Assembly and Analysis of the First Complete Mitochondrial Genome of Ficus carica Linn.

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Lingzhu Wei Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China

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Ting Zheng Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China

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Jiang Xiang Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China

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Jianhui Cheng Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China

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Jiang Wu Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China

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Abstract

Ficus carica Linn. is an important economic tree species with high developmental prospects and scientific research for edible and medicinal value. The F. carica chloroplast genome has recently been reported; however, the mitochondrial genome is still unexplored. We assembled the complete mitogenome of F. carica using reads from PacBio Biosciences sequencing platforms. The circular mitogenome F. carica has a length of 480,902 base pairs (bp), which contain 46 genes, including 27 protein-coding genes, 16 transfer RNA (tRNA) genes, and three ribosomal RNA (rRNA) genes. The base composition, codon usage, sequence repeats, RNA editing, and selective pressure were examined. We also conducted the phylogenetic analysis based on the mitogenomes of F. carica and 21 other taxa to know the evolutionary and taxonomic status of F. carica. Our analyses provided comprehensive information on the F. carica mitochondrial genome, which would facilitate evolutionary research in other fruit trees in the future.

Edible fig [Ficus carica Linn. (Moraceae)], is a heterozygous species (2n = 26) tree fruit (Mori et al. 2017), widely planted and consumed worldwide because of its culinary and medicinal properties (Li et al. 2021; Turco et al. 2020); its cultivation has been practiced for 12,000 years (Kislev et al. 2006). This species has traditionally been used to treat wounds, infection, hemorrhoids, warts, viruses, and insect bites (Li et al. 2021; Park et al. 2013), and some studies have addressed its chemistry, biological activity, and ethno-pharmacological applications (Arvaniti et al. 2019; Qi et al. 2021). Moreover, F. carica leaves are used in tea or medicine because of their abundant chemical constituents (Barolo et al. 2014). Clinical studies have demonstrated the beneficial effects of fig leaves in the treatment of respiratory, gastrointestinal, and cardiovascular diseases and especially diabetes, hemorrhoids, and herpes zoster (Mawa et al. 2013; Rubnov et al. 2001; Saeed and Sabir 2002).

Mitochondria convert biomass energy and provide energy for life activities (Bonora et al. 2014; Ye et al. 2017). In most seed plants, nuclear genetic information is inherited from both parents, whereas chloroplast DNA (cpDNA) and mitochondrial DNA (mtDNA) are derived from the maternal parent (Birky 1995; Ye et al. 2017). With the development of sequencing technology, an increasing number of organellar genomes has been reported, with 2515 complete mitochondrial (mt) genomes currently deposited in the GenBank Organelle Genome Resources database (Schoch et al. 2020). The integration of DNA elements into the mt genome via intracellular and horizontal transfer has been a common phenomenon during plant evolution (Bergthorsson et al. 2005; Ma et al. 2022). As a consequence, plant mt genomes vary considerably in length, gene content, and gene sequence (Richardson et al. 2013; Shengxin et al. 2013). The largest land plant mitogenome is ∼11.3 Mb (Silene conica) (Sloan et al. 2012), and the smallest is ∼66 kb (Viscum scurruloideum) (Skippington et al. 2015), but most genomes comprise 200–800 kb (Guo et al. 2016). This wide variation in mitogenome size can be attributed to the presence of repetitive sequences [e.g., simple sequence repeats (SSRs), tandem repeats, and dispersed repeats] and the acquisition of foreign DNA from other organisms during evolution (Bergthorsson et al. 2003; Wynn and Christensen 2019). As a result, gene content also varies considerably, typically ranging between 32 and 67 genes (Hsu and Mullin 1989). Some genes, such as those related to ATP synthase, cytochrome c biogenesis, NADH dehydrogenase, and ubiquinol cytochrome (Bi et al. 2020), are highly conserved, whereas others, including sdh3, sdh4, cox2, and rps11, have been lost, which is thought to be the result of evolution and adaptation to the environment (Choi et al. 2019).

The F. carica whole genome was sequenced using the SMRT technology of PacBio, a total of 333.4 Mb genome sequence was produced (Usai et al. 2020). No mitogenomes in the genus Ficus have been previously sequenced. In this study, we first assembled the complete mitogenome of F. carica and analyzed its gene content, repetitive sequences, RNA editing sites, selective pressures, and phylogenetic relationships. We conducted a survey of gene transfer among nuclear, chloroplast, and mitochondria genomes of F. carica. The data presented herein expand genetic information available for the genus Ficus. The data presented in this study contribute to the expansion of genetic information available for the Ficus genus.

Materials and Methods

Plant materials and DNA sequencing.

Plants of F. carica were grown under natural conditions in the greenhouse area of the Zhejiang Academy of Agricultural Sciences (Jianggan District, Hangzhou, China; 30°31′N, 120°19′E). DNA was isolated from fresh leaves using the plant genomic DNA kit (Tiangen Biotech, Beijing, China) (Vieira et al. 2014) and then evaluated for quality by 1% agarose gel electrophoresis. The qualified samples were sequenced by Nanjing Jisi Huiyuan Biotechnology (Nanjing, China) for sequencing using PacBio and Illumina NovasEq. 6000 platforms, respectively (Illumina, San Diego, CA, USA). The experimental procedures were carried out according to the standard protocol (Bolger et al. 2014). In brief, the raw reads were filtered according to sequencing quality, the presence of adapter contamination, and duplication. Only high-quality reads were used for genome assembly.

Mitogenome assembly and annotation.

The F. carica mt genome was assembled from the generated sequences using Canu v1.4 (Koren et al. 2017). The assembled contigs were polished (Pilon ver.1.18) with Illumina reads to correct read errors (Walker et al. 2014). Mitogenome annotation was performed with the GE-Seq tool on the MPI-MP CHLOROBOX website (https://chlorobox.mpimp-golm.mpg.de), with Morus notabilis (NC_041177.1) and Cannabis sativa (NC_029855.1) mitogenomes used as references. Mitochondrial protein-coding genes were predicted using the MITOFY websever (Lowe and Eddy 1997), and tRNAscan-SE was used with default settings to identify tRNA and rRNA genes (Lowe and Eddy 1997). After manual confirmation of the output GenBank format file, a circular mt map was drawn using Organellar Genome DRAW (Greiner et al. 2019).

Analysis of repeat sequences.

Forward, palindromic, and tandem repeats were identified with REPuter. SSRs were analyzed with the MISA program (http://pgrc.ipkgatersleben.de/misa/) (Thiel et al. 2003). Motif sizes of one- to six-nucleotide SSRs were set to 10, 5, 4, 3, 3, and 3, respectively.

Genome alignment and RNA editing analysis.

The F. carica mitogenome was searched against the cp genome of F. carica (NC_035237.1) using BLASTN 2.9.0+ according to the following screening criteria: matching rate ≥ 70%, E-value ≤ 1 × 10−6, and length ≥ 40. A BLASTN search (maximum E-value = 1 × 10−50) of the complete mitogenome was performed against all contigs from the F. carica nuclear genome sequence (PRJNA565858) to identify regions of potential nuclear origin in the mitogenome of F. carica.

RNA editing sites in protein-coding genes (PCGs) of F. carica were predicted using the online PREP-Mt suite of servers (http://prep.unl.edu/) with a cutoff value of 0.2 (Mower 2005).

Phylogenetic tree construction and ka/ks analysis.

In total, 22 complete mitogenomes (Supplemental Table 1) were used to ascertain the phylogenetic position of F. carica. The 26 mt PCG genes (atp1, atp4, atp6, atp8, atp9, ccmB, ccmC, ccmFc, ccmFn, cob, cox1, cox2, cox3, matR, nad1, nad2, nad3, nad4, nad4L, nad5, nad6, nad7, nad9, rps12, rps3, and rps4) conserved across the 22 analyzed species were aligned in Muscle with default parameters, with the alignment then manually modified to eliminate gaps and missing data. A maximum-likelihood tree was then constructed in MEGA X (Kumar et al. 2018) using the JTT+G+I+F nucleotide substitution model. A bootstrap consensus tree was inferred from 1000 bootstrap replicates. Vitis vinifera and Ginkgo biloba were used as outgroups.

Results

Features of the F. carica mitogenome.

F. carica plant DNA was extracted from young leaf and sequenced using a combination of PacBio and Illumina sequencing technologies. To obtain the full-length mitochondrial genome with high accuracy, the fastp and filtlong software were used to filter the original data and obtain high-quality reads. We got 1.6 million reads (MRs) (QC > 30) with a total length of 15,705 million nucleotides (nt) by PacBio sequencing. The average read length is 9987 bp. Thirty-eight million reads were obtained with 11.4 Gb data by Illumina sequencing technology. After the complete mt genome of F. carica was assembled, which was submitted to GenBank under accession No. OQ629317 (https://www.ncbi.nlm.nih.gov/nuccore/OQ629317), spanning a length of 480,902 bp, it exhibited the characteristic circular structure commonly found in genomes of terrestrial plants (Fig. 1). The overall base composition of the complete mitogenome was 27.24% A, 27.30% T, 22.64% G, and 22.81% C, with a GC content of 45.45% (Table 1). PCGs, cis introns, and tRNA and rRNA genes respectively accounted for 5.42%, 7.66%, 0.35%, and 1.13% of the whole mitogenome. Overall, 46 unique genes, including 27 protein-coding, 16 tRNA, and 3 rRNA genes, were identified in the F. carica mitogenome (Table 2).

Fig. 1.
Fig. 1.

Circular map of the Ficus carica mitogenome. Genes shown on the outside and inside of the circle are transcribed clockwise and counterclockwise, respectively. Genes belonging to different functional groups are color-coded. The dark gray region in the inner circle depicts GC content. Asterisks besides genes denote intron-containing genes.

Citation: J. Amer. Soc. Hort. Sci. 148, 6; 10.21273/JASHS05328-23

Table 1.

Genomic features of the F. carica mitogenome.

Table 1.
Table 2.

Gene profile and organization of the F. carica mitogenome.

Table 2.

Codon usage analysis of PCGs.

PCGs in F. carica had a total length of 26,079 nucleotides. Most PCGs had the typical ATG start codon; the exception, in atp6, was ACG, which may have been altered by C-to-U RNA editing (Table 2). Similar to the situation in other mitogenomes, TAA, TGA, and TAG served as stop codons. Interestingly, evidence of C-to-U RNA editing was also observed in the stop codons of atp9 and ccmFc (Ma et al. 2022).

We analyzed the relative synonymous codon usage (RSCU) of 27 PCGs in the F. carica mitogenome, which showed that all codon types were present (Fig. 2). The 27 PCGs comprised 26,079 bp encoding 8693 codons, excluding termination codons. In addition, all RSCU values of NNT and NNA codons, except for Ala (GCA), Ile (ATA), and Thr (ACA), were higher than 1.0. This result indicates the existence of a strong A or T bias at the third codon position in the F. carica mitogenome, which is a very common phenomenon in mitogenomes of all studied land plant species (Ma et al. 2022).

Fig. 2.
Fig. 2.

Relative synonymous codon usage (RSCU) in the Ficus carica mitogenome. Codon families are shown on the x-axis. RSCU values are the number of times a particular codon is observed relative to the number of times that codon would be expected for a uniform synonymous codon usage.

Citation: J. Amer. Soc. Hort. Sci. 148, 6; 10.21273/JASHS05328-23

Analysis of synonymous and nonsynonymous substitution rates.

To understand the evolutionary dynamics of genes, the nonsynonymous-to-synonymous substitution ratio (Ka/Ks) is usually analyzed. In this study, we determined the Ka/Ks ratio of 22 PCGs common to F. carica, Arabidopsis thaliana, and Prunus davidiana (Fig. 3). We found that nearly all Ka/Ks ratios were less than 1.0, which is indicative of stabilizing selection during evolution. In contrast, the Ka/Ks ratios of three genes (ccmB, nad3, and nad7) were greater than 1.0, which suggests these genes have been under positive selection during evolution. Finally, the Ka/Ks ratio of atp4 was close to 1, thus indicating that this gene has experienced neutral evolution since the divergence of F. carica from the common ancestor of the three plant species.

Fig. 3.
Fig. 3.

Ka/Ks ratios of 26 protein-coding genes in Ficus carica, Arabidopsis thaliana, and Prunus davidiana.

Citation: J. Amer. Soc. Hort. Sci. 148, 6; 10.21273/JASHS05328-23

Prediction of RNA editing sites in PCGs.

RNA editing is a posttranscriptional process, and cytidine (C)-to-uridine (U) RNA editing is enriched in mt and cp genomes (Fang et al. 2021; Ngadhnjim et al. 2023). The PREP-mt program was used to predict 397 RNA editing sites in 27 PCGs of the F. carica mt genome and 100% C-to-U RNA editing. As shown in Fig. 4, the nad4 gene encoded the most RNA editing sites (44 sites), whereas atp8, cox3, and nad4L only encoded one. Among the 397 predicted sites, 31.49% and 68.51% were present at first and second codon positions, respectively, whereas none were found at the third position. Further analysis of the RNA-edited amino acids revealed the following conversions had taken place: hydrophilic to hydrophobic (48.1%; 191 sites), hydrophobic to hydrophilic (8.56%; 34 sites), hydrophilic to hydrophilic (13.35%; 53 sites), and hydrophobic to hydrophobic (29.47%; 117 sites), with two amino acids of atp9 and ccmFc genes also converted from arginine to a stop codon (Table 2).

Fig. 4.
Fig. 4.

The distribution of RNA editing sites in the Ficus carica mitogenome. The number shown by the gray box represents the RNA editing sites of each gene.

Citation: J. Amer. Soc. Hort. Sci. 148, 6; 10.21273/JASHS05328-23

Analysis of repeats in the F. carica mitogenome.

SSRs, which are tandemly repeated motifs of one to six bases, are useful molecular markers for studying genetic diversity and identifying species (Ma et al. 2017). In this study, 149 perfect SSRs were identified in the F. carica mitogenome, including 54 (36.24%) mono, 31 (20.81%) di-, 17 (11.41%) tri, 45 (30.20%) tetra-, and 2 (1.34%) penta-repeats (Table 3). Further analysis of SSR repeat units indicated that 94.44% of monomers were A/T repeats and that 41.94% of dinucleotide repeats were AT/TA motifs, with smaller numbers of tri, tetra-, and penta-nucleotide repeats. The high AT content of SSRs contributed to the AT richness (54.55%) of the complete F. carica mitogenome.

Table 3.

Frequency of identified SSR motifs in the F. carica mitogenome.

Table 3.

Apart from SSRs, 247 short (<1 kb) and large (≥1 kb) repeats, including 103 forward (Supplemental Table 2), 141 palindromic (Supplemental Table 3), and 13 tandem ones (Supplemental Table 4), were identified in the F. carica mitogenome. These repeats had a total length of 39,767 bp, corresponding to 8.27% of the mitogenome. As shown in Fig. 5 and Supplemental Table 3, most repeats ranged from 29 to 100 bp; 65 were longer than 100 bp, and only six were longer than 1 kb. The longest repeat was 2000 bp (Fig. 5).

Fig. 5.
Fig. 5.

The frequency distribution of repeat lengths in the Ficus carica mt genome.

Citation: J. Amer. Soc. Hort. Sci. 148, 6; 10.21273/JASHS05328-23

Phylogenetic analysis.

The increased number of complete plant mitogenomes that have been assembled provides an important opportunity to use mitogenomes for phylogenetic analysis. To determine the phylogenetic position of F. carica, we downloaded 21 plant mitogenomes from GenBank (https://www.ncbi.nlm.nih.gov/genome/browse/) (Supplemental Table 1) and constructed a phylogenetic tree based on a set of 26 conserved single-copy genes present in all 22 analyzed mitogenomes. As shown in Fig. 6, 15 of the 19 nodes in the generated tree had bootstrap support values over 70%, including nine nodes with 100% support. The phylogenetic tree strongly supports (bootstrap support = 100%) the close phylogenetic relationship between F. carica and two other members of the Moraceae, M. notabilis and C. sativa. Overall, the result of our analysis of mitogenomes provides a valuable foundation for future analyses of the phylogenetic affinities of Ficus species.

Fig. 6.
Fig. 6.

Maximum-likelihood phylogenetic tree based on 26 single-copy orthologous genes shared among 22 species. Numbers at nodes are bootstrap support values. The position of Ficus carica is indicated in bold. Vitis vinifera and Ginkgo biloba served as outgroups.

Citation: J. Amer. Soc. Hort. Sci. 148, 6; 10.21273/JASHS05328-23

Plastid-derived and nuclear-shared sequence transfer events.

DNA fragment transfers among nuclear and organellar genomes are common events during plant evolution (Bi et al. 2020; Ma et al. 2022). We obtained 619 hits covering 237.8 kb of sequences of the nuclear genome transferred to the mitogenome. The number of hits and percent coverage differed among chromosomes (Fig. 7). Chromosome 7 had the maximum total length of hits (37.56 kb), which was much larger than that on other chromosomes, and the highest percent coverage (0.16%) also occurred on this chromosome (Fig. 8A). The lengths of transferred fragments, which included genes such as trnF-GAA, trnM-CAT, trnV-GAC, trnR-ACG, trnC-GCA, cox2, and nad4, were mainly between 200 and 500 bp (Fig. 8B).

Fig. 7.
Fig. 7.

Schematic for the chloroplast-to-mitochondrial gene transfer in Ficus carica species. A colored line within the circle represents the areas of the chloroplast genome that were transferred across the specified position in the mitochondrial genome.

Citation: J. Amer. Soc. Hort. Sci. 148, 6; 10.21273/JASHS05328-23

Fig. 8.
Fig. 8.

Characteristics of nuclear-mitochondrial sequences in Ficus carica. (A) Distributions of percent identities between shared nuclear-mitochondrial matches. The number of matches is shown by blue boxes and is plotted on the left ordinate. The orange lines, which represent the coverage of matches on nuclear and mitochondrial genomes, are plotted on the right ordinate. (B) Distributions of lengths between shared nuclear-mitochondrial matches.

Citation: J. Amer. Soc. Hort. Sci. 148, 6; 10.21273/JASHS05328-23

The length of the generated F. carica mitogenome was ∼3.0 times longer than that of the cp genome (160,602 bp). We identified five large mitogenome fragments in the cp genome; these fragments had lengths ranging from 1266 to 5756 bp and harbored five genes (trnA-UGC, trnI-GAU, trnV-GAC, trnR-ACG, and trnN-GUU) (Fig. 7, Table 4). The remaining fragments were partial sequences of transferred genes or intergenic spacer regions in the cp genome. The transferred fragments had a total length of 26,687 bp and accounted for ∼5.55% of the mitogenome.

Table 4.

Fragments transferred from chloroplasts to mitochondria in Ficus carica.

Table 4.

Discussion

Characterization of the F. carica mt genome.

Mitochondria produce the energy required to carry out life processes. Because plant mitogenomes are characterized by extensive variations in size, sequence arrangements, and repeat contents, they are generally more complex than those of animals (Cheng et al. 2021; Kozik et al. 2019). Knowledge of the function, inheritance, and evolutionary trajectories of mitogenomes is key to the understanding of mitogenome structure (Ma et al. 2017). In this study, we first characterized the complete F. carica mitogenome in detail. The F. carica mitogenome, like that of Brassica, is moderate in size relative to most other genomes (Chang et al. 2021). Similar to most mitogenomes, the F. carica mitogenome is a circular structure comprising 480,902 bp. GC content is an important factor for assessing species. The GC content of the F. carica mitogenome is 45.45%, which is close to that of other sequenced plant mitogenomes, such as Arabidopsis thaliana (44.8%) (Unseld et al. 1997), Phaseolus vulgaris (45.11%) (Bi et al. 2016), and Acer truncatum (Ma et al. 2017). Most sequences in the F. carica mitogenome are noncoding, with PCGs accounting for only 5.42% of the total length. This paucity of coding genes is probably due to a gradual increase in sequence duplication during evolution (Ma et al. 2017).

Identification of repeat sequences and RNA editing sites.

Repeat sequences, including tandem, short, and large repeats, are widely present in mitogenomes (Gualberto et al. 2014; Guo et al. 2017). Because they can contribute to structural variation and the formation of extremely large mitogenomes, repeat sequences generally have an important role in intermolecular recombination in mtDNA (Yong et al. 2021). In the present study, we found that AT motifs were a common component of many SSR repeats. We also identified forward, palindromic, and tandem repeats in the F. carica mitogenome. The longest repeat had a length of 2000 bp. These findings suggest that intermolecular recombination has frequently occurred in the F. carica mitogenome during evolution.

RNA editing, a posttranscriptional process that occurs in cp and mt genomes, plays an important role in protein folding (Bi et al. 2016; Ma et al. 2017). Previous studies have revealed ∼491 RNA editing sites within 34 genes in rice (Dong et al. 2018) and 441 within 36 genes in Arabidopsis. In our study, we identified 397 RNA editing sites in 27 PCGs in the F. carica mt genome. Although the number of RNA editing sites varied greatly among genes, our identification of RNA editing sites provides essential clues to the functions of genes with novel codons. We found that the largest numbers of RNA editing sites were present in cytochrome c biogenesis and NADH dehydrogenase genes, which is similar to Acer truncatum (Ma et al. 2017) and P. vulgaris (Bi et al. 2020).

DNA fragment transfer events.

Previous studies have shown that the most prominent transfer direction in angiosperms is from organellar genomes to the nuclear genome, followed in importance by transfer from nuclear and plastid genomes to the mitogenome (Notsu et al. 2002; Rice et al. 2013; Stegemann et al. 2012; Wang et al. 2012). The total length of transferred DNA varies among plant species, with lengths ranging from 50 kb (Arabidopsis thaliana) to 1.1 Mb (Oryza sativa ssp. japonica) (Zhao et al. 2018). In our study, we found that 237.8 kb of sequences of the nuclear genome have been transferred to the mitogenome of F. carica. Although evidence of nuclear-mitochondrial transfer was found on every F. carica chromosome, the amount and percentage of shared material differed among chromosomes. This result is similar to findings in soybean (Smith et al. 2011). With regard to cp genome to mitogenome migration events, we found that 25 fragments, accounting for 5.55% of the F. carica mitogenome, were derived from the cp genome. The integrated fragments include five genes, which are, interestingly, all tRNA genes.

Conclusions

In this study, we assembled and annotated the mitogenome of F. carica and performed extensive analyses based on the sequences of annotated genes. The F. carica mitogenome features are similar to other fruits, which is circular, with a length of 480,902 bp. We annotated 46 genes, including 27 protein-coding, 16 tRNA, and 3 rRNA genes. The evolutionary status of F. carica was verified by phylogenetic analysis based on the 22 mitogenomes. Gene conservation between chloroplast and mitochondrial genomes and between nuclear and mitochondrial genomes were also detected in F. carica by analyzing gene migration. Our study has yielded extensive information about the F. carica mitogenome. More importantly, the data provided valuable information and theoretical basis for F. carica in the future.

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  • Lowe T, Eddy S. 1997. tRNAscan-SE: A programfor improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25(5):955964. https://doi.org/10.1093/nar/25.5.955.

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  • Ma Q, Li S, Bi C, Hao Z, Sun C, Ye N. 2017. Complete chloroplast genome sequence of a major economic species, Ziziphus jujuba (Rhamnaceae). Curr Genet. 63:117129. https://doi.org/10.1007/s00294-016-0612-4.

    • Search Google Scholar
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  • Ma Q, Wang Y, Li S, Wen J, Li Q. 2022. Assembly and comparative analysis of the first complete mitochondrial genome of acer truncatum bunge: A woody oil-tree species producing nervonic acid. BMC Plant Biol. 22(1):117. https://doi.org/10.1186/s12870-021-03416-5.

    • Search Google Scholar
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  • Mawa S, Husain K, Jantan I. 2013. Ficus carica L. (Moraceae): Phytochemistry, traditional uses and biological activities, evidence-based complement. Altern. Med. 2013:113. https://doi.org/10.1155/2013/974256.

    • Search Google Scholar
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  • Mower J. 2005. PREP-Mt: Predictive RNA editor for plant mitochondrial genes. BMC Bioinformatics. 6:96. https://doi.org/10.1186/1471-2105-6-96.

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  • Mori K, Shirasawa K, Nogata H, Hirata C, Tashiro K, Habu T, Kim S, Himeno S, Kuhara S, Ikegami H. 2017. Identification of RAN1orthologue associated with sex determination through whole genomesequencing analysis in fig (Ficus carica L.). Sci Rep. 7:41124. https://doi.org/10.1038/srep41124.

    • Search Google Scholar
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  • Ngadhnjim L, Maria MA, Irem T, Salvatore DG, Thorsten S. 2023. Precise and efficient C-to-U RNA base editing with SNAP-CDAR-S. Nucleic Acids Res. 2023:112. https://doi.org/10.1093/nar/gkad598.

    • Search Google Scholar
    • Export Citation
  • Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K. 2002. The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: Frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics. 268:434445. https://doi.org/10.1007/s00438-002-0767-1.

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  • Park S, Han J, Im K, Whang WK, Min H. 2013. Antioxidative and antiinflammatory activities of an ethanol extract from fig (Ficus carica) branches. Food Sci Biotechnol. 22(4):10711075. https://doi.org/10.1007/s10068-013-0185-7.

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  • Qi ZY, Zhao JY, Lin FJ, Zhou WL, Gan RY. 2021. Bioactive compounds, therapeutic activities, and applications of ficus pumila L. Agronomy. 11(1):120. https://doi.org/10.3390/agronomy11010089.

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  • Stegemann S, Keuthe M, Greiner S, Bock R. 2012. Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci USA. 109(7):24342438. https://doi.org/10.1073/pnas.1114076109.

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  • Turco VL, Potortì AG, Tropea A, Dugo G, Di Bella G. 2020. Element analysis of dried figs (Ficus carica L.) from the Mediterranean areas. J Food Compos Anal. 90:103503. https://doi.org/10.1016/j.jfca.2020.103503.

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  • Fig. 1.

    Circular map of the Ficus carica mitogenome. Genes shown on the outside and inside of the circle are transcribed clockwise and counterclockwise, respectively. Genes belonging to different functional groups are color-coded. The dark gray region in the inner circle depicts GC content. Asterisks besides genes denote intron-containing genes.

  • Fig. 2.

    Relative synonymous codon usage (RSCU) in the Ficus carica mitogenome. Codon families are shown on the x-axis. RSCU values are the number of times a particular codon is observed relative to the number of times that codon would be expected for a uniform synonymous codon usage.

  • Fig. 3.

    Ka/Ks ratios of 26 protein-coding genes in Ficus carica, Arabidopsis thaliana, and Prunus davidiana.

  • Fig. 4.

    The distribution of RNA editing sites in the Ficus carica mitogenome. The number shown by the gray box represents the RNA editing sites of each gene.

  • Fig. 5.

    The frequency distribution of repeat lengths in the Ficus carica mt genome.

  • Fig. 6.

    Maximum-likelihood phylogenetic tree based on 26 single-copy orthologous genes shared among 22 species. Numbers at nodes are bootstrap support values. The position of Ficus carica is indicated in bold. Vitis vinifera and Ginkgo biloba served as outgroups.

  • Fig. 7.

    Schematic for the chloroplast-to-mitochondrial gene transfer in Ficus carica species. A colored line within the circle represents the areas of the chloroplast genome that were transferred across the specified position in the mitochondrial genome.

  • Fig. 8.

    Characteristics of nuclear-mitochondrial sequences in Ficus carica. (A) Distributions of percent identities between shared nuclear-mitochondrial matches. The number of matches is shown by blue boxes and is plotted on the left ordinate. The orange lines, which represent the coverage of matches on nuclear and mitochondrial genomes, are plotted on the right ordinate. (B) Distributions of lengths between shared nuclear-mitochondrial matches.

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  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 35(6):15471549. https://doi.org/10.1093/molbev/msy096.

    • Search Google Scholar
    • Export Citation
  • Li Z, Yang Y, Liu M, Zhang C, Cui Q. 2021. A comprehensive review on phytochemistry, bioactivities, toxicity studies, and clinical studies on Ficus Carica Linn. leaves. Biomed Pharmacother. 137:111393. https://doi.org/10.1016/j.biopha.2021.111393.

    • Search Google Scholar
    • Export Citation
  • Lowe T, Eddy S. 1997. tRNAscan-SE: A programfor improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25(5):955964. https://doi.org/10.1093/nar/25.5.955.

    • Search Google Scholar
    • Export Citation
  • Ma Q, Li S, Bi C, Hao Z, Sun C, Ye N. 2017. Complete chloroplast genome sequence of a major economic species, Ziziphus jujuba (Rhamnaceae). Curr Genet. 63:117129. https://doi.org/10.1007/s00294-016-0612-4.

    • Search Google Scholar
    • Export Citation
  • Ma Q, Wang Y, Li S, Wen J, Li Q. 2022. Assembly and comparative analysis of the first complete mitochondrial genome of acer truncatum bunge: A woody oil-tree species producing nervonic acid. BMC Plant Biol. 22(1):117. https://doi.org/10.1186/s12870-021-03416-5.

    • Search Google Scholar
    • Export Citation
  • Mawa S, Husain K, Jantan I. 2013. Ficus carica L. (Moraceae): Phytochemistry, traditional uses and biological activities, evidence-based complement. Altern. Med. 2013:113. https://doi.org/10.1155/2013/974256.

    • Search Google Scholar
    • Export Citation
  • Mower J. 2005. PREP-Mt: Predictive RNA editor for plant mitochondrial genes. BMC Bioinformatics. 6:96. https://doi.org/10.1186/1471-2105-6-96.

    • Search Google Scholar
    • Export Citation
  • Mori K, Shirasawa K, Nogata H, Hirata C, Tashiro K, Habu T, Kim S, Himeno S, Kuhara S, Ikegami H. 2017. Identification of RAN1orthologue associated with sex determination through whole genomesequencing analysis in fig (Ficus carica L.). Sci Rep. 7:41124. https://doi.org/10.1038/srep41124.

    • Search Google Scholar
    • Export Citation
  • Ngadhnjim L, Maria MA, Irem T, Salvatore DG, Thorsten S. 2023. Precise and efficient C-to-U RNA base editing with SNAP-CDAR-S. Nucleic Acids Res. 2023:112. https://doi.org/10.1093/nar/gkad598.

    • Search Google Scholar
    • Export Citation
  • Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K. 2002. The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: Frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics. 268:434445. https://doi.org/10.1007/s00438-002-0767-1.

    • Search Google Scholar
    • Export Citation
  • Park S, Han J, Im K, Whang WK, Min H. 2013. Antioxidative and antiinflammatory activities of an ethanol extract from fig (Ficus carica) branches. Food Sci Biotechnol. 22(4):10711075. https://doi.org/10.1007/s10068-013-0185-7.

    • Search Google Scholar
    • Export Citation
  • Qi ZY, Zhao JY, Lin FJ, Zhou WL, Gan RY. 2021. Bioactive compounds, therapeutic activities, and applications of ficus pumila L. Agronomy. 11(1):120. https://doi.org/10.3390/agronomy11010089.

    • Search Google Scholar
    • Export Citation
  • Richardson AO, Rice DW, Young GJ, Alverson AJ, Palmer JD. 2013. The “fossilized” mitochondrial genome of Liriodendron tulipifera: Ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate. BMC Biol. 11:117. https://doi.org/10.1186/1741-7007-11-29.

    • Search Google Scholar
    • Export Citation
  • Rice DW, Alverson AJ, Richardson AO, Young GJ, Sanchez-Puerta MV, Munzinger J, Barry K, Boore JL, Zhang Y, dePamphilis CW, Knox EB, Palmer JD. 2013. Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science. 342:14681473. https://doi.org/10.1126/science.1246275.

    • Search Google Scholar
    • Export Citation
  • Rubnov S, Kashman Y, Rabinowitz R, Schlesinger M, Mechoulam R. 2001. Suppressors of cancer cell proliferation from fig (Ficus carica) resin: Isolation and structure elucidation. J Nat Prod. 64:993996. https://doi.org/10.1021/np000592z.

    • Search Google Scholar
    • Export Citation
  • Saeed MA, Sabir AW. 2002. Irritant potential of triterpenoids from Ficus carica leaves. Fitoterapia. 73:417–420. https://doi.org/10.1016/S0367-326X(02)00127-2.

  • Schoch CL, Ciufo S, Domrachev M, Hotton CL, Kannan S, Khovanskaya R, Leipe D, Mcveigh R, O’Neill K, Robbertse B, Sharma S, Soussov V, Sullivan JP, Sun L, Turner S, Karsch-Mizrachi I. 2020. NCBI taxonomy: A comprehensive update on curation, resources and tools. Database (Oxford). 2020:121. https://doi.org/10.1093/database/baaa062.

    • Search Google Scholar
    • Export Citation
  • Shengxin C, Yankun W, Jiangjie L, Junyi G, Jijie L, Pu C, Rongzhan G, Tuanjie Z. 2013. The mitochondrial genome of soybean reveals complex genome structures and gene evolution at intercellular and phylogenetic levels. PLoS One. 8:114. https://doi.org/10.1371/journal.pone.0056502.

    • Search Google Scholar
    • Export Citation
  • Skippington E, Barkman T, Rice D, Palmer J. 2015. Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes. Proc Natl Acad Sci USA. 112(27):E3515. https://doi.org/10.1073/pnas.1504491112.

    • Search Google Scholar
    • Export Citation
  • Sloan D, Alverson A, Chuckalovcak J, Wu M, Mccauley D. 2012. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 10(1):117. https://doi.org/10.1371/journal.pbio.1001241.

    • Search Google Scholar
    • Export Citation
  • Smith D, Crosby K, Lee R. 2011. Correlation between nuclear plastid DNA abundance and plastid number supports the limited transfer window hypothesis. Genome Biol Evol. 3:365371. https://doi.org/10.1093/gbe/evr001.

    • Search Google Scholar
    • Export Citation
  • Stegemann S, Keuthe M, Greiner S, Bock R. 2012. Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci USA. 109(7):24342438. https://doi.org/10.1073/pnas.1114076109.

    • Search Google Scholar
    • Export Citation
  • Thiel T, Michalek W, Varshney R, Graner A. 2003. Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet. 106:411422. https://doi.org/10.1007/s00122-002-1031-0.

    • Search Google Scholar
    • Export Citation
  • Turco VL, Potortì AG, Tropea A, Dugo G, Di Bella G. 2020. Element analysis of dried figs (Ficus carica L.) from the Mediterranean areas. J Food Compos Anal. 90:103503. https://doi.org/10.1016/j.jfca.2020.103503.

  • Unseld M, Marienfeld J, Brandt P, Brennicke A. 1997. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet. 15:5761. https://doi.org/10.1038/ng0197-57.

    • Search Google Scholar
    • Export Citation
  • Usai G, Mascagni F, Giordani T, Vangelisti A, Bosi E, Zuccolo A, Ceccarelli M, King R, Hassani-Pak K, Zambrano LS, Cavallini A, Natali L. 2020. Epigenetic patterns within the haplotype phased fig (Ficus carica L.) genome. Plant J. 102(3):600614. https://doi.org/10.1111/tpj.14635.

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Supplementary Materials

Lingzhu Wei Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China

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Ting Zheng Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China

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Jiang Xiang Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China

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Jianhui Cheng Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China

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Jiang Wu Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China

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Contributor Notes

The complete mitgenome sequences of Ficus carica were deposited in the GenBank database with accession numbers OQ629317.

J.C. and J.W. are the corresponding authors. Email: jianhuicheng@126.com and wujiang@zaas.ac.cn.

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  • Fig. 1.

    Circular map of the Ficus carica mitogenome. Genes shown on the outside and inside of the circle are transcribed clockwise and counterclockwise, respectively. Genes belonging to different functional groups are color-coded. The dark gray region in the inner circle depicts GC content. Asterisks besides genes denote intron-containing genes.

  • Fig. 2.

    Relative synonymous codon usage (RSCU) in the Ficus carica mitogenome. Codon families are shown on the x-axis. RSCU values are the number of times a particular codon is observed relative to the number of times that codon would be expected for a uniform synonymous codon usage.

  • Fig. 3.

    Ka/Ks ratios of 26 protein-coding genes in Ficus carica, Arabidopsis thaliana, and Prunus davidiana.

  • Fig. 4.

    The distribution of RNA editing sites in the Ficus carica mitogenome. The number shown by the gray box represents the RNA editing sites of each gene.

  • Fig. 5.

    The frequency distribution of repeat lengths in the Ficus carica mt genome.

  • Fig. 6.

    Maximum-likelihood phylogenetic tree based on 26 single-copy orthologous genes shared among 22 species. Numbers at nodes are bootstrap support values. The position of Ficus carica is indicated in bold. Vitis vinifera and Ginkgo biloba served as outgroups.

  • Fig. 7.

    Schematic for the chloroplast-to-mitochondrial gene transfer in Ficus carica species. A colored line within the circle represents the areas of the chloroplast genome that were transferred across the specified position in the mitochondrial genome.

  • Fig. 8.

    Characteristics of nuclear-mitochondrial sequences in Ficus carica. (A) Distributions of percent identities between shared nuclear-mitochondrial matches. The number of matches is shown by blue boxes and is plotted on the left ordinate. The orange lines, which represent the coverage of matches on nuclear and mitochondrial genomes, are plotted on the right ordinate. (B) Distributions of lengths between shared nuclear-mitochondrial matches.

 

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