwhile, in other branches, Rru was found to have a unique gene doubling event.

2.4. Phylogenetic Analysis of OSCs

The phylogenetic tree of OSCs retrieved from Pan, Fve, Rru, Pmi, Pyrus pyrifolia (Ppy), and Vitis vinifera (Vvi) was constructed along with the published/verified OSCs of Arabidopsis thaliana (Ath) and Oryza sativa (Osa) as outgroups (Figure 4; Tables S1 and S3). According to the functional annotation of KEGG and Swissport, products of OSCs were classified into eight categories (Figure 4). OSCs from Vvi, Fve, Rru, Ppy, and Pmi were classified into the CAS, LUS, and β-AS clades. OSCs from Pan were divided into two branches of CAS and β-AS. CASs were entirely distributed on the A sub-genome and divided into three sub-clades of Pan7G00204 and Pan7G00839-1, Pan7G00207 and Pan7G00837, and Pan11G02732-1, and the first two sub-clades on chromosome 7 (A4) had tandem duplication events. Meanwhile, β-ASs located on chromosomes 11 (A6) and 12 (B6) were divided into two branches, as shown in Figure 4 (clades I and II), characterized by a large number of tandem-duplicated genes.

3. Discussion

3.1. Gene Families Identified by the Pfam Database and the HBP Method

The development of sequencing technology and sophisticated genome assembly methods promotes the release of more genomes of plants. Generally, the reliability of subsequent genome analysis depends on the quality of assembly and the integrity of annotation. In this study, we used high-threshold Pfam results, along with the HBP method as a supplement, to identify genes in the pathway of triterpenes. We found that the HBP method had a correct rate (new copy and genes refined, merged, and split by HBP/all gene numbers) of 14–17% for SQS, SQE, and OSC gene families in different species (Table 1 and Table S3). There were merged OSCs in Pan and Ppy, according to the results (Table S3), possibly due to incomplete or low-accuracy annotation leading to fragmentation, or the wide existence of variable splicing in the genome. The split genes that appeared in Fve (i.e., FvH4_2g02660) and Rru were confirmed by the transcriptome data (Figure 1D, Table S4), which may be caused by tandem-duplicated genes, resulting in overly long annotation. The sequence of Pan12G01345-1 obtained from the HBP method contained a premature termination codon which may be introduced during evolution.
Eleven SQSs were obtained via a search in the Pfam database (Figure S2), of which three SQS-like genes (Pan4G02790, Pan3G00908, and Pan3G00874) were located in independent branches with incomplete motifs. The other two SQSs (Pan9G01625 and Pan10G01518) had complete PF00494 alignment information, but no corresponding motif, and KEGG annotation information. A possible explanation is that SQSs and the phytoene synthase family (PSYs) have structural similarities and share three conservative regions [17]. Thus, we included the remaining six SQSs in this study. In HBP analysis, only three SQS-like genes (Pan4G02790, Pan3G00908, and Pan3G00874) were obtained (Figure S2), probably because there were few reference genes for HBP. Therefore, accurate gene sets for homologous prediction and reliable databases for functional verification are critical in HBP analysis.

3.2. SQS/SQE/OSC Gene Family Expression and Evolution

Gene duplications were recognized as contributors to the evolution of genes with divergence functions. Sub-functional, hypofunctional, and neo-functional genes, as well as compensatory drift and neutral variation, may result from gene duplications [18]. Multiple paralogous genes may be generated by whole-genome polyploidization, segmental duplication, or tandem duplication [18]. The divergence of Vitales and Rosales occurred at about 121.9 Mya, while the Rosoideae divergence from Amygdaloideae occurred at 84.4 Mya [19]. The Potentilla genus was separated from Fragaria genus at about 40.68 Mya, followed by the divergence between Pan and Pmi (28.52 Mya) [16]. Pmi and Fve diverged at about 34.5 Mya [19], and Fve diverged from Rru at about 52.3 Mya [19]. An ancient genome-wide tripling event occurred in Vvi [20]. Plants in Rosaceae have experienced an ancient genome triplication, though no evidence of large-scale genome replication was found in Fve. It is speculated that chromosome rearrangement and genome shrinkage (or the selective loss of replication genes) cover up the ancient triplication event in Fve [21]. Rru has no additional genome-wide duplication after whole-genome triplication (WGT) [22]. The genome of Pan underwent a recent WGD event to form an allotetraploid after the divergence of Rosaceae, and the A sub-genome and the B sub-genome were found to have good collinearity [16].
According to the OSC phylogenetic trees and the distribution of OSCs on chromosomes, we discussed the characterization of OSCs. On the CAS clade, the Fve:Rru:Pan ratio was 3:2:5, and all CASs of Pan were distributed on the A sub-genome (Figure 4). Four copies of OSCs (Pan7G00207, Pan7G00837, Pan7G00204, and Pan7G00839-1) in chr7 were distributed into two branches, indicating that a tandem duplication event had taken place. The copies mentioned in chr7 showed a discrepant expression in root or tuberous root yields, and we speculated that the low expression may result from the shortening of coding sequences, resulting in sub-functionalization (Table S2).
In clade I of β-AS (Rru6g04897~Pan12G01344) (Figure 4), we hypothesized that β-AS has three ancestral copies, based on three genes of Vvi in the outgroup (clade III). The ratio of Fve:Rru:Pan was 4:5:7, and it was found that Pan has five OSC copies in chr12 and two copies in chr11. Pan12G01344, Pan12G01400-1, and Pan12G01353 showed similar transcription levels (Table S2), and two copies of them may have expanded due to tandem duplication. In clade II of β-AS (Rru6g04906~Pan12G01345-1), the ratio of Fve:Rru:Pan was 3:3:8. The ratio of the sub-branch (Rru6g05056~Pan11G02823) of Fve:Rru:Pan was 1:1:4. Furthermore, the OSCs of Pan (Pan11G02822, Pan11G02823, Pan12G01259-1, and Pan12G01261) were evenly distributed in the A and B sub-genomes, and the genes generated by tandem duplication were not uniformly expressed in the tuberous root (Table S2).
Similarly, according to the phylogenetic tree of SQSs and SQEs (Figure 3), Fve and Pan had three and six SQSs, respectively. The SQSs of Pan distributed on the A and B sub-genomes symmetrically may result from the WGD event of Pan. For SQEs, one of Pan2G00943 and Pan2G00944 seemed to expand in clade I, while tandem duplication occurred in Pan3G00304 or Pan3G00105 and Pan4G03465 or Pan4G03385, and the expression of duplicated genes was consistent in transcriptome data of root (Table S2). In clade II, Pan8G00700, Pan8G00721, and Pan8G00699-1 were duplicated genes, and Pan8G00699-1 had a higher expression in transcriptome data of root. In clade III, Pan11G01188 had no expression in root and tuberous root yields, which may be attributed to spatio-temporal specific expression (Figure 3, Table S2).

3.3. The Functional Prediction of OCSs and Triterpene Synthesis in Pan

In the phylogenetic tree of eight species of OSCs, CASs were located in the outermost branch, which is in agreement with previous findings that LASs, LUSs, and β-ASs evolved from ancient CASs [5,6]. The classification of enzymes has been extensively studied with Osa as the outgroup [4]. OsOSC2 converts 2,3-oxidosqualene to cycloartenol [23] when using the CBC conformation as the precursor under the catalyzation of S-adenosyl-L-methionine-sterol-C24-methyltransferase 1 (SMT1) and CYP450 [24], and cycloartenol could be converted into phytosterols [25] and cholesterol [26]. Moreover, steroidal diosgenin was obtained with further hydroxylation and cyclization [27]. OsPS (japonica subspecies) is a tetracyclic parkeol synthase. In contrast, OsOS (indica subspecies) synthesizes a novel pentacyclic triterpene orysatinol and 12 other triterpenes, and key amino acid residues were found to determine the functional divergence between OsPS and OsOS [28]. OsABAS is a multifunctional enzyme annotated as the achilleol B synthase, showing functions of both α-AS and β-AS enzymes [29]. The OSCs of Pan have been classified into two groups of CAS and β-AS. CASs synthesize the tetracyclic triterpene skeleton and may be involved in the synthesis of sterols. SQEs act as a rate-limiting enzyme in the steroid biosynthesis pathway [30]. The β-ASs detected in Pan are pentacyclic triterpene (oleanane) synthetases, which is consistent with a lot of oleanane-type triterpenoids isolated from Pan [10,14,15].

4. Materials and Methods

4.1. SQS/SQE/OSC Gene Family Identification

The sequenced and annotated genome data of Potentilla anserina (Pan) [16], Potentilla micrantha (Pmi) [31], Fragaria vesca (Fve) [32], Rosa rugosa (Rru) [22], and Pyrus pyrifolia (Ppy) [33] of Rosaceae were requested from the Genome Database for Rosaceae (GDR) (https://www.rosaceae.org/tools/jbrowse, accessed on 14 March 2023), while the sequence of Vitis vinifera (Vvi) [20] was downloaded from the National Center for Biotechnology Information (NCBI) database. Oryza sativa (Osa) and Arabidopsis thaliana (Ath), serving as outgroups, were also downloaded from the NCBI. PF13249 and PF13243 downloaded from Pfam (http://pfam.xfam.org/, accessed on 14 March 2023) were applied to search for OSC coding proteins using the hidden Markov model (HMM) (E-value < 1 × 10−20). In order to reduce the deviation caused by different gene annotation methods on a variety of genomes, we used homolog-based prediction (HBP) to predict the number of genes. The strategy of HBP is as follows. Firstly, the OSC (Table S1) protein sequences downloaded from the NCBI were aligned to the genome using TBLASTN with an E-value < 1 × 10−5. Secondly, the conjoined high-scoring pairs (HSPs) by Solar (https://github.com/gigascience/papers/tree/master/zhou2013/MTannotationBGI/solar, accessed on 14 March 2023) were applied to determine the rough genomic region for each gene. Thirdly, we extracted and extended 2 kb both upstream and downstream of the Solar region, and defined gene models using GeneWise (v2.4.1) [34]. We also filtered the predictions with less than 30% coverage. The functional annotation of resulted genes was actualized by the Pfam, KEGG (https://www.genome.jp/kegg/, accessed on 14 March 2023), and Swissprot (http://www.ebi.ac.uk/sprot, accessed on 14 March 2023) databases. The motif was recognized using Meme (https://meme-suite.org/meme/tools/meme, accessed on 14 March 2023), with a default number of 6. Furthermore, the domain was predicted under the CDD (https://www.ncbi.nlm.nih.gov/cdd/, accessed on 14 March 2023) database. We combined the two prediction results of Pfam and HBP, and then retained the accurate ones. The identification of SQSs (PF00494) and SQEs (PF08491) was realized using the same method (Table S1).

4.2. Physicochemical Properties of OSCs/SQEs/SQSs from Pan

Various physicochemical properties, including the number of amino acids, the molecular weight, the isoelectric point, the grand average of hydropathicity (GRAVY), and subcellular localization (Table S2), were analyzed. ExPASy (http://expasy.org/, accessed on 14 March 2023) was used to predict the molecular weight and isoelectric points. GRAVY was calculated using the GRAVY calculator (http://www.gravy-calculator.de/, accessed on 14 March 2023), and the subcellular localization was predicted using BUSCA (http://busca.biocomp.unibo.it/, accessed on 14 March 2023) [35].

4.3. Sequence Alignment and Phylogenetic Analysis

Protein sequence alignments were conducted by muscle5.1 [36]. The phylogenetic tree was established using iqtree1.5.5 [37] with the MFP model and 1000 replicates of bootstrap, and was displayed by itol (https://itol.embl.de/upload.cgi, accessed on 14 March 2023).

4.4. RNA-seq Analysis

The transcriptome data of Pan in root (SRR12053561, SRR12053562, and SRR12053563) and tuberous root (SRR12053557, SRR12053559, and SRR12053560) yields were analyzed by the HISAT2 + StringTie + Ballgown [38] pipeline. Meanwhile, the transcriptome data of Fve (SRR19907785, SRR19907789, SRR19907792, ERR9861197, ERR9861198, and ERR9861199) and Rru (SRR20883375, SRR20883380, and SRR20883382) were analyzed using the same method.

5. Conclusions

Triterpenes are major pharmacodynamic substances of Pan, which show good anti-inflammatory and hepatoprotective activity. In this study, we analyzed members of OSC, SQS, and SQE gene families in the triterpene synthesis pathway using Pfam and HBP methods. The results provide a research basis for understanding the biosynthetic pathway of triterpenes in Pan by clarifying the function and evolutionary relationship of triterpene-synthesis-related genes.

Supplementary Materials

References [39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56] are cited in Table S1. The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/molecules28062782/s1. Figure S1: The biosynthetic pathway of triterpenes, Figure S2: The positions of five SQS genes inappropriately annotated by Pfam in the evolutionary tree. Supplementary Tables S1–S6: The supporting information of OSC/SQE/SQS gene families analyzed in this study. Table S1: Functional genes of SQSs/SQEs/OSCs in different species. Table S2: Expression and physicochemical properties of SQSs/SQEs/OSCs in Pan. Table S3: SQSs/SQEs/OSCs annotated by HBP and Pfam in different species. Table S4: Analysis of FvH6g36500/FvH2g02660/Rru6g2221 structure and alternative splicing by RNA-seq. Table S5: NCBI under accession number for transcriptomes and genome resource of different species. Table S6: Protein sequences of OSCs/SQSs/SQEs in different species.

Author Contributions

Conceptualization, L.C. and Z.Z.; methodology and bioinformatics analysis, Y.J. and X.L.; writing, L.C., Y.J., X.L., X.H. and F.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Hunan Provincial Key Laboratory of Dong Medicine (grant numbers 2015TP1020 and 2017CT5025), and the Natural Science Foundation of Hunan Province, China (grant number 2022JJ30425).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets analyzed in the current study are available in public databases of GDR and NCBI (https://www.rosaceae.org/ and https://www.ncbi.nlm.nih.gov/, accessed on 14 March 2023). The genomes of Potentilla anserina from https://figshare.com/projects/The_genome_assembly_and_annotation_files_of_Potentilla_anserina/83771 (accessed on 25 November 2021), Potentilla micrantha from https://www.rosaceae.org/rosaceae_downloads/Potentilla_micrantha/Pmicrantha-draft.v1.0/assembly/Potentilla_draft_genome.fasta.gz (accessed on 4 May 2018), Fragaria vesca from https://www.rosaceae.org/rosaceae_downloads/Fragaria_vesca/Fvesca-genome.v4.0.a1/assembly/Fragaria_vesca_v4.0.a1.fasta.gz (accessed on 1 January 2018), Rosa rugosa from https://www.rosaceae.org/rosaceae_downloads/Rosa_rugosa/Rosa_rugosa_v1.0/assembly/Rosa_rugosa_genome.fasta.gz (accessed on 31 August 2021), Pyrus pyrifolia from https://www.rosaceae.org/rosaceae_downloads/Pyrus_pyrifolia/ppyrifolia_v1.0/assembly/PPY_r1.0.pmol.fasta.gz (accessed on 11 January 2021), and Vitis vinifera from https://ftp.ncbi.nlm.nih.gov/genomes/all/GCF/000/003/745/GCF_000003745.3_12X/GCF_000003745.3_12X_genomic.fna.gz (accessed on 7 November 2019). The transcriptome data of Potentilla anserina (SRR12053557, SRR12053559, SRR12053560, SRR12053561, SRR12053562, and SRR12053563) (accessed on 19 June 2020), Fragaria vesca (SRR19907785, SRR19907789, SRR19907792) (accessed on 3 August 2022), (ERR9861197, ERR9861198, and ERR9861199) (accessed on 20 June 2022), and Rosa rugosa (SRR20883375, SRR20883380, and SRR20883382) (accessed on 14 September 2022) are download from https://www.ncbi.nlm.nih.gov/sra (accessed on 14 March 2023). All functional genes of different species are listed in Table S1. The origins of all genomes and transcriptomes are listed in Table S5.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Zhang, M.F.; Shen, Y.Q. Research advances on effects of ursolic acid and oleanolic acid against hepatic steatosis and fibrosis. Drug Eval. Res. 2017, 40, 270–278. [Google Scholar]
  2. Ji, Z.X.; Li, J.Q.; Wang, J.B. Research status on pharmacological effects of ginsenoside Rh3. SH. J. TCM. 2021, 55, 97–100. [Google Scholar]
  3. Wang, Y.; Zhang, H.; Ri, H.C.; An, Z.Y.; Wang, X.; Zhou, N.J.; Zheng, D.R.; Wu, H.; Wang, P.C.; Yang, J.F.; et al. Deletion and tandem duplications of biosynthetic genes drive the diversity of triterpenoids in Aralia elata. Nat. Commun. 2022, 13, 2224. [Google Scholar] [CrossRef] [PubMed]
  4. Wang, J.; Guo, Y.H.; Yin, X.; Wang, X.N.; Qi, X.Q.; Xue, Z.Y. Diverse triterpene skeletons are derived from the expansion and divergent evolution of 2,3-oxidosqualene cyclases in plants. Crit. Rev. Biochem. Mol. Biol. 2022, 57, 113–132. [Google Scholar] [CrossRef]
  5. Xue, Z.Y.; Duan, L.X.; Liu, D.; Guo, J.; Ge, S.; Dicks, J.; ÓMáille, P.; Osbourn, A.; Qi, X.Q. Divergent evolution of oxidosqualene cyclases in plants. New. Phytol. 2012, 193, 1022–1038. [Google Scholar] [CrossRef]
  6. Chen, C.Y.; Pang, Y.R.; Chen, Q.B.; Li, C.; Lü, B. Oxidosqualene cyclases in triterpenoids biosynthesis: A review. Chin. J. Biotech. 2022, 38, 443–459. [Google Scholar]
  7. Hoshino, T. β-Amyrin biosynthesis: Catalytic mechanism and substrate recognition. Org. Biomol. Chem. 2017, 15, 2869–2891. [Google Scholar] [CrossRef]
  8. Tao, H.; Lauterbach, L.; Bian, G.K.; Chen, R.; Hou, A.; Mori, T.; Cheng, S.; Hu, B.; Lu, L.; Mu, X.; et al. Discovery of non-squalene triterpenes. Nature 2022, 606, 414–419. [Google Scholar] [CrossRef]
  9. Morikawa, T.; Ninomiya, K.; Imura, K.; Yamaguchi, T.; Akagi, Y.; Yoshikawa, M.; Hayakawa, T.; Muraoka, O. Hepatoprotective triterpenes from traditional Tibetan medicine Potentilla anserina. Phytochemistry 2014, 102, 169–181. [Google Scholar] [CrossRef]
  10. Morikawa, T.; Imura, K.; Akagi, Y.; Muraoka, O.; Ninomiya, K. Ellagic acid glycosides with hepatoprotective activity from traditional Tibetan medicine Potentilla anserina. J. Nat. Med. 2018, 72, 317–325. [Google Scholar] [CrossRef]
  11. Chen, J.R.; Yang, Z.Q.; Hu, T.J.; Yan, Z.T.; Niu, T.X.; Wang, L.; Cui, D.A.; Wang, M. Immunomodulatory activity in vitro and in vivo of polysaccharide from Potentilla anserina. Fitoterapia 2010, 81, 1117–1124. [Google Scholar] [CrossRef]
  12. Guo, T.; Wei, J.Q.; Ma, J.P. Antitussive and expectorant activities of Potentilla anserina. Pharm. Biol. 2016, 54, 807–811. [Google Scholar] [CrossRef] [Green Version]
  13. Yang, D.; Han, N.; Wang, Y.W.; Zhai, J.X.; Liu, Z.H.; Li, S.K.; Yin, J. Pentacyclic triterpenoid saponins, poterinasides A–J, from Silverweed Cinquefoil Roots promising hepatoprotective and anti-inflammatory Agents. J. Org. Chem. 2021, 86, 11220–11236. [Google Scholar] [CrossRef]
  14. Wu, J.; Zhang, Z.Q.; Yu, H.H.; Huang, F.B.; Chen, Z.L.; Chu, L.L.; Wang, W. Research progress on chemical constituents and pharmacological activities of Potentilla. China J. Chin. Mater. Med. 2022, 47, 1509–1538. [Google Scholar]
  15. Wu, J.; Zhang, Z.Q.; Zhou, X.D.; Yao, Q.Y.; Chen, Z.L.; Chu, L.L.; Yu, H.H.; Yang, Y.P.; Li, B.; Wang, W. New terpenoids from Potentilla freyniana Bornm. and their cytotoxic activities. Molecules 2022, 27, 3665. [Google Scholar] [CrossRef] [PubMed]
  16. Gan, X.L.; Li, S.M.; Zong, Y.; Cao, D.; Li, Y.; Liu, R.J.; Cheng, S.; Liu, B.L.; Zhang, H.G. Chromosome-level genome assembly provides new insights into genome evolution and tuberous root formation of Potentilla anserina. Genes 2021, 12, 1993. [Google Scholar] [CrossRef] [PubMed]
  17. Summers, C.; Karst, F.; Charles, A.D. Cloning, expression and characterisation of the cDNA encoding human hepatic squalene synthase, and its relationship to phytoene synthase. Gene 1993, 136, 185–192. [Google Scholar] [CrossRef]
  18. Birchler, J.A.; Yang, H. The multiple fates of gene duplications: Deletion, hypofunctionalization, subfunctionalization, neofunctionalization, dosage balance constraints, and neutral variation. Plant Cell 2022, 34, 2466–2474. [Google Scholar] [CrossRef] [PubMed]
  19. Zhang, T.C.; Qiao, Q.; Du, X.; Zhang, X.; Hou, Y.; Wei, X.; Sun, C.; Zhang, R.G.; Yun, Q.Z.; Crabbe, M.C.; et al. Cultivated hawthorn (Crataegus pinnatifida var. major) genome sheds light on the evolution of Maleae (apple tribe). J. Integr. Plant Biol. 2022, 64, 1487–1501. [Google Scholar] [CrossRef] [PubMed]
  20. Zhou, Y.F.; Minio, A.; Massonnet, M.; Solares, E.; Lv, Y.D.; Beridze, T.; Cantu, D. The population genetics of structural variants in grapevine domestication. Nat. Plants 2019, 5, 965–979. [Google Scholar] [CrossRef]
  21. Shulaev, V.; Sargent, D.J.; Crowhurst, R.N.; Mockler, T.C.; Folkerts, O.; Delcher, A.L.; Jaiswal, P.; Mockaitis, K.; Liston, A.; Mane, S.P.; et al. The genome of woodland strawberry (Fragaria vesca). Nat. Genet. 2011, 43, 109–116. [Google Scholar] [CrossRef]
  22. Chen, F.; Su, L.Y.; Hu, S.Y.; Xue, J.Y.; Liu, H.; Liu, G.H.; Jiang, Y.F.; Du, J.K.; Qiao, Y.S.; Fan, Y.N.; et al. A chromosome-level genome assembly of rugged rose (Rosa rugosa) provides insights into its evolution, ecology, and floral characteristics. Hortic. Res. 2021, 8, 141. [Google Scholar] [CrossRef] [PubMed]
  23. Hua, W.P.; Kong, W.W.; Cao, X.Y.; Chen, C.; Liu, Q.; Li, X.M.; Wang, Z.Z. Transcriptome analysis of Dioscorea zingiberensis identifies genes involved in diosgenin biosynthesis. Genes Genom. 2017, 39, 509–520. [Google Scholar] [CrossRef]
  24. Song, Y.D.; Chen, S.; Wang, X.J.; Zhang, R.; Tu, L.C.; Hu, T.Y.; Liu, X.H.; Zhang, Y.F.; Huang, L.Q.; Gao, W. A novel strategy to enhance terpenoids production using cambial meristematic cells of Tripterygium wilfordii Hook. f. Plant Methods 2019, 15, 129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Guan, H.Y.; Su, P.; Zhao, Y.J.; Zhang, X.N.; Dai, Z.B.; Guo, J.; Tong, Y.R.; Liu, Y.J.; Hu, T.Y.; Yin, Y.; et al. Cloning and functional analysis of two sterol-C24-methyltransferase 1 (SMT1) genes from Paris polyphylla. J. Asian Nat. Prod. Res. 2018, 20, 595–604. [Google Scholar] [CrossRef]
  26. Lu, Y.D.; Zhou, W.X.; Wei, L.; Li, J.; Jia, J.; Li, F.; Smith, S.M.; Xu, J. Regulation of the cholesterol biosynthetic pathway and its integration with fatty acid biosynthesis in the oleaginous microalga Nannochloropsis oceanica. Biotechnol. Biofuels 2014, 7, 81. [Google Scholar] [CrossRef] [Green Version]
  27. Christ, B.; Xu, C.C.; Xu, M.L.; Li, F.S.; Wada, N.; Mitchell, A.J.; Han, X.L.; Wen, M.L.; Fujita, M.; Weng, J.K. Repeated evolution of cytochrome P450-mediated spiroketal steroid biosynthesis in plants. Nat. Commun. 2019, 10, 3206. [Google Scholar] [CrossRef] [Green Version]
  28. Xue, Z.Y.; Tan, Z.W.; Huang, A.C.; Zhou, Y.; Sun, J.C.; Wang, X.N.; Thimmappa, R.B.; Stephenson, M.J.; Osbourn, A.; Qi, X.Q. Identification of key amino acid residues determining product specificity of 2,3-oxidosqualene cyclase in Oryza species. New Phytol. 2018, 218, 1076–1088. [Google Scholar] [CrossRef] [Green Version]
  29. Sun, J.C.; Xu, X.; Xue, Z.Y.; Snydera, J.H.; Qi, X.Q. Functional analysis of a rice oxidosqualene cyclase through total gene synthesis. Mol. Plant 2013, 6, 1726–1729. [Google Scholar] [CrossRef] [Green Version]
  30. Lu, J.J.; Luo, M.F.; Wang, L.; Li, K.P.; Yu, Y.Y.; Yang, W.F.; Gong, P.C.; Gao, H.H.; Li, Q.R.; Zhao, J.; et al. The Physalis floridana genome provides insights into the biochemical and morphological evolution of Physalis fruits. Hortic. Res. 2021, 8, 244. [Google Scholar] [CrossRef]
  31. Buti, M.; Moretto, M.; Barghini, E.; Mascagni, F.; Natali, L.; Brilli, M.; Lomsadze, A.; Sonego, P.; Giongo, L.; Alonge, M.; et al. The genome sequence and transcriptome of Potentilla micrantha and their comparison to Fragaria vesca (the woodland strawberry). GigaScience 2018, 7, giy010. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. Edger, P.P.; VanBuren, R.; Colle, M.; Poorten, T.J.; Wai, C.M.; Niederhuth, C.E.; Alger, E.I.; Ou, S.; Acharya, C.B.; Wang, J.; et al. Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry (Fragaria vesca) with chromosome-scale contiguity. GigaScience 2018, 7, gix124. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Shirasawa, K.; Itai, A.; Isobe, S. Chromosome-scale genome assembly of Japanese pear (Pyrus pyrifolia) variety ‘Nijisseiki’. DNA Res. 2021, 28, dsab001. [Google Scholar] [CrossRef] [PubMed]
  34. Birney, E.; Clamp, M.; Durbin, R. GeneWise and genomewise. Genome Res. 2004, 14, 988–995. [Google Scholar] [CrossRef] [Green Version]
  35. Savojardo, C.; Martelli, P.L.; Fariselli, P.; Profiti, G.; Casadio, R. BUSCA: An integrative web server to predict subcellular localization of proteins. Nucleic Acids Res. 2018, 46, W459–W466. [Google Scholar] [CrossRef]
  36. Edgar, R.C.; Batzoglou, S. Multiple sequence alignment. Curr. Opin. Struct. Biol. 2006, 16, 368–373. [Google Scholar] [CrossRef]
  37. Minh, B.Q.; Schmidt, H.A.; Chernomor, O.; Schrempf, D.; Woodhams, M.D.; Haeseler, A.; Lanfear, R. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Bio. Evol. 2020, 37, 1530–1534. [Google Scholar] [CrossRef] [Green Version]
  38. Pertea, M.; Kim, D.; Pertea, G.M.; Leek, J.T.; Salzberg, S.L. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat. Protoc. 2016, 11, 1650–1667. [Google Scholar] [CrossRef]
  39. Xue, Z.Y.; Xu, X.; Zhou, Y.; Wang, X.M.; Zhang, Y.C.; Liu, D.; Zhao, B.B.; Duan, L.X.; Qi, X.Q. Deficiency of a triterpene pathway results in humidity-sensitive genic male sterility in rice. Nat. Commun. 2018, 9, 604. [Google Scholar] [CrossRef] [Green Version]
  40. Inagaki, Y.S.; Etherington, G.; Geisler, K.; Field, B.; Dokarry, M.; Ikeda, K.; Mutsukado, K.; Dicks, J.; Osbourn, A. Investigation of the potential for triterpene synthesis in rice through genome mining and metabolic engineering. New Phytol. 2011, 191, 432–448. [Google Scholar] [CrossRef]
  41. Sun, R.; Liu, S.; Tang, Z.Z.; Zheng, T.R.; Wang, T.; Chen, H.; Li, C.L.; Wu, Q. β-Amyrin synthase from Conyza blinii expressed in Saccharomyces cerevisiae. FEBS Open Bio. 2017, 7, 1575–1585. [Google Scholar] [CrossRef] [PubMed]
  42. Su, W.B.; Jing, Y.; Lin, S.K.; Yue, Z.; Yang, X.H.; Xu, J.B.; Wu, J.C.; Zhang, Z.K.; Rui, X.; Zhu, J.J.; et al. underlies co-option and diversification of biosynthetic triterpene pathways in the apple tribe. Proc. Natl. Acad. Sci. USA 2021, 118, e2101767118. [Google Scholar] [CrossRef]
  43. Busquets, A.; Keim, V.; Closa, M.; Arco, A.; Boronat, A.; Arró, M.; Ferrer, A. Arabidopsis thaliana contains a single gene encoding squalene synthase. Plant Mol. Biol. 2008, 67, 25–36. [Google Scholar] [CrossRef]
  44. Daccord, N.; Celton, J.M.; Linsmith, G.; Becker, C.; Choisne, N.; Schijlen, E.; Geest, H.; Bianco, L.; Micheletti, D.; Velasco, R.; et al. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat. Genet. 2017, 49, 1099–1106. [Google Scholar] [CrossRef] [PubMed]
  45. Manavalan, L.P.; Chen, X.; Clarke, J.; Salmeron, J.; Nguyen, H.T. RNAi-mediated disruption of squalene synthase improves drought tolerance and yield in rice. J. Exp. Bot. 2012, 63, 163–175. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. The French–Italian Public Consortium for Grapevine Genome Characterization. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007, 449, 463–467. [Google Scholar] [CrossRef] [Green Version]
  47. Shen, L.Y.; Luo, H.; Wang, X.L.; Wang, X.M.; Qiu, X.J.; Liu, H.; Zhou, S.S.; Jia, K.H.; Nie, S.; Bao, Y.T.; et al. Chromosome-scale genome assembly for Chinese sour jujube and insights into its genome evolution and domestication signature. Front. Plant Sci. 2021, 12, 773090. [Google Scholar] [CrossRef]
  48. Lang, D.; Ullrich, K.K.; Murat, F.; Fuchs, J.; Jenkins, J.; Haas, F.; Piednoel, M.; Gundlach, H.; Bel, M.; Meyberg, R.; et al. The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. Plant J. 2018, 93, 515–533. [Google Scholar] [CrossRef] [Green Version]
  49. Wang, X.; Chen, D.J.; Wang, Y.Q.; Xie, J. De novo transcriptome assembly and the putative biosynthetic pathway of steroidal sapogenins of Dioscorea composita. PLoS ONE 2015, 10, e0124560. [Google Scholar] [CrossRef] [Green Version]
  50. Minx, P.; Cordum, H.; Wilson, R. Sequence, annotation, and analysis of synteny between rice chromosome 3 and diverged grass species. Genome Res. 2005, 15, 1284–1291. [Google Scholar]
  51. Laranjeira, S.; Amorim-Silva, V.; Esteban, A.; Arró, M.; Ferrer, A.; Tavares, R.M.; Botella, M.A.; Rosado, A.; Azevedo, H. Arabidopsis squalene epoxidase 3 (SQE3) complements SQE1 and is important for embryo development and bulk squalene epoxidase activity. Mol. Plant 2015, 8, 1090–1102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  52. Lin, X.; Kaul, S.; Rounsley, S.; Shea, T.; Benito, M.; Town, C.; Fujii, C.; Mason, T.; Bowman, C.; Barnstead, M.; et al. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 1999, 402, 761–768. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Zhang, L.; Cai, X.; Wu, J.; Liu, M.; Grob, S.; Cheng, F.; Liang, J.L.; Cai, C.C.; Liu, Z.Y.; Liu, B.; et al. Improved Brassica rapa reference genome by single-molecule sequencing and chromosome conformation capture technologies. Hortic. Res. 2018, 5, 50. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Varshney, R.K.; Chen, W.; Li, Y.; Bharti, A.; Saxena, R.; Schlueter, J.; Donoghue, M.; Azam, S.; Fan, G.; Whaley, A.; et al. Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat. Biotechnol. 2012, 30, 83. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Schmutz, J.; Cannon, S.B.; Schlueter, J.; Ma, J.X.; Mitros, T.; Nelson, W.; Hyten, D.; Song, Q.J.; Thelen, J.; Cheng, J.L.; et al. Genome sequence of the palaeopolyploid soybean. Nature 2010, 463, 178–183. [Google Scholar] [CrossRef] [Green Version]
  56. Nakayasu, M.; Shioya, N.; Shikata, M.; Thagun, C.; Abdelkareem, A.; Okabe, Y.; Ariizumi, T.; Arimura, G.; Mizutani, M.; Ezura, H.; et al. JRE4 is a master transcriptional regulator of defense-related steroidal glycoalkaloids in tomato. Plant J. 2018, 94, 975–990. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Molecules 28 02782 g001 550
Figure 1. The phylogenetic relationship (A), gene expression (B), and conserved domain (C) of SQSs/SQEs/OSCs from Potentilla anserina (Pan). (A) The phylogenetic tree of SQEs (clades I and II), the phylogenetic tree of OSCs (clades III and IV), and the phylogenetic tree of SQSs (clades V and VI). (B) The expression level of SQSs/SQEs/OSCs in the tissue of tuberous root (T1–T3) and root (R1–R3) yields. (C) The conserved domains of SQSs/SQEs/OSCs. (D) The correction of the HBP method to Pfam analysis. New copy: a new copy of genes was obtained by the HBP method; Refined: genes were adjusted; Merged: multiple genes were merged into a complete gene; Split: one gene was split into multiple genes.
Figure 1. The phylogenetic relationship (A), gene expression (B), and conserved domain (C) of SQSs/SQEs/OSCs from Potentilla anserina (Pan). (A) The phylogenetic tree of SQEs (clades I and II), the phylogenetic tree of OSCs (clades III and IV), and the phylogenetic tree of SQSs (clades V and VI). (B) The expression level of SQSs/SQEs/OSCs in the tissue of tuberous root (T1–T3) and root (R1–R3) yields. (C) The conserved domains of SQSs/SQEs/OSCs. (D) The correction of the HBP method to Pfam analysis. New copy: a new copy of genes was obtained by the HBP method; Refined: genes were adjusted; Merged: multiple genes were merged into a complete gene; Split: one gene was split into multiple genes.
Molecules 28 02782 g001
Molecules 28 02782 g002 550
Figure 2. SQS/SQE/OSC locations on the Potentilla anserina (Pan) chromosomes. A Sub-genome (up, A1–A7), B sub-genome (bottom, B1–B7).
Figure 2. SQS/SQE/OSC locations on the Potentilla anserina (Pan) chromosomes. A Sub-genome (up, A1–A7), B sub-genome (bottom, B1–B7).
Molecules 28 02782 g002
Molecules 28 02782 g003 550
Figure 3. The phylogenetic tree of SQSs and SQEs. SQSs and SQEs of Potentilla anserina (Pan), Fragaria vesca (Fve), and Rosa rugosa (Rru) were included in the phylogenetic tree. Clade I to clade IV included genes of SQEs; the right clade was SQSs.
Figure 3. The phylogenetic tree of SQSs and SQEs. SQSs and SQEs of Potentilla anserina (Pan), Fragaria vesca (Fve), and Rosa rugosa (Rru) were included in the phylogenetic tree. Clade I to clade IV included genes of SQEs; the right clade was SQSs.
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Molecules 28 02782 g004 550
Figure 4. Phylogenetic tree of OSCs. OSCs of Potentilla anserina (Pan), Potentilla micrantha (Pmi), Fragaria vesca (Fve), Rosa rugosa (Rru), Pyrus pyrifolia (Ppy), Vitis vinifera (Vvi), Arabidopsis thaliana (Ath), and Oryza sativa (Osa) were included in the phylogenetic tree. PS: parkeol synthase, LUS: lupeol synthase, LAS: lanosterol synthase, β-AS: beta-amyrin synthase, CAS: cycloartenol synthase, CAMS: camelliol C synthase, ACBS: achilleol B synthase.
Figure 4. Phylogenetic tree of OSCs. OSCs of Potentilla anserina (Pan), Potentilla micrantha (Pmi), Fragaria vesca (Fve), Rosa rugosa (Rru), Pyrus pyrifolia (Ppy), Vitis vinifera (Vvi), Arabidopsis thaliana (Ath), and Oryza sativa (Osa) were included in the phylogenetic tree. PS: parkeol synthase, LUS: lupeol synthase, LAS: lanosterol synthase, β-AS: beta-amyrin synthase, CAS: cycloartenol synthase, CAMS: camelliol C synthase, ACBS: achilleol B synthase.
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Table
Table 1. HBP predictions of SQSs, SQEs, and OSCs in four species.
Table 1. HBP predictions of SQSs, SQEs, and OSCs in four species.
Resource aPanFveRruPpy
Total gene numbers52212024
New copies3100
Refined genes3022
Merged genes 3002
Split genes0210
Correct rates17.3%14.2%15.0%16.6%
a The data in Table 1 are summarized from Table S3.
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Jiao, Y.; Li, X.; Huang, X.; Liu, F.; Zhang, Z.; Cao, L. The Identification of SQS/SQE/OSC Gene Families in Regulating the Biosynthesis of Triterpenes in Potentilla anserina. Molecules 2023, 28, 2782. https://doi.org/10.3390/molecules28062782

AMA Style

Jiao Y, Li X, Huang X, Liu F, Zhang Z, Cao L. The Identification of SQS/SQE/OSC Gene Families in Regulating the Biosynthesis of Triterpenes in Potentilla anserina. Molecules. 2023; 28(6):2782. https://doi.org/10.3390/molecules28062782

Chicago/Turabian Style

Jiao, Yangmiao, Xu Li, Xueshuang Huang, Fan Liu, Zaiqi Zhang, and Liang Cao. 2023. "The Identification of SQS/SQE/OSC Gene Families in Regulating the Biosynthesis of Triterpenes in Potentilla anserina" Molecules 28, no. 6: 2782. https://doi.org/10.3390/molecules28062782

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