Next Article in Journal
The Use of Multilayer Perceptron (MLP) to Reduce Delamination during Drilling into Melamine Faced Chipboard
Next Article in Special Issue
Effect of Different Presowing Treatments to Break Seed Dormancy and Seed Collection Methods on the Germination of Dracaena steudneri Schweinf. Ex Engl.
Previous Article in Journal
Soil Respiration in Planted and Naturally Regenerated Castanopis carelesii Forests during Three Years Post-Establishment
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 13
Issue 6
10.3390/f13060932
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Communication

Characterization of the Complete Chloroplast Genome Sequence of the Socotra Dragon`s Blood Tree (Dracaena cinnabari Balf.)

by
Konrad Celiński
1,*,
Joanna Sokołowska
1,
Hanna Fuchs
2,
Petr Maděra
3 and
Justyna Wiland-Szymańska
4,5
1
Department of Genetics, Institute of Experimental Biology, Faculty of Biology, School of Natural Sciences, Adam Mickiewicz University, Poznań, Uniwersytetu Poznańskiego 6, 61-614 Poznań, Poland
2
Institute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035 Kórnik, Poland
3
Department of Forest Botany, Dendrology and Geobiocoenology, Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemedelska 1, 61300 Brno, Czech Republic
4
Department of Systematic and Environmental Botany, Institute of Environmental Biology, Faculty of Biology, School of Natural Sciences, Adam Mickiewicz University, Poznań, Uniwersytetu Poznańskiego 6, 61-614 Poznań, Poland
5
Botanical Garden, Adam Mickiewicz University, Poznań, ul. Dąbrowskiego 165, 60-594 Poznań, Poland
*
Author to whom correspondence should be addressed.
Forests 2022, 13(6), 932; https://doi.org/10.3390/f13060932
Submission received: 22 April 2022 / Revised: 30 May 2022 / Accepted: 13 June 2022 / Published: 14 June 2022
(This article belongs to the Special Issue New Knowledge in Dragon Tree Research)
Browse Figures
Versions Notes

Abstract

:
The Socotra dragon`s blood tree (Dracaena cinnabari Balf.) is endemic to the island of Socotra in Yemen. This iconic species plays an essential role in the survival of associated organisms, acting as an umbrella tree. Overexploitation, overgrazing by livestock, global climate change, and insufficient regeneration mean that the populations of this valuable species are declining in the wild. Although there are many studies on the morphology, anatomy, and physiology of D. cinnabari, no genomic analysis of this endangered species has been performed so far. Therefore, the main aim of this study was to characterize the complete chloroplast sequence genome of D. cinnabari for conservation purposes. The D. cinnabari chloroplast genome is 155,371 bp with a total GC content of 37.5%. It has a quadripartite plastid genome structure composed of one large single-copy region of 83,870 bp, one small single-copy region of 18,471 bp, and two inverted repeat regions of 26,515 bp each. One hundred and thirty-two genes were annotated, 86 of which are protein-coding genes, 38 are transfer RNAs, and eight are ribosomal RNAs. Forty simple sequence repeats have also been identified in this chloroplast genome. Comparative analysis of complete sequences of D. cinnabari chloroplast genomes with other species of the genus Dracaena showed a very high conservativeness of their structure and organization. Phylogenetic inference showed that D. cinnabari is much closer to D. draco, D. cochinchinensis, and D. cambodiana than to D. terniflora, D. angustifolia, D. hokouensis, and D. elliptica. The results obtained in this study provide new and valuable omics data for further phylogenetic studies of the genus Dracaena as well as enable the protection of genetic resources of highly endangered D. cinnabari.

1. Introduction

Dragon trees [1] of the genus Dracaena Vand. ex L. (Asparagaceae, Nolinoideae) are an interesting group of arbors renowned for their red sap [2]. One of them, Dracaena cinnabari Balf., was already valued in ancient times as it is today. This species is endemic to the Socotra Island in Yemen, where its sap has been harvested for medical and cultural uses since ancient time [3,4]. Individuals of this iconic species play an important role as umbrella trees, vital to the survival of organisms associated with them [5,6]. Unfortunately, due to over-exploitation, overgrazing by livestock, global climate change, and insufficient regeneration, the number of trees of this valuable species is currently decreasing [7,8,9,10], despite attempts to regenerate it in situ and ex situ [11,12]. The decline in the population of D. cinnabari is clearly documented. Adolt and Pavliš [7] predicted the disappearance of the population of D. cinnabari on Socotra within 50–144 years. Maděra et al. [13] published an extinction model for D. cinnabari with different results; the extinction time of individual sub-populations varies from 31 to 564 years, but the model indicates a population decline of more than 40% in 100 years. Attorre et al. [8] concluded that the current potential habitat of D. cinnabari would be reduced by 45% in 2080. The International Union for Conservation of Nature ranked D. cinnabari as a vulnerable species [14].
Although representatives of the genus Dracaena are quite well described in terms of morphological or anatomical features [15,16], secondary growth in steam and roots [17,18], growth dynamic [10], or chemical diversity of resins [19], there is relatively little genetic and genomic studies [20,21]. According to Madera et al. [2], population genetic analyses are required for assessing contemporary and historical breeding systems and potential bottlenecks to enhance conservation management strategies. Surprisingly for such an iconic species as D. cinnabari, no genomic studies have been published to date. Therefore, it is difficult to develop any genetic conservation plans for this species without prior knowledge of its genetic and genomic diversity.
The sequences of chloroplast (cp) genomes obtained as a result of next-generation sequencing (NGS) are a valuable source of data for taxonomy, conservation genetics, and phylogenetics. Their high usefulness in these areas has been repeatedly confirmed, both in the case of representatives of the Asparagaceae family, i.e., Asparagus officinalis L. [22], Asparagus setaceus (Kunth) Jessop [23], Convallaria keiskei Miq. or Liriope spicata (Thunb.) Lour. [24] and in the genus Dracaena, i.e., D. cochinchinensis (Lour.) S.C. Chen, D. cambodiana Pierre ex Gagnep, D. angustifolia (Medik.) Roxb., D. terniflora Roxb., D. hokouensis G.Z. Ye and D. elliptica Thunb. [25] or recently, D. draco (L.) L. [26]. However, no similar study has been published to date on the detailed characterization of the chloroplast genome features for D. cinnabari. There is an urgent need to fill this gap and provide missing data.
Therefore, taking into account the lack of genomic studies and the high risk of extinction of D. cinnabari, the main objectives of this study are: (1) characterization of the complete genome sequence of D. cinnabari chloroplast; (2) comparison of its features with chloroplast genomes of other members of the genus Dracaena and (3) determination of the position of D. cinnabari within the genus based on the analysis of complete sequences of chloroplast genomes. Our results provide new and valuable omics data for further phylogenetic studies of the genus Dracaena and enable the protection of genetic resources of endangered D. cinnabari.

2. Materials and Methods

2.1. Plant Material and DNA Isolation

Dracaena cinnabari leaves were obtained from the Botanical Gardens and Arboretum of the Mendel University in Brno (Czech Republic) (49°21′ N, 16°61′ E) from a specimen cultivated there since 2001 (collection number BZA-7886). The CTAB method [27] was used to extract total DNA. Agarose gel electrophoresis and a NanoDrop spectrophotometer (Thermo Fisher Scientific, Carlsbad, CA, USA) were used to check the quality and purity of the extracted DNA.

2.2. Library Preparing and Sequencing

Ion Xpress Plus Fragment Library Kit (Thermo Fisher Scientific, Waltham, MA, USA) was used to prepare Ion Torrent libraries. Size selection of the obtained DNA fragments was performed using the E-Gel Precast Agarose Electrophoresis System (Thermo Fisher Scientific, Waltham, MA, USA). The resulting Ion Torrent libraries were then sequenced on the Ion Torrent GeneStudio™ S5 System.

2.3. Genome Assembly and Annotation

The filtering of low-quality reads, as well as trimming ends and adapters, were performed with BBDuk Adapter/Quality Trimming V. 35.82 implemented in Geneious Prime 2020.0.49.1.7 [28]. The filtered reads were de novo assembled into contigs using Geneious Assembler with default options.
Contigs were mapped to Dracaena cambodiana (NC_039776) using Geneious Mapper with a minimum mapping quality of 30. The obtained reads were used to assemble the complete chloroplast genome of D. cinnabari de novo, which was then annotated with CPGAVAS2 [29] and GeSeq [30]. The location of the large single-copy region (LSC) and the small single-copy region (SSC), as well as the calculation of GC content, was done in Geneious Prime 2020.0.49.1.7 [28]. Detection of transfer RNAs was performed with tRNAscan-RE v2.0.3. [31] implemented in GeSeq [30]. The circular gene map of the D. cinnabari cp genome was drawn in OGDRAW 1.3.1 [32]. The complete D. cinnabari chloroplast genome sequence has been deposited in GenBank under accession number OM961177.

2.4. Genome Comparative Analysis

Genome-wide evolutionary dynamics and events in Dracaena species were analyzed using the progressive MAUVE algorithm with default settings and MAUVE [33] plugin v1.1.1 available in Geneious Prime 2020.0.49.1.7 [28]. The chloroplast genome of Dracaena cinnabari as a reference sequence was used for comparisons with previously published Dracaena species, i.e., D. angustifolia [25], D. draco [26], and D. elliptica [25].

2.5. Identification of Simple Sequence Repeats and Phylogenetic Inference

MIcroSAtellite (MISA) [34], with parameters set at ≥10 for mononucleotides, ≥6 for dinucleotides, and ≥5 for tri-, tetra-, penta- and hexanucleotides, respectively, was used to identify simple sequence repeats (SSRs) in the D. cinnabari cp genome sequence. Detailed microsatellite characteristics were conducted using the following indices: Total counts, Total Repeat Length (bp), and Mean Length (bp). Total Repeat Length was calculated as SSR repeat motif × number of repeats (bp).

2.6. Phylogenetic Analysis

Phylogenetic inference was carried out by the maximum likelihood (ML) method using nine complete sequences of chloroplast genomes of various Asparagaceae members, i.e., Dracaena angustifolia [MN200193]; Dracaena cambodiana [MN200194]; Dracaena cochinchinensis [MN200195]; Dracaena cinnabari [OM961177]; Dracaena draco [MN990038]; Dracaena elliptica [MN200196]; Dracaena hokouensis [MN200197]; Dracaena terniflora [MN200198] and Asparagus officinalis [NC_034777] as the outgroup. Complete chloroplast genomes were aligned with MAFFT 7.450 using default settings [35]. A General Time Reversible + Proportion Invariation + Gamma nucleotide substitution model (GTR + I + G) was used as the substitution model for the ML analysis [26]. The ML analysis was performed in RaxML v8.2.11 [36], with 1000 rapid bootstrap replicates along with a search for the best-scoring ML tree in every run and parsimony random seed set to 10.

3. Results

The complete chloroplast genome of Dracaena cinnabari is 155,371 bp in length (Figure 1) and exhibits a typical quadripartite structure of large (LSC, 83,870 bp) and small (SSC, 18,471 bp) single-copy regions, which are separated by a pair of inverted regions (IRs, 26,515 bp each). The size of the D. cinnabari cp genome, as well as the length of its individual regions, LSC, SSC, and IR, are very similar to those found recently in other members of the genus Dracaena (Table 1).
The lengths of the LSC and SSC regions of D. angustifolia, D. cinnabari, D. draco, and D. elliptica are very similar at approximately 83 kbp and 18.4 kbp, respectively. There were also no major differences between the four Dracaena species in the IR regions. The total percentage of GC content in the D. cinnabari cp genome is equal to 37.5%.
There are 132 genes (113 unique) described in the D. cinnabari chloroplast genome. Of these, eighty-six genes encode proteins, thirty-eight transfer RNA genes, and eight ribosomal RNA genes (Table 1). Eighteen genes found in the D. cinnabari genome were duplicated, and one gene exists in three copies. Thirteen genes had one intron, while two genes possessed two introns. The list of genes annotated in the complete cp genome sequence of D. cinnabari is presented in Table 2.
Complete chloroplast genomes alignment of four selected species of Dracaena, i.e., D. angustifolia, D. cinnabari, D. draco, and D. elliptica, was done using Mauve software (Figure 2). The results obtained in the previous paragraph clearly showed that no major changes in the structural organization of the cp genomes in Dracaena could be expected. In fact, genome-wide alignment revealed the presence of only one locally collinear block (LCB) between all the complete chloroplast genomes analyzed. This indicates an extremely high level of similarity in the genome organization between the analyzed Dracaena species and the absence of any evolutionary events such as gene loss, duplication, rearrangements, and translocations.
The obtained results of the whole genomes comparison are also confirmed by the contraction and expansion analysis of the IR regions. In general, the IRb/LSC border is located between rps19 and rpl22 genes, and the IRa/LSC border is located between rps19 and psbA genes. The ycf1 gene spanned the JSA (SSC/IRa) region, and the ndhF gene spanned the JSB (IRb/SSC) region in the species studied. Moreover, in the JSB region, the ycf1 pseudogene is present only in D. angustifolia and D. elliptica, but not in D. cinnabari and D. draco. A comparison of the IR/SSC and IR/LSC boundaries for the four Dracaena cp genomes is shown in Figure 3.
A total of forty simple sequence repeats (SSRs) of at least 10 bp length were identified in the D. cinnabari cp genome. The number of SSRs detected in this study is slightly lower than those obtained from other Dracaena species, in which the number of SSRs ranged from 42 for D. angustifolia and 47 for D. elliptica to 60 for D. draco using the same methodology (Table 3). Most SSRs identified in this study (Table 3) had a mononucleotide motif (85.0%). The genome sequence of D. cinnabari chloroplast compared to three Dracaena species was characterized by the shortest total repeat length (363 bp) and lowest mean length (10.68 bp).
In order to investigate the phylogenetic position of D. cinnabari within the Dracaena genus, we constructed a phylogenetic tree using the maximum likelihood (ML) algorithm and the complete sequences of cp genomes of nine members of Asparagaceae. As shown in Figure 4, the resulting ML phylogenetic tree clearly indicates that all species of the Dracaena genus formed one distinct cluster. This cluster consists of two monophyletic groups. The first solely includes species of the dragon blood’s trees: Asian D. cochinchinensis and D. cambodiana, which create a sister clade, more distant D. draco from Morocco and Atlantic islands and the Socotran D. cinnabari. The second group includes four Asian species of Dracaena, which represent a different ecological group of mesophytic forest plants: D. hokouensis, D. elliptica, and a sister clade of D. terniflora and D. angustifolia. Asparagus officinalis was outside the two main distinguished Dracaena groups.

4. Discussion

The main aim of the study was to characterize the complete chloroplast genome sequence of D. cinnabari, compare it with the chloroplast genomes of other members of the genus Dracaena and determine the position of D. cinnabari within the genus based on the analysis of complete sequences of chloroplast genomes. Since D. cinnabari is a highly endangered species, it is necessary to undertake all actions that could reduce this undesirable phenomenon. The ideal solution for this purpose seems to be the use of conservation genetics methods and omics data.
Chloroplast genome sequences are commonly used in various areas of biology, i.e., phylogenetics [37,38], DNA barcoding [39,40], taxonomy, evolution, and population genetics [41] of both angiosperms and gymnosperms. In the last five years, many genomic studies of various representatives of the genus Dracaena [25,26] and the family Asparagaceae [22,23,42,43] have also been published, but so far, none have included D. cinnabari. Taking into account the lack of genomic study on this iconic species, we decided to provide new and valuable omics data which enable the protection of its genetic resources as well as for further phylogenetic studies of the genus Dracaena. Especially since Zhang et al. [25] and Takawira-Nyenya et al. [44] postulate that the analysis of chloroplast genome and next-generation sequencing should be the preferred method of analyzing the complex evolutionary history of dracenoids.
The length of the complete sequence of the chloroplast genome of D. cinnabari (155,371 bp) is very similar to recently published features of chloroplast genomes for other Asparagaceae members, i.e., Convallaria keiskei (162,109 bp) or Liriope spicata (157,055 bp) [24] and almost identical to other species of Dracaena, i.e., D. angustifolia (155,332 bp) or D. draco (155,422) [25,26]. The differences in the length of the Dracaena genomes are really small and do not exceed 400 bp [25]. We also found no major differences in the number of annotated genes in D. cinnabari and other Dracaena species. The complete chloroplast genome of D. cinnabari has a typical quadripartite structure, consisting of a pair of inverted repeats (IRs), separated by a large single-copy region (LSC) and a small single-copy region (SSC) that occurs in many other plant species [45,46,47], including those of the genus Dracaena [25,26] and the family Asparagaceae [23,24,42,43]. Our findings in this study regarding the organization of the D. cinnabari cp genome are very similar to those previously published for other members of the genus Dracaena [25,26]. On this basis, it can therefore be concluded that the chloroplast genomes in this genus are highly conserved. These observations are also confirmed by the results of whole-genome alignment as well as the analysis of contraction and expansion of the boundaries of the IR regions.
Microsatellites seem to be an ideal DNA marker for conducting population, ecological, and conservation genetics studies. The level of genetic polymorphism detected as well as the wide distribution throughout the genome, make them highly informative molecular markers [48,49]. In our study, we observed some differences between the analyzed Dracaena species in the number of microsatellite loci. Recently published data show a higher number of SSR loci in Dracaena species (64–71) [25] than those we found for D. cinnabari (40) in this study. The differences in numbers, however, result from different parameters of the microsatellite sequence identification and not from changes in the size of the cp genome, and when analyzed under the same conditions, the observed differences between individual species are smaller but still noticeable. The small number of microsatellites found in D. cinnabari may mean potential problems with the development of a sufficient number of highly polymorphic microsatellite markers to analyze the genetic diversity of this species population. Nevertheless, the SSRs identified in this study still have some analytical potential that requires testing on a larger number of individuals before being used to characterize D. cinnabari genetic resources. Moreover, taking into account the high conservation of the genomes of the genus Dracaena, confirmed both in this study and previously by Zhang et al. [25] and Celiński et al. [26], it seems possible to develop one universal set of primers amplifying microsatellite loci in several species. There are many studies showing the usefulness of such universal primers [50,51] as well as the cross-species amplification [52,53] approach. Understanding genetic resources is the first point in developing conservation plans. Hence, knowing the level of genetic variation is crucial. For some species of Asparagaceae, such development of SSR sets has already been done, incl. for Maianthemum bicolor [54]. To the best of the authors’ knowledge, there is no such study so far for species of the genus Dracaena.
In this study, we paid particular attention to determining the phylogenetic position of D. cinnabari within the Dracaena genus. Therefore, we constructed a phylogenetic tree using the maximum likelihood algorithm and the complete cp genome sequences of nine members of Asparagaceae. The phylogenetic inference revealed that all species of the Dracaena genus formed one separate cluster and that D. cinnabari is much closer to D. draco, D. cochinchinensis, and D. cambodiana than to D. terniflora, D. angustifolia, D. hokouensis, and D. elliptica. Such grouping of species is consistent with their morphological and physiological characteristics. The results obtained in this study confirm the previously published phylogeny of the Dracaena genus reported by Zhang et al. [25] and Celiński et al. [26]. However, the cited studies did not include D. cinnabari, and our current research fills this gap perfectly. Moreover, our findings strongly support the conclusions of Takawira-Nyenya et al. [44] about the monophyletic origins of Dracaena.

5. Conclusions

This study characterized for the first time the complete chloroplast genome sequence of the Dracaena cinnabari. The obtained results broaden our genomic knowledge about this iconic species and help protect its endangered genetic resources. Future work should focus on the development of a microsatellite marker set to characterize the level and distribution of genetic diversity present in the Socotra dragon`s blood tree populations. Since the phylogeny of the genus Dracaena is still not fully understood, further research in this area should be carried out. These should include both mesophytic and dragon species of Dracaena throughout its range, especially from Africa and the Arabian Peninsula.

Author Contributions

Conceptualization, K.C. and J.W.-S.; data curation, K.C., J.S. and H.F.; formal analysis, K.C., J.S. and H.F.; funding acquisition, J.W.-S.; investigation, K.C., J.S. and H.F.; methodology, K.C., J.S. and H.F.; resources, K.C., P.M. and J.W.-S.; supervision, J.W.-S.; visualization, K.C. and J.S.; writing—original draft preparation, K.C., J.S., H.F., P.M. and J.W.-S.; writing—review & editing, K.C. and J.W.-S. All authors have read and agreed to the published version of the manuscript.

Funding

This research and the APC were funded by the Faculty of Biology, School of Natural Sciences, and the Botanical Garden, Adam Mickiewicz University, Poznań, Poland.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data are available within the article.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study, in the collection, analyses, or interpretation of data, in the writing of the manuscript, or in the decision to publish the results.

References

  1. Marrero, A.; Almeida, R.; Gonzalez-Martin, M. A new species of the wild dragon tree, Dracaena (Dracaenaceae) from Gran Canaria and its taxonomic and biogeographic implications. J. Linn. Soc. Bot. 1998, 128, 291–314. [Google Scholar] [CrossRef]
  2. Maděra, P.; Forrest, A.; Hanáček, P.; Vahalík, P.; Gebauer, R.; Plichta, R.; Jupa, R.; Van Rensburg, J.J.; Morris, M.; Nadezhdina, N.; et al. What We Know and What We Do Not Know about Dragon Trees? Forests 2020, 11, 236. [Google Scholar] [CrossRef] [Green Version]
  3. Miller, A.G.; Morris, M. Ethnoflora of the Soqotra Archipelago, 1st ed.; Atkinson, R., Ed.; Royal Botanic Gardens: Edinburgh, UK, 2004; p. 759. [Google Scholar]
  4. Al-Okaishi, A. Exploring the Historical Distribution of Dracaena cinnabari Using Ethnobotanical Knowledge on Socotra Island, Yemen. J. Ethnobiol. Ethnomed. 2021, 17, 22. [Google Scholar] [CrossRef] [PubMed]
  5. Rejžek, M.; Svátek, M.; Šebesta, J.; Adolt, R.; Maděra, P.; Matula, R. Loss of a Single Tree Species Will Lead to an Overall Decline in Plant Diversity: Effect of Dracaena cinnabari Balf. f. on the Vegetation of Socotra Island. Biol. Conserv. 2016, 196, 165–172. [Google Scholar] [CrossRef]
  6. Vasconcelos, R.; Pujol-Buxó, E.; Llorente, G.A.; Saeed, A.; Carranza, S. Micro-Hotspots for Conservation: An Umbrella Tree Species for the Unique Socotran Reptile Fauna. Forests 2020, 11, 353. [Google Scholar] [CrossRef] [Green Version]
  7. Adolt, R.; Pavlis, J. Age Structure and Growth of Dracaena cinnabari Populations on Socotra. Trees Struct. Funct. 2004, 18, 43–53. [Google Scholar] [CrossRef]
  8. Attorre, F.; Francesconi, F.; Taleb, N.; Scholte, P.; Saed, A.; Alfo, M.; Bruno, F. Will Dragonblood Survive the next Period of Climate Change? Current and Future Potential Distribution of Dracaena cinnabari (Socotra, Yemen). Biol. Conserv. 2007, 138, 430–439. [Google Scholar] [CrossRef]
  9. Habrova, H.; Cermak, Z.; Pavlis, J. Dragon’s Blood Tree—Threatened by Overmaturity, Not by Extinction: Dynamics of a Dracaena cinnabari Woodland in the Mountains of Soqotra. Biol. Conserv. 2009, 142, 772–778. [Google Scholar] [CrossRef]
  10. Maděra, P.; Habrová, H.; Šenfeldr, M.; Kholová, I.; Lvončík, S.; Ehrenbergerová, L.; Roth, M.; Nadezhdina, N.; Němec, P.; Rosenthal, J.; et al. Growth Dynamics of Endemic Dracaena cinnabari Balf. f. of Socotra Island Suggest Essential Elements for a Conservation Strategy. Biologia 2019, 74, 339–349. [Google Scholar] [CrossRef]
  11. Hubálková, I.; Maděra, P.; Volařík, D. Growth Dynamics of Dracaena cinnabari under Controlled Conditions as the Most Effective Way to Protect Endangered Species. Saudi J. Biol. Sci. 2017, 24, 1445–1452. [Google Scholar] [CrossRef] [Green Version]
  12. Nadezhdina, N.; Al-Okaishi, A.; Madera, P. Sap Flow Measurements in a Socotra Dragon’s Blood Tree (Dracaena cinnabari) in Its Area of Origin. Trop. Plant Biol. 2018, 11, 107–118. [Google Scholar] [CrossRef]
  13. Maděra, P.; Volařík, D.; Patočka, Z.; Kalivodová, H.; Divín, J.; Rejžek, M.; Vybíral, J.; Lvončík, S.; Jeník, D.; Hanáček, P.; et al. Sustainable Land Use Management Needed to Conserve the Dragon’s Blood Tree of Socotra Island, a Vulnerable Endemic Umbrella Species. Sustainability 2019, 11, 3557. [Google Scholar] [CrossRef] [Green Version]
  14. Miller, A. Dracaena cinnabari, Dragon’s Blood Tree. IUCN Red List Threat. Species 2004, e.T30428A9548491. [Google Scholar] [CrossRef]
  15. Klimko, M.; Nowińska, R.; Wilkin, P.; Wiland-Szymańska, J. Comparative Leaf Micromorphology and Anatomy of the Dragon Tree Group of Dracaena (Asparagaceae) and Their Taxonomic Implications. Plant Syst. Evol. 2018, 304, 1041–1055. [Google Scholar] [CrossRef] [Green Version]
  16. Lautenschläger, T.; Frommherz, L.; Monizi, M.; Neinhuis, C.; Henle, T.; Förster, A. Anatomy and Nutritional Value of Dracaena Camerooniana Baker—An African Wild Vegetable. S. Afr. J. Bot. 2021, 145, 149–156. [Google Scholar] [CrossRef]
  17. Jura-Morawiec, J.; Wiland-Szymańska, J. A Novel Insight into the Structure of Amphivasal Secondary Bundles on the Example of Dracaena draco L. Stem. Trees Struct. Funct. 2014, 28, 871–877. [Google Scholar] [CrossRef]
  18. Jura-Morawiec, J. Formation of Amphivasal Vascular Bundles in Dracaena draco Stem in Relation to Rate of Cambial Activity. Trees Struct. Funct. 2015, 29, 1493–1499. [Google Scholar] [CrossRef] [Green Version]
  19. Lu, W.; Wang, X.; Chen, J.; Lu, Y.; Wu, N.; Kang, W.; Zheng, Q. Studies on the Chemical Constituents of Chloroform Extract of Dracaena Cochinchinensis. Acta Pharm. Sin. 1998, 33, 755–758. [Google Scholar]
  20. Lu, P.L.; Morden, C.W.; Manning, J. Phylogenetic Relationships among Dracaenoid Genera (Asparagaceae: Nolinoideae) Inferred from Chloroplast DNA Loci. Syst. Bot. 2014, 39, 90–104. [Google Scholar] [CrossRef]
  21. Edwards, C.E.; Bassüner, B.; Birkinshaw, C.; Camara, C.; Lehavana, A.; Lowry, P.P.; Miller, J.S.; Wyatt, A.; Jackson, P.W. A Botanical Mystery Solved by Phylogenetic Analysis of Botanical Garden Collections: The Rediscovery of the Presumed-Extinct Dracaena Umbraculifera. Oryx 2018, 52, 427–436. [Google Scholar] [CrossRef] [Green Version]
  22. Sheng, W.; Chai, X.; Rao, Y.; Tu, X.; Du, S. The Complete Chloroplast Genome Sequence of Asparagus (Asparagus officinalis L.) and Its Phylogenetic Positon within Asparagales. Int. J. Plant Biol. Res. 2017, 5, 1075. [Google Scholar]
  23. Li, J.R.; Li, S.F.; Wang, J.; Dong, R.; Zhu, H.W.; Li, N.; Deng, C.L.; Gao, W.J. Characterization of the Complete Chloroplast Genome of Asparagus Setaceus. Mitochondrial DNA Part B Resour. 2019, 4, 2639–2640. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Raman, G.; Park, S.; Lee, E.M.; Park, S.J. Evidence of Mitochondrial DNA in the Chloroplast Genome of Convallaria Keiskei and Its Subsequent Evolution in the Asparagales. Sci. Rep. 2019, 9, 5028. [Google Scholar] [CrossRef] [PubMed]
  25. Zhang, Z.; Zhang, Y.; Song, M.; Guan, Y.; Ma, X. Species Identification of Dracaena Using the Complete Chloroplast Genome as a Super-Barcode. Front. Pharmacol. 2019, 10, 1441. [Google Scholar] [CrossRef]
  26. Celiński, K.; Kijak, H.; Wiland-Szymańska, J. Complete Chloroplast Genome Sequence and Phylogenetic Inference of the Canary Islands Dragon Tree (Dracaena draco L.). Forests 2020, 11, 309. [Google Scholar] [CrossRef] [Green Version]
  27. Doyle, J.J.; Doyle, J.L. Isolation of Plants DNA from Fresh Tissue. Focus 1990, 12, 13–15. [Google Scholar]
  28. Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; Buxton, S.; Cooper, A.; Markowitz, S.; Duran, C.; et al. Geneious Basic: An Integrated and Extendable Desktop Software Platform for the Organization and Analysis of Sequence Data. Bioinformatics 2012, 28, 1647–1649. [Google Scholar] [CrossRef]
  29. Shi, L.; Chen, H.; Jiang, M.; Wang, L.; Wu, X.; Huang, L.; Liu, C. CPGAVAS2, an Integrated Plastome Sequence Annotator and Analyzer. Nucleic Acids Res. 2019, 47, W65–W73. [Google Scholar] [CrossRef]
  30. Tillich, M.; Lehwark, P.; Pellizzer, T.; Ulbricht-Jones, E.S.; Fischer, A.; Bock, R.; Greiner, S. GeSeq—Versatile and Accurate Annotation of Organelle Genomes. Nucleic Acids Res. 2017, 45, W6–W11. [Google Scholar] [CrossRef]
  31. Chan, P.P.; Lin, B.Y.; Mak, A.J.; Lowe, T.M. TRNAscan-SE 2.0: Improved Detection and Functional Classification of Transfer RNA Genes. Nucleic Acids Res. 2021, 49, 9077–9096. [Google Scholar] [CrossRef]
  32. Greiner, S.; Lehwark, P.; Bock, R. OrganellarGenomeDRAW (OGDRAW) Version 1.3.1: Expanded Toolkit for the Graphical Visualization of Organellar Genomes. Nucleic Acids Res. 2019, 47, W59–W64. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Darling, A.C.E.; Mau, B.; Blattner, F.R.; Perna, N.T. Mauve: Multiple Alignment of Conserved Genomic Sequence with Rearrangements. Genome Res. 2004, 14, 1394–1403. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Beier, S.; Thiel, T.; Münch, T.; Scholz, U.; Mascher, M. MISA-Web: A Web Server for Microsatellite Prediction. Bioinformatics 2017, 33, 2583–2585. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Katoh, K.; Standley, D.M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef] [Green Version]
  36. Stamatakis, A. RAxML Version 8: A Tool for Phylogenetic Analysis and Post-Analysis of Large Phylogenies. Bioinformatics 2014, 30, 1312–1313. [Google Scholar] [CrossRef]
  37. Wang, Y.; Wang, S.; Liu, Y.; Yuan, Q.; Sun, J.; Guo, L. Chloroplast genome variation and phylogenetic relationships of Atractylodes species. BMC Genomics 2021, 22, 103. [Google Scholar] [CrossRef]
  38. Xu, J.; Shen, X.; Liao, B.; Xu, J.; Hou, D. Comparing and phylogenetic analysis chloroplast genome of three Achyranthes species. Sci Rep. 2020, 10, 10818. [Google Scholar] [CrossRef]
  39. Chen, Q.; Hu, H.; Zhang, D. DNA Barcoding and Phylogenomic Analysis of the Genus Fritillaria in China Based on Complete Chloroplast Genomes. Front. Plant Sci. 2022, 13, 764255. [Google Scholar] [CrossRef]
  40. Hong, Z.; He, W.; Liu, X.; Tembrock, L.R.; Wu, Z.; Xu, D.; Liao, X. Comparative Analyses of 35 Complete Chloroplast Genomes from the Genus Dalbergia (Fabaceae) and the Identification of DNA Barcodes for Tracking Illegal Logging and Counterfeit Rosewood. Forests 2022, 13, 626. [Google Scholar] [CrossRef]
  41. Sokołowska, J.; Fuchs, H.; Celiński, K. New Insight into Taxonomy of European Mountain Pines, Pinus Mugo Complex, Based on Complete Chloroplast Genomes Sequencing. Plants 2021, 10, 1331. [Google Scholar] [CrossRef]
  42. Gu, L.; Su, T.; Luo, G.L.; Hu, G.X. The complete chloroplast genome sequence of Heteropolygonatum ginfushanicum (Asparagaceae) and phylogenetic analysis. Mitochondrial DNA Part B 2021, 6, 1799–1802. [Google Scholar] [CrossRef] [PubMed]
  43. Yang, J.; Choi, M.-J.; Kim, S.-H.; Choi, H.-J.; Kim, S.-C. Plastome Characterization and Phylogenomic Analysis Yield New Insights into the Evolutionary Relationships among the Species of the Subgenus Bryocles (Hosta; Asparagaceae) in East Asia. Plants 2021, 10, 1980. [Google Scholar] [CrossRef] [PubMed]
  44. Takawira-Nyenya, R.; Mucina, L.; Cardinal-Mcteague, W.M.; Thiele, K.R. Sansevieria (Asparagaceae, Nolinoideae) is a herbaceous Glade within Dracaena: Inference from non-coding plastid and nuclear DNA sequence data. Phytotaxa 2018, 376, 254–276. [Google Scholar] [CrossRef]
  45. Ge, J.; Cai, L.; Bi, G.Q.; Chen, G.; Sun, W. Characterization of the Complete Chloroplast Genomes of Buddleja colvilei and B. sessilifolia: Implications for the Taxonomy of Buddleja L. Molecules 2018, 23, 1248. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Sun, Y.; Zou, P.; Jiang, N.; Fang, Y.; Liu, G. Comparative Analysis of the Complete Chloroplast Genomes of Nine Paphiopedilum Species. Front. Genet. 2022, 12, 772415. [Google Scholar] [CrossRef] [PubMed]
  47. Krawczyk, K.; Wiland-Szymańska, J.; Buczkowska-Chmielewska, K.; Drapikowska, M.; Maślak, M.; Myszczyński, K.; Szczecińska, M.; Ślipiko, M.; Sawicki, J. The Complete Chloroplast Genome of a Rare Orchid Species Liparis loeselii (L.). Conserv. Genet. Resour. 2018, 10, 305–308. [Google Scholar] [CrossRef] [Green Version]
  48. Ellegren, H. Microsatellites: Simple Sequences with Complex Evolution. Nat. Rev. Genet. 2004, 5, 435–554. [Google Scholar] [CrossRef]
  49. Oliveira, E.J.; Pádua, J.G.; Zucchi, M.I.; Vencovsky, R.; Vieira, M.L.C. Origin, Evolution and Genome Distribution of Microsatellites. Genet. Mol. Biol. 2006, 29, 249–307. [Google Scholar] [CrossRef]
  50. Scarcelli, N.; Barnaud, A.; Eiserhardt, W.; Treier, U.A.; Seveno, M.; d’Anfray, A.; Pintaud, J.C. A set of 100 chloroplast DNA primer pairs to study population genetics and phylogeny in monocotyledons. PLoS ONE 2011, 6, e19954. [Google Scholar] [CrossRef] [Green Version]
  51. Vendramin, G.G.; Lelli, L.; Rossi, P.; Morgante, M. A set of primers for the amplification of 20 chloroplast microsatellites in Pinaceae. Mol. Ecol. 1996, 5, 595–598. [Google Scholar] [CrossRef] [PubMed]
  52. González-Martinez, S.C.; Robledo-Arnuncio, J.J.; Collada, C.; Díaz, A.; Williams, C.G.; Alía, R.; Cervera, M.T. Cross-amplification and sequence variation of microsatellite loci in Eurasian hard pines. Theor Appl Genet. 2004, 109, 103–111. [Google Scholar] [CrossRef] [PubMed]
  53. Celiński, K.; Pawlaczyk, E.M.; Wojnicka-Półtorak, A.; Chudzińska, E.; Prus-Głowacki, W. Cross-species amplification and characterization of microsatellite loci in Pinus mugo Turra. Biologia 2013, 68, 621–626. [Google Scholar] [CrossRef] [Green Version]
  54. Park, H.; Kim, C.; Lee, Y.M.; Kim, J.H. Development of chloroplast microsatellite markers for the endangered Maianthemum bicolor (Asparagaceae s.l.). Appl. Plant Sci. 2016, 4, 1600032. [Google Scholar] [CrossRef] [PubMed]
Forests 13 00932 g001 550
Figure 1. Gene map of the Dracaena cinnabari chloroplast genome. The genes inside the circle are transcribed clockwise, while those on the outside are transcribed counterclockwise. Genes belonging to different functional groups are color-coded. The darker gray in the inner circle shows the GC content, while the lighter gray corresponds to the AT content. IRA, IRB, inverted repeats; LSC, large single-copy region; SSC, small single-copy region.
Figure 1. Gene map of the Dracaena cinnabari chloroplast genome. The genes inside the circle are transcribed clockwise, while those on the outside are transcribed counterclockwise. Genes belonging to different functional groups are color-coded. The darker gray in the inner circle shows the GC content, while the lighter gray corresponds to the AT content. IRA, IRB, inverted repeats; LSC, large single-copy region; SSC, small single-copy region.
Forests 13 00932 g001
Forests 13 00932 g002 550
Figure 2. Comparison of four Dracaena chloroplast genomes using a progressive MAUVE algorithm.
Figure 2. Comparison of four Dracaena chloroplast genomes using a progressive MAUVE algorithm.
Forests 13 00932 g002
Forests 13 00932 g003 550
Figure 3. Comparison of the borders of LSC, SSC, and IR regions among the four Dracaena chloroplast genomes.
Figure 3. Comparison of the borders of LSC, SSC, and IR regions among the four Dracaena chloroplast genomes.
Forests 13 00932 g003
Forests 13 00932 g004 550
Figure 4. The ML phylogenetic tree of the Dracaena genus based on nine complete chloroplast genomes. The numbers near each node are bootstrap support values obtained by ML.
Figure 4. The ML phylogenetic tree of the Dracaena genus based on nine complete chloroplast genomes. The numbers near each node are bootstrap support values obtained by ML.
Forests 13 00932 g004
Table
Table 1. Comparison of basic features of chloroplast genomes among four Dracaena species.
Table 1. Comparison of basic features of chloroplast genomes among four Dracaena species.
SpeciesD. angustifoliaD. cinnabariD. dracoD. elliptica
Total length (bp)155,332155,371155,422155,055
IR length (bp)53,06053,03053,00452,978
LSC length (bp)83,80783,87083,94683,621
SSC length (bp)18,46518,47118,47218,456
Total gene number130132132130
rRNA8888
tRNA38383838
GC content (%)37.537.537.637.5
GenBan accessionMN200193OM961177MN990038MN200196
Reference[25]This study[26][25]
Table
Table 2. List of genes present in the D. cinnabari chloroplast genome.
Table 2. List of genes present in the D. cinnabari chloroplast genome.
No.Group of GenesName of GenesNumber
1Photosystem IpsaA, psaB, psaC, psaI, psaJ5
2Photosystem IIpsbA, psbB, psbC, psbD, psbE, psbF, psbH, psbI, psbJ, psbK, psbL, psbM, psbNpsbT, psbZ15
3Cytochrome
b/f complex		petA, petB *, petD *, petG, petL, petN,6
4ATP synthaseatpA, atpB, atpE, atpF *, atpH, atpI,6
5NADH dehydrogenasendhA *, ndhB *(×2), ndhC, ndhD, ndhE, ndhF, ndhG, ndhH, ndhI, ndhJ, ndhK12
6RubisCO
large subunit		rbcL1
7RNA polymeraserpoA, rpoB, rpoC1 *, rpoC24
8Ribosomal proteins
–small units (SSU)		rps2, rps3, rps4, rps7(×2), rps8, rps11, rps12 *(×2), rps14, rps15, rps16 *,
rps18, rps19(×2),		15
9Ribosomal proteins
–large units (LSU)		rpl2 *(×2), rpl14, rpl16 *, rpl20, rpl22, rpl23(×2), rpl32, rpl33, rpl36,11
10Other genes/
Miscellaneous		accD, ccsA, cemA, clpP **, infA, matK,6
11Protein
of unknown function		ycf1, ycf2(×2), ycf3 **, ycf45
12Transfer RNAstrnA-UGC(x2), trnC-GCA, trnD-GUC, trnE-UUC, trnF-GAA, trnfM-CAU, trnG-GCC, trnH-GUG(×2),
trnI-CAU(×2), trnI-GAU *(×2), trnK-UUU *, trnL-CAA(×2), trnL-UAA *, trnL-UAG, trnM-CAU, trnN-GUU(×2),
trnP-UGG, trnQ-UUG, trnR-ACG(×2), trnR-UCU, trnS-GCU, trnS-GGA, trnS-UGA, trnT-GGU, trnT-UGU, trnV-GAC(×3), trnV-UAC *, trnW-CCA, trnY-GUA		38
13Ribosomal RNAsrrn4.5(×2), rrn5(×2), rrn16(×2), rrn23(×2)8
Total 132
* Gene contains one intron. ** Gene contains two introns. (×2) indicates that the number of repeat units is 2.
Table
Table 3. Characteristics of SSRs present in the four Dracaena chloroplast genomes.
Table 3. Characteristics of SSRs present in the four Dracaena chloroplast genomes.
SpeciesIndicesMotifTotal
MononucleotideDinucleotide
Total counts38442
D. angustifoliaTotal Repeat Length (bp)40954
Mean Length (bp)10.7613.5
Total counts34640
D. cinnabariTotal Repeat Length (bp)36378
Mean Length (bp)10.6813
Total counts56460
D. dracoTotal Repeat Length (bp)63850
Mean Length (bp)11.3912.5
Total counts44347
D.ellipticaTotal Repeat Length (bp)47336
Mean Length (bp)10.7512
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Celiński, K.; Sokołowska, J.; Fuchs, H.; Maděra, P.; Wiland-Szymańska, J. Characterization of the Complete Chloroplast Genome Sequence of the Socotra Dragon`s Blood Tree (Dracaena cinnabari Balf.). Forests 2022, 13, 932. https://doi.org/10.3390/f13060932

AMA Style

Celiński K, Sokołowska J, Fuchs H, Maděra P, Wiland-Szymańska J. Characterization of the Complete Chloroplast Genome Sequence of the Socotra Dragon`s Blood Tree (Dracaena cinnabari Balf.). Forests. 2022; 13(6):932. https://doi.org/10.3390/f13060932

Chicago/Turabian Style

Celiński, Konrad, Joanna Sokołowska, Hanna Fuchs, Petr Maděra, and Justyna Wiland-Szymańska. 2022. "Characterization of the Complete Chloroplast Genome Sequence of the Socotra Dragon`s Blood Tree (Dracaena cinnabari Balf.)" Forests 13, no. 6: 932. https://doi.org/10.3390/f13060932

APA Style

Celiński, K., Sokołowska, J., Fuchs, H., Maděra, P., & Wiland-Szymańska, J. (2022). Characterization of the Complete Chloroplast Genome Sequence of the Socotra Dragon`s Blood Tree (Dracaena cinnabari Balf.). Forests, 13(6), 932. https://doi.org/10.3390/f13060932

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop