Skip to main content
Download PDF

Chloroplast genome sequence of triploid Toxicodendron vernicifluum and comparative analyses with other lacquer chloroplast genomes

BMC Genomics volume 24, Article number: 56 (2023) Cite this article

Abstract

Background

Toxicodendron vernicifluum, belonging to the family Anacardiaceae, is an important commercial arbor species, which can provide us with the raw lacquer, an excellent adhesive and painting material used to make lacquer ware. Compared with diploid, triploid lacquer tree has a higher yield of raw lacquer and stronger resistance to stress. Triploid T. vernicifluum was a newly discovered natural triploid lacquer tree. However, the taxonomy of triploid T. vernicifluum has remained uncertain. Here, we sequenced and analyzed the complete chloroplast (cp) genome of triploid T. vernicifluum and compared it with related species of Toxicodendron genus based on chloroplast genome and SSR markers.

Results

The plastome of triploid T. vernicifluum is 158,221 bp in length, including a pair of inverted repeats (IRs) of 26,462 bp, separated by a large single-copy region of 86,951 bp and a small single-copy region of 18,346 bp. In total, 132 genes including 87 protein-coding genes, 37 tRNA genes and 8 rRNA genes were identified in the triploid T. vernicifluum. Among these, 16 genes were duplicated in the IR regions, 14 genes contain one intron, while three genes contain two introns. After nucleotide substitutions, seven small inversions were analyzed in the chloroplast genomes, eight hotspot regions were found, which could be useful molecular genetic markers for future population genetics. Phylogenetic analyses showed that triploid T. vernicifluum was a sister to T. vernicifluum cv. Dahongpao and T. vernicifluum cv. Hongpigaobachi. Moreover, phylogenetic clustering based on the SSR markers showed that all the samples of triploid T. vernicifluum, T. vernicifluum cv. Dahongpao and T. vernicifluum cv. Hongpigaobachi in one group, while the samples of T. vernicifluum and T. succedaneum in another group, which is consistent with the cp genome and morphological analysis.

Conclusions

The current genomic datasets provide pivotal genetic resources to determine the phylogenetic relationships, variety identification, breeding and resource exploitation, and future genetic diversity-related studies of T. vernicifluum.

Peer Review reports

Background

Polyploidy, that is having multiple sets of chromosomes as a consequence of whole-genome duplication, is common in nature and provides a major mechanism for adaptation and speciation [1, 2]. The polyploidy genotypes may lead to differences in morphology, physiology and molecular characteristics, etc [3]. Toxicodendron vernicifluum, belonging to the family Anacardiaceae, is a deciduous tree species with a toxic sap [4]. The resin and sap which was extracted from lacquer trees were used as paint for culture assets and lacquer wares, making it a natural material of cultural and social significance [5,6,7]. In addition, lacquer tree is also used as a food additive, natural dye, or in herbal medicine to improve blood circulation and to prevent blood stasis, while the metabolic extract of the leaves has neuroprotective and anti-inflammatory activity [8]. The economic value of different varieties of lacquer can be judged by lacquer yield, the growth rate of lacquer and genetic diversity [9].

Compared with the diploid lacquer tree, the triploid lacquer tree has a higher yield of raw lacquer and stronger resistance to stress [10]. T. vernicifluum cv. Dahongpao (2n=3x=45) was the first nature triploid lacquer tree which was discovered at Bashan Mountain in Shaanxi Province, China and now is widely introduced into the planting area of lacquer tree [11, 12]. Han et al [13] determined the pseudo-polyploidy of T. vernicifluum was a natural triploid lacquer (2n=3x=45) by observation of the stomatal characteristic of leaf lower epidermis, analysis of lower epidermis, flow cytometry and measurement of genome size, and it was named as triploid T. vernicifluum. However, as an economic tree species, T. vernicifluum has been widely introduced and cultivated [14], which lead to the taxonomy classification was difficult to resolve because of considerable phenotypic variability with overlapping morphologies.

Chloroplast (cp) genomes have assembled notable contributions in diverse plant families, setting evolutionary within phylogenetic clades [15,16,17], because the lack of recombination and maternal transmission means the chloroplast genome is also useful for tracking source populations [18,19,20] and chloroplast genomes variation could provide valuable genetic markers for the analysis of polyploids [21]. In addition, the cp genome plays an important role in reconstruction of the plant phylogeny and understanding the origins of economically important cultivated species and changes that have taken place during domestication [22]. Microsatellites are powerful markers to detect genetic variation, because of their high mutation rate and high polymorphism, allowing us to distinguish between closely related individuals, and thus to assess parentage and kinship relationships [23].

In this study, we reported the characteristics of the complete chloroplast genome sequences of triploid T. vernicifluum for the first time and compared with other Toxicodendron cp genomes to investigate the relationship among chloroplast genome. To understand the relationships of the triploid T. vernicifluum, we constructed the phylogenetic tree using their fully sequenced chloroplast genome sequenced and SSR molecular markers. The results will provide a theoretical basis for variety identification, breeding and resource exploitation.

Results

Morphological traits of five Toxicodendron accessions

The leaf length, leaflet number, leaflet length and leaflet width were compared among the five accessions (Table 1), the results showed that the leaf length of triploid T. vernicifluum (TZT) was significantly higher than other four accessions. The leaflet number, leaflet length and leaflet width were significantly lower than T. vernicifluum cv. Dahongpao (DHP) and T. vernicifluum cv. Hongpigaobachi (GBC), and higher than T. vernicifluum (TZG) and T. succedaneum (TRB). The leaf shape index of TZT, DHP and GBC (2.03, 2.11 and 2.18, respectively) were lower than TZG (3.21) and TRB (3.31). In addition, all the morphological traits both showed that there were no significant difference between T. vernicifluum cv. Dahongpao (DHP) and T. vernicifluum cv. Hongpigaobachi (GBC).

Table 1 Leaf morphological characteristics of five Toxicodendron accessions
Full size table

General features of Toxicodendron chloroplast genome

The results showed that the cp genomes of triploid T. vernicifluum (TZT), T. vernicifluum cv. Hongpigaobachi (GBC), T. succedaneum (TRB) and T. vernicifluum (TZG) have a typical circular tetramerous structure like other related plants [24, 25], with a genome size of 158,221 bp, 159,571 bp, 159,636 bp and 159,710 bp, respectively. Both the cp genomes comprised of four distinctive parts in which the LSC (86,951 bp, 87,475 bp, 87,523 bp and 87,636 bp) and SSC (18, 346 bp, 19,074 bp, 19,045 bp and 19, 041 bp) are separated by two IRs (26,462 bp, 26,511 bp, 26,534 bp and 26,525 bp) (Fig. 1, Table 2).

Fig. 1
figure 1

Gene map of the four new sequenced Toxicodendron cp genomes. Genes shown outside the outer circle are transcribed clockwise and those inside are transcribed counterclockwise. Genes belonging to different functional groups are color-coded. The dashed area in the inner circle indicates the GC content of the cp genome of Toxicodendron

Full size image
Table 2 Features of ten Toxicodendron cp genomes
Full size table

The four cp genomes were analyzed and compared with T. succedaneum (Ts), T. griffithii (Tg), T. sylvestre (Tsy), T. diversilobum (Tdi), and T. vernicifluum cv. Yanggangdamu (Tyg) which belong to the same genus. The nine Toxicodendron cp genomes have minor differences in length, except TZT. The size of these cp genomes ranges from 158,221 bp (TZT) to 159,710 bp (TZG and Ts). The size of the IR region ranges from 26,462 bp (TZT) to 26,534 bp (TRB), while the SSC and LSC size varies from 18,346 bp (TZT) to 19,074 bp (DHP, GBC and Tyg) and from 86,951 bp (TZT) to 87,693 bp (Tdi) (Table 2). The overall GC content in the whole genome sequences was practically identical among these plastomes (37.9-38.0%). Furthermore, the GC contents are unevenly distributed across regions of the cp genome, which were found 36.0-36.1%, 42.9-43.0% and 32.4-32.7% for the LSC, IR and SSC regions, respectively (Table 2).

The ten Toxicodendron cp genomes encoded the same 132 functional genes, consisting of 87 protein-coding genes, 8 rRNA genes and 37 tRNA genes and a total of 16 genes were duplicated in the IR regions (Table 2 and Table S1). For both accessions, 14 genes (atpF, ndhA, ndhB, petB, petD, rpl2, rpl16, rpoC1, rps16, trnA-UGC, trnG-UCC, trnI-GAU, trnL-UAA and trnV-GAC) contain one intron, while three genes (clpP, rps12 and ycf3) contain two introns (Table S1)

SSR polymorphisms and long repeat analyses

The number of cp genome SSRs (cpSSRs) ranged from 52 to 70 among the ten Toxicodendron plastomes (Table 3). The number of cpSSRs in the four accessions TZT, DHP, GBC and Tyg were similar (52), and the numbers of cpSSRs in TZG (70) was the same as that in Tsy (70). The mononucleotide repeat (P1) number with the highest variability ranged from 45 (TZT) to 60 (TZG and Tsy), and most of the P1s were composed of poly A and T repeats. Dinucleotide (P2) repeat sequences in the ten accessions were AT or TA repeats. Only one pentanucleotide (P5) repeat was detected in Tdi. Within the ten plastomes, SSR loci were primarily in the LSC region (Table 3 and Table S2). In addition, 6 (TRB, TZG, Ts and Tsy) and 7 (TZT, DHP, GBC, Tg, Tdi and Tsy) SSR loci were detected in the protein-coding genes rpoC2, atpB, ycf1, ndhI (only in DHP, GBC and Tyg) and ndhF (only in Tg), other situated in intergenic spacers and introns (Table S2)

Table 3 Simple sequence repeats (SSRs) in the ten Toxicodendron cp genomes
Full size table

In the ten Toxicodendron plastomes, four repeat types were detected using REputer software (Fig. 2A). We found 50 repeats in DHP (22 F, 1R, 1 C and 26 P), GBC (22 F, 1R, 1 C and 26 P) and Tyg (21 F, 1R, 1 C and 27 P), which was lower than those found in the other seven accessions. 52 repeat (22 F, 1 C and 29 P) was found in the plastomes of TZT. In addition, the majority of repeats varied from 30 to 39 bp in length (Fig. 2B).

Fig. 2
figure 2

Comparison of long repeats among ten Toxicodendron cp genomes. A Number of repeats, P: palindromic repeats, R: reverse repeats, C: complement repeats, F: forward repeats. B Frequency of each type by length

Full size image

IR expansion and contraction

Although cp genomes are highly conserved in terms of genomic structure and size, the IR/SC junction position change caused by expansion and contraction of the IR/SC boundary regions was usually considered as a primary mechanism in creating the length variation of the higher plant cp genomes [26, 27]. The border regions of the ten Toxicodendron cp genomes were compared. The IR regions’ lengths correlate across all the compared cp genomes with only slight expansion and contraction (Fig. 3), ranged from 26,462 bp (TZT) to 26,534 bp (TRB) in size, of which rps19, rpl2, ycf1, ndhF and trnH genes were present at the junctions of the LSC/IR and SSC/IR borders. At the LSC/IRb junction (JLB), the gene rps19 in the LSC of TZT, DHP, GBC, TRB, TZG, Ts, Tg, Tsy and Tdi contracted 71 to125 bp, whereas Tyg extended 4 bp into the IR region. The gene rpl2 in the IRa region also contracted by a different number of bases (65-103 bp). The distance between trnH and JLA is 11-64 bp. In contrast, the SSC/IR boundary regions were relatively stable. The ycf1 gene is located at the IRa/SSC (JSA) border in the ten cp genomes, and the junctions of IRa/SSC (JSA) located in ycf1 within the SSC and IRa regions almost had the same length. The gene ycf1 in the IRb region and gene ndhF in the SSC region interlaced at the IRb/SSC (JSB) border and ycf1 in the SSC region was astride the border of SSC/IRa (JSA).

Fig. 3
figure 3

Comparison of the LSC, IR, SSC junction positions among ten Toxicodendron cp genomes. JLB: junction of LSC and IRb; JSB: junction of SSC and IRb; JSA: junction of SSC and IRa; JLA: junction of LSC and IRa. Boxes above and below the mainline indicate the adjacent border genes. The gaps between the genes and the boundaries are indicated by the base lengths (bp)

Full size image

Comparative analysis of genome structure

To investigate the intergeneric divergence of cp genome sequences, the percentage of identity was plotted for ten Toxicodendron accessions using mVISTA program with DHP as a reference. The alignment revealed high sequence similarity across the ten cp genomes and no rearrangement occurred (Fig. 4), which suggests that they are highly conserved.

Fig. 4
figure 4

Identity plots comparing the cp genomes of ten Toxicodendron accessions using T. vernicifluum cv. Dahongpao as a reference sequence. The vertical scale indicates the percentage of identity, ranging from 50 to 100%. The horizontal axis indicates the coordinates within the cp genome. Genome regions are color coded as protein-coding, rRNA, tRNA, intron, and conserved non-coding sequences (CNS)

Full size image

The cp genome sequences of the ten Toxicodendron accessions were aligned by MAUVE, and DHP was used as a reference to compare the gene orders among these cp genomes (Fig. 5). The results showed that all sequences show perfect synteny conservation with no inversion or rearrangements.

Fig. 5
figure 5

MAUVE alignment of ten Toxicodendron accessions cp genomes. The T. vernicifluum cv. Dahongpao genome is shown at the top as the reference genome. Within each of the alignments, local collinear blocks are represented by blocks of the same color connected by lines

Full size image

The nucleotide variability (Pi) values of the ten cp genomes were calculated with the DnaSP software. A total of 1794 polymorphic sites were detected and the Pi values ranged from 0.0000 to 0.0240, with the mean of 0.0037. Eight hotspots (Pi>0.0120) were uncovered among the ten cp genomes. They are four intergenic spacers (trnH-psbA, trnK-rps16, ycf4-cemA, petL-psbJ) from the LSC region, three intergenic spacers (ndhF-rpl32, trnL-ndhD and ndhD-ndhE) and one gene regions (ycf1) from the SSC regions (Fig. 6). The results indicated that the non-coding regions exhibited more variations than the coding regions. The sequences of these highly variable regions could be developed as barcodes for species identification, phylogenetic analysis, and population genetics research in Toxicodendron.

Fig. 6
figure 6

Sliding window analysis of the whole cp genomes of ten Toxicodendron accessions. Window length: 600 bp, step size: 200 bp. X-axis, the position of the midpoint of a window; Y-axis, nucleotide diversity of each window

Full size image

We investigated SNPs, the most abundant type of mutation, in the ten cp genomes, with T. vernicifluum cv. Dahongpao (DHP) as the reference. In the gene-coding regions, we detected two SNPs in the comparative combination of GBC-DHP, including one transition (Ts) and one transversion (Tv) SNPs, one Ts were detected in Tyg-DHP, as well as 121 (67 Ts and 54 Tv), 227 (114 Ts and 113 Tv), 102 (46 Ts and 56 Tv), 239 (119 Ts and 120 Tv), 209 (111 Ts and 98 Tv), 244 (124 Ts and 120 Tv) and 199 (95 Ts and 104 Tv) SNPs were detected in the combinations of TZT-DHP, TZG-DHP, TRB-DHP, Ts-DHP, Tg-DHP, Tsy-DHP and Tdi-DHP (Table 4). Furthermore, 5 (4 Ts and 1 Tv), 260 (96 Ts and 164 Tv), 462 (181 Ts and 281 Tv), 126 (10 Ts and 116 Tv), 462 (177 Ts and 285Tv), 430 (145 Ts and 285 Tv), 463 (181 Ts and 282 Tv), 324 (118 Ts and 206Tv) and 1 (1 Tv) SNPs were detected in noncoding regions among the nine comparative combinations, respectively (Table S3).

Table 4 Transitions (Ts) and transversions (Tv) in the protein-coding regions of the nine plastomes, compared with DHP
Full size table

It has been reported that each small inversion is commonly associated with a hairpin secondary structure in the chloroplast genomes [26, 28]. Small inversions are generally detected by performing pairwise comparisons between sequences of closely related taxa [26]. Seven small inversions were identified in the Toxicodendron cp genomes and their inverted repeating flanking sequences formed stem-loop structures (Fig. 7). All the inversions were located in noncoding regions including 6 in intergenic spacers (ccsA-ndhD, trnS-psbZ, atpF-atpH, trnW-trnP, trnG-trnR and trnQ-psbK) and one in intron regions (rpl16 intron). Among the seven small inversions, six were located in LSC region, one in SSC region (rpl16 intron). The small inversions from trnW-trnP occurred only in DHP, GBC, TZT and Tyg. The small inversions from atpF-atpH, trnW-trnP, trnG-trnR and trnQ-psbK and rpl16 intron have been occurred in DHP, GBC and TZT.

Fig. 7
figure 7

Predicted hairpin loops of small inversions in the ten plastomes of Toxicodendron. The arrows in the figure indicate the break points in inversion events

Full size image

Phylogenetic analysis based on the chloroplast complete genome and SSR molecular markers

To identified the phylogenetic position of triploid T. vernicifluum in Toxicodendron, we used 12 cp genomes to phylogenetic analyse. Maximum likelihood (ML) and Bayesian inference (BI) were used to construct phylogenetic tree with Pistacia weinmaniifolia and Mangifera indica as outgroup (Fig. 8). The topologies of the ML and BI trees were nearly identical, which both showed that Toxicodendron species formed a monophyletic clade (BS=100, PP=1). The ten Toxicodendron species were divided into two main clades. Clade I contained six accessions (T. vernicifluum cv. Dahongpao, T. vernicifluum cv. Hongpigaobachi, T. vernicifluum cv. Yanggangdamu, triploid T. vernicifluum, T. diversilobum and T. griffithii) and the results showed that T. vernicifluum cv. Dahongpao is closely related to T. vernicifluum cv. Hongpigaobachi and sister to triploid T. vernicifluum and T. vernicifluum cv. Yanggangdamu. Clade II consists of T. succedaneum (MT211614), T. vernicifluum, T. sylvestre and T. succedaneum (OP235437). The phylogenetic tree was very helpful for us to understand the phylogenetic relationship among more Toxicodendron species.

Fig. 8
figure 8

Phylogeny of ten Toxicodendron accessions inferred from ML (A) and BI (B) analyses of different cp genome sequences. Numbers in the clade represent bootstrap (BP) and posterior probability (PP) values

Full size image

Genetic distance among the 15 samples was calculated according to the software GenoDive (Table S4) [29]. Based on Nei’s genetic distance coefficient, a dendrogram was obtained using UPGMA cluster analysis. With this result, two groups could be distinguished. The first group was further divided into two subgroups, three samples of T. succedaneum (T. succedaneum 1#, T. succedaneum 2# and T. succedaneum 3#) were included in subgroup 1, and the three samples of T. vernicifluum (T. vernicifluum 1#, 2# and 3#) were included in the subgroup II. Group II included three accessions of T. vernicifluum cv. Dahongpao, T. vernicifluum cv. Hongpigaobachi and triploid T. vernicifluum, and T. vernicifluum cv. Dahongpao was sister to triploid T. vernicifluum (Fig. 9).

Fig. 9
figure 9

Dendrogram generated by UPGMA from genetic distance data based on SSR markers

Full size image

Discussion

There are obvious differences in leaf morphology between diploid and polyploidy, which is one of the simpler methods to identify plant ploidy by morphological differences [30]. Leaf shape index (length/width) is an important parameter of leaf shape. The larger the leaf shape index of plant is, the longer and narrower the leaves are, while the smaller the leaf shape index is, the rounder the leaves are [31]. Liu et al [32] used the observational method and paraffin section technique to analyze the intraspecific differences in four kinds of Toxicodendron species and the results showed that the sharp differences presented in height, shape, bark and leaves of the four varieties. In this study, morphological traits of five Toxicodendron accessions were determined and the leaf length of triploid T. vernicifluum, T. vernicifluum cv. Dahongpao and T. vernicifluum cv. Hongpigaobachi were significantly higher than T. vernicifluum and T. succedaneum. Therefore, the morphological characteristics of diploid and triploid can be distinguished by the leaf shape characteristics [33]. In addition, all four morphological characteristics (leaf length, leaflet number, leaflet length and width) were shown that T. vernicifluum cv. Dahongpao and T. vernicifluum cv. Hongpigaobachi had no significant difference, and there were no significant difference between T. vernicifluum and T. succedaneum in the morphological traits of leaflet number, leaflet length and width. In conclusion, certain accessions are similar in terms of morphological characteristics.

The chloroplast genomes of plants are a valuable resource for developing molecular markers to study intra-species and interspecies evolution [34, 35]. In this study, we sequenced and annotated the cp genomes of four Toxicodendron accessions and compared their characteristics with those of six other related species from Toxicodendron. Like other angiosperms, Toxicodendron cp genome is a circular double-standed DNA molecular, exhibiting a conserved quadripartite structure [24, 25, 36], and the ten cp genomes were relatively conserved, which is consistent with the slow rates of sequence and structure evolution of plant plastomes [37, 38]. The cp genomes ranged from 158,221 bp (triploid T. vernicifluum) to 159,710 bp [T. vernicifluum and T. succedaneum (Ts)], with a difference in size of 1489 bp. Large variation in LSC length (742 bp) accounted for most of this genome-wide variation, which indicated that variation in genome length appears to be mainly caused by variation in LSC length [39]. The GC content of the ten Toxicodendron accessions ranged from 37.9-38.0%, which is closely related to species affinity [40]. High GC content is conducive to the stability of the genome and maintaining the complexity of the sequence. The four rRNAs genes have high GC content, which results are a high GC content in the IR regions [41]. Usually, a higher GC content indicated a more stable genome sequence [42].

The expansion and contraction of IR and SC boundaries are thought to be the main cause of CP genome size changes, although CP genomes in plants are highly conserved [37]. The change of the IR and SC junction is a common phenomenon and plays an important role in evolution [43, 44]. After comparing CP genomes among the ten Toxicodendron accessions in this study, changes in the IR (26,462-26,534 bp) and boundary between the IR and LSC or SSC of the cp genome of ten accessions were found to be small. Some variations were observed in these cp genomes, mainly due to variation in the LSC regions rather than contraction and expansion of IR region [45, 46]. Comparison between IR regions and the chloroplast genomes of T. vernicifluum cv. Dahongpao and T. vernicifluum cv. Hongpigaobachi showed similarity, which was the same as for the boundary gene of LSC/IRa, SSC/IRa and LSC/IRb regions and the size of genes and fragments in two adjacent regions. Therefore, we speculate that the genetic relationship between T. vernicifluum cv. Dahongpao and T. vernicifluum cv. Hongpigaobachi is closer than other accessions, and our subsequent phylogenetic analysis validates our inference.

Previous studies have shown that tRNA activity may be a key factor triggering the inversions events [47]. Small inversions in the cp genome of angiosperms are ubiquitous and commonly associated with a hairpin secondary structure and are generally detected by performing pairwise comparisons between sequences of closely related taxa [26]. Many small inversions are generated by parallel or back mutation events during chloroplast genome evolution [26, 48]. In the present study, seven small inversions were discovered based on the sequence alignment of the ten cp genomes and the inversion in ccsA-ndhD have been reported in other studies [16, 49,50,51]. trnW-trnP were specific in T. vernicifluum cv. Dahongpao and T. vernicifluum cv. Hongpigaobachi, triploid T. vernicifluum and T. vernicifluum cv. Yanggangdamu. The small inversions from atpF-atpH, trnW-trnP, trnG-trnR and trnQ-psbK and rpl16 intron have been occurred in T. vernicifluum cv. Dahongpao and T. vernicifluum cv. Hongpigaobachi and triploid T. vernicifluum. These small inversion regions will provide abundant information for marker development in phylogenetic analyses of related Toxicodendron species [48, 52, 53]. However, small inversions of noncoding sequences may influence sequence alignment and character interpretation in phylogeny reconstructions, so caution is necessary when using cp noncoding sequences for phylogenetic analysis [51, 54].

To solve phylogenetic problems at the species level, or to identify species using DNA barcodes, the high evolutionary rates regions were needed to identify [55]. Eight intergenic spacer regions including trnH-psbA, trnK-rps16, ycf4-cemA, petL-psbJ, ndhF-rpl32, trnL-ndhD, ndhD-ndhE and one gene regions ycf1 are highly variable regions in the Toxicodendron cp genome. These variable regions may also be useful for assessing phylogenetic relationships and interspecific differences of Toxicodendron species [56]. Among these, trnH-psbA, ycf4-cemA and ycf1 have been regarded as a candidate DNA barcodes for Toxicodendron and other plants [25, 55, 57].

Complete chloroplast genome provides sufficient information sites for resolving phylogenetic relationships of plant, and have been examined to be effective in the ability of differentiation in lower taxonomic levels and provide valuable data for resolving complex evolutionary relationships [58, 59]. Within the Anacardiaceae, Wang et al [25] indicated that T. vernicifluum cv. Yanggangdamu was more closely to R. chinensis and two Pistacia species, due to lack of more Toxicodendron cp genomes. In the current study, ten Toxicodendron accessions were used to reconstruct the phylogenetic, two distinct clades were recognized: one consisting of T. vernicifluum cv. Dahongpao, T. vernicifluum cv. Hongpigaobachi, T. vernicifluum cv. Yanggangdamu, triploid T. vernicifluum T. diversilobum and T. griffithii and the other comprised of the remaining accessions. The result is consistent with previous studies, which shown that T. sylvestre was more closely related to T. succedaneum based on five nuclear and chloroplast DNA regions [60].

Compared to morphological trait classification systems, molecular markers can reveal genetic differences at the DNA reveal genetic differences and are effective for evaluating the genetic diversity of germplasm in breeding programs [61]. SSR markers were testified to be a more advanced tool than all of these markers, which are very suitable for the identification and classification of Toxicodendron species [62]. In our study, five accessions can be distinguished clearly by these SSR markers. All the samples of T. vernicifluum cv. Dahongpao, T. vernicifluum cv. Hongpigaobachi, and triploid T. vernicifluum grouped together in one group, and all the samples of T. vernicifluum and T. succedaneum grouped together in another group, which is consistent with the cp genome and morphological analysis.

Conclusions

The current study primarily explored the chloroplast genome of triploid T. vernicifluum and compared it with related species of Toxicodendron genus. The size of genome, structure and organization of gene were shown to be conservative, which is similar to those reported Toxicodendron cp genomes. Eight hotspot regions were identified and may be utilized as potential molecular markers for population genetic and phylogenetic studies in Toxicodendron. Phylogenetic analysis based on cp genomes and SSR markers both showed that triploid T. vernicifluum can be distinguished with T. vernicifluum cv. Dahongpao, while T. vernicifluum cv. Dahongpao had a close relationship with T. vernicifluum cv. Hongpigaobachi. Therefore, complete cp genomes is useful for species identification, taxonomic clarification, and genomic evolutionary analysis. Further research on the relationships within Toxicodendron genus and the identification of ploidy should incorporate morphology and genome wide analyses to enhance the results.

Materials and methods

Plant materials

In this study, triploid sumac of T. vernicifluum cv. Dahongpao (DHP) and triploid T. vernicifluum (TZT) were cultivated in the germplasm resource nursery in Yangling Shaanxi Province (108.08E, 34.27N), and Zhaotong Yunnan Province (103.72E, 27.34 N), respectively [11, 13]. Three diploid sumac of T. vernicifluum cv. Hongpigaobachi (GBC) were cultivated in the germplasm resource nursery in Yangling Shaanxi Province, T. succedaneum (TRB) and T. vernicifluum (TZG) were cultivated in the germplasm resource nursery in Southwest Forestry University, in Kunming Yunnan Province (102.76 E, 25.06 N) which were introduced from Changsha Hunan Province and Wenshan Yunnan Province, respectively. These five accessions (DHP, GBC, TZT, TRB and TZG) were used for morphological characterization (Table 1) and SSR molecular markers analysis. GBC, TZT, TRB and TZG were sequenced and combined with the six previously sequenced accessions DHP, T. succedaneum (Ts), T. griffithii (Tg), T. sylvestre (Tsy), T. diversilobum (Tdi) and T. vernicifluum cv. Yanggangdamu (Tyg) for comparative analysis of chloroplast genome (Table 2).

Morphological characterization

In order to compare the differences of leaf shapes among the five accessions (DHP, GBC, TZT, TRB and TZG), three trees per accession were selected for data collection on leaves, and five foliar traits (leaf length, leaflet number, leaflet length, leaflet width; and leaf shape index) were measured. All variables were measured using a ruler (0.1 mm resolution) and are recorded in mm and each sample was tested for three biological replicates.

DNA extraction

Fresh leaves of T. vernicifluum cv. Hongpigaobachi (GBC), triploid T. vernicifluum (TZT), T. succedaneum (TRB) and T. vernicifluum (TZG) were collected from different regions and quickly frozen in liquid nitrogen, and stored at ultra-low-temperature refrigerator at -80℃ until use. The voucher specimen deposited in the Herbarium of Southwest Forestry University. The total genomic DNA was extracted with the TGuide plant genomic DNA prep kit (Tiangen Biotech, Beijing, China) and DNA quality was inspected in 0.8% agarose gels, DNA quantification was performed using a NanoDrop spectrophotometer, DNA samples were stored at -80℃ at the Key Laboratory of State Forestry Administration on Biodiversity Conservation in Southwest China, Southwest Forestry University, Kunming, China.

Plastid genome sequencing, assembly and annotation

Total DNA was used to generate libraries with an average insert size of 350 bp with the Illumina Novaseq 6000 platform. Approximately 8 Gb raw data were produced with 150 bp pair-end read lengths. GetOrganelle software [63] was used to assemble the complete cp genome of the four accessions, with Pistacia weinmaniifolia as the reference. Geneious R8 (Biomatters Ltd, Auckland, New Zealand) software was used for initial cp genome annotation. Start and stop condos were checked and adjusted manually when necessary by comparing them to the reference genome P. weinmaniifolia. The tRNA genes were further confirmed through online tRNA scane-SE web servers [64]. The gene map of annotated Toxicodendron chloroplast genome was drawn by OGdraw online [65]. The annotated sequences have been deposited to the NCBI GenBank database under the accession numbers OP235457, OP271782, OP279729 and OP279730 (Corresponding to T. succedaneum (TRB), triploid T. vernicifluum (TZT), T. vernicifluum cv. Hongpigaobachi (GBC) and T. vernicifluum (TZG)).

Identification of simple sequence repeats (SSRs) and long sequence repeats

Chloroplast SSR loci in ten Toxicodendron cp genomes were detected using MISA [66] with the minimal repeat number set to 10, 6, 5, 5, 5 and 5 for mononucleotide (momo-), dinucleotide (di-), trinucleotide (tri-), tetranucleotide (tetra-), pentanucleotide (penta-), and hexanucleotide (hexa-) nucleotide sequences, respectively.

Morever, the online REPuter [67] software was used to estimate and locate forward (F), reverse (R), complemented (C) and palindromic (P) repeats. The following settings for repeat identification were used: (1) Hamming distance equal to 3; (2) minimal repeat size was set to 30 bp; (3) 90% or greater sequence identity.

Comparative analysis of the chloroplast genomes

To investigate divergence in cp genomes, identity across the whole cp genomes was visualized using the online genome comparison tool mVISTA viewer with Shuffle-LAGAN mode among the ten accessions with T. vernicifluum cv. Dahongpao (DHP) [24] as a reference to show inter-and intraspecific variations [68]. The software MAUVE alignment [69] was employed to analyze and compare the plastome structure of triploid T. vernicifluum with the other accessions of Toxicodendron. Furthermore, events of IR expansion and contraction were compared between these accessions; the junction regions between the IR, SSC, and LSC of ten accessions were compared using the online program IR scope [70].

To identify the mutational hotspot regions for Toxicodendron, we calculated nucleotide diversity (Pi) across the whole plastome. The plastome sequences were aligned using MAFFT version 7 software [71] and the nucleotide diversity was detected using DnaSP version 5 software [72] with sliding window strategy. The step size was set to 200 bp, with a 600 bp window length. Single nucleotide polymorphisms (SNPs) were detected using the “find variation” function in Geneious.

Amplification of SSR marker

The materials used were T. vernicifluum cv. Dahongpao (DHP), triploid T. vernicifluum (TZT), T. vernicifluum cv. Hongpigaobachi (GBC), T. succedaneum (TRB) and T. vernicifluum (TZG). Three samples per accession were selected for SSR analysis. The fresh leaves from each sample were immediately dried with silica gel for further DNA extraction. Total genomic DNAs were extracted from each sample using the TGuide plant genomic DNA prep kit (Tiangen Biotech, Beijing, China), DNA quality was inspected in 0.8% agarose gels, and DNA quantification was performed using a NanoDrop spectrophotometer. A total of 116 SSR primers [73,74,75,76,77] were used to identify the polymorphic markers among 15 samples, 7 primer pairs amplified well-distributed fragments with good distinctness. Sequence information of the SSRs was listed in Table 5, and the forward of which (F) was labeled 5(6)-carboxyfluorescein (FAM) by the 5’-terminal. PCR reactions were carried out in 25 µL, containing 12.5 µL 2×PCR Mix, 1 µL of each primer, respectively, 1 µL template DNA. The PCR cycling conditions were as follows: pre-denaturation at 94 ℃ for 4 min, followed by 35 cycles of denaturation at 94 ℃ for 30 s, annealing at the corresponding temperature (52 ℃-61 ℃) for 30 s, extension at 72 ℃ for 1 min and the final extension for 10 min at 72 ℃. Amplified SSR alleles were rechecked in 1.5 % binary gels by electrophoresis at 80 volts for 50 min and gel documentation was performed with Gel Logic 200 imaging system. Capillary electrophoresis-based fragment analyses of single pollen amplified SSR alleles were conducted on an ABI3730XL Genetic Analyzer following the manufacture’s instruction to generate GeneScan files. Scoring of alleles was done using ‘GeneMaker’ version 2.2. Genetic distance among the 15 samples was calculated according to the software GenoDive [29] and the cluster analysis was carried out based on the matrix using MEGA 5.0.

Table 5 Information of SSR markers
Full size table

Phylogenetic analysis

Phylogenetic analysis was conducted using the complete chloroplast genome sequences of the ten Toxicodendron accessions mentioned above, with two Anacardiaceae species [Pistacia weinmaniifolia (MF630953) and Mangifera indica (KY635882)] that were used as outgroup. The nucleotide sequences were aligned using MAFFT version 7 software [71]. The phylogenetic analyses were performed using maximum likelihood (ML) and Bayesian inference (BI). ModelFinder [78] was used to select the best-fit model with default setting and the maximum likelihood (ML) analysis was performed using IQ-TREE 1.5.5 [79] with 1000 bootstrap replications. The BI analysis was performed by Mybayes 3.2.6 [80]. The jModelTest 2.0 program [81] was used to determine the best-fitting model for each dataset based on the Akaike information criterion and the optimal model of “GTR+F+R3”. The Markov chain Monte Carlo (MCMC) algorithm was run for 1,000,000 generations, and a burn-in of 25% was used for the analysis.

Availability of data and materials

The datasets generated during the current study are available in the NCBI GenBank (Accession number OP235457, OP271782, OP279729, OP279730)

References

  1. Otto SP, Whitton J. Polyploid incidence and evolution. Annu Rev Genet. 2000;34:401–37.

    Article  CAS  Google Scholar 

  2. Van de Peer Y, Ashman TL, Soltis PS, Soltis DE. Polyploidy: an evolutionary and ecological force in stressful times. Plant Cell. 2021;33:11–26.

    Article  Google Scholar 

  3. Yao H, Kato A, Mooney B, Birchler JA. Phenotypic and gene expression analyses of a ploidy series of maize inbred OH43. Plant Mol Biol. 2011;75(3):237–51.

    Article  CAS  Google Scholar 

  4. Hashida K, Tabata K, Kuroda K, Otsuka Y. Phenolic extractives in the trunk of Toxicodendron vernicifluum: chemical characteristics, contents and radial distribution. Journal of Wood Science. 2014;60(2):160–8.

    Article  CAS  Google Scholar 

  5. Kakuda A, Miyamoto M. An exhibition of ShisuiRokkaku, who established Japanese ‘National Treasure’. Executive committee on an exhibition of ShisuiRokkaku. 2008. p. 82–111.

    Google Scholar 

  6. Snyder DM. An overview of oriental lacquer. J Chem Educ. 1989;66(12):977–980.

  7. Takano M, Masaya N, Tabata M. Comprehensive analysis of the isozyme composition of laccase derived from Japanese lacquer tree, Toxicodendron vernicifluum. Journal of Wood Science. 2021;67:9.

    Article  CAS  Google Scholar 

  8. Cho N, Choi J, Yang H, Jeong EJ, Lee KY, Kim YC, Sung SH. Neuroprotective and anti-inflammatory effects of flavonoids isolated from Rhus vernicifluum in neuronal HT22 and microglial BV2 cell lines. Food Chem Toxicol. 2012;50(6):1940–5.

  9. Li WM, Bai GQ, Chen H, Li B, Li SF. Advance in research on genetic diversity of Toxicodencron vernicifluum. Shaanxi Forest Sci Technol. 2017;2:97–100, 104.

    Google Scholar 

  10. Zhao M, Liu C, Zheng G, Wei S, Hu Z. Comparative studies of bark structure, lacquer yield and urushiol content of cultivated Toxicodendron vernicifluum varieties. New Zealand J Botany. 2013;51(1):13–21.

    Article  Google Scholar 

  11. Shang ZY, Zhang JZ, Liu QH, Li RJ. The observation on chromosome of Rhus verniciflua stokes and the discovery of triploid lacquer tree. Act Bot Bor. 1985;5(8):187–91.

    Google Scholar 

  12. Zhao XP, Wei SN. Genetic evaluation of Toxicodendron vernicifluum cultivars using amplified fragment length polymorphism markers. J Mol Cell Biol. 2007;40:262–6.

    CAS  Google Scholar 

  13. Han GW, Li D, Zhao YM, Tian B, He RX, Ou GL, Yin WY, He CZ. Ploidy identification of pseudo-polyploidy in Toxicodendron vernicifluum. J Southwest Forestry Univ. 2016;36(3):7–11.

    Google Scholar 

  14. Suzuki M, Yonekura K, Noshiro S. Distribution and habitat of Toxicodendron vernicifluum (Stokes) F.A. Barkl (Anacardiaceae) in China. Jpn J Histor Bot. 2007;15:58–62.

    Google Scholar 

  15. Cao J, Jiang D, Zhao Z, Yuan SB, Zhang YJ, Zhang T, Zhong WH, Yuan QJ, Huang LQ. Development of chloroplast genomic resources in Chinese Yam (Dioscorea polystachya). Biomed Res Int. 2018;1:6293847.

  16. Dong WP, Xu C, Li WQ, Xie XM, Lu YZ, Liu YL, Jin XB, Suo ZL. Phylogenetic resolution in Juglans based on complete chloroplast genomes and nuclear DNA sequences. Front Plant Sci. 2017;8:1148.

    Article  Google Scholar 

  17. Cui HN, Ding Z, Zhu QL, Wu Y. Population structure, genetic diversity and fruit-related traits of wild and cultivated melons based on chloroplast genome. Genet Resour Crop Evol. 2020;68(6):1–11.

    Google Scholar 

  18. McCauley DE, Stevens JE, Peroni PA, Raveill JA. The spatial distribution of chloroplast DNA and allozyme polymorphisms within a population of Silenealba (Caryophyllaceae). Am J Bot. 1996;83:727–31.

    Article  CAS  Google Scholar 

  19. Small RL, Cronn RC, Wendel JF. Use of nuclear genes for phylogeny reconstruction in plants. Austsyst Bot. 2004;17:145–70.

    CAS  Google Scholar 

  20. Daniell H, Lin CS, Yu M, Chang WJ. Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol. 2016;17:134.

    Article  Google Scholar 

  21. Li L, Hu YF, He M, Zhang B, Wu W, Cai PM, Huo D, Hong YC. Comparative chloroplast genomes: insights into the evolution of the chloroplast genome of Camellia sinensis and the phylogeny of Camellia. BMC Genomics. 2021;22(1):138.

    Article  CAS  Google Scholar 

  22. Liu L, Wang Y, He P. Chloroplast genome analyses and genomic resource development for epilithic sister genera Oresitrophe and Mukdenia (Saxifragaceae), using genome skimming data. BMC Genomics. 2018;19(1):235–52.

    Article  Google Scholar 

  23. Hoshino AA, Bravo JP, Nobile PM, Morelli KA. Microsatellites as tools for genetic diversity analysis. In: Calistkan M, editor. Genetic diversity in microorganisms. Rijeka: In Tech; 2012. p. 149–70.

    Google Scholar 

  24. Zhong YY, Zong D, Zhou AP, He XF, He CZ. The complete chloroplast genome of the Toxicodendron vernicifluum cv. Dahongpao, an elite natural triploid lacquer tree. Mitochondrial DNA Part B. 2019;4:1227–8.

    Article  Google Scholar 

  25. Wang L, He N, Fang YM, Zhang FL. Complete chloroplast genome sequence of Chinese lacquer tree (Toxicodendron vernicifluum, Anacardiaceae) and its phylogenetic significance. Biomed Res Int. 2020;1:1–13.

    Google Scholar 

  26. Kim KJ, Lee HL. Wide spread occurrence of small inversions in the chloroplast genomes of land plants. Molecules and Cells. 2005;19(1):104–13.

    CAS  Google Scholar 

  27. Wang RJ, Cheng CL, Chang CC, Wu CL, Su TM, Chaw SM. Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evol Biol. 2008;8(1):36.

    Article  CAS  Google Scholar 

  28. Santiago AC, Beatriz OS, Juan CV. Evolution of small inversions in chloroplast genome: a case study from a recurrent inversion in angiosperms. Cladistics. 2009;25:93–104.

    Article  Google Scholar 

  29. Meirmans PG. GenoDive version 3.0: Easy-to-use software for the analysis of genetic data of diploids and polyploids. Mol Ecol Resour. 2020;20(4):1126–31.

    Article  CAS  Google Scholar 

  30. Chang YM. The advances in identification of fruit tree polyploidy. Shanxi Forestry Sci Technol. 2000;3(1):1–4.

    Google Scholar 

  31. Li Q, Wang S, Liu G, Zhou P, Zheng X, Ceng W, Chen Z, Chen A. Response of tobacco leaf shape index and auxin to low temperature stress and growth recovery. Jiangsu Agric Sci. 2019;47:60–5.

    CAS  Google Scholar 

  32. Liu CQ, Zhao M, Wei SN, Hu ZH. Comparative anatomy of secondary phloem and morphology among 4 varieties of Toxicodendron vernicifluum in Shaanxi. Acta Bot Boreal. 2010;30(2):269–74.

    CAS  Google Scholar 

  33. Chansler MT, Ferguson CJ, Fehlberg SD, Prather LA. The role of polyploidy in shaping morphological diversity in natural populations of Phlox amabilis. Am J Botany. 2016;103(9):1546–58.

    Article  Google Scholar 

  34. Dong WP, Liu H, Xu C, Zuo YJ, Chen ZJ, Zhou SL. A chloroplast genomic strategy for designing taxon specific DNA mini-barbcodes: a case study on ginsengs. BMC Genet. 2014;15(1):138.

    Article  Google Scholar 

  35. Li X, Yang Y, Henery RJ, Rossetto M, Wang Y, Chen S. Plant DNA barcoding: from gene to genome. Biol Rev. 2015;90:157–66.

    Article  Google Scholar 

  36. Wang L, He N, Li Y, Fang YM, Zhang FL. The complete chloroplast genome sequence of Toxicodendron succedaneum (Anacardiaceae). Mtochondrial DNA Part B. 2020;5(2):1956–7.

    Article  Google Scholar 

  37. Zhu A, Guo W, Gupta S, Fan W, Mower J. Evolutionary dynamics of the plastid inverted repeat: The effects of expansion, contraction, and loss on substitution rates. New Phytol. 2015;209(4):1747–56.

    Article  Google Scholar 

  38. Liu W, Kong H, Zhou J, Fritsch P, Hao G, Gong W. Complete chloroplast genome of Ceris chuniana (Fabaceae) with structure and genetic comparison to six species in Caesalpinioideae. Int J Mol Sci. 2018;19(5):1286.

    Article  Google Scholar 

  39. Long LX, Li YT, Wang SJ, Liu ZL, Wang JM, Yang MS. Complete chloroplast genomes and comparative analysis of Ligustrun species. Sci Rep. 2023;13(1):512.

    Article  Google Scholar 

  40. Budhi DA, Yohei T, Sri S, Afifin ZMS, Toyoko S, Petr H. The origin and evolution of fibromelanosis in domesticated chickens: genomic comparison of Indonesian Cemani and Chinese Silkie breeds. PloS One. 2017;12(4):e0173147.

    Article  Google Scholar 

  41. Kaila T, Chaduvla PK, Saxena S, Bahadur K, Gahukar SJ, Chaudhury A, Sharma TR, Singh NK, Gaikwad K. Chloroplast genome sequence of Pigeonpea (Cajanuscajan (L.) Millspaugh) and Cajanus scarabaeoides (L.) thouars: genome organization and comparison with other legumes. Front Plant Sci. 2016;7:1847.

    Article  Google Scholar 

  42. Luo C, Huang WL, Sun HY, Yer H, Li XY, Li Y, Yan B, Wang Q, Wen YH, Huang MJ, Huang HQ. Comparative chloroplast genome analysis of Impatiens species (Balsaminaceae) in the karst area of China: insights into genome evolution and phylogenomic implications. BMC Genomics. 2021;22:571.

    Article  Google Scholar 

  43. Liu X, Chang EM, Liu JF, Huang YN, Wang Y, Yao N, Jiang ZP. Complete chloroplast genome sequence and phylogenetic analysis of Quercus bawangligensis Huang, Li et Xing, a Vulnerable Oak Tree in China. Forests. 2019;10(7):587.

    Article  Google Scholar 

  44. Huo YM, Gao LM, Liu BJ, Yang YY, Wu X. Complete chloroplast genome sequences of four Allium species: comparative and phylogenetic analyses. Sci Rep. 2019;97(5):874–92.

    Google Scholar 

  45. Asaf S, Jan R, Khan AL, Lee IJ. Complete chloroplast genome characterization of oxalis Corniculata and its comparison with related species from family Oxalidaceae. Plants. 2020;9:928.

    Article  Google Scholar 

  46. Asaf S, Khan AL, Khan A, Al-Harrasi A. Unraveling the chloroplast genomes of two Prosopis species to identify its genomic information, comparative analyses and phylogenetic relationship. Int J Mol Sci. 2020;21(9):3280.

    Article  CAS  Google Scholar 

  47. Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M. The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet. 1989;217(2):185–94.

    Article  CAS  Google Scholar 

  48. Catalano SA, Saidman BO, Vilardi JC. Evolution of small inversions in chloroplast genome: a case study from a recurrent inversion in angiosperms. Cladistics. 2009;25(1):93–104.

    Article  Google Scholar 

  49. Song Y, Dong WP, Liu B, Xu C, Yao X, Gao J, Coelett RT. Comparative analysis of complete chloroplast genome sequences of two tropical trees Machilus yunnanensis and Machilus balansae in the family Lauraceae. Front Plant Sci. 2015;6:662–70.

    Article  Google Scholar 

  50. Song Y, Yao X, Tan YH, Gan Y, Coelett RT. Complete chloroplast genome sequence of the avocado: gene organization, comparative analysis, and phylogenetic relationships with other Lauraceae. Can J Forest Res. 2016;46(11):1293–301.

    Article  Google Scholar 

  51. Zong D, Gan PH, Zhou AP, Zhang Y, Zou XL, Duan AA, Song Y, He CZ. Plastome sequences help to resolve deep-level relationships of Populus in the family Salicaceae. Front Plant Sci. 2019;10:5.

    Article  Google Scholar 

  52. Graham SW, Reeves PA, Burns ACE, Olmstead RG. Microstructure changes in noncoding chloroplast DNA: interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inference. Int J Plant Sci. 2000;161(S6):S83-96.

    Article  CAS  Google Scholar 

  53. Wolf PG, Duffy AM, Roper JM. Phylogenetic use of inversions in fern chloroplast genomes. Am Fern J. 2009;99(2):132–4.

    Google Scholar 

  54. Ren FM, Wang LQ, Li Y, Zhuo W, Xu ZC, Guo HJ, Liu Y, Gao RR, Song JY. Highly variable chloroplast genome from two endangered Papaveraceae lithophytes Corydalis tomentella and Corydalis saxicola. Ecol Evol. 2021;11:4158–71.

    Article  Google Scholar 

  55. Dong WP, Liu J, Yu J, Wang L, Zhou SL. Highly variable chloroplast markers for evaluating plant phylogeny at low taxonomic levels and for DNA barcoding. PLoS One. 2012;7(4):e35071.

    Article  CAS  Google Scholar 

  56. Njuguna AW, Li ZZ, Saina JK, Munywoki JM. Comparative analyses of the complete chloroplast genomes of Nymphoides and Menyanthes species (Menyanthaceae). Aquatic Botany. 2019;156:73–81.

    Article  Google Scholar 

  57. Fan WB, Wu Y, Yang J, Shahzad K, Li ZH. Comparative chloroplast genomics of Dipsacales species: insight into sequence variation, adaptive evolution, and phylogenetic relationships. Front Plant Sci. 2018;9:689.

    Article  Google Scholar 

  58. Jansen RK, Cai ZQ, Raubeson LA, Baniell H, dePamphilis CW, Mack JL, Müller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee S, Peery R, McNeal JR, Kuehl JV, Boore JL. Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA. 2007;104(49):19369–74.

    Article  CAS  Google Scholar 

  59. Moore MJ, Soltis PS, Bell CD, Burleigh G, Soltis DE. Phylogenetic analysis of 83 plastid genes further resolves the early diversification of edicots. Proc Natl Acad Sci USA. 2010;107(10):4623–8.

    Article  CAS  Google Scholar 

  60. Jiang Y, Gao M, Meng Y, Wen J, Ge XJ, Nie ZL. The importance of the North Atlantic land bridges and eastern Asia in the post-Boreotropical biogeography of the Northern Hemisphere as revealed from the poison ivy genus (Toxicodendron, Anacardiaceae). MolPhylogenet Evol. 2019;139:106561.

    Article  Google Scholar 

  61. Jia J. Molecular germplasm diagnostics and molecular marker assisted breeding. SciAgric Sin. 1996;29:1–10.

    CAS  Google Scholar 

  62. Luo C, Chen GL, Chen XX, Liu H, Li YH, Huang CL. Analysis of genetic relationship and classification in Chrysanthemum germplasm collection. Horticultural Plant Journal. 2018;4(2):73–82.

    Article  Google Scholar 

  63. Jin JJ, Yu WB, Yang JB, Song Y, dePamphilis CW, Yi TS, Li DZ. GetOrganelle: a fast and versatile toolkit for accurate de novo assemble of organelle genomes. Genome Biol. 2020;21(1):241–72.

    Article  Google Scholar 

  64. Chan PP, Lin BY, Mak AJ, Lowe TM. tRNA scan-SE 2.0: improved detection and functional classification of transfer RNA genes. Nucleic Acids Res. 2021;49(16):9077–96.

    Article  CAS  Google Scholar 

  65. Lohse M, Drechsel O, Kahlau S, Bock R. Organellar Genome DRAW-A suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res. 2013;41:575–81.

    Article  Google Scholar 

  66. Thiel T, Michalek W, Varshney RK. Exploiting EST databases for the development and characterization of gene-derived SSR markers in barley (Hordeum vulgare L.). Theor Appl Genet. 2003;106(3):411–22.

    Article  CAS  Google Scholar 

  67. Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R. REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 2001;29(22):4633–42.

    Article  CAS  Google Scholar 

  68. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 2004;32:W273-9.

    Article  CAS  Google Scholar 

  69. Darling AC, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14(7):1394–403.

    Article  CAS  Google Scholar 

  70. Amiryousefi A, Hyvönen J, Poczai P. IRscope: an online program to visualize the junction sites of chloroplast genomes. Bioinformatics. 2018;34(17):3030–1.

    Article  CAS  Google Scholar 

  71. Katoh K, Kuma K, Toh H, et al. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005;33(2):511–8.

    Article  CAS  Google Scholar 

  72. Librado P, Rozas J. Dnasp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25(11):1451–2.

    Article  CAS  Google Scholar 

  73. Vu DD, Bui TTX, Nguyen THN, Shah SNM, Ha VN, Zhu YH, Zhang L, Zhang Y, Huang XH. Isolation and characterization of polymorphic microsatellite markers in Toxicodendron vernicifluum. Czech J Genet Plant Breed. 2018;54(1):17–25.

    Article  CAS  Google Scholar 

  74. Hsu TW, Shih HC, Kuo CC, Chiang TY, Chiang YC. Characterization of 42 Microsatellite markers from Poison Ivy, Toxicodendron radicans (Anacardiaceae). Int J Mol Sci. 2013;14(10):20414–26.

    Article  Google Scholar 

  75. Hiraoka Y, Watanabe A. Development and characterization of microsatellites, clone identification, and determination of genetic relationships among Rhus succedaneu L. individuals. J Japan SocHort Sci. 2010;79(2):141–9.

    CAS  Google Scholar 

  76. Huang LF. Study on genetic diversity of rootstock germplasm resources from main mango producing areas by SSR marker. Master dissertation. Haikou: Hainan University; 2010.

    Google Scholar 

  77. Wang W. The phylogeography and landscape genetic studies of Cotinuscoggygria (Anacardiaceae). Master dissertation. Zhenzhou: Henan Agricultural University; 2015.

    Google Scholar 

  78. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587–9.

    Article  CAS  Google Scholar 

  79. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74.

    Article  CAS  Google Scholar 

  80. Ronquist F, Huelsenbeck JP. Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.

    Article  CAS  Google Scholar 

  81. Darriba D, Taboada GL, Doallo R, Posada D. jModeTest2: more models, new heuristics and parallel computing. Nat Methods. 2012;9(8):772.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

This work was supported by Yunnan Provincial Expert Workstation (202005AF150020) and Yunnan Provincial Ten-Thousand Program -Industry Leading Talents (YNWR-CYJS-81210420) and Applied Basic Research Foundation of Yunnan Province (202101AU070144).

Author information

Authors and Affiliations

  1. Key Laboratory for Forestry Resources Conservation and Utilization in the Southwest Mountains of China, Ministry of Education, Southwest Forestry University, Kunming, China

    Dan Zong, Zhensheng Qiao, Jintao Zhou, Peiling Li, Peihua Gan & Chengzhong He

  2. Key Laboratory for Forest Genetics and Tree Improvement & Propagation in Universities of Yunnan Province, Southwest Forestry University, Kunming, China

    Dan Zong, Zhensheng Qiao, Jintao Zhou, Peiling Li, Peihua Gan & Chengzhong He

  3. Key Laboratory of Biodiversity Conservation in Southwest China, State Forestry Administration, Southwest Forestry University, Kunming, China

    Dan Zong, Meirong Ren & Chengzhong He

Authors
  1. Dan Zong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhensheng Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jintao Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peiling Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peihua Gan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Meirong Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chengzhong He
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Dan Zong designed the experiments and organized the manuscript; Zhensheng Qiao, Jintao Zhou, Peiling Li, Peihua Gan, Meirong Ren analyzed and interpreted the data. Dan Zong and Chengzhong He Original edited the manuscript; All authors revised, read, and approved the final version of the manuscript.

Corresponding author

Correspondence to Chengzhong He.

Ethics declarations

Ethics approval and consent to participate

We have obtained the permission of Southwest Forestry University to collect the species of Toxicodendron. The collection and usage of plant specimens in current study complied with the IUCN Policy Statement on Research Involving Species at Risk of Extinction and is allowed by the Convention on the Trade in Endangered Species of Wild Fauna and Flora. Ethical approval was not applicable for this study.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1: Table S1.

List of genes in the Toxicodendron chloroplast genomes. Table S2. SSR repeats in the ten cp genomes. Table S3. Ts and Tv in non-coding regions of the nine plastomes, compared with DHP. Table S4. Genetic distance among the 15 samples.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zong, D., Qiao, Z., Zhou, J. et al. Chloroplast genome sequence of triploid Toxicodendron vernicifluum and comparative analyses with other lacquer chloroplast genomes. BMC Genomics 24, 56 (2023). https://doi.org/10.1186/s12864-023-09154-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12864-023-09154-2

Keywords

BMC Genomics

ISSN: 1471-2164

Contact us