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BMC Plant Biology
Phylogenetic incongruence inanAsiatic
species complex ofthegenus Caryodaphnopsis
(Lauraceae)
Shiting Yang1, Jiepeng Huang1, Yaya Qu2, Di Zhang3, Yunhong Tan3, Shujun Wen4* and Yu Song1*
Abstract
Background Caryodaphnopsis, a group of tropical trees (ca. 20 spp.) in the family Lauraceae, has an amphi-Pacific
disjunct distribution: ten species are distributed in Southeast Asia, while eight species are restricted to tropical
rainforests in South America. Previously, phylogenetic analyses using two nuclear markers resolved the relationships
among the five species from Latin America. However, the phylogenetic relationships between the species in Asia
remain poorly known.
Results Here, we first determined the complete mitochondrial genome (mitogenome), plastome, and the nuclear
ribosomal cistron (nrDNA) sequences of C. henryi with lengths of 1,168,029 bp, 154,938 bp, and 6495 bp, respec-
tively. We found 2233 repeats and 368 potential SSRs in the mitogenome of C. henryi and 50 homologous DNA
fragments between its mitogenome and plastome. Gene synteny analysis revealed a mass of rearrangements
in the mitogenomes of Magnolia biondii, Hernandia nymphaeifolia, and C. henryi and only six conserved clustered
genes among them. In order to reconstruct relationships for the ten Caryodaphnopsis species in Asia, we created
three datasets: one for the mitogenome (coding genes and ten intergenic regions), another for the plastome (whole
genome), and the other for the nuclear ribosomal cistron. All of the 22 Caryodaphnopsis individuals were divided
into four, five, and six different clades in the phylogenies based on mitogenome, plastome, and nrDNA datasets,
respectively.
Conclusions The study showed phylogenetic conflicts within and between nuclear and organellar genome data of
Caryodaphnopsis species. The sympatric Caryodaphnopsis species in Hekou and Malipo SW China may be related
to the incomplete lineage sorting, chloroplast capture, and/or hybridization, which mixed the species as a complex
in their evolutionary history.
Keywords Phylogenetic incongruence, Species complex, Tropical tree, Mitochondrial genome, Plastome, nrDNA
*Correspondence:
Shujun Wen
wenshujun@gxib.cn
Yu Song
songyu@gxnu.edu.cn
Full list of author information is available at the end of the article
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Page 2 of 18
Yangetal. BMC Plant Biology (2024) 24:616
Background
Trees remain a fundamental component in forest eco-
system stability with around 73,000 species and almost
20% of global plant species diversity [1]. ere are an
estimated 9,000 undiscovered tree species, among which
roughly half to two-thirds of all is still waiting to be iden-
tified in tropical and subtropical forests [1]. ese broad-
leaved tree species often refer to rapid diversification and
frequent introgression and compound taxonomic confu-
sion. For instance, studies on Chinese oaks have revealed
negative linear relationships between diversification rates
and genetic variation, suggesting complex associations
between morphological divergence and species diversi-
fication [2]. Similarly, the Pedicularis siphonantha com-
plex in southwest China has shown rapid diversification,
frequent introgression, and cryptic species complexes,
highlighting the challenges of species delimitation based
on morphological characters [3]. e phenotypes and
genetic lineages of the tropical and subtropical tree spe-
cies have narrowed over time in similar environments
[4]. Species identification, delimitation, and description
usually depend on morphological characters, but these
traits often fail to distinguish the recently diverged spe-
cies in tropical and subtropical forests, leading to a long
and controversial debate such as species complex [4, 5].
Species complexes are a group of taxa consisting of
multiple species-level lineages that cannot be reliably
separated using ordinary knowledge [6]. Resolution is
often hindered by their cryptic nature, making it diffi-
cult to distinguish them using traditional methods like
external morphology [4, 6]. To study species complexes,
a variety of methodswere continuouslyimproved, which
mightinvolve analyzing differences in individual traits,
conducting reproductive isolation tests, and utilizing
DNA-based techniques like molecular phylogenetics [7].
ese approaches help researchers determine the bound-
aries between closely related organisms within a species
complex. By examining the genetic, morphological, and
ecological characteristics of these organisms, it is pos-
sible to identify cryptic species, hidden sibling species,
and other components of a species complex [8, 9]. Recent
researches have revealed that the species in difficult line-
ages such as bamboos, palms, oaks, rosids, and camellias
[10–14], believed to be nominal species actually repre-
senting a group of closely related species, are sometimes
morphologically indistinguishable.
In plants, mitochondrion and chloroplast are two
DNA-containing organelles. Both have low rates of
nucleotide substitution, significant variation in genome
sizes, and abundant repetitive sequences [15]. Recom-
bination is crucial for DNA replication in all organisms
[16]. Mitochondrial homologous recombination essen-
tially refers to reversible, frequent exchange of large
repeats, which, if not harmful to mitochondrial func-
tion, could be retained, leading to an overall increase in
mitogenome size [17]. Assembly of the mitogenomes is
challenging due to their large repetitive sequences and
multipartite structures. Second-togetherwiththird-gen-
eration sequencing methods help in assembling and dis-
covering these structures [18].
Recent advances in sequencing technologies have
greatly improved the acquisition of large amounts of
genomic data, making it ideal for phylogenetic analy-
sis. Plastomes, the complete DNA sequences of chlo-
roplast, are widely utilized in phylogenetic studies
inthe familyLauraceaedue to their ease of sequenc-
ing, assembly, and annotation [19–21]. The inclusion
of the mitogenome in phylogenetic analysis has been
increasingly applied in the angiosperm [22–24]. It is
the diversity of genomic data that has brought the dis-
cordance of organelle and nuclear signalling into focus
[25, 26]. Cytonuclear discordance refers to the incon-
gruence between the evolutionary histories of nuclear
and cytoplasmic genomes within a species or a group
of species. The discordance always refers tohybridi-
zation, incomplete lineage sorting, or horizontal gene
transfer [27]. Recent studies have indeed highlighted
the prevalence of cytonuclear discordance in various
plant species [28–30].
e amphi-Pacific genus Caryodaphnopsis Airy Shaw
in the family Lauraceae includes about 20 tropical tree
species distributed in Southeast Asia and South Amer-
ica [31–35]. e Caryodaphnopsis species in Asia dif-
fer from Alseodaphne and Nothaphoebe species by their
opposite leaves, unequal filaments, and unaltered fruit
pedicels, although the species in the three groups have
unequal tepals and large staminodes [31, 32]. In 1940,
the leaves of C. baviensis (Lecomte) Airy Shaw, C. henryi
Airy Shaw, and C. tonkinensis (Lecomte) Airy Shaw were
described as being similar to those of Cryptocarya laevi-
gata Blume, while their flowers and fruits looked much
like those of Dehaasia Blume species [31]. Recent stud-
ies have reported six new species of Caryodaphnopsis,
including C. laotia Airy Shaw [36], C. latifolia W.T. Wang
[37], C. metalliea Kosterm, C. poilanei Kosterm [32], C.
bilocellata van der Werff & Dao [38], andC. malipoensis
Bing Liu & Y. Yang [39]. On the other side of the Pacific
Ocean, there are eight accepted species, such as C. fos-
terivan der Werff [40], C. cogolloi van der Werff [41], C.
tomentosa van der Werff [42], and C. parviflora van der
Werff [43].
Caryodaphnopsis has no reliable fossil record, but two
molecular analyses have dated the separation between
species in Asia and America to the middle Eocene (44
or 48 million years ago) [44, 45]. Both geographical
groups were supported as monophyletic by previous
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Page 3 of 18
Yangetal. BMC Plant Biology (2024) 24:616
phylogenetic analyses. e first reported chloroplast
marker in Caryodaphnopsis was matK, which was used
for phylogenetic analysis within the Lauraceae and sug-
gested that C. tonkinensis formed a weakly supported
monophyletic clade [46]. After that, Chanderbali et al.
used a nuclear marker 26S ribosomal DNA sequence and
four chloroplast regions (psbA-trnH, rpll6, trnL-trnF, and
trnT-trnL) to recover a Caryodaphnopsis clade, which
included C. bilocellata and C. tonmentosa[44]. Rohwer
etal. (2005), using the chloroplast sequence trnKintron
[47], found a weakly supported group comprising C. bilo-
cellata, C. tonmentosa, and Neocinnamomum mekon-
gense. Nie etal. (2007) displayed a clade comprising C.
tonmentosaand N. mekongensebased on ITS, trnL-trnF,
rpll6, and psbA-trnH regions [48]. Recently, Li et al.
(2016) used nuclear barcoding markers ITS and RPB2
and found that a monophyleticCaryodaphnopsis clade
[45], which comprised species from two geographical
groups, was strongly supported. In those phylogenetic
analyses, the relationships among five South American
species were well resolved, i.e., an unidentified Caryo-
daphnopsis species and its sister group containing C.
burger, C. fosteri, and C. inaequalis, followed by C.cogol-
loi[41]. However, the relationships among species in Asia
have not been resolved due to low sequence divergence
in the ITSand RPB2 markers. e separation of three
individuals of C. tonkinensis into two branches may rep-
resent sample misidentifications or indicate intraspecific
diversity [45].
In this study, we completed the assembly and annota-
tion of the mitogenome of C. henryi. Data from 21Car-
yodaphnopsis individuals in Asia were collected. e
goals of this study were to (1) determine the first com-
plete mitogenome in the Lauraceae family; (2) reveal
the genomic characteristics and structural features of C.
henryi; and (3) reconstruct the nuclear, chloroplast, and
mitochondrial phylogenies of the Caryodaphnopsisspe-
cies in Asia.
Methods
Plant material andgeographic distributions
Fresh leaves and silica-gel dried materials were collected
from ten Caryodaphnopsis species from China and Viet-
nam. Distribution data was compiled using herbarium
records, and the voucher specimens were deposited in
the Herbarium of Guangxi Normal University (Table1).
Figure1 depicts the fruits of six Caryodaphnopsis spe-
cies. In addition, the plastome sequence of C. henryi was
deposited in the Lauraceae Chloroplast Genome Data-
base (LCGDB, LAU00015,https:// lcgdb. wordp ress. com)
[20]. And the complete mitogenome sequence of C. hen-
ryi was deposited in NCBI (OR987149).
Table 1 Sampled species of Caryodaphnopsis and their voucher specimens in this study
Species Herbarium Voucher Geographic Origin Latitude Longitude
Caryodaphnopsis laotica Airy Shaw GXNU SONG Yu SY34973 Hekou, Yunnan 104.607492 23.102
Caryodaphnopsis laotica Airy Shaw GXNU SONG Yu SY36893 Hekou, Yunnan 104.048425 22.739892
Caryodaphnopsis sp. 1 GXNU SONG Yu SY37063 Hekou, Yunnan 103.969734 22.708797
Caryodaphnopsis sp. 1 GXNU SONG Yu SY36821 Hekou, Yunnan 104.068275 22.767897
Caryodaphnopsis sp. 2 GXNU SONG Yu SY35907 Hekou, Yunnan 104.031533 22.67455
Caryodaphnopsis sp. 2 GXNU SONG Yu SY34883 Hekou, Yunnan 104.032433 22.662531
Caryodaphnopsis sp. 3 GXNU SONG Yu SY36729 Malipo, Yunnan 104.848122 22.969744
Caryodaphnopsis sp. 3 GXNU SONG Yu SY36734 Malipo, Yunnan 104.843201 22.984373
Caryodaphnopsis tonkinensis (Lec.) Airy Shaw GXNU SONG Yu SY37141 Hekou, Yunnan 103.938156 22.672583
Caryodaphnopsis tonkinensis (Lec.) Airy Shaw GXNU SONG Yu SY36875 Hekou, Yunnan 103.938283 22.673356
Caryodaphnopsis tonkinensis (Lec.) Airy Shaw GXNU SONG Yu SY34707 Hekou, Yunnan 103.938522 22.673214
Caryodaphnopsis tonkinensis (Lec.) Airy Shaw GXNU SONG Yu SY34705 Hekou, Yunnan 103.938621 22.673386
Caryodaphnopsis latifolia W. T. Wang GXNU SONG Yu SY35963 Hekou, Yunnan 103.981613 22.714413
Caryodaphnopsis latifolia W. T. Wang GXNU SONG Yu SY35972 Hekou, Yunnan 103.969734 22.708797
Caryodaphnopsis malipoensis Bing Liu & Y. Yang GXNU SONG Yu SY36712 Malipo, Yunnan 104.848489 22.974842
Caryodaphnopsis malipoensis Bing Liu & Y. Yang GXNU SONG Yu SY36715 Malipo, Yunnan 104.828323 22.987118
Caryodaphnopsis bilocellata van der Werff & Dao GXNU SONG Yu SY37158 Hekou, Yunnan 103.960899 22.69406
Caryodaphnopsis bilocellata van der Werff & Dao GXNU SONG Yu SY35356 Hekou, Yunnan 103.960750 22.69325
Caryodaphnopsis metallica Kosterm GXNU SONG Yu SY37885 Vietnam 104.0557 22.6575
Caryodaphnopsis henryi Airy Shaw GXNU SONG Yu SY34716 Honghe, Yunnan 103.108022 23.038376
Caryodaphnopsis henryi Airy Shaw GXNU SONG Yu SY34708 Honghe, Yunnan 103.09825 23.027934
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Page 4 of 18
Yangetal. BMC Plant Biology (2024) 24:616
DNA extraction andsequencing
High-quality genomic DNA of ten Caryodaph-
nopsis leaves were delivered to Tianjin Novogene
Company for Illumina library preparation and second-
generation sequencings. Genomic DNA was isolated
from 2g of fresh or silica-dried leaves using the CTAB
technique using 4% CTAB [49], 1% PVP, and 0.2% DL
dithiothreitol. e cleaved DNA fragments were tilized
to build 500 bp short-insert libraries, according to the
manufacturer’s handbook (Illumina). Each DNA sample
received > 4.0Gb of data from a Genome Analyzer (Illu-
mina HiSeq 2500) at BGI-Shenzhen after being indexed
by tags and pooled in one lane. A total of 27.9 Gb of
sequence reads with a length of 150bp were obtained for
C. henyri using second-generation sequencing. Young
leaves from C. henryi was extracted and sequenced using
Oxford Nanopore PromethION platforms for third-gen-
eration sequencings. High-quality genomic DNA was
extracted from the leaves using the SDS method. After
library construction using SQK-LSK109 (Oxford Nanop-
ore Technology), DNA sequencing was performed using
Oxford Nanopore sequencing based on the promethION
platform and 20.7Gb of raw data with an average reads
size of 27,600bp were produced.
Genome assembly andannotation
e unlooped mitogenome, complete plastome, and
nrDNA sequences for the Caryodaphnopsis samples
were assembled using GetOrganelle 1.7.5 [50]. To assem-
ble a complete mitogenome of Caryodaphnopsis henryi,
the Illumina sequencing data of C. henryi were initially
assembled using GetOrganelle [50]. After obtaining the
Nanopore third-generation sequencing reads of C. hen-
ryi, the adaptors were first trimmed using Porechop,
and then, by aligning the trimmed reads to the scaf-
folds assembled by GetOrganelle using BLAST + with
the parameter -evalue 1e-200 [51], the subset of long
sequences that was similar to the mitochondria was
obtained. Finally, these long reads and the mitochondria-
related short reads that were extended by GetOrganelle
were used together for hybrid assembly, which was per-
formed by the Unicycler pipeline [52]. In the assembly
result of C. henryi, two putative mitochondrial sequences
were obtained, including a linear sequence of length
Fig. 1 Fruits of six Caryodaphnopsis species (A: C. tonkinensis, B: C. henryi, C: C. malipoensis, D: C. sp. 1, E: C. sp. 2, F: C. sp. 3)
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Page 5 of 18
Yangetal. BMC Plant Biology (2024) 24:616
968,798bp, and a circular sequence of length 199,231bp.
Mitogenomes were annotated using GeSeq [53], with
Liriodendron tulipifera (KC821969) and Magnolia bion-
dii (MN206019) as references. Subsequently, a detailed
annotation was performed with references in Geneious
Prime [54]. e circular mitogenome map was visualized
using OGDRAW [55].
Repeat andHomologous DNA Analysis
REPuter (https:// bibis erv. Cebit ec. uni- biele feld. de/ reput
er) [56] was used to visualize forward, palindrome,
reverse and complement sequences in the mitogenome
of Caryodaphnopsis henryi, with a minimum repeat size
of 30 bp, hamming distance of three and a sequence
identity > 90%. And Tandem Repeats Finder (TRF) pro-
grams (https:// tandem. bu. edu/) [57] was used to visu-
alize tandem sequences with default parameters. e
simple sequence repeats (SSRs) in the mitogenome of
C. henryi was identified using MISA-web (http:// pgrc.
ipkga tersl eben. de/ misa/), with a motif size of one to six
nucleotides and thresholds of 8, 5, 5, 4, 4 and 4, respec-
tively. BLASTN was used to detect transferred DNA
fragments by analysing sequence similarity between the
plastome and the mitogenome, with an e-value cut-off of
1e-5. e results were visualized using the Circos module
in TBtools v2.012 [58]. Mauve v.2.4.0 software was used
for determining the mitogenome rearrangements among
Caryodaphnopsis henryi, Hernandia nymphaeifolia
(ON023262), and Magnolia biondii (MN206019). RAW-
Graphs (https:// app. rawgr aphs. io/) was used to describe
the collinearity relationships among the gene orders in
the mitogenomes of C. henryi, H. nymphaeifolia, and M.
biondii.
Phylogenectic analysis
All the sequence matrices were aligned with MAFFT
program (version 7.31) [59] and manually modified
with Geneious (version 9.1.7) [54]. ree datasets of
mitochondrial, chloroplast, and nuclear ribosomal cis-
tron sequences were comprised of the following cases:
the mitochondrial dataset had 41 protein-coding genes,
nine intron sequences, and ten intergenic regions; the
chloroplast dataset used complete chloroplast genome
sequences; and the nrDNA dataset was ETS-18S-ITS1-
5.8S-ITS2-26S. A maximum likelihood (ML) analysis was
carried out with IQ-TREE (version 2.1.2) [60] using 1000
ultrafast bootstrap replicates. e DNA substitution
modelswere chosen as TVM+I+G (mtDNA), GTR+I+G
(cpDNA), and GTR+G (nrDNA). e bayesian infer-
ence (BI) analysis based on the GTR+F+I (mtDNA),
GTR+F+I+G4 (cpDNA), and GTR+F+I (nrDNA) mod-
els was performed with MrBayes (version 3.2.7) [61].e
BI analysis started with a random tree andsampled every
1000 generations. e first 20% of the trees was discarded
as burn‐in, and the remainingtrees were used to generate
a majority‐rule consensus tree [62].Visualizing and edit-
ing phylogenetic trees were performed with FigTree soft-
ware(version 1.4.0).
Results
Organelle genome features
e DNA of C. henryi was extracted and sequenced using
the Illumina HiSeq 2500 and Oxford Nanopore Pro-
methION platforms for second- and third-generation
sequencing, respectively. A total of 27.9Gb raw reads of
150bp in length and about 20.7Gb Nanopore long read
data with an average read size of 27,600bp were used for
genome assembly. We successfully assembled the whole
mitogenome and chloroplast of C. henryi by using Illu-
mina short reads and Nanopore long reads, which con-
sists of one big linear contig and two tiny circular contigs
with lengths of 968,798bp, 199,231bp, and 154,938bp,
respectively. With a total length of 1,168,029bp, the over-
all base composition of the entire mitogenome is as fol-
lows: A: 26.7%, T: 26.5%, G: 23.4%, C: 23.4%, and G + C
content is 46.8%. e positions of all the genes identi-
fied in the C.henryi mitogenome and the functional cat-
egorization of these genes are presented (Fig. 2A). e
mitogenome contains 65 unique genes, including 41
protein-coding genes (PCGs), 21 transfer RNA (tRNA)
genes, and 3 ribosomal RNA (rRNA) genes (Table2). e
chloroplast genome, with a length of 154,938 bp (39%
G + C content), contains 113 unique genes, including 79
protein-coding genes, 30 tRNA genes, and 4 rRNA genes
(Fig.2B).
Repeat elements andDNA transfer analysis
In the mitogenome of C. henryi, we detected 2233
repeats, and these repeats include 1093 forward repeats
of 30–366bp, 982 palindromic repeats of 30–25,242bp,
40 reverse repeats of 30-39 bp, 37 complement repeats of
30-38bp, and 81 tandem repeats of 2–53bp (Fig.3A). A
total of 368 potential SSRs were detected in the mitog-
enome of C. henryi, of which 279 are mononucleotides,
66 are dinucleotides, nine are trinucleotides, eight are
tetranucleotides, five are pentanucleotides, and one is
hexanucleotides. Of the mononucleotide repeats, A/T
(86.74%) occupied the main proportion (Fig.3B).
e C. henryi mitogenome sequence was approxi-
mately 7.5 times longer than its chloroplast genome.
Between the mitogenome and plastome we found a total
of 50 homologous DNA fragments (TableS1, Fig.4). e
length of fragments ranged from 39 to 5262bp. e total
insert fragments were 23,583 bp in length, accounting
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Page 6 of 18
Yangetal. BMC Plant Biology (2024) 24:616
for 2.02% of the length of mitogenome. Six tRNAgenes
were located in these fragments (trnH-GUG, trnM-CAU,
trnN-GUU, trnV-GAC, trnW-CCA, trnP-UGG). We also
detected that the fragments of chloroplast genes, such as
rrnS and trnD-GUC, were located in the mitogenome.
Mitochondrial genome comparisons
We performed synteny and rearrangement analy-
ses between C. henryi mitogenome sequences and two
published mitogenome sequences of H. nymphaeifolia and
M. biondii. Frequent rearrangement events were detected
in both coding segments and noncoding regions (Fig-
ureS1). For the PCGs, eleven segments (Fig.5) including
matR-nad1, nad1-ccmB-rps11, nad5-nad3-rps12, cob-
rps14-rpl5, rpl2-rps19-rps3-rpl16, rps1-rps7, cox2-nad6-
nad5-nad7, sdh4-cox3-atp8, atp4-nad4L, nad1-nad5, and
rps13-nad1 were extensively conserved between C. hen-
ryi and M. biondii mitogenomes, while seven segments
Fig. 2 Gene maps of the Caryodaphnopsis henryi mitogenome (A) and chloroplast genome (B). The annotation of the genomes was performed
using GeSeq. The genes that are drawn outside of the circle are transcribed clockwise, whereas those that are drawn inside the circle are transcribed
counter clockwise
Table 2 Genes, separated by category, encoded by Caryodaphnopsis henryi mitogenome
A single asterisk (*) preceding gene names indicate intron-containing genes
Group of genes Name of gene
Maturases matR
Transport membrane protein mttB
NADH dehydrogenase *nad1, *nad2, nad3, *nad4, nad4L, *nad5, nad6, *nad7, nad9
ATP synthase atp1, atp4, atp6, atp8, atp9
Cytochrome c biogenesis ccmB, *ccmC, ccmFC, ccmFN
Cytochrome c oxidase cox1, *cox2, cox3
Ubiquinol cytochrome c reductase cob
Ribosomal proteins (SSU) rps1, rps2, *rps3, rps4, rps7, *rps10, rps11, rps12, rps13, rps14,rps19
Ribosomal proteins (LSU) *rpl2, rpl5, rpl10, rpl16
Succinate dehydrogenase sdh3, sdh4
Ribosomal RNA rrn5, rrnL, rrnS
Transfer RNA trnC-GCA, trnD-GUC, trnE-UUC, trnF-GAA, trnfM-CAU, trnG-GCC, trnH-GUG,
trnI-CAU, trnK-UUU, trnM-CAU, trnN-GUU, trnN-GUU, trnP-UGG, trnP-UGG,
trnP-UGG, trnQ-UUG, trnS-GCU, rnS-UGA, trnV-GAC, trnW-CCA, trnY-GUA
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Yangetal. BMC Plant Biology (2024) 24:616
including rps11-nad9, rps19-rps3-rpl16-rpl10, nad5-nad7,
rpl5-rps14-cob, sdh4-cox3-atp8, nad5-nad3-rps12, and
sdh3-atp4-nad4L were extensively conserved between C.
henryi and H. nymphaeifolia mitogenomes.
Phylogeny ofmitochondrial sequences
With the reference mitogenome of C. henryi, we fur-
ther assembled 60 mitochondrial regions, including
41 mitochondrial protein-coding gene sequences, nine
intron sequences, and ten intergenic region sequences
for 21 individuals of ten Caryodaphnopsis species in
Asia. e mitochondrial matrix (Table 3) based on
the 60 regions comprises 166,057 characters, and 363
of which (depending on the consensus threshold) are
parsimony-informative characters (PICs). e mito-
chondrial matrix was used to reconstruct phylogenetic
trees, with two Neocinnamomum species serving as
outgroups (Fig.6A). e 22 Caryodaphnopsis individu-
als were divided into four distinct groups. e group I
only included one C. burger individual (ML-BS = 100%,
BI-PP = 1.00). e group II included two C. henryi
individuals (ML-BS = 95%, BI-PP = 1.00). e group
III included individuals of C. bilocellata, C. latifolia,
and a suspected new species C. sp. 2 (ML-BS = 97%,
BI-PP = 1.00). And the group IV included individuals of
C. laotica, C. malipoensis,C.metallica, C. tonkinensis,
and two suspected new species C. sp. 1 andC. sp. 3(ML-
BS = 97%, BI-PP = 1.00).
Phylogeny ofplastome sequences
e complete chloroplast genomes of 21 individuals from
tenCaryodaphnopsis species in Asia were newlydeter-
mined in the present study.ey were all assembled into
single circular genomes with a typical quadripartite struc-
ture, including one LSC with the lengths of 86,035 bp
(C. henryi) to 91,966 bp (C. sp. 2), one SSC with the
lengths of 17,310bp (C. sp. 3) to 17,701bp (C. henryi),
and a pair of IR with the lengths of 19,694 (C. sp. 2) to
25,601bp (C. henryi) (Table4). e chloroplast genome
alignment has 155,629 characters, 705 (0.45%) of which
are PICs. e matrix of complete plastomes was used
to reconstruct a phylogenetic tree of Caryodaphnopsis
Fig. 3 Number and distribution of long repeats (A) and SSRs (B) in mitogenome sequence of Caryodaphnopsis henryi
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Yangetal. BMC Plant Biology (2024) 24:616
(Fig. 6B). Five well-supported groups were identified
within the Caryodaphnopsis: the group I included one
C. burger individualand two C. henryiindividuals(ML-
BS = 100%, BI-PP = 1.00), the group II included four indi-
viduals of C. laotica and C. tonkinensis(ML-BS = 98%,
BI-PP = 1.00),thegroup III only included one individual
of C. metallica (ML-BS=98%, BI-PP=1.00), the group
IV includedother two individuals of C. tonkinensis and
individuals of a suspected new species C. sp. 1 (ML-BS =
71%,BI-PP = 0.41), and the group V includedindividu-
alsof C. bilocellata, C. latifolia, C.malipoensis, and two
suspected new species C. sp. 2 and C. sp. 3 (ML-BS =
71%, BI-PP = 0.41).
Phylogeny ofnuclear ribosomal cistron sequences
e nrDNA sequence of 21 individuals from ten Car-
yodaphnopsis species in Asia were newly determind
in the study.e lengths of nrDNA sequences ranged
from 6482bp (C. bilocellata) to 6537bp (C. metallica)
(Table5). ree rRNA genes and three transcribed spac-
ers were found in these nrDNA sequences. Forthe 26S
large-subunit rRNA (26S) region, the length varied from
3386 to 3388bp; for the 18S small-subunit rRNA (18S)
region, 1811bp; for the 5.8S rRNA (5.8S) region, 159bp;
for the external transcribed spacer (ETS) region, from
653 to 656bp; for the ITS1 region, from 214 to 271bp;
and for the ITS2 region, from 213 to 222bp. e nuclear
ribosomal matrix is 6,672 bp and contains 175 (2.62%)
PICs.e 22 Caryodaphnopsis individuals were divided
into sixgroups(Fig.6C).e group I includedthe only
one individual of C. burger (ML-BS = 100%, BI-PP =
1.00). e group II includedthe two individuals of C. hen-
ryi (ML-BS = 90%, BI-PP = 0.95). e group III included
the only oneindividual of C. metallica and two individu-
als of C. bilocellata (ML-BS = 98%, BI-PP = 0.99). e
groupIV included the two individuals of C. malipoensis
(ML-BS = 83%, BI-PP = 1.00). e group V includedthe
individuals of C. latifolia and C. tonkinensis (ML-BS =
94%, BI-PP = 1.00). And the group VI included theindi-
viduals of C. laotica and three suspected new species C.
sp. 1, C. sp. 2, and C. sp. 3 (ML-BS = 94%, BI-PP= 1.00).
Fig. 4 Homological sequences between mitogenome and plastome of C. henryi. The blue circular segment represents the mitogenome, the green
circular segment represents the plastome, and the line represents the homologous fragment. Different colors in the inner circle represent gene
density
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Yangetal. BMC Plant Biology (2024) 24:616
Discussion
General features ofmitogenome
is study presents thecomplete mitogenome for woody
plants in the family Lauraceaeobtained by Illuminaand
Nanopore sequencing technologies (Fig. 2A). To date,
there are now three orders and eight families whose
mitogenomes have been sequenced within the magnoli-
ids. e mitogenome of Caryodaphnopsis henryi, witha
length of 1,168,029bp, is larger than bothmitogenomes
of Hernandia nymphaeifolia and Magnolia biondii
[63].e length of mitochondrial genes is similar among
C.henryi, M. biondii,and H. nymphaeifolia. A total of 65
mitochondrial genes in C.henryi, with a total length of
41,938bp, is 800bp smaller than those of M.biondiiand
49bp larger than those of H. nymphaeifolia. e mito-
chondrial intronic and intergenic regions of C. henryi,
with a total length of 1,126,191bp, are 201,829bp larger
than those of M. biondiiand 632,275bp larger than those
Fig. 5 Gene order in the mitogenomes of Hernandia nymphaeifolia, Magnolia biondii, and Caryodaphnopsis henryi. H. nymphaeifolia mitochondrial
genes are shown on the left, C. henryi mitochondrial genes in the middle, and M. biondii mitochondrial genes on the right, with different colors
signifying the relevant collinear sections
Table 3 The 60 mitochondrial segments were used to reconstruct the phylogenetic relationships
Types Regions
Intergenic regions nad4-cox2, cox2-nad6, rps14-cob, rps7-atp6, rps13-nad1, nad5-rps4, cox3-atp8, nad1-ccmB, atp1-sdh4, nad5-nad7
Intron regions ccmFC-ccmFC, cox2-cox2, nad2-nad2, nad4-nad4, nad5-nad5, nad7-nad7, rpl2-rpl2, rps3-rps3, rps10-rps10
PCGs atp1, atp4, atp6, atp8, atp9, ccmB, ccmC, ccmFC, ccmFN, cob, cox1, cox2, cox3, matR, mttB, nad1, nad2, nad3, nad4, nad4L, nad5,
nad6, nad7, nad9, rpl10, rpl16, rpl2, rpl5, rps1, rps10, rps11, rps12, rps13, rps14, rps19, rps2, rps3, rps4, rps7, sdh3, sdh4
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
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Yangetal. BMC Plant Biology (2024) 24:616
Fig. 6 Molecular phylogenetic trees of eleven species of Caryodaphnopsis based on mitochondrial (A), complete plastomes (B), and nrDNA (C)
sequences using unpartitioned Bayesian inference (BI) and maximum likelihood (ML). The trees were rooted with thesequences of Neocinnamomum
fargesii and N. lecomtei. Numbers associated with the branches are ML bootstrap values (BS) and BI posterior probabilities (PP)
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Yangetal. BMC Plant Biology (2024) 24:616
Table 4 Summary of ten complete plastomes of Caryodaphnopsis
Types C. henryi C. tonkinensis C. metallica C.sp.3 C. malipoensis C. bilocellata C. latifolia C. laotica C. sp.1 C. sp.2
Total cpDNA size (bp) 154,938 148,829 148,977 149,299 149,314 148,970 148,970 148,838 148,977 149,027
Length of LSC region (bp) 86,035 91,762 91,910 91,917 91,932 91,912 91,912 91,771 91,935 91,966
Length of IR region (bp) 25,601 19,695 19,700 20,036 20,036 19,695 19,695 19,695 19,695 19,694
Length of SSC region (bp) 17,701 17,677 17,667 17,310 17,311 17,668 17,668 17,677 17,652 17,673
Total GC content 39.00% 39.00% 39.10% 39.00% 39.00% 39.00% 39.00% 39.00% 39.00% 39.00%
Total number of genes (unique) 131(113) 128(113) 128(113) 128(113) 128(113) 128(113) 128(113) 128(113) 128(113) 128(113)
Protein Coding Genes 86 83 84 84 84 84 84 84 84 84
tRNA 37 36 36 36 36 36 36 36 36 36
rRNA 8 8 8 8 8 8 8 8 8 8
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Table 5 Summary of ten complete nrDNAs of Caryodaphnopsis
Types C. henryi C. tonkinensis C. metallica C.sp.3 C. malipoensis C. bilocellata C. latifolia C. laotica C. sp.1 C. sp.2
External transcribed spacer (bp) 653 653 654 654 654 656 654 654 654 654
18S small subunit rRNA (bp) 1811 1811 1811 1811 1811 1811 1811 1811 1811 1811
Internal transcribed spacer 1 (bp) 271 266 214 266 264 256 266 267 257 266
5.8S rRNA (bp) 159 159 159 159 159 159 159 159 159 159
Internal transcribed spacer 2 (bp) 213 222 222 213 213 213 215 213 213 213
26S large subunit rRNA (bp) 3388 3387 3386 3387 3387 3387 3388 3387 3387 3387
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
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Yangetal. BMC Plant Biology (2024) 24:616
of H. nymphaeifolia. ere is no substantial difference in
the number of mitochondrial genes, variations in non-
coding DNA content are statistically linked to variations
in mitogenome size [64]. In addition, siginificant length
variation of mitochondrial intergenic regions has also
been reported in nine species in Piperales [23].
e size variation of mitogenomes in land plants can
be influenced by a variety of factors, including retrotrans-
poson proliferation, the generation of repetitive DNA
through homologous recombination, the incorpora-
tion of foreign sequences via intracellular transfer from
the chloroplast or nuclear genome, or horizontal trans-
fer of mitochondrial DNA [63, 64]. is variety has been
reported in many plant species, with mitogenome sizes
ranging from 66kb in Viscum scurruloideum [65] to as
large as 11Mb in Silene conica [66]. However, in different
species, the increase in mitogenome size could be caused
by different factors [67].
On the one hand, a total of 2233 repeats and 368 SSRs
were identified in the mitogenome of Caryodaphnopsis
henryi (Fig.3B). e mitogenome exhibited a significant
number of dispersed repeats, primarily consisting of tan-
dem, forward, and palindromic repeats (Fig. 3A). ese
repeats are critical for the recombination of the mitog-
enome, as they are one of the causes of variation affect-
ing the size and structure of the mitogenome [65]. e
presence of repeated sequences in the mitogenome can
increase the possibility of recombination, leading to vari-
ations in the genome structure, which in turn could relate
to gene expression and function [66].
On the other hand, the structure and evolutionary pro-
cessof plantmitogenomemake it more prone to accept-
ing and integrating foreign DNA [64]. Horizontal gene
transfer from chloroplasts to mitochondria has been
reported multiple times, but the length and number of
transfer fragments vary significantly between species.
In this study, we found 50 homologous DNA fragments
in Caryodaphnopsis henryi (Fig. 4), transferred from
the chloroplast genome to the mitogenome. us, the
length variation of intergenic regions might contribute
to the length difference of the mitogenome inmagnoli-
ids lineages, primarily due to frequent recombination of
repeated sequences and integration of foreign ones dur-
ing evolution [67].
Genome rearrangement events, such as gene order
changes, can reflect evolutionary distance and niche
adaptation between species [68]. ese events are
responsible for creating extant species with conserved
genes in different positions across genomes, and close
species tend to have a similar set of genes or share
most of them [69, 70]. Gene synteny analysis revealed
a succession of rearrangements in the mitogenomes of
Magnolia biondii, Hernandia nymphaeifolia, and Car-
yodaphnopsis henryi (Fig. 5). Only six gene clusters in
Fig. 7 Phylogenies obtained from the three different datasets: a mitochondrial; b nuclear ribosomal; c chloroplast
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Yangetal. BMC Plant Biology (2024) 24:616
mitogenomewere found to be highly conserved acrossC.
henryi, H. nymphaeifolia, and M. biondii. In addition,
unlike H. nymphaeifolia, the mitogenomes of C. henryi
and M. biondii contained elevengene clusters. Although
C. henryi has a closer relationship with H. nymphaeifo-
lia, the number of conserved gene clusters between C.
henryi and H. nymphaeifolia arelessthan those between
C. henryi and M. biondii. e location of protein-coding
genes may be poorly conserved in plant mitogenomes.
e genome rearrangement events revealed by gene col-
linearity analysis can indeed reflect the evolutionary dis-
tance and niche adaptation between species [
71, 72].
Cytonuclear discordance
Cytonuclear discordance, which shows markedly different
phylogenetic patterns between nuclear markers and cyto-
plasmic genes such as mitochondrial and chloroplast genes,
has been observed in various plant populations and is often
attributed to processes such as hybridization and incom-
plete lineage sorting [30, 73, 74]. e species in thegenus
ofCaryodaphnopsis, with different positions in the chloro-
plast and mitochondrial phylogenies relative to the nuclear
phylogeny(Fig. 7). Our phylogenetic analyses revealed sig-
nificantcytonuclear discordance in thegenus ofCaryodaph-
nopsis. e species of C. bilocellata and C. metallica are
generally grouped together in the nuclear phylogeny, with
different positions in the mitochondrial and chloroplast
phylogenies. e speciesof C. sp. 1, C. sp. 2, C. sp. 3, andC.
laoticaare grouped together in the nuclearphylogeny, with
different positionsin the mitochondrial and chloroplast phy-
logenies. is finding is comparable with prior studies on
nuclear and cytoplasmic genes inconsistencies in other plant,
including in the apple genus Malus [
73], balsam poplars [30], the Australian plant genus
Adenanthos [74]. is inconsistency may reveal complex
patterns of gene flow that these species may have experi-
enced over the course of their evolution [75]. In addition,
four individuals of the C. tonkinensis species are clustered
together in nuclear phylogeny but separated in different
clades of the mitochondrial and chloroplast phylogenies.
is separation of C. tonkinensis may represent intraspecific
Fig. 8 The geographic distribution and the fruit feature of Caryodaphnopsis are represented in the phylogenetic tree based on their mitochondrial,
chloroplast, and nrDNA phylogenetic trees
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Yangetal. BMC Plant Biology (2024) 24:616
diversity, indicating that Caryodaphnopsis may have a spe-
cies complex.
Mitochondrial and chloroplast capture in plants is a
phenomenon that occurs when a plant species acquires
these organelles from another species through hybridi-
zation [76, 77]. In our study, the species of Caryodaph-
nopsis, with different positions in the nuclear phylogeny,
are grouped together in the mitochondrial and chloro-
plast phylogenies. e individuals of C. latifolia and C.
bilocellata collected from Hekou, China. Based on the
mtDNA and cpDNA data, our phylogenomic analy-
sisshows sisterhood of the species of C. latifolia and the
species of C. bilocellata.Our phylogeny appears to reflect
theorganellar capture from another species.Maybe the
overlap of their geographic distributions results in mito-
chondrial and chloroplast capture. e overlapping geo-
graphic (Fig.8) distribution of species can lead to gene
flow and hybridization, potentially resulting in gene trans-
fer between mitochondria and chloroplasts, which can
affect their clustering on the phylogenetic tree [78, 79].
Distribution sites of Caryodaphnopsis species shows an
interesting pattern of genetic diversity across regions with
comparable species richness. Malipo county of China has
only two Caryodaphnopsis species, which share similar
chloroplast and mitochondrial genomes (Fig.9). In con-
trast, Hekou county of China has six Caryodaphnopsis
species with multiple types of chloroplast, mitochondrial,
and nrDNA sequences. e genetic diversity within and
between species could trace implications for evolutionary
processes, including adaptation to environmental stress,
natural selection, and disease susceptibility [80]. e high
genetic diversity observed in Hekou suggests that it may
be a center of Caryodaphnopsis species distribution in
Asia and a source of genetic resources for future conser-
vation and breeding efforts. e phenomenon of higher
genetic diversity in areas with greater species richness
has been observed in other plant groups, such as tropical
rainforests and alpine regions [81–83].
Conclusions
We assembled the complete mitogenome sequence of
Caryodaphnopsis henryi, a tropical tree in the family
Lauraceae. e whole mitogenome of C. henryi consists
of one big linear contig, with length of 968,798bp, and
one tiny circular contig, with length of 199,231bp. e
mitogenome contains 65 genes, including 41 protein-
coding genes, 21 tRNA genes, and three rRNA genes.
ere are 50 homologous DNA fragments between
Fig. 9 Distribution of Caryodaphnopsis species in this study. Each site of the species is represented by a square point. The color of the square
corresponds to the species’ grouping with nrDNA data. The circle is divided into three parts, representing the groupings with nrDNA, mtDNA,
and cpDNA data respectively. Same color indicates the species within the consistent group of the phylogenetic topologies. The world map
was downloaded from the website of the Resource and Environment Science and Data Center (http:// www. resdc. cn)
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Page 16 of 18
Yangetal. BMC Plant Biology (2024) 24:616
the mitogenome and plastome of C. henryi. Com-
parative genomic analysis indicated that the sizes and
geneorders of the three sequenced mitogenomesof C.
henryi, Magnolia biondii, and Hernandia nymphaeifo-
lia differed greatly. We found significant incongruence
between the mitochondrial and nuclear or chloroplast
phylogenies in a Caryodaphnopsis group.e study also
revealed that Caryodaphnopsis species with sympatry
often cluster together in the chloroplast and mitochon-
drial phylogenetic trees.
Abbreviations
PCGs Protein-Coding Genes
tRNA Transfer RNA Genes
rRNA Ribosomal RNA Genes
SSRs Simple Sequence Repeats
cpDNA Chloroplast DNA
nrDNA Nuclear Ribosomal Cistron
mtDNA Mitochondrial DNA
PICs Parsimony-Informative Characters
ML Maximum Likelihood
BI Bayesian Inference
LSC Large Single-Copy Region
SSC Small Single-Copy Region
IRs Inverted Repeats
Supplementary Information
The online version contains supplementary material available at https:// doi.
org/ 10. 1186/ s12870- 024- 05050-3.
Supplementary Material 1.
Supplementary Material 2.
Acknowledgements
The authors would like to thank Dr. Bing Liu at Institute of Botany, Chinese
Academy of Sciences (CAS) for species collection.
Authors’ contributions
S.T.Y., S.J.W., and Y.S. designed the work. Y.Y.Q. and J.P.H. prepared the datasets.
S.T.Y., Y.Y.Q., D.Z., J.P.H., Y.H.T, S.J.W., and Y.S. contributed materials/analysis tools.
S.T.Y. wrote the manuscript. D.Z., J.P.H., S.J.W., and Y.S. revised the manuscript.
All authors approved the final manuscript.
Funding
This work was supported by the Guangxi Key Laboratory of Landscape
Resources Conservation and Sustainable Utilization in Lijiang River Basin,
Guangxi Normal University (Grant No. LRCSU21Z0103) and Key Laboratory
of Ecology of Rare and Endangered Species and Environmental Protection
(Guangxi Normal University), Ministry of Education (AB21220057). This work
was also supported by the National Natural Science Foundation of China
(No. 32260060, 31970223) and the Special Program for Technology Bases and
Talents of Guangxi (Grant No. 2022AC20002).
Availability of data and materials
All relevant phylogenomic matrices were deposited in the the manuscript’s
supplementary files. The assembled mitochondrial genome sequence was
submittted to National Center for Biotechnology Information with accession
number OR987149 (https:// www. ncbi. nlm. nih. gov).
Declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Author details
1 Key Laboratory of Ecology of Rare and Endangered Species and Environmen-
tal Protection (Ministry of Education) and Guangxi Key Laboratory of Land-
scape Resources Conservation and Sustainable Utilization in Lijiang River
Basin, Guangxi Normal University, Guilin 541004, Guangxi, China. 2 Southwest
Forestry University, Kunming 650224, Yunnan, China. 3 Southeast Asia Biodiver-
sity Research Institute, Chinese Academy of Sciences & Center for Integrative
Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy
of Sciences, Menglun, Mengla, Yunnan 666303, China. 4 Guangxi Key Labora-
tory of Plant Conservation and Restoration Ecology in Karst Terrain, Guangxi
Zhuang Autonomous Region and Chinese Academy of Sciences, Guangxi
Institute of Botany, Guilin 541006, China.
Received: 9 December 2023 Accepted: 19 April 2024
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