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Intracellular gene transfer (IGT) events from the mitochondrial genome to the plastid genome of the subtribe Ferulinae Drude (Apiaceae) and their implications

BMC Plant Biology volume 24, Article number: 1172 (2024) Cite this article

A Correction to this article was published on 27 December 2024

This article has been updated

Abstract

Background

Intracellular gene transfer (IGT) is a phenomenon in genome evolution that occurs between the nuclear and organellar genomes of plants or between the genomes of different organelles. The majority of the plastid genomes (plastomes) in angiosperms have a conserved structure, but some species exhibit unexpected structural variations.

Results

In this study, we focused on the Ferulinae, which includes Ferula, one of the largest genera in the Apiaceae family. We discovered IGTs in the rps12-trnV IGS region of the plastome’s inverted repeat (IR). We found that partial mitochondrial genome (mitogenome) sequences, ranging in length from about 2.8 to 5.8 kb, were imported into the plastome. In addition to these, that are known from other Scandiceae subtribes, the Ferulinae plastomes contained two unique mitogenome sequences. We have named these sequences Ferula Mitochondrial Plastid sequences (FeMP). FeMP1 varies in length from 336 bp to 1,100 bp, while FeMP2 ranges from 50 bp to 740 bp in length, with the exception of F. conocaula and F. kingdon-wardii, which do not possess FeMP2. Notably, FeMP2 includes a complete rps7 gene of mitogenome origin. In the maximum likelihood (ML) tree constructed from 79 protein-coding genes, Ferulinae appears as a monophyletic group, while Ferula shows paraphyly. Dorema and Fergania are nested within the Ferula clade, sharing the unusual characteristics of the Ferula plastome. Based on these findings, a reclassification of Dorema and Fergania is warranted.

Conclusions

Our results shed light on the mechanism of plastome evolution in the Scandiceae with a focus on the unique plastome structure found in the Apiaceae. These findings enhance our understanding of the evolution of plant organellar genomes.

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Background

Plants possess three distinct organelles: the Nucleus (nr), Mitochondrion (mt), and Plastid (pt), each harboring its own genome. These organelles have evolved independently. Plant plastid genomes (plastomes) are notable for their conservation in gene content, gene order, and genome length, making them valuable in phylogenetic and evolutionary studies of angiosperms. The length of angiosperm plastomes typically ranges between 120 and 170 kb [1, 2]. A typical plastome is characterized by a quadripartite structure, comprising a large single copy (LSC), a small single copy (SSC), and two inverted repeats (IRs). While most angiosperms display a typical structure, some species demonstrate unexpected structural changes, including genomic rearrangements, indels, IR expansion/contraction, and intracellular/horizontal gene transfer (IGT). IGT refers to the transfer of genomic segments between the organelle genomes within a cell. It predominantly involves transfers from the plastid or mitochondrion to the nucleus (PTNR or MTNR), with NRMT being common. The plastome’s structure remains relatively conserved owing to the IRs. However, instances of MTPT or NRPT transfers have been documented in several taxa, including Anacardium [3], Asclepias [4], Convallaria [5], Pariana [6], and Paspalum [7]. Additionally, IGT studies focusing on MTPT or NRPT have been reported within the Apiaceae family [8,9,10,11,12].

Ferulinae Drude represents one of the four subtribes within the Scandiceae tribe of the Apiaceae family. It encompasses five genera with a total of over 240 species according to Plants of the World Online (POWO, https://powo.science.kew.org/). The majority of these species are classified under the genus Ferula Tourn. ex L., which alone comprises about 220 species. This is followed by the genus Leutea Pimenov, which includes 9 species, and Autumnalia Pimenov, with 2 species. Additionally, the subtribe contains the genera Fergania Pimenov and Kafirnigania Kamelin & Kinzik, each represented by a single species.

Ferula stands as the second-largest genus in the Apiaceae family, trailing only behind Eryngium, which encompasses about 250 species according to POWO. The genus Ferula boasts a wide distribution across Asia, Africa, and Europe, with no presence in America and Oceania. Similar to other genera in the Apiaceae family, Ferula has undergone numerous taxonomic reevaluations alongside related taxa. This is due to its broad distribution and morphological similarities among species [13,14,15]. Recent studies have shed light on the complete plastome of Ferula [16,17,18], providing evidence to support the previous assertions that the genera Schumannia, Soranthes, and Talassia, previously considered distinct from Ferula, should be reclassified under Ferula.

Dorema D. Don is a taxon that has sparked considerable debate within botanical taxonomy. Originally encompassing 12 accepted species, Dorema was differentiated from the closely related genus Ferula based on specific morphological features, such as the structure of simple umbels and the length of pedicels in flowers and fruits. However, Dorema and Ferula exhibit very similar morphological characteristics [19], blurring the lines between the two genera. Phylogenetic studies employing molecular markers (nrITS, rpoB-trnC, rps16 intron, and rpoC1 intron) have further supported the integration of Dorema species within the Ferula clade. Consequently, several researchers have proposed that Dorema should be subsumed into Ferula [14, 20,21,22]. This perspective is mirrored in widely recognized plant lists such as POWO and the Global Biodiversity Information Facility (GBIF, https://www.gbif.org), which now treat Dorema as synonymous with Ferula.

Fergania is a monotypic genus, comprising sole the species Fergania polyantha (Korovin) Pimenov, endemic to Central Asia. Its unique fruit morphology—specifically the characteristics of the pericarp, jugular veins, and aerenchyma—sets it apart from the closely related genus Ferula [23]. Molecular research utilizing nuclear ribosomal internal transcribed spacer (nrITS) sequences has placed Fergania within the Ferula clade, similar to Dorema [24]. This alignment further underscores the intricate phylogenetic relationships and challenges in delineating clear boundaries among these closely related taxa within the Apiaceae family.

In the Apiaceae, more than 400 complete plastome sequences have been reported in the NCBI GenBank, most of which maintain the typical quadripartite structure seen in flowering plants. However, the Scandiceae tribe exhibits an exceptionally unusual plastome compared to other Apiaceae groups. Notably, sequences transferred from the mitochondrion to the plastid (MTPT) were identified for the first time in Apiaceae within the rps12-trnV noncoding region of the carrot (genus Daucus) plastome, marking a groundbreaking discovery [9, 10]. This sequence, confirmed to have originated from four regions of the D. carota mitogenome (NC_017855), was designated as the D. carota Mitochondrial Plastid (DcMP) sequence. Subsequently, MTPT sequences have been detected in the genera Cuminum [25] and Thapsia, which are part of the Daucinae subtribe, demonstrating the occurrence of these sequences beyond a single genus. The genus Caucalis also showcases this phenomenon, with the Caucalis platycarpos Mitochondrial Plastid (CpMP) sequence incorporating both MTPT and NRPT sequences, in addition to the DcMP sequence [12]. Moreover, the MTPT sequence was confirmed in Torilis scabra [26], a member of the same subtribe, underscoring the prevalence of IGT within this lineage. Despite these findings, such events have not been confirmed in Scandicinae, another subtribe of Scandiceae [8]. Recently, complete plastomes of the Ferulinae were reported [17, 18], yet these studies did not delve into discussions of IGT events, leaving room for further exploration within this subtribe.

In our study, we present the complete plastome sequences of six species from the Ferulinae subtribe, including four from the genus Ferula, one from Dorema, and one from Fergania (Fig. 1). The research was conducted with the following objectives in mind: (1) This study aimed to identify sequences transferred from the mitochondrion to the plastid (MTPT) within the complete plastomes of Ferulinae species, marking the first investigation of intergenomic gene transfer (IGT) within the Scandiceae tribe where such events have not been previously explored. (2) By uncovering these sequences, we sought to enhance our understanding of the patterns of plastome evolution influenced by IGT within the Scandiceae. (3) Additionally, the identification of these MTPT sequences is anticipated to provide critical insights necessary for reevaluating the phylogenetic relationships of Ferulinae, a subtribe whose classification has been subject to uncertainty.

Fig. 1
figure 1

Field photos of six Ferulinae Species. A Dorema microcarpum, B Ferula karatavica, C Ferula prangifolia, D Ferula tschimganica, E Ferula peeninervis, F Fergania polyanth

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Results

Characteristics of the ferulinae plastome

The six complete plastomes of the Ferulinae display the characteristic quadripartite structure common to most flowering plants, as illustrated in Fig. 2. The total lengths of these plastomes vary, ranging from 165,316 base pairs (bp) in Fergania polyantha to 166,517 bp in Ferula tschimganica. The large single-copy (LSC), small single-copy (SSC), and one inverted repeat (IR) regions are approximately 85 kb, 17 kb, and 31 kb in length, respectively. Table 1 summarizes the detailed length information for each region. All six plastomes share identical gene content, comprising 79 protein-coding genes, 30 tRNA genes, and 4 rRNA genes. The guanine-cytosine (GC) content is consistent across the plastomes at 38.0%, with the exception of Fergania polyantha, which has a slightly lower GC content of 37.9%.

Table 1 General features of six Ferulinae complete plastomes
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Fig. 2
figure 2

Circular plastome map of six Ferulinae Species. The total length ranged from 165,316 bp in Fergania polyantha to 166,517 bp in Ferula tschimganica. Their gene contents are similar to the typical plastome of flowering plants. They have the MTPT sequences (5.1–5.8 kb) in both IR regions. The dark grey and light grey in the inner circle indicate GC and AT contents, respectively. Asterisks indicate genes containing introns

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Codon usage

The relative synonymous codon usage (RSCU) values were calculated using 79 protein-coding genes (PCGs) commonly present in six Ferulinae plastomes (Fig. S1 and Table S2). A total of 64 codons were identified, including three stop codons (UAA, UAG, and UGA). The number of encoded codons ranged from 22,636 (Fergania polyantha) to 22,650 (Ferula prangifolia). Among these, leucine (Leu), encoded by six codons (CUA, CUC, CUG, CUU, UUA, and UUG), was the most abundant (2,381–2,387 codons), whereas tryptophan (Trp), encoded by a single codon (UGG), was the least abundant (398 codons in all plastomes). The RSCU values of all codons ranged from 0.309 (AGC for serine, in F. penninervis) to 1.987 (UUA for leucine, in F. karatavica) across all species. Among these, UUA is the most commonly used codon (RSCU > 1.9), whereas AGC is the least used (RSCU < 0.32).

Large and simple sequence repeats (LSRs and SSRs)

Four types of large sequence repeats (LSRs) were detected: forward, reverse, palindromic, and complement repeats (Fig. S2 and Table S3). Of the total 349 LSRs, palindromic repeats (22–31) were the most common, followed by forward repeats (25–30). Complement repeats were identified in both Fergania polyantha (1) and Ferula tschimganica (2). The only reverse repeat was identified in Fergania polyantha. LSRs were also categorized by length (Table S3), with the most common length ranging from 30 to 45 bp (35–47).

A total of 365 simple sequence repeats (SSRs) were identified in six Ferulinae plastomes (Fig. S2 and Table S4). Fergania polyantha and Ferula karatavica contained the highest number of SSRs (65), whereas Ferula prangifolia contained the fewest (51). The majority of SSRs were mono-nucleotides (32–40), followed by di- (6–17), tetra- (8–9), tri-nucleotides (2–4), and one penta-nucleotide. The penta-nucleotide in Fergania polyantha was located in the SSC region, while the others were found in the LSC region. Most SSRs were distributed in the LSC region (32–44), followed by the SSC (10–14) and IR (8–9) regions. Additionally, the majority of SSRs were located in intergenic spacers (IGS) (32–45), followed by protein-coding genes (PCGs) (10–13) and introns (7–11).

Divergence hotspot region of the ferulinae plastome

Divergence hotspot regions play a pivotal role in species identification and phylogenetic analyses. To identify regions of high divergence, we calculated nucleotide diversity (Pi) values across 44 complete plastomes of the Ferulinae. This analysis revealed 12 regions with notably high divergence (Pi > 0.006), as illustrated in Fig. 3: ycf1 (Pi = 0.00965), ndhF-rpl32 (Pi = 0.00899), trnT-GGU-psbD (Pi = 0.00867), petD intron (Pi = 0.00722), rps15-ycf1 (Pi = 0.00713), petA-psbJ (Pi = 0.00712), rps16-psbK (Pi = 0.00708), rpoB-petN (Pi = 0.00683), ndhC-trnV-UAC (Pi = 0.00663), petN-psbM (Pi = 0.00635), ycf3-trnS-GGA (Pi = 0.00634), and trnS-GCU-trnG-UCC (Pi = 0.00632). These regions were identified exclusively in the large single-copy (LSC) and small single-copy (SSC) regions. In the inverted repeat (IR) region, the highest Pi value observed was for trnR-ACG-trnN-GUU (Pi = 0.0033). Areas exhibiting zero Pi values over an 800 bp sliding window were identified at only five sites within the IR region.

Fig. 3
figure 3

Comparison of nucleotide diversity (Pi) values among the 44 Ferulinae complete plastomes. Twelve regions indicate high divergence hotspot region (Pi > 0.006). The window length and step size are 800 bp and 200 bp, respectively. The X-axis indicates the midpoint of each window, while the Y-axis indicate Pi values in each window

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New mitochondrial to plastid (MTPT) transfer sequences in the ferulinae plastome

The MTPT sequences, spanning approximately 5.1 to 5.8 kb, were identified within the rps12-trnV-GAC intergenic spacer (IGS) of Ferulinae plastomes. These plastomes also harbor DcMP1, DcMP2, DcMP3, and DcMP4, as well as partial sequences of CpMP5 and CpMP6, mirroring those found in the plastomes of the Daucinae and Torilidinae (Fig. 4 and S3). The specifics of these lengths are detailed in Table S5. Moreover, novel MTPT sequences, distinct from those in the Daucinae and Torilidinae plastomes, were discovered in the Ferulinae plastome. We term these newly identified sequences Ferula Mitochondrial Plastid (FeMP) sequences. This referred to the naming method of the MTPT sequences (DcMP and CpMP) in previous Daucinae and Torilidinae studies [9, 12]. Within the six Ferulinae plastomes, the structure of the MTPT region can be summarized as follows: DcMP1 → FeMP1 → CpMP5-5’ → FeMP2 → CpMP5-3’ → DcMP2 → CpMP6 → DcMP3-5’ → DcMP4 → DcMP3-3’. The length of FeMP1 varies from 1,093 bp in Fergania polyantha to 1,100 bp in Ferula penninervis, while FeMP2 maintaines a consistent length of 740 bp. Notably, FeMP2 encompasses a complete rps7 gene, measuring 447 bp with 100% nucleotide identity to its mitochondrial counterpart. This discovery was consistent across all six species studied. Detailed length information for these sequences is also compiled in Table S5.

Fig. 4
figure 4

Movement of MTPT sequences from the Ferula sinkiangensis mitogenome (OK585063) to six Ferulinae plastomes. Red and Purple indicate the same region of 1,158 bp MTPT sequence. Orange and Blue indicate the same region of 2,049 bp MTPT sequence. Green indicates a 3,738 bp MTPT sequence. Fergania polyantha and Ferula karatavica have gaps of 691 bp and 116 bp (Red boxes) in DcMP3, respectively

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Phylogenetic analysis

To determine the phylogenetic relationship of Scandiceae, including Ferulinae, a maximum likelihood (ML) tree was constructed (Fig. 5). Each of the four subtribes of Scandiceae was monophyletic. Along with this, the Acronema clade was located within the Scandiceae clade (BS 100%). Scandicinae formed the basal clade, and the Acronema clade formed the sister of the remaining subtribes. Daucinae and Torilidinae were sisters (BS 98%). The Ferula clade included Dorema and Fergania was divided into two clades (BS 100%). The four newly sequenced Ferula species in this study were located in the Ferula-A clade, and Ferula karatavica, F. penninervis, and F. prangifolia formed one clade (BS 50%). D. microcarpum was located in the Ferula-A clade and was identified as the sister of the F. akitschkensis, F. feruloides, and F. songarica clades (BS 96%). Fergania was identified as the sister of the Ferula-A clade (BS 97%), excluding F. kirialovii and F. equisetacea. Aside from the three F. transiliensis accessions, the two species (F. bungeana and F. sinkiangensis) along with the other two accessions did not form a monophyletic group. This is thought to be due to various factors such as misidentification or regional differences, based on the sequences used by the two research groups. Further verification seems necessary. In particular, since the two F. sinkiangensis accessions were located in different clades, re-identification is essential.

Fig. 5
figure 5

Maximum likelihood (ML) tree for 82 Scandiceae and seven Acronema clade based on 79 protein-coding genes. The aligned sequence was 68,786 bp in length. The ML tree was constructed by RAxML with -In L = 165694.775490. Blue, red, and green boxes indicate insertions of DcMP, FeMP, and CpMP sequences, respectively. The numbers on nodes indicate ML tree bootstrap support (BS) value above BS 80%

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Discussion

Characteristics and comparison of ferulinae plastomes

Since the initial reporting of the complete plastome sequence of tobacco (Nicotiana tabacum cv. Bright Yellow 4) by Shinozaki et al. in 1986 [27], the emergence of next-generation sequencing (NGS) technology in the 2000s has led to the cataloging of over 40,000 complete plastomes in the NCBI database. This wealth of plastome sequences has been instrumental in advancing the field of plant phylogenomics. In our study, we contribute new complete plastome sequences for six species within the Ferulinae subtribe, facilitating a comparative analysis with 38 other complete plastomes from the genus Ferula that have been previously documented. These plastomes exhibit the characteristic quadripartite structure typical of angiosperms, alongside similar gene contents and G-C content, with an average length of about 166 kb. This addition to the existing body of research not only enriches our understanding of plastome architecture but also aids in the phylogenetic and evolutionary study of the Ferulinae subtribe within the Apiaceae family.

Relative Synonymous Codon Usage (RSCU) was created to indicate how frequently a specific codon is used compared to other codons when coding for a specific amino acid [28]. This allows for the comparison of differences in codon usage frequency. The RSCU values in the six Ferulinae plastomes were very similar. These results align closely with previous studies on Ferula plastomes [17, 18]. In all studies, the RSCU value for the UUA (L) codon was the highest, consistently exceeding 1.9. Additionally, the AUU (I) codon was the most frequently observed in the Ferulinae plastomes, with over 900 occurrences. In these plastomes, the third position of the codon was biased towards A or U. Similar patterns have been observed in other groups within the Apiaceae family [29,30,31,32]. Analyzing differences in codon usage between different species or genes can help elucidate the evolutionary relationships within Ferulinae.

In general, repeat sequences (LSRs and SSRs) are analyzed to investigate the causes of genome rearrangements or to be used as DNA barcoding markers [33,34,35,36,37]. In the six Ferulinae plastomes, 349 LSRs and 365 SSRs were identified. Most LSRs were palindromic repeats, which is consistent with previous studies on Ferula plastomes [17, 18]. The majority of SSRs were mono-SSRs, more than twice as many as di-SSRs, and this pattern is also consistent with previous studies on Ferula plastomes [17, 18].

Divergence hotspot regions within plastomes are crucial for species identification and phylogenetic analyses. In our evaluation of 44 Ferulinae plastomes, we calculated nucleotide diversity (Pi) values to identify these hotspots. The ycf1 region exhibited the highest Pi value, aligning with findings from previous research on Ferula plastomes [17, 18]. We identified twelve regions with notably high divergence (Pi > 0.06), making them suitable candidates for DNA barcoding studies. Notably, apart from ycf1, all regions demonstrating high Pi values were intergenic spacer (IGS) regions, highlighting their potential for taxonomic differentiation. The Pi value of the inverted repeat (IR) region was significantly lower than those of the large single-copy (LSC) and small single-copy (SSC) regions, reinforcing earlier observations that IR regions tend to be more conserved [1, 33, 38,39,40,41]. This study underlines the significance of certain plastome regions for understanding species divergence and provides a foundation for future taxonomic and phylogenetic research within the Ferulinae subtribe.

Intracellular gene transfer (IGT) between organelles in ferulinae

The structure of the plastome is generally conservative, yet intracellular gene transfer (IGT) events such as mitochondrial to plastid DNA transfer (MTPT) or plastid to mitochondrial transfer (PTMT) have been documented across various plant families. For instance, IGT phenomena have been reported in Anacardium within the Anacardiaceae family [3]; within the Asclepideae tribe of the Apocynaceae family [4]; in Convallaria of the Asparagaceae family [5]; and in both Paspalum and Pariana within the Poaceae family [6, 7]. Notably, MTPT sequences have been identified in the plastomes of several Apiaceae taxa, including Caucalis, Crithmum, Cuminum, Daucus, Dystaenia, and Petroselinum [8,9,10,11,12, 42], marking a significant occurrence within this family.

Most MTPT sequences in the Apiaceae have been inserted into the inverted repeat (IR) regions of the plastome. However, for species within the Asclepiadeae, Crithmum, Dystaenia, and Petroselinum, MTPT sequences were located in the large single-copy (LSC) region. These sequences have also been identified in the rps12-trnV intergenic spacer (IGS) region of Cuminum, Daucus, and Thapsia (members of the Daucinae) as well as in Caucalis and Torilis (members of the Torilidinae), all within the Scandiceae tribe [9, 10, 12, 25, 26, 42]. The sequences designated as DcMP and CpMP predominantly occur in certain IGS regions of the Apiaceae mitogenome, highlighting the intricate patterns of genetic exchange between organelles in plants.

In our investigation of the Ferula plastomes, we identified two distinct sequences, referred to as Ferula Mitochondrial Plastid (FeMP) sequences, in the same region. FeMP1 varies in length from 336 bp to 1,100 bp, while FeMP2 spans from 50 bp to 740 bp in length, with the latter not present in F. conocaula and F. kingdon-wardii. Notably, FeMP2 encompasses the complete rps7 gene (447 bp) of mitochondrial origin. Rps7 is located in the head of the small subunit, one of the two subunits that make up the ribosome [43, 44]. This gene is a primary ribosomal RNA (rRNA) binding protein that aids in the folding of rRNA and the binding of other proteins. Notably, the plastome already contains the rps7 gene located in the IR region. However, the similarity between the two genes is very low, with only 43.4% identity. It is very rare for a gene located in the mitogenome to be found intact in the plastome. This phenomenon of a complete mitochondrial gene insertion within the plastome has previously been observed only in Anacardium (with the ccmB gene) [3]. Further research is needed to understand how these genes influence plant evolution. Both FeMP1 and FeMP2 sequences were also detected in Dorema and Fergania, members of the Ferulinae subtribe.

We observed significant variation in the length of these MTPT sequences among some Ferula species. For instance, F. caspica lacks CpMP5-3’, DcMP2, and CpMP6; F. conocaula is missing FeMP2, CpMP5-3’, DcMP2, and CpMP6; and F. kingdom-wardii lacks CpMP5-3’, FeMP2, and CpMP5-3’. The MTPT sequence length in Dorema is 5.8 kb, exceeding the average Ferula length of 5,588 bp. Meanwhile, the Fergania MTPT sequence measures 5.1 kb, with DcMP3-5’ being 656 bp shorter than the average Ferula length of 1,259 bp. This variability highlights the complex nature of MTPT sequences within the Ferulinae, underscoring the potential for these sequences to inform phylogenetic and evolutionary studies.

The exchange of materials between organelles through physical contact has been documented in various studies, highlighting a fundamental aspect of cellular dynamics [45, 46]. Recent advancements have further confirmed that such exchanges, including that of DNA, can occur via the endoplasmic reticulum (ER), expanding our understanding of inter-organelle communication [47]. Various mechanisms have been proposed for the movement of mitochondrial to plastid transfer (MTPT) sequences, including the presence of repeating sequences, long terminal repeat (LTR) retrotransposons, and double-strand break (DSB) repair by homologous recombination, as well as invasion mechanisms [3,4,5, 9,10,11].

Our findings complement these studies, as we have identified a substantial number of nucleotide sequences that originated from the inverted repeat (IR) of the plastome in 18 Apiaceae mitogenomes (Fig. 6 and S4). This observation underscores the frequent DNA exchanges between the IR region of the Ferulinae plastome and the mitogenome. Specifically, the occurrence of double-strand breaks (DSBs) during the replication of IR sequences in the Ferulinae plastome suggests that MTPT sequences could be integrated into the plastome during the repair of DSBs. This evidence of regular DNA exchange not only highlights the dynamic nature of organelle genomes but also contributes to our understanding of the mechanisms underlying the evolution and complexity of plant genomes.

Fig. 6
figure 6

Results of repeating sequence analysis (>200 bp) between the Ferula penninervis plastome (excluding one IR) and eight Scandiceae mitogenomes. Red and blue lines indicate the movement of PTMT sequences (IR and LSC) from the Ferula plastome to Scandiceae mitogenomes, respectively. Green lines indicate the movement of MTPT sequences. No movement of the SSC sequences was confirmed. Fepe (F. penninervis_this study), Cucy (Cuminum cyminum_OP800912), Daca 1 (Daucus carota subsp. sativus_CP093352), Daca 2 (Daucus carota subsp. sativus_JQ248574), Daca 3 (Daucus carota subsp. sativus_OP801825), Daca 4 (Daucus carota subsp. sativus_ OP801826), Daca 5 (Daucus carota subsp. sativus_ OP801827), Daca 6 (Daucus carota subsp. sativus_ OP801828), Fesi (F. sinkiangensis_OK585063)

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Redefining the generic limits of the genera in Ferulinae

The application of molecular markers for classification has significantly altered traditional classification systems, leading to the integration and separation of various taxa. For instance, Heterogaura from the Onagraceae family, which was once considered monotypic, was integrated into the genus Clarkia based on molecular phylogenetic evidence [48]. Similarly, Echinosophora koreensis from the Fabaceae family, an endemic plant of Korea, was merged into the closely related genus Sophora following molecular phylogenetic analysis [49]. In the Asteraceae family, certain species of Parasenecio were reclassified into the genera Japonicalia and Taimingasa based on molecular data [50], while Ligularia sect. Stenostegia was elevated to its own genus, Vickifunkia, utilizing morphological, cytological, and molecular evidence [51]. In the Clusiaceae family, some species of Tovomita were reclassified into the genus Arawakia [52].

In the Apiaceae family, the reevaluation of phylogenetic relationships has led to significant taxonomic revisions, particularly due to the ambiguity of morphological characters among several taxa. For instance, various species initially grouped under Carum have been segregated into distinct genera such as Aegopodium and Trocdaris [53], reflecting the intricate genetic relationships that morphological analyses alone could not resolve. Moreover, comprehensive molecular studies have unveiled that Pleurospermum sensu lato encompasses multiple distinct clades, necessitating the reclassification of several species. Consequently, species previously included in Pleurospermum—beyond the narrow definition of Pleurospermum sensu stricto—have been reallocated into genera such as Hymenidium, Pterocyclus, among others, according to various studies [29, 54, 55].

Similarly, species of Ligusticum belonging to the Acronema clade underwent reclassification into Hymenidium, Rupiphila, and Tilingia following a phylogenetic analysis of the genus [56]. This adjustment highlights the dynamic nature of botanical taxonomy, where genetic insights provide a more nuanced understanding of species relationships and classifications. These examples underscore the critical role of molecular phylogenetic analyses in clarifying taxonomic relationships within the Apiaceae family, thereby enabling a more accurate representation of its biodiversity and evolutionary history.

Ferula, originally placed within Ferulinae of Peucedaneae by Shishkin in 1951 [57], underwent significant reclassification following phylogenetic studies using nuclear ribosomal internal transcribed spacer (nrITS) and various plastid DNA (ptDNA) markers. These studies demonstrated Ferula’s polyphyly within other subtribes of Peucedaneae [58,59,60], leading to the reassignment of Ferulinae, including Ferula, to the Scandiceae tribe. Additionally, morphological and molecular evidence facilitated the transfer of several related species, such as Schumannia, Pinacantha, Sornathus, and Talassia, into Ferula [17, 18, 24]. Furthermore, a majority of Dorema species, closely related to Ferula, were incorporated into Ferula based on molecular studies [13, 20,21,22], though three species remained under Dorema in POWO. Recent suggestions have been made to synonymize D. microcarpum and D. sabulosum as Ferula species, along with D. balchanorum [22, 61].

Our findings support the inclusion of D. microcarpum within the Ferula clade, echoing previous studies. This evidence, combined with the observation that Fergania (monotypic with F. polyantha) shares significant morphological and molecular characteristics with Ferula, underscores the necessity for reclassification within the Ferulinae. Despite Fergania’s previous distinction based on certain morphological traits, our analysis revealed no substantial differences from Ferula, including in plastome structure, gene content, and IGT events. Phylogenetically, Fergania plastids fall within the Ferula clade, a conclusion supported by prior research using the nrITS marker [24].

Prior studies have demonstrated the inclusion of the other genera in Ferulinae—Autumnalia, Kafirnigania, and Leutea—within the Ferula clade. Leutea, in particular, has shown varying positions relative to Ferula in phylogenetic analyses. Studies utilizing the nuclear ribosomal internal transcribed spacer (nrITS) marker placed Leutea within the Ferula clade [13, 20, 21, 62, 63]. However, phylogenetic trees generated using plastid DNA (ptDNA) or a combination of ptDNA and nrITS markers have indicated a separation between Leutea and Ferula [13, 14, 22]. This discrepancy may be attributed to the differing inheritance patterns of these genetic markers—nrITS exhibits biparental inheritance, whereas the plastome is maternally inherited. Such differences suggest that hybridization events and ancient plastome capture could have played significant roles in shaping the current genetic landscape of Leutea and its relation to Ferula. Given the close morphological and molecular relationships observed among the genera of Ferulinae, there is a compelling argument for their reclassification into the genus Ferula. To substantiate this proposal, however, it is crucial to re-evaluate the phylogenetic relationships within Ferulinae by integrating morphological analyses with comprehensive plastome studies of Autumnalia, Kafirnigania, and Leutea, especially since plastome studies for these genera remain unexplored. This integrated approach will provide a more detailed understanding of the evolutionary dynamics within Ferulinae and offer stronger evidence for any proposed taxonomic revisions.

Conclusions

Our findings provide the complete plastome sequences of six species within the subtribe Ferulinae, valuable medicinal resources. Notably, we identified unique mitochondrial-to-plastid transfer (MTPT) sequences in the inverted repeat (IR) regions of these Ferulinae plastomes. These results shed light on the mechanism of plastome evolution in the Scandiceae with a focus on the unique plastome structure found in the Apiaceae. These findings enhance our understanding of the evolution of plant organellar genomes. Additionally, our phylogenetic analysis reveals that the genera Dorema and Fergania, closely related to Ferula, form a single clade with Ferula. Most species of Dorema have already been reclassified under Ferula based on molecular analysis results. Our findings provide further evidence suggesting that Fergania should also be reclassified into Ferula. Future discussions are warranted regarding genomic analyses and the reclassification of the remaining genera within the subtribe Ferulinae.

Materials and methods

Plant materials and DNA extraction

Plant materials were collected from various locations in Uzbekistan (Fig. 1; Table 2). Silica-dried leaves were used for DNA extraction. Voucher specimens of Dorema and Ferula were deposited in the Korea Research Institute of Bioscience & Biotechnology (KRIBB) Herbarium (KRIB), identified by Jin-Hyub Paik (Table 2). The voucher specimen of Fergania polyantha was deposited in the National Herbarium of Uzbekistan (TASH), identified by Yusupov and Tojibaev (Table 2). The total DNAs using the silica-dried leaves were extracted using the DNeasy Plant Mini Kit (QIAGEN). The genomic DNAs are deposited at the International Biological Material Research Center (IBMRC).

Table 2 Summary of specimen information and sequencing results for six Ferulinae species
Full size table

Sequencing, assembly and annotation

Approximately 5 GB of raw data were generated using the Illumina NovaSeq platform (Illumina Inc., San Diego, CA). The total reads were deposited on the NCBI Sequence Read Archive (SRA) under accession number SRR27908099-SRR27908104 (Table 2). To improve sequence accuracy, we generated complete plastome sequences using two methods. First, we performed de novo assembly in Novoplasty v.4.3.1 [64] using trimmed reads. The total reads were trimmed in Trimmomatic v.0.36 [65]. Second, we performed a map to reference on Geneious prime v.2023.2.1 (Biomatters Ltd.) [66]. Here, total reads were trimmed to BBduk 37.64 in Geneious Prime v.2023.2.1. In both methods, Ferula sinkiangensis (MW411057) was used as the reference sequence. Sequencing results are summarized in Table 2. The complete plastome was annotated using the Geneious Prime v.2023.2.1, National Centre for Biotechnology Information (NCBI) BLAST, and tRNAscan-SE 2.0 programs [67]. The circular plastome map was constructed by OrganellarGenomeDraw (OGDRAW) [68]. The newly sequenced genomes were deposited in GenBank (Table 2).

Comparison of ferulinae plastomes

The 79 protein-coding genes (PCGs) were extracted from the six Ferulinae plastomes for RSCU analysis using the RSCU calculator webserver (jamiemcgowan.ie/bioinf/rscu.html). The large and simple sequence repeats (LSRs and SSRs) were detected with the REPuter [69] and Phobos v. 3.3.12 program [70], respectively. LSRs were counted with forward, reverse, and palindromic repeats in six Ferulinae plastomes. The parameters were as follows: (1) a minimum repeat size of 30 bp, (2) hamming distance = 3. We counted the SSRs if they were repeated more than ten times for mono-SSRs, five times for di-SSRs, four times for tri-SSRs, three times for tetra-SSRs, and two times for penta-SSRs in the six Ferulinae plastomes (excluding one IR).

Sliding window analysis was performed to calculate the nucleotide diversity (Pi) of 44 Ferulinae complete plastomes using DnaSP v.6.10 [71]. The window length and step size were set to 800 bp and 200 bp, respectively. The 44 Ferulinae complete plastomes were aligned using MAFFT v.7.017 [72].

Identification of intracellular gene transfer (IGT) between organellar genomes

To identify MTPT and PTMT sequences in Ferulinae organelle genomes, 18 Apiaceae mitogenomes were downloaded from NCBI GenBank. To identify MTPT sequences in the Ferulinae plastome, Daucus carota subsp. sativus (JQ248574) and Ferula sinkiangensis (OK585063) mitogenomes were used as reference sequences to find annotation (similarity > 70%, length > 200 bp). The searched regions were compared with two mitogenomes using MAFFT alignment v.7.490 to determine the MTPT sequence. To identify PTMT sequences in 18 Apiaceae mitogenomes, find annotation (similarity > 70%, length > 200 bp) in Geneious Prime v.2023.2.1 was performed using Ferula penninervis plastome as a reference sequence. The searched regions were compared with the F. penninervis plastome using MAFFT alignment v.7.490 to determine the PTMT sequence. The movement of MTPT and PTMT sequences between Ferulinae organelle genomes was schematized using shinyCircos-V2.0 [73].

Phylogenetic analysis

For phylogenetic analysis, eighty-two complete plastome sequences of Scandiceae were downloaded from the NCBI GenBank database (Table S6). Additionally, seven complete plastome sequences of the Acronema clade, which are closely related to Scandiceae, were downloaded. We extracted 79 PCGs from 95 species and aligned each gene using MAFFT v.7.490. All alignments were concatenated to a length of 68,786 bp. The dataset was subjected to jModeltest2 on ACCESS in the CIPRESS Science Gateway to determine the best fit model. A maximum likelihood (ML) tree based on the best-fit model (GTR + I + G) was constructed using RAxML in CIPRESS Science Gateway with 100 bootstrap replicates.

Data availability

Voucher specimens of Dorema and Ferula were deposited in the Korea Research Institute of Bioscience & Biotechnology (KRIBB) Herbarium (KRIB), identified by Jin-Hyub Paik (Table 1). The voucher specimen of Fergania polyantha was deposited in the National Herbarium of Uzbekistan (TASH), identified by Yusupov and Tojibaev (Table 1). The data sets supporting the results of this article are included in additional files. Complete plastome sequences are available in GenBank (https://www.ncbi.nlm.nih.gov, PP314217-PP314221, PP336431). Raw data are available in Sequence Read Archive (SRA) (https://www.ncbi.nlm.nih.gov/sra, SRR27908099-SRR27908104).

Change history

  • 29 December 2024

    The original online version of this article was revised: the author identified minor error typo error in the article title and Table 1 and Table 2 were switched

  • 27 December 2024

    A Correction to this paper has been published: https://doi.org/10.1186/s12870-024-06001-8

Abbreviations

LSC:

Large single copy

SSC:

Small single copy

IR:

Inverted repeat

IGT:

Intracellular gene transfer

MTPT:

Transfer from the mitochondrion to plastid

PTMT:

Transfer from the plastid to mitochondrion

FeMP:

Ferula mitochondrial plastid sequence

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Acknowledgements

Not applicable.

Funding

This research was supported by the KRIBB Initiative Program [KGM4582423] of the Republic of Korea.

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Authors and Affiliations

  1. International Biological Material Research Center (IBMRC), Korea Research Institute of Bioscience and Biotechnology (KRIBB), Daejeon, 34141, South Korea

    Sangjin Jo, Minsu Park, Sangho Choi & Jin-Hyub Paik

  2. Institute of Botany, Academy of Sciences, Durmon yuli str. 32, Tashkent, 100125, Uzbekistan

    Ziyoviddin Yusupov & Komiljon Sh. Tojibaev

  3. Royal Botanical Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, UK

    Gregory J. Kenicer

Authors
  1. Sangjin Jo
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  2. Minsu Park
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  3. Ziyoviddin Yusupov
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  4. Komiljon Sh. Tojibaev
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  5. Gregory J. Kenicer
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  6. Sangho Choi
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  7. Jin-Hyub Paik
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Contributions

ZY, KT, GK, SC, and JP conceived and designed the project. ZY and KT collected all samples. SJ and MP performed the experiments and analyzed data. SJ, MP, and JP wrote the manuscript. GK and JP supervised and revised the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Jin-Hyub Paik.

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Ethics approval and consent to participate

The sample collections completely compiles with the Regulations on the Protection and Management of Wild Plants of the Uzbekistan. All samples were collected from various locations in Uzbekistan. Since they are not a protected species, they do not require special collection permits. Dr. Yusupov and Dr. Tojibaev formally identified the plant materials used in this study. All the experimental studies on the plants, including collection of the material, complied with institutional, national, and international guidelines.

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Not applicable.

Competing interests

The authors declare no competing interests.

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The original online version of this article was revised: the author identified minor error typo error in the article title and Table 1 and Table 2 were switched.

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Jo, S., Park, M., Yusupov, Z. et al. Intracellular gene transfer (IGT) events from the mitochondrial genome to the plastid genome of the subtribe Ferulinae Drude (Apiaceae) and their implications. BMC Plant Biol 24, 1172 (2024). https://doi.org/10.1186/s12870-024-05891-y

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  • DOI: https://doi.org/10.1186/s12870-024-05891-y

Keywords

BMC Plant Biology

ISSN: 1471-2229

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