Characterization of the complete chloroplast genome of Camellia tienii (Theaceae) and its relatives

Abstract

Camellia tienii, an indigenous plant species in Vietnam, is renowned for its remarkable medicinal properties. However, the current methods for plant identification are not reliable due to shared characteristics with other species in Camellia genus. To address this, the present study aimed to sequence and characterize the complete chloroplast (cp) genome of C. tienii. The resulting cp genome is 162,167 bp in size and encompasses 154 genes, including 98 protein-coding genes, 8 rRNA genes, and 48 tRNA genes. Notably, this genome contains 55 simple sequence repeats, specifically type A and T motifs. It is worth mentioning that the ndhF gene was not detected in this genome, while the trnL gene was present. Phylogenetic analysis revealed that C. tienii shares a close relationship with C. tamdaoensis. These significant findings contribute with valuable insights that can aid in the accurate taxonomy, plant identification, and conservation efforts concerning this herb in Vietnam.

Keywords:
Chloroplast genome; medicinal plant; next generation sequencing; simple sequence repeat

INTRODUCTION

The Camellia genus, belonging to the Theaceace family, stands as one of the largest genera in East and Southeast Asia, with an estimated number of 120 to 300 documented species (Ly et al. 2022). These diverse Camellia species find daily application in various domains, such as the production of beverages like green tea, culinary uses, cosmetics (Le et al. 2023), ornamental purposes, and traditional medicine applications (Lu et al. 2012). Additionally, essential oils derived from Camellia plants have been explored (Pereira et al. 2022). Within the Camellia genus, numerous medicinal compounds have been identified, including alkaloids, steroids, terpenoids, saponins, carotenoids, and polyphenols (An et al. 2023, Tran et al. 2023). These compounds are commonly employed for the treatment of various ailments caused by bacteria, fungi, viruses, and oxidative stress, as well as for their potential anti-tumour effects in humans (Maslov et al. 2022, An et al. 2023). Furthermore, they have been investigated for their potential to reduce hypertension, high cholesterol levels, and obesity (Le et al. 2023).

To date, the classification of Camellia species has primarily relied on morphological characteristics, including leaf anatomy data (Erxu et al. 2009, Jiang et al. 2013), as well as the examination of fruits, flowers, and leaves (Syahbudin et al. 2019, Hoi et al. 2021), or biochemical compounds (Gao et al. 2022). However, due to the limitations of morphological taxonomy in terms of accuracy, various studies have sought to enhance classification through the application of molecular markers. These markers involve different DNA regions, such as RAPD, AFLP, and ISSR (Guinasekare 2007), ITS (Vijayan et al. 2009), or barcode regions like matK, rbcL, and ITS2 (Viet et al. 2019), as well as matK, rbcL, ycf1, and trnL-F (Pang et al. 2022). Nevertheless, these markers have relatively narrow coverage of plant genomes, resulting in limited effectiveness in the classification and identification of plants.

In recent years, there has been a significant increase in the cost and time required to sequence the complete chloroplast (cp) genomes of various plant species, including Goodyera schlechtendaliana (Oh et al. 2019) and jackfruit (Artocarpus heterophyllus) (Lin et al. 2022), due to advancements in next-generation sequencing (NGS) technology. The available cp genomes have provided useful information to develop molecular marker to identify corresponding plant species (Andrade et al. 2018) or investigate the effectiveness of different DNA barcode regions located on cp genome for plant identification (Inglis et al. 2021). For the Camellia genus, there have also been several reports of complete cp genomes from different species, such as Camellia japonica (Li et al. 2019), Camellia chuongtsoensis (Yu et al. 2020), and Camellia leyeensis (Xiao et al. 2022). In Vietnam alone, over 40 species have been documented (Dung et al. 2016), with more than 30 species of yellow-flowered Camellia identified, establishing Vietnam as a centre of diversity for this particular type of Camellia (Do et al. 2019). The number of newly discovered species has experienced a substantial increase (Do et al. 2019, Ly et al. 2022, Quach et al. 2022). However, only a few cp genomes of Camellia species endemic to or originating from Vietnam have been published, such as Camellia vietnamensis (Lyu et al. 2019, Chen et al. 2023, Hao et al. 2023).

In 2014, Camellia tienii, a species endemic to Vietnam, was first discovered in Tam Dao National Park (Ninh and Ninh 2014). Since then, extensive studies have been conducted on various aspects of this species, including the identification of suitable planting areas (Manh et al. 2020), analysis of genotypic and phenotypic diversity (Le et al. 2023), and investigation of its antioxidant activity (Nga et al. 2023). Recently, Anh and colleagues utilized fluorescence microscopy to distinguish C. tienii from five other Camellia species based on leaf anatomy (Anh et al. 2023). However, this method is time-consuming and costly. Moreover, relying solely on the morphological features for classifying Camellia species is not highly accurate (Lu et al. 2012), as these features can vary due to environmental factors and geographic diversity within the Camellia genus (Gao et al. 2022, Tran et al. 2023). In our study, we employed next-generation sequencing (NGS) to sequence the chloroplast (cp) genome of C. tienii, an endemic species collected in Vietnam. We compared its genome with published cp genomes of Camellia species found in or near Vietnam to identify distinct genomic features. The information obtained from this research has significant implications for the taxonomy, botanical identification, breeding, and conservation programs of C. tienii in Vietnam.

MATERIAL AND METHODS

Sample collection and DNA sequencing

The specimen of C. tienii was obtained from Dong Bua commune, Tam Quan ward, Tam Dao district, Vinh Phuc province, Vietnam. The voucher sample is currently stored at the laboratory of Ho Chi Minh University of Industry and Trade in Vietnam. To extract the total DNA, fresh leaves were processed using the Isolate II Plant DNA Kit from Bioline (UK). The quality of DNA was assessed through 1% gel electrophoresis, while the quantity was measured using Nanodrop from ThermoScientific (Delaware, USA).

First, 500 ng of DNA was fragmented using the S220 Focused-ultrasonicator from Covaris (USA). Subsequently, dA tails were added, adapters were ligated, and the resulting fragments were purified. The library preparation, quality control, cluster generation, and DNA sequencing processes were conducted at Azenta Life Sciences (USA) using the Illumina Novaseq 6,000 sequencer. To assess the quality of the raw reads, FastQC in the Galaxy portal (http://usegalaxy.org) was employed (Nguyen et al. 2024). The NGS data was submitted to the Sequence Read Archive (SRA) database in NCBI under the PRJNA1081179 project and can be accessed at https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1081179.

Chloroplast genome assembly and annotation

The reads from both ends were aligned to the Camellia vietnamensis reference sequence with NCBI accession number NC_060778.1 for the assembly process. Subsequently, the Pilon tool (v.1.21) was employed to generate a FASTA file for further analysis (Villanueva-Corrales et al. 2021). The Geseq program (https://chlorobox.mpimp-golm.mpg.de/geseq.html) was utilized to annotate and locate genes within the chloroplast genomes (Tillich et al. 2017). To identify the counts of protein-coding genes, rRNA, and tRNA in the cp genome, the Chloroplot program (http://irscope.shinyapps.io/Chloroplot/) was utilized (Zheng et al. 2020).

Comparative analysis among Camellia cp genomes

The cp genomes were aligned using the MAFFT program (v.7) available at http://mafft.cbrc.jp/alignment/server/. The alignment parameters proposed by Katoh et al. (2019) were used. The junctions of LSC/IRB/SSC/IRA were visualized using IRscope, accessible at http://irscope.shinyapps.io/irapp/ (Hao et al. 2023). The visualization was based on the cp genome annotations of related species available in Genbank, as described by Amiryousefi et al. (2018). To identify SSR motifs, the MIcroSAttelite (MISA) identification tool was utilized. The tool can be accessed at https://webblast.ipk-gatersleben.de/misa/ as described by Beier et al. (2017).

Phylogenetic analysis

The NCBI Genbank (https://www.ncbi.nlm.nih.gov/nucleotide/) was utilized to access additional complete cp genome sequences of various species from the Camellia genus. This included retrieving eight cp genomes of C. vietnamensis (NC_060778.1; MN078093.1; MN078092.1; MN078084.1; MN078085.1; PP155504.1; PP155501.1; and OL689024.1), five cp genomes of C. indochinensis (ON208846; OK135162; ON411685; NC_067091.1; and OM055647.1), one cp genome of C. tamdaoensis (NC_069227) and four other cp genomes which are closely related to C. vietnamensis, namely C. oleifera (MF541730.2), C. yuhsienensis (OL689025.1), C. gauchowensis (NC_053541.1) and C. suaveolens (ON418963.1).

The phylogenetic relationships between the cp genomes were established using the MAFFT alignment mentioned earlier. A phylogenetic tree comprising 14 cp genomes was constructed using Maximum Likelihood (ML) methods with 500 bootstrap replicates, employing MEGA X software. The tree files were then converted to Newick format and annotated using iTOL- Interactive Tree of Life tool (https://itol.embl.de/), as described by Letunic and Bork (2021). Three cp genomes from three genera in the Theaceae family, namely NC_035709.1 (Anneslea fragrans), NC_035704.1 (Pyrenaria diospyricarpa), and NC_035706.1 (Ternstroemia gymnanthera), were utilized as outgroups (Luna and Ochoterena 2004).

RESULTS AND DISCUSSION

Assembly and comparison of cp genomes

In this research, we conducted the first-ever sequencing and annotation of the complete cp genome of C. tienii in Vietnam. A dataset of 7.318 GB of 150 bp paired-end reads was generated, resulting in a total of 24,396,390 reads with a Phred score of 96.64%, where the majority of reads (greater than 96.64%) had a quality score greater than Q20. The assembled cp genome exhibited a conserved circular structure with a total length of 162.167 bp, following the typical organization of a plant cp genome. It consisted of four main regions: a Large Single Copy (LSC), a Small Single Copy (SSC), and two Inverted Repeat (IR) regions. These IR regions were located between the LSC and SSC regions (Figure 1). While previous studies have reported the size of Camellia cp genomes to be approximately 157 mb (Li et al. 2019, Xiao et al. 2022, Hao et al. 2023), the assembled cp genome of C. tienii was found to be significantly longer. Nevertheless, other large cp genomes have been reported, such as 161,078 bp in C. grijsii (Xie et al. 2021) and 161,958 bp in C. vietnamensis (Lyu et al. 2019), indicating considerable variation in cp genome size within the Camellia genus.

Figure 1
The cp genome map of Camellia tienii, generated with http://irscope.shinyapps.io/Chloroplot/, displays the genes transcribed in clockwise and counterclockwise directions, depicted outside and inside of the circle, respectively. The LSC, SSC, IRA, and IRB are labelled as the primary parts of the cp genome. The inner circle's dark and light grey colours represent the GC and AT content, respectively.

A total of 13 cp genomes from three Camellia species, available in the NCBI GenBank, were downloaded and compared to the cp sequence of C. tienii. The gene compositions are provided in Table 1. A notable distinction was observed between the cp genome of C. tienii and the other cp genomes, particularly in terms of the number of coding genes and tRNA genes. The obtained cp genome of C. tienii was annotated with a total of 154 genes, including 98 protein-coding genes, 8 rRNA genes, and 48 tRNA genes. In Camellia cp genomes, the number of genes encoding rRNA remains constant at 8. However, the number of genes encoding proteins and tRNA shows significant variation across different studies (Li et al. 2019, Xu et al. 2023, Ran et al. 2024). These variations in gene content among cp genomes contribute to our understanding of the genetic structure of the C. tienii species.

Table 1
Size comparison of plastome features of 14 Camellia species

Accession	Taxon	Genome size (bp)	Coding genes	rRNA	tRNA
NC_060778.1	C. vietnamensis	156,999	91	8	37
MN078093.1	C. vietnamensis	156,999	91	8	37
MN078092.1	C. vietnamensis	157,004	91	8	37
MN078084.1	C. vietnamensis	157,003	91	8	37
MN078085.1	C. vietnamensis	157,089	91	8	37
PP155504.1	C. vietnamensis	157,000	90	8	37
PP155501.1	C. vietnamensis	157,003	90	8	37
OL689024.1	C. vietnamensis	156,910	90	8	37
ON208846	C. indochinensis	156,621	88	8	37
ON411685	C. indochinensis	156,633	92	8	39
NC_067091.1	C. indochinensis	156,574	86	8	36
OM055647.1	C. indochinensis	156,574	86	8	36
NC_069227	C. tamdaoensis	156,633	90	8	35
	C. tienii	162,167	98	8	48

Simple sequence repeats

Previous studies have highlighted the presence of repeated motifs in cp genomes, which have been associated with various genome rearrangements, recombination events, and large inversions. These motifs have proven valuable for phylogenetic studies. In our analysis of 14 cp genomes, a total of 718 simple sequence repeats (SSRs) were identified. The number of SSRs ranged from 48 in C. tamdaoensis to 55 in C. tienii, with an average of approximately 51 SSRs per cp genome (Figure 2). Three types of SSR motifs were identified: mononucleotide (A), dinucleotide (T), and trinucleotide (AT). The majority of the identified SSR motifs belonged to the mononucleotide type, with A/T repeat units accounting for 43.3% (311 SSRs) and 56.5% (406 SSRs) of the total, respectively. Interestingly, only one dinucleotide type AT motif was found in C. vietnamensis (MN078085.1). The abundance of A/T SSR motifs in Camellia cp genomes aligns with findings from several previous publications on Camellia cp genomes (Wu et al. 2020, Hao et al. 2023, Xu et al. 2023).

Figure 2
The different simple sequence repeat types in the cp genomes of 14 Camellia species.

A notable point is that the number and complexity of SSR in the four Camellia species analysed in this study in Vietnam are all lower than in other Camellia species. In a study by Li et al. (2019), six Camellia cp genomes were analysed, revealing up to four types of SSRs, including mononucleotide, dinucleotide, trinucleotide, and tetranucleotide, with 67 to 74 SSRs per cp genome. Similarly, in a recent study by Ran et al. (2024), a total of 13 Camellia species in the Tubeculata section were analysed, uncovering up to six types of SSRs, ranging from mononucleotide to hexanucleotide, with SSR numbers ranging from 69 to 75 per genome. The novel and specific microsatellites detected in our study in the cp genome of C. tienii hold promise for evolutionary investigations within this species. Additionally, they can aid in the identification and conservation efforts of different species within the Camellia genus.

IR contraction and expansion

While the Camellia cp genomes generally exhibit a high degree of conservation in terms of genomic structure and size, there are notable variations observed within each species, particularly in the boundary regions between the Inverted Repeat (IR) and Single Copy (SC) regions (Figure 3). However, it is worth mentioning that some variations were also detected within each species. For instance, the ycf1 gene was found to be present in only three out of seven cp genomes of C. vietnamensis. Similarly, this gene was observed in only one out of three cp genomes of C. indochinensis. Although previous publications have reported the presence of ndhF genes in all characterized genomes of different Camellia species (Wu et al. 2020, Hao et al. 2023, Ran et al. 2024), Figure 3 demonstrates the translocation of this gene, which has also been reported in other studies (Hao et al. 2023). Interestingly, we found that the ndhF gene is absent in C. tienii. Furthermore, the presence of trnL and ycf15 genes further contributes to the distinct features of C. tienii.

Figure 3
The LSC, IR, and SSC border regions were compared among 14 Camellia cp genomes. Genes located at the IR/SC borders are represented by boxes above or below the main lines, with the numbers above the gene indicating the distance in bp from the gene terminal to the boundary region.

Phylogenetic relationship

The analysis of phylogenetic relationships among the 18 Camellia cp genomes revealed a distinct clustering pattern with a high bootstrap value (Figure 4). In the phylogenetic tree, the three cp genomes used as outgroups formed a single clade, indicating the accuracy of the phylogenetic analysis. The cp genome sequence of C. tienii in this study is closely related to those of C. indochinensis, highlighting a close relationship between these two species. This is expected, as C. indochinensis is native to the Indo-China Peninsula, including Laos, Cambodia, and Vietnam. Although Ho et al. (2023) found genetic relatedness between C. tienii and C. tamdaoensis using rbcL or trnH-psbA DNA barcodes, our data aligns with the study by Le et al. (2023). When using up to three DNA barcodes (matK, rbcL, and psbA-trnH), Le et al. demonstrated that these two species were separated into distinct clades. The discrepancy in clustering may be attributed to the use of different combinations of DNA barcodes, suggesting the necessity of additional loci to increase discrimination power among closely related species (Letsiou et al. 2024). Furthermore, Ho et al. (2023) observed disagreements in Camellia phylogenetic analysis when comparing the use of a single DNA barcode versus a combination of DNA barcodes. Due to the variability in using DNA barcodes for specimen identification, recent studies emphasize the importance of using next-generation sequencing methods to characterize the whole genome as a super barcode. This approach will enhance our ability to distinguish different species (Coissac et al. 2016, Wu et al. 2021, Ahmed and Zaman 2022).

Figure 4
Phylogenetic tree showing the relatedness of Camellia tienii with other Camellia species using Maximum Likelihood method (Three cp genomes belonging to three genera in Theaceae family consisting of NC_035709.1 (A. fragrans), NC_035704.1 (P. diospyricarpa), NC_035706.1 (T. gymnanthera) were used as outgroups. Numbers near branches are bootstrap values).

In this research, we conducted a sequencing and characterization of the complete cp genome of C. tienii, an endemic Camellia species found in Vietnam. Through comparative analysis with closely related species, distinct features were identified, including variations in genome size, gene numbers, and sequence repeat motifs. The findings from this study offer valuable insights into the typical structure and composition of C. tienii cp genomes. These observed differences among cp genomes contribute to our understanding of the genetic makeup within the Camellia genus. Additionally, the discovery of unique repeat motifs and highly divergent regions in the cp genome of C. tienii presents the potential for the development of molecular markers. These markers could be utilized in future studies focusing on taxonomy and conservation efforts for this valuable herbaceous plant in Vietnam.

Data Availability

The datasets generated and/or analyzed during the current research are available from the corresponding author upon reasonable request.

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Publication Dates

• Publication in this collection
  16 Dec 2024
• Date of issue
  2024

History

• Received
  07 Mar 2024
• Accepted
  03 Sept 2024
• Published
  01 Nov 2024