Next Article in Journal
Non-Specific Epileptic Activity, EEG, and Brain Imaging in Loss of Function Variants in SATB1: A New Case Report and Review of the Literature
Previous Article in Journal
Statistical Genetic Approaches to Investigate Genotype-by-Environment Interaction: Review and Novel Extension of Models
Previous Article in Special Issue
Intraspecific and Intrageneric Genomic Variation across Three Sedum Species (Crassulaceae): A Plastomic Perspective
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Genes
Volume 15
Issue 5
10.3390/genes15050546
genes-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:
Article

Complete Chloroplast Genome of Krascheninnikovia ewersmanniana: Comparative and Phylogenetic Analysis

by
Peng Wei
1,*,
Youzheng Li
2,
Mei Ke
1,
Yurong Hou
1,
Abudureyimu Aikebaier
1 and
Zinian Wu
3,*
1
Grassland Research Institute, Xinjiang Academy of Animal Sciences, Urumqi 830000, China
2
College of Grassland Science, Xinjiang Agricultural University, Urumqi 830052, China
3
Institute of Grassland Research, Chinese Academy of Agricultural Sciences, Hohhot 010011, China
*
Authors to whom correspondence should be addressed.
Genes 2024, 15(5), 546; https://doi.org/10.3390/genes15050546
Submission received: 21 March 2024 / Revised: 22 April 2024 / Accepted: 24 April 2024 / Published: 25 April 2024
(This article belongs to the Special Issue Advances in Evolution of Plant Organelle Genome (Volume II))
Browse Figures
Versions Notes

Abstract

:
Krascheninnikovia ewersmanniana is a dominant desert shrub in Xinjiang, China, with high economic and ecological value. However, molecular systematics research on K. ewersmanniana is lacking. To resolve the genetic composition of K. ewersmanniana within Amaranthaceae and its systematic relationship with related genera, we used a second-generation Illumina sequencing system to detect the chloroplast genome of K. ewersmanniana and analyze its assembly, annotation, and phylogenetics. Total length of the chloroplast genome of K. ewersmanniana reached 152,287 bp, with 84 protein-coding genes, 36 tRNAs, and eight rRNAs. Codon usage analysis showed the majority of codons ending with base A/U. Mononucleotide repeats were the most common (85.42%) of the four identified simple sequence repeats. A comparison with chloroplast genomes of six other Amaranthaceae species indicated contraction and expansion of the inverted repeat boundary region in K. ewersmanniana, with some genes (rps19, ndhF, ycf1) differing in length and distribution. Among the seven species, the variation in non-coding regions was greater. Phylogenetic analysis revealed Krascheninnikovia ceratoides, Dysphania ambrosioides, Dysphania pumilio, and Dysphania botrys to have a close monophyletic relationship. By sequencing the K. ewersmanniana chloroplast genome, this research resolves the relatedness among 35 Amaranthaceae species, providing molecular insights for germplasm utilization, and theoretical support for studying evolutionary relationships.

1. Introduction

K. ewersmanniana is a perennial, strongly drought-tolerant shrub belonging to the genus Krascheninnikovia in the family Amaranthaceae [1]. In addition, the shrub has tolerance to salt and alkali, cold resistance, and other beneficial characteristics [2,3,4]. This species is widely distributed in China, Kazakhstan, Russia, and Mongolia; in China, K. ewersmanniana grows exclusively in the arid desert grasslands of the Xinjiang Altay and Tianshan Mountains [5,6,7]. K. ewersmanniana is highly effective as a windbreak and aids in sand fixation and water and soil conservation. It is thereby considered the main species in the arid desert area of Xinjiang and plays an indispensable role in restoration and improvement of grassland vegetation [8]. As well as its significance for ecological construction, K. ewersmanniana is a good forage shrub for livestock, with high crude protein content and nutritional value [9]. Since K. ewersmanniana plants grow tall, they can be used as a life-saving grass in winter and spring in Xinjiang and play an important role in disaster relief [9]. Therefore, K. ewersmanniana has high economic and ecological value and is a valuable germplasm resource. Extensive research on the development and utilization of K. ewersmanniana has elucidated its morphology, anatomy, physiological and biochemical characteristics, ecology, and cultivation management technology [10,11,12,13,14]. However, few studies have genetically analyzed K. ewersmanniana, particularly to uncover its origin, evolution, and genomics.
Chloroplasts are important organelles for plants that convert light energy into chemical energy [15,16] and have independent genome structures and genetic functions [17,18]. Since chloroplast genomes of angiosperms are mostly maternally inherited, their gene sequences are highly conserved and stable, with unique advantages for determining genus or interspecies relationships and phylogeny; as such, chloroplast genomes play a prominent role in phylogeny, plant taxonomy, and species identification [19]. The double-stranded circular configuration is the most typical structure of chloroplast genes, and is highly conserved. The common plant chloroplast genome is generally 120–160 kb, comprising four different DNA fragments: a large single copy (LSC) region, a small single copy (SSC) region, and two separate inverted repeat (IR) regions (IR a/b, IR a/b) [20,21,22,23]. With advances in science and technology, especially the continuous improvement of sequencing technology, the phylogenetic relationships of various groups can be reconstructed through chloroplast genomics, and the taxonomic status and relationships among different plant taxa can be examined to promote better understanding and utilization of plants. Therefore, the use of chloroplasts to study the origin, structure, and evolution of organelles has received increasing attention, resulting in the sequencing and analysis of a rising number of plant chloroplast genomes.
Previous research on Krascheninnikovia plants has primarily focused on their ecological and physiological characteristics, with only a few performing chloroplast genome and phylogenetic analyses. Random amplified polymorphic DNA (RAPD) was used to disclose the genetic diversity of seven Krascheninnikovia plant samples and the results revealed that the ecotypes of Ningxia, Xinjiang, desert, and Horqin (Inner Mongolia) were grouped together at the molecular level, and were identified as a northern China species (K. arborescens), and has close genetic relationship with K. latens, K. ewersmanniana, and K. lanata are differentiated into two independent species [24]. Liu et al. [25] assembled and annotated the chloroplast genome of K. ceratoides, and reported that K. ceratoides to be closely related to Atriplex, Chenopodium, Dysphania, and Suaeda, which is consistent with studies based on nuclear ribosomal internal transcribed spacer and chloroplast (cp) DNA data. However, the did not conduct analysis to distinguish between species or families. Amaranthaceae, which was a global family, was a transitional group from entomophilous plants to anemophilous. The variability in flowers resulted in mass identification of species or genus and taxonomy. Especially, the Amaranthaceae family has recently been extended to include the Chenopodiaceae family based on morphological and phylogenetic analyses [26]. Moreover, according to the flora of Inner Mongolia, the genus Ceratoides (Tourn) Gagnebin was proved invalid and the name was then changed to Krascheninnikovia [27].
To better synthetically comprehend the Krascheninnikovia genus’s origin, evolution, and polygenetic relationships, we aimed to analyze the genetic composition of K. ewersmanniana. Second-generation high-throughput sequencing technology and bioinformatic analysis methods were used to sequence, assemble, and annotate the whole genome of K. ewersmanniana and resolve sequence variations and structural features. Based on the chloroplast genome information of six Amaranthaceae species and K. ewersmanniana published in the NCBI database, we have analyzed and summarized the chloroplast genome structures of related groups, followed by selection of chloroplast genomes of 35 related species to establish a phylogenetic tree with common protein-coding gene (PCG) sequences. The purpose of this study is to investigate the phylogeny of Amaranthaceae plants using the chloroplast genome of K. ewersmanniana, and to lay a theoretical foundation for the phylolocation, plant classification, and resource utilization of Amaranthaceae.

2. Materials and Methods

2.1. Experimental Materials

K. ewersmanniana germplasm material was collected from Hutubi County, Xinjiang, China (Xinjiang Ministry of Agriculture of China, E 86°37′, N 44°14′, altitude 504 m). A certified specimen was collected along with the leaves (collector: Youzheng Li). The specimen was identified as K. ewersmanniana, a Krascheninnikovia plant of family Amaranthaceae, by Mei Ke, a researcher at the Grassland Research Institute of the Xinjiang Academy of Animal Sciences. Specimens were stored in the plant specimen library of the Grassland Research Institute, Xinjiang Academy of Animal Sciences. Seedlings were raised in the Xinjiang Academy of Animal Sciences AI climate chamber. Fresh and young leaves from healthy plants were collected for sequencing.

2.2. Genomic DNA Extraction and Sequencing

Genomic DNA was extracted from fresh leaves of plants using cetyltrimethyl ammonium bromide, and the DNA concentration was measured using a NanoDrop Spectrophotometer (Thermo Scientific, Waltham, MA, USA) and a Qubit Fluorometer (Invitrogen, Carlsbad, CA, USA). The Illumina Miseq platform was used to sequence the chloroplast genome of the sample (Personalbio, Shanghai, China).
The data quality control was performed by fastp (v0.19.4) and high-quality sequences were produced. Junction contamination at the 3′ end was removed by Adapter Removal (version 2) [28], and the sliding window method was used to filter the quality. The average Q value of the bases in the window was calculated. If the Q value was <20, the bases in the window were deleted, and if Q was ≥20, sliding was stopped. If the length of any reads in the double-end is ≤50 bp and the number of bases in the double-end is ≥5, the double-end sequence is removed to ensure that the sequences contained in the dataset have sufficient length and quality.

2.3. Chloroplast Genome Assembly and Annotation

The plant chloroplast genome was assembled using default parameters of GetOrganelles (version 1.7.5.3) [29]. Chloroplast genome annotation was performed using the Plastid Genome Annotator [30]. Error codons were corrected using Geneious (version 9.0.2) [31]. Chloroplast genome data were submitted to GenBank (accession number: PP191169). Finally, a chloroplast genome map was drawn using Organellar Genome Draw software (OGDRAW, version 1.3.1) [32].

2.4. Analysis of Chloroplast Genome Repeats and Codon Usage Preferences

Misa software (version 2.1) was used to predict simple sequence repeats (SSRs) of K. ewersmanniana chloroplast genomes, with the minimum number of repetitions for single nucleotide, double nucleotide, trinucleotide, tetranucleotide, pentanucleotide, and hexanucleotide sets as 10, 6, 4, 3, 3, and 3, respectively [33]. The online tool REPuter [34] was used to analyze dispersed repeat, with the Hamming distance and minimum repeat fragment size parameters set to 3 and 30, respectively. The relative synonymous codon usage (RSCU) value was calculated using CodonW software v.1.4.2 [35]. RSCU is the ratio of the actual codon frequency to expected frequency. A RSCU value of 1 depicts codon usage without bias, while RSCU value < 1 indicates its relative rarity and >1 indicates that codon usage is greater than expected [36].

2.5. Comparison of Chloroplast Genomes

The IRscope online tool was used to analyze the infrared boundary information of the chloroplast genomes of seven Amaranthaceae plants [37]. mVISTA software [38] was used to perform collinearity analysis of the chloroplast genomes of different species, with Chenopodium quinoa as a reference.

2.6. Phylogenetic Analysis

A phylogenetic tree of 35 species in the Amaranthaceae family was established, in which the annotated K. ewersmanniana chloroplast genome was assembled, and the genome sequences of 34 other Amaranthaceae species were downloaded from NCBI (Table S1), with Oryza sativa and Arabidopsis thaliana as outgroups. Nucleotide sequences corresponding to PCG in the selected genome were connected, and multiple sequence alignments were performed using the MAFFT program [39]. A phylogenetic tree was constructed using the maximum likelihood (ML) algorithm and Bayesian analysis, and the best model was selected using ModelFinder [40]. The ML method uses the software RAxML and selects the nucleotide substitution model as GTR + F + I + G4 [41]. The best-fit GTR + F + I + G4 model was selected using Bayesian imputation in MrBayes v3.2.6 [42].

3. Results

3.1. Genomic Features of K. ewersmanniana

Second-generation Illumina sequencing on the K. ewersmanniana chloroplast genome generated 36,875,778 raw reads, of which 712,889 were used for subsequent genome assembly. In this study, we assembled and annotated the complete chloroplast genome of K. ewersmanniana for the first time. The chloroplasts of K. ewersmanniana comprised four parts (SSC, IRa, LSC, and IRb) and exhibited a unique double-stranded circular structure with a genome size of 152,287 bp (Figure 1). The lengths of the IR, SSC, and LSC sequences were 49,182, 19,007, and 84,098 bp, respectively. The GC levels of the IR, SSC, and LSC regions were 41.99%, 30.58%, and 34.74%, respectively (Table S2).
The annotation results revealed that the K. ewersmanniana chloroplast genome can be divided into four categories based on function: self-replication, photosynthesis, other genes, and unknown genes. A total of 128 genes were annotated (84 PCGs, 36 tRNAs, and eight rRNAs). The most abundant were tRNA genes, followed by subunits of the ribosome, with a total of 21 genes, including nine large subunit genes and 15 small subunit genes. Among the tRNA genes, trnV-GAC, trnA-UGC, trnL-CAA, trnI-CAU, trnR-ACG, trnN-GUU, and trnI-GAU had two copies each; among the ribosomal protein large and small subunit genes, rpl2, rps7, and rps12 had two copies each; among the four rRNA genes, rrn5S, rrn23S, rrn16S, and rrn4.5S had two copies each; and the NADH-dehydrogenase gene, ndhB, had two copies (Table 1).
Among the 128 annotated genes, a total of 19 genes contained exons and introns. Among these, only two genes (ycf3 and clpP) had three exons and two introns. The remaining 17 genes, namely ndhB(2), trnI-GAU(2), petD, ndhA, atpF, petB, trnV-UAC, rpl16, trnA-UGC, rpoC1, trnR-UCU, rps12, trnL-UAA, trnK-UU, and rps16 had two exons and one intron. The two introns of clpP were 811 bp and 603 bp long, whereas those of ycf3 were 779 bp and 805 bp long. Among all genes containing introns, trnK-UUU has the longest length of 2493 bp and rps12 has the shortest length of 543 bp. Among all genes containing exons, ndhB had the largest number of exons (1533 bp); 777 bp for exon I and 756 bp for exon II. The three genes with the smallest number of exons were trnA-UGC, trnA-UGC, and trnK-UUU, all with 72 exons. Among them, the length of exon I of the three genes was 37 bp, whereas that of exon II was 35 bp (Table 2).

3.2. Analysis of the Codon Usage Profiles

According to codon analysis, we detected 22,696 codons in K. ewersmanniana, encoding 20 amino acids (Figure 2, Table 3). Of these, 2395 codons encoded leucine (Leu), accounting for 10.55% of the total codons, exhibiting the highest coding rate. However, only 253 codons encoded cysteines, accounting for the smallest proportion (1.11%). According to the RSCU analysis, 30 codons had RSCU > 1, implying overrepresentation of these codons, whereas 32 codons had RSCU < 1, implying that these codons were used less frequently. In Leu, the UUA had the largest RSCU value, at 2.07, and the GUG encoding Leu had the lowest at 0.32. Moreover, 29 codons had bases ending in A/U, whereas the one remaining codon ended in G. The proportion of codons ending in A/U was 96.67%. Consequently, K. ewersmanniana favors codons ending in A/U.

3.3. Repeat Analysis

Repeat sequence analysis performed on the genomes of two plants of Krascheninnikovia (K. ewersmanniana and K. ceratoides) detected two different types of scattered repetitive sequences: palindromic (P) and forward (F) (Figure 3A). The number of scattered repetitive sequences, arranged according to length, differed significantly between the two Krascheninnikovia species (Figure 3B). A total of 48 SSRs sequences were identified in the chloroplast genome of K. ewersmanniana, encompassing seven sequence types. Among them, mononucleotide repeats were the dominant sequence (all A/T), with 41 sequences, accounting for 85.42%. Similar SSRs were found in chloroplast genomes of two Krascheninnikovia plants. The total number of SSRs in the K. ceratoides chloroplast genome was 45, encompassing eight sequence types. Among them, 37 were single nucleotide repeats (A/T). ACTAT/AGTAT was the only different repeat sequence type identified in K. ceratoides (Figure 4A; Table S3). Most of the SSRs in both species were distributed in the intergenic spacer region (26 in K. ewersmanniana and 22 in K. ceratoides), accounting for more than 50% of all SSRs (Figure 4B). The number of SSRs distributed in the intergenic spacer, PCG, and intron regions was 22, 10, and 10, respectively (Figure 4B). There are 48 SSRs located in the intergenic spacer, and 19 SSRs had introns (Table S4).

3.4. Comparison of the Chloroplast Genomes of Seven Amaranthaceae Plants

We compared the IR boundary regions and locations of the adjacent genes of K. ewersmanniana and six other species of Amaranthaceae (Figure 5). The chloroplast genome structure of K. ewersmanniana was highly conserved; however, structural changes were observed in the IR boundary regions. The rps19 gene exhibited variable expansion at the LSC/IRb regional junction in seven species, including K. ewersmanniana, K. ceratoides, Atriplex canescens, and Dysphania ambrosioidis. Among these species, expansion ranged from 139–149 bp in four species and 64–79 bp in three species (Atriplex gmelinii, C. quinoa, and Dysphania botris). The ndhF gene exhibited variable contraction or expansion at the IRb/SSC region junction in five species: K. ewersmanniana, A. canescens, A. gmelinii, D. botrys, and C. quinoa. Except for K. ewersmanniana, which exhibited contraction of 3 bp, expansion of 31–57 bp was observed in the other species. Except for K. ewersmanniana and C. quinoa, the ycf1 gene was expanded at the IRb/SSC region junction, with a range of 1–55 bp. In all seven species, ycf1 showed similar expansion at the SSC/IRa region junction. The psbA-trnH gene exhibited variable expansion at the IRA/LSC region junction in all species except K. ewersmanniana, K. ceratoides, and C. quinoa. Contraction of 82 bp and 1 bp was observed in A. gmelinii and D. ambrosioides, respectively, and rpl2-rps19 contraction of 1 bp was only observed at the IRa/LSC region junction in A. canescens.
The comparison showed similar chloroplast genome sequences for the seven species; however, the variation of non-coding region was significantly higher than that of coding region. PCGs such as ycf3 and rpl16 showed significant variation. The regions between genes with a high degree of variation included psbA-trnK-UUU, rps2-rpoC2, atpI-atpF, rpl32-ccsn, and dhB-tmL-CAA (Figure 6).
Analysis of the nucleotide diversity of the two Krascheninnikovia species revealed average Pi values of 0–0.00758 (Figure 7). Three highly variable regions were identified with Pi > 0.005, including psaJ, psbK, and psbK; these sites may contain more rapidly evolving site information and show potential as molecular markers.

3.5. Phylogenetic Analysis

To determine the phylogenetic position of K. ewersmanniana, we extracted and analyzed the shared PCGs of 35 representative Amaranthaceae species (Figure 8) with O. sativa and A. thaliana as outgroups. A total of 16 species of Chenopodium, Atriplex, and Beta were grouped into a single cluster. The 10 species of Salicornis, Suaeda, Bassia, and Salsola were incorporated into one group. Nine species of Ostosia, Celosia, and Amaranth were incorporated into another group. Each genus of plants, all of which are monophyletic, was clustered together. Alternanthera philoxeroides was located in the bottom of the phylogenetic tree and is the earliest isolated species among the 35 species in the Amaranthaceae family. Krascheninnikovia was located in the middle of the phylogenetic tree. K. ewersmanniana and K. ceratoides form a separate clade, which was most closely related to two other clades, comprising, respectively, D. ambrosioides, D. botrys, D. pumilio, and Beta vulgaris, Beta intermedia, Beta lomatogona, Atriplex (A. gmelinii and A. canescens), and Chenopodium (C. petiolare and C. quinoa). These clades were located at the top of the phylogenetic tree and are the most recently isolated of the 35 species of the Amaranthaceae family.

4. Discussion

The Amaranthaceae family, formerly also named Chenopodiaceae, harbors 80 genera and approximately 2500 species [27], including Krascheninnikovia, earlier referred to as Ceratoides or Eurotia, whose taxonomic position remains unclear. Prior studies have focused on the botanical, biological, and ecological characteristics of this plant [43,44,45]. With the development of sequencing technology, more complete cp genomes have been reported. According to incomplete statistics, approximately 86 complete genomes of the Amaranthaceae family were deposited in the National Center for Biotechnology Information (NCBI, https://www.ncbi.nlm.nih.gov/ (accessed on 22 April 2024) [27,46,47,48,49,50]. However, merely one Krascheninnikovia species, K. ceratoides, was reported. Genetic and phylogenetic characteristics, therefore, have been significantly lacking for the Krascheninnikovia species. K. ewersmanniana is a major species of high-quality wild forage grass, providing wind-resistance and sand-fixation for the vegetation in northern Xinjiang. It plays a vital role in vegetation restoration and ecological construction of the desert steppe in Xinjiang. To construct the phylogeny and lay a solid foundation for the evolution of Krascheninnikovia and the Amaranthaceae family, the K. ewersmanniana complete cp genome was assembled and annotated. The results depict that the chloroplast genome length of K. ewersmanniana is 152,287 bp and 128 genes, similar to that of Chenopodium acuminatum Willd. (152,200 bp, 113 genes) [51], Chenopodium album (152,200 bp, 110 genes) [52], and Amaranthaceae (149,726–153,474 bp, according to NCBI). Their complete cp genomes were all typical tetrad structures and composed of SSC, LSC, and two IRs. Overall, the basic features of the K. ewersmanniana chloroplast genome were consistent with those of most Amaranthaceous species, especially for congeners such as K. ceratoides, indicating that chloroplast genome size and structures of Krascheninnikovia species are highly conserved. The GC content in the IR region was higher than that in the LSC and SSC regions, which may be attributed to the presence of GC-rich genes in the IR region.
Repetitive sequences were the main force of chloroplast genome repeat, deletion, and rearrangement which resulted in the evolution of chloroplast [53]. The two tandem types identified in the K. ewersmanniana chloroplast genome were forward (F) and palindromic (P), which is consistent with those of K. ceratoides, C. album, and B. vulgaris [46,54]. Only one tandem type was detected in the chloroplast genomes of spinach and quinoa, both of which are F-types [55]. These results also differ from those of Carthamus (Asteraceae) species [27]. Thus, a correlation exists between the genetic relationships among species and the type and number of repeats. DNA molecular markers are useful tools widely applied in genetic structure analysis, identification of generational relations, and evolution of species. Being highly polymorphic and codominant, SSR markers were given more prominence than RAPD, ISSR, and other markers [56]. In another study, 48 SSRs were detected in K. ewersmanniana cp genomes, and mononucleotide A/T as a repeat unit was dominant. Compared with K. ceratoides, there was no pentanucleotide [25]. Chloroplast SSR markers can greatly facilitate species detection since they are maternally inherited. For example, a difference only in SSRs (ACTAT/AGTAT) found in the cp genome of two plants allowed for the differentiation and identification of species. Whether this hypothesis is true requires further validation via publication of more cp genomes along with development of SSR molecular markers.
DNA barcoding has been an effective tool to carry out species identification [57], and greatly promoted the development of species classification and phylogeny [58]. DNA barcoding research in higher plants mainly focuses on the chloroplast and nuclear genomes. According to the Consortium for the Barcode of Life, Chloroplast DNA fragments such as psbA-trnH and ribosomal DNA fragments such as ITS are widely used DNA barcodes [59]. In the literature, several variations in hotspots, such as psbA-trnK-UUU, rps2-rpoC2, atpI-atpF, rpl32-ccsn, and dhB-tmL-CAA and genes, psaJ, psbK, and psbK have been elucidated. Nevertheless, accD-psaI, ndhF-trnL, petA-psbJ, psbF-petL, trnC-psbM, trnS-trnG, and ycf2-trnL and PCGs such as accD, matK, ndhF, ndhK, ycf1, and ycf2 are those with significant variation [25]. Hence, further developing and screening structural variations in the chloroplast genome of K. ewersmanniana could be applied to species identification and phylogenetic development for K. ewersmanniana with its related species.
The main reason for the structural variation of the chloroplast genome is the variation of IR/LSC boundaries, and its contraction and expansion play key roles in the evolution of plant chloroplast DNA. Compared with that in other species, genetic structural changes in K. ewersmanniana occurred in all IR boundary regions. Genes and regions with high degrees of variation were identified and validated as potential molecular markers.
The phylogenetic tree based on chloroplast genome construction showed that 35 species of Amaranthaceae plants were clustered into one group. K. ewersmanniana and K. ceratoides were grouped together with 100% bootstrap values, and were most closely related to the clade of Atriplex, Chenopodium, and Dysphania, species with 100% bootstrap values; this is consistent with previous research results on the comparative analysis of K. ceratoides chloroplast genomes [25]. Atriplex and Dysphania were inserted in the Chenopodium, along with Krascheninnikovia, together divided into Tribe Chenopodieae [60]. Among Amaranthaceae, Liu et al. [25] found that Suaeda had the closest phylogeny to Atriplex. Atriplex and Suaeda formed different topological structures with other genera in this study. Determining the taxonomy based on morphology of Krascheninnikovia species has been difficult due to their characteristic transition from entomophily to anemophily and minor flowers. A comprehensive analysis of the morphology has not yet been attained due to lack of research at the molecular level, and the identification and taxonomy of Krascheninnikovia and even Amarathaceae are therefore yet to be elucidated.

5. Conclusions

To sum up, our study for the first time assembled the chloroplast genome of K. ewersmanniana, a plant that is widely distributed in the Xinjiang desert and has important ecological and economic value. This research not only enriches existing molecular biology data for this species, but also expands available genomic resources. In addition, we reported the evolutionary relationship between K. ewersmanniana and other species of Amaranthaceae. The results of the phylogenetic tree analysis suggested that K. ewersmanniana and K. ceratoides, along with D. ambrosioids, D. pumilio, and D. botrys, form a closely related monophyletic group. The phylogenetic insights gained from this study can help address future taxonomic and nomenclature challenges associated with K. ewersmanniana. In addition to expanding the available genetic resources of the Krascheninnikovia species, this work provides a scientific basis for future research on population genetic diversity and the sustainable utilization of K. ewersmanniana resources.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/genes15050546/s1, Table S1: Accession number and sampled chloroplast genomes obtained from GenBank; Table S2: Characteristics of the chloroplast genome of K. ewersmanniana; Table S3: Identified SSRs motifs in the chloroplast genomes of two Krascheninnikovia species; Table S4: SSR locations in the chloroplast genomes of two Krascheninnikovia species.

Author Contributions

P.W. conducted experiments, collected and analyzed data, and drafted the manuscript. Z.W. designed the experiment, and revised the manuscript. Y.L. collected plant materials. M.K., A.A. and Y.H. contributed to the interpretation of results. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Xinjiang Tianshan Talents Training Program “Agriculture, Rural Backbone” Talent Training Program (2022SNGGNT096), National Key Research and Development Program of China (2023YFD1200305), Xinjiang Tianshan Talents “Program—Science and Technology Innovation Leading Talents (team) (20221100619), Key Projects in Science and Technology of Inner Mongolia (2021ZD0031), and the Hohhot Science and Technology Plan (2022-she-zhong-1-2).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets presented in this paper can be found in online repositories. The names of the repositories and their accession number(s) are available at https://www.ncbi.nlm.nih.gov/ (accessed on 22 April 2024).

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Editorial Committee of Chinese Journal of Plant of Chinese Academy of Sciences. Flora China Tomus; Science Press: Beijing, China, 1996; Volume 25, pp. 26–27. [Google Scholar]
  2. Ke, M.; Hou, Y.R.; Wei, P.; Lan, J.Y.; Kang, S.; Li, C. Physiological responses of Krascheninnikovia ewersmannia under drought stress. Pratacultural. Sci. 2023, 40, 1349–1357. [Google Scholar]
  3. Cai, D.H.; Li, C.J.; Wei, Y. Germination behavior of Cerateoides latens seed in Junggar desert. Acta Agrestia Sin. 2016, 24, 384–388. [Google Scholar]
  4. Khan, M.A.; Gul, B.; Weber, D.J. Action of plant growth regulators and salinity on seed germination of Ceratoides lanata. Anim. Husb. Feed Sci. 2012, 82, 37. [Google Scholar] [CrossRef]
  5. Mao, Z.M. Flora Xinjiang Gensis Tomus; Xinjiang Science & Technology & Hygiene Publishing House: Urumqi, China, 1994; p. 2 (I). [Google Scholar]
  6. Wang, M.R.; Wei, Y. Germination behavior of Ceratoides ewersmanniana seeds in northern Xinjiang. Pratacultural. Sci. 2018, 35, 1836–1842. [Google Scholar]
  7. Chu, G.L.; Sergei, L.M.; Steven, E.C. Chenopodiaceae. Flora of China; Science Press: Beijing, China, 2003; Volume 5, pp. 351–414. [Google Scholar]
  8. Jia, M. Ceratoides latens resources and utilization indesert steppe. Anim. Husb. Feed Sci. 2012, 33, 123–124. [Google Scholar]
  9. Tao, Y.; Liu, T.; Jia, Y.M.; Cui, Y.H.; Luo, C.; Wei, P.; Jiangbo, X. Fractal characteristics of spatial distribution pattern of Ceratoides ewersmanniana and Haloxylon ammodendron population in the southern Gurbantunggut desert, Xinjiang. Arid Land Geogr 2008, 31, 365–372. [Google Scholar]
  10. Liu, T.; Li, Z.; An, S.Z.; Xu, G.Y. A study on root system of Ceratoides ewersmanniana. Grassl. Turf 2008, 1, 13–17. [Google Scholar]
  11. Jia, Y.M. Research on the Bioecological Characteristics of Spatial Distribution Pattern of Ceratoides ewersmanniana in the Southern Edge of Mosuowan Desert; Shihezi University: Shihezi, China, 2007. [Google Scholar]
  12. Li, L.; Jia, N.T.; Liu, M. Study on the physiological and biochemical index of drought resistance for Ceratoides Ewersmanniana ‘Yili’. Grass Feed Livest 2013, 1, 41–45. [Google Scholar]
  13. Zheng, X.H.; Li, Z.; Fu, A.L.; Yang, G.; Sha, W.L. Study in regenerated plants induced from embryo of Ceratoides ewersmanniana. China J. Grassl. 2007, 4, 50–55. [Google Scholar]
  14. Li, D.L.; Wang, J.H.; Li, A.D.; Liu, H.J.; An, F.B. Salt tolerance of 3 Ceratoides pps varieties in germination period. J. Desert Res. 2006, 26, 1009–1014. [Google Scholar]
  15. Mohajery, A.; Rasti, M. Germination temperature for Bromus tomentellus Boiss and Eurotia ceratoides (L.) C.A.M. Seed. Sci. Technol. 1995, 23, 241–243. [Google Scholar]
  16. Aranda-Sicilia, M.N.; Aboukila, A.; Armbruster, U.; Cagnac, O.; Schumann, T.; Kunz, H.H.; Jahns, P.; Rodríguez-Rosales, M.P.; Sze, H.; Venema, K. Envelope K+/H+ antiporters AtKEA1 and AtKEA2 function in plastid development. Plant Physiol. 2016, 172, 441–449. [Google Scholar] [CrossRef] [PubMed]
  17. Freyer, R.; Hoch, B.; Neckermann, K.; Maier, R.M.; Kössel, H. RNA editing in maize chloroplasts is a processing step independent of splicing and cleavage to monocistronic mRNAs. Plant J. 1993, 4, 621–629. [Google Scholar] [CrossRef] [PubMed]
  18. Neuhaus, H.E.; Emes, M.J. Nonphotosynthetic metabolism in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2000, 51, 111–140. [Google Scholar] [CrossRef] [PubMed]
  19. Zhang, Y.J.; Li, D.Z. Advances in phylogenomics based on complete chloroplast genomes. Plant Divers Res. 2011, 33, 365–375. [Google Scholar] [CrossRef]
  20. Chen, C.H.; Zheng, Y.J.; Liu, S.A.; Zhong, Y.; Wu, Y.; Li, J.; Xu, L.A.; Xu, M. The complete chloroplast genome of Cinnamomum camphora and its comparison with related Lauraceae species. Peer J. 2017, 5, e3820. [Google Scholar] [CrossRef] [PubMed]
  21. Wang, Y.H. Chloroplast Genome Sequences of Vitis: Structural Organization and Phylogenetic Analyses; Huazhong Agricultural University: Wuhan, China, 2018. [Google Scholar]
  22. Michał, M.; Alžběta, N.; Minasiewicz, J.; Selosse, M.A.; Jakalski, M. The complete chloroplast genome sequence of Dactylorhiza majalis (Rchb.) P.F. Hunt et Summerh. (Orchidaceae). Mitochondrial DNA 2019, 4, 2821–2823. [Google Scholar] [CrossRef] [PubMed]
  23. Wang, L.; He, N.; Li, Y.; Fang, Y.; Zhang, F. Complete chloroplast genome sequence of Chinese lacquer Tree (Toxicodendron vernicifluum, Anacardiaceae) and its phylogenetic significance. BioMed Res. Int. 2020, 2020, 9014873. [Google Scholar] [CrossRef] [PubMed]
  24. Han, B.; Wang, X.M.; Yin, J.; Zhao, M.L.; Yang, Y.Y. Genetic diversity of Ceratoides germplasm by RAPD analysis. Acta Agrestia Sin. 2003, 2, 154–158. [Google Scholar] [CrossRef]
  25. Liu, Y.; Zheng, C.; Su, X.; Chen, J.; Li, X.; Sun, C.; Nizamani, M.M. Comparative analysis and characterization of the chloroplast genome of Krascheninnikovia ceratoides (Amarathaceae): A xerophytic semi-shrub exhibiting drought resistance and high-quality traits. BMC Genom. Data 2024, 25, 10. [Google Scholar] [CrossRef] [PubMed]
  26. Bremer, B.; Bremer, K.; Chase, M.W.; Fay, M.F.; Reveal, J.L.; Soltis, D.E.; Soltis, P.S.; Stevens, P.F.; Anderberg, A.A.; Moore, M.J.; et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 2009, 161, 105–121. [Google Scholar] [CrossRef]
  27. Liang, C.Z.; Zhu, Z.Y.; Tian, Y.; Wang, W. The correction for scientific name of Ceratoides and Prinsepia in the second edition of (Flora Intramongolica). J. Inn. Mong. Univ. (Nat. Sci. Ed.) 2003, 5, 503–505. [Google Scholar]
  28. Schubert, M.; Lindgreen, S.; Orlando, L. AdapterRemoval v2: Rapid adapter trimming, identification, and read merging. BMC Res. Notes 2016, 9, 88. [Google Scholar] [CrossRef] [PubMed]
  29. Jin, J.J.; Yu, W.B.; Yang, J.B.; Song, Y.; dePamphilis, C.W.; Yi, T.S.; Li, D.Z. GetOrganelle: A fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 2020, 21, 241. [Google Scholar] [CrossRef] [PubMed]
  30. Qu, X.J.; Moore, M.J.; Li, D.Z.; Yi, T.S. PGA: A software package for rapid, accurate, and flexible batch annotation of plastomes. Plant Methods 2019, 15, 50. [Google Scholar] [CrossRef] [PubMed]
  31. 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] [PubMed]
  32. Greiner, S.; Lehwark, P.; OrganellarGenomeDRAW, B.R. (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]
  33. 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]
  34. Kurtz, S.; Choudhuri, J.V.; Ohlebusch, E.; Schleiermacher, C.; Stoye, J.; Giegerich, R. REPuter: The manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 2001, 29, 4633–4642. [Google Scholar] [CrossRef] [PubMed]
  35. Tamura, K.; Stecher, G.; Mega, K.S. Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 2021, 38, 3022–3027. [Google Scholar] [CrossRef] [PubMed]
  36. Mazumdar, P.; Binti, O.R.; Mebus, K.; Ramakrishnan, N.; Ann, H.J. Codon usage and codon pair patterns in non-grass monocot genomes. Ann. Bot. 2017, 120, 893–909. [Google Scholar] [CrossRef] [PubMed]
  37. Amiryousefi, A.; Hyvönen, J.; Poczai, P. IRscope: An online program to visualize the junction sites of chloroplast genomes. Bioinformatics 2018, 34, 3030–3031. [Google Scholar] [CrossRef] [PubMed]
  38. Mayor, C.; Brudno, M.; Schwartz, J.R.; Poliakov, A.; Rubin, E.M.; Frazer, K.A.; Pachter, L.S.; Dubchak, I. VISTA: Visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 2020, 16, 1046–1047. [Google Scholar] [CrossRef] [PubMed]
  39. 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] [PubMed]
  40. Kalyaanamoorthy, S.; Minh, B.Q.; Wong, T.K.F.; von Haeseler, A.; Jermiin, L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 2017, 14, 587–589. [Google Scholar] [CrossRef] [PubMed]
  41. Stamatakis, A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22, 2688–2690. [Google Scholar] [CrossRef] [PubMed]
  42. Ronquist, F.; Teslenko, M.; van der Mark, P.; Ayres, D.L.; Darling, A.; Höhna, S.; Larget, B.; Liu, L.; Suchard, M.A.; Huelsenbeck, J.P. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012, 61, 539–542. [Google Scholar] [CrossRef] [PubMed]
  43. Liu, T.; Zhao, X.J.; Jia, Y.M.; Cui, Y.H.; Luo, C.; Wei, P.; Zhang, Y.H.; Lin, H.R. Spatial pattern of population recruitment of C. ewersmanniana in South of Gurbantunggut Desert. J. Desert Res. 2008, 28, 258–265. [Google Scholar]
  44. Shawulie, S.B.H.; An, S.Z.; Yang, G.; Nuerjialili, N.; Zhang, H.H.; Fu, A.L.; Zheng, X.H. Study on the Botanical-biological and ecological characteristics of Ceratoides ewersmanniana cv. YiLi. Xinjiang Agric. Sci. 2010, 47, 1842–1846. [Google Scholar]
  45. Deng, Y.B.; Jiang, Y.C.; Liu, J. The xeromorphic and saline morphic structure of leaves and assimilating branches in ten Chenopodiaceae species in Xinjiang. Chin. J. Plant Ecol. 1998, 22, 69–75. [Google Scholar]
  46. Park, J.; Min, J.; Kim, Y.; Chung, Y. The comparative analyses of six complete chloroplast genomes of morphologically diverse Chenopodium album L. (Amaranthaceae) collected in Korea. Int. J. Genom. 2021, 2021, 6643444. [Google Scholar] [CrossRef] [PubMed]
  47. Wei, Z.; Chen, F.; Ding, H.; Liu, W.; Yang, B.; Geng, J.; Chen, S.; Guo, S. Comparative analysis of six chloroplast genomes in Chenopodium and its related genera (Amaranthaceae): New insights into phylogenetic relationships and the development of species-specific molecular markers. Genes 2023, 14, 2183. [Google Scholar] [CrossRef] [PubMed]
  48. Liu, T.; Zuo, Z.; He, Y.; Miao, J.; Yu, J.; Qu, C. The complete chloroplast genome of a halophyte glasswort Salicornia europaea. Mitochondrial DNA B Resour. 2023, 8, 1165–1168. [Google Scholar] [CrossRef] [PubMed]
  49. Xie, W.; Zhang, C.; Wang, Y.; Zhang, Y. The complete chloroplast genome of Caroxylon passerinum (Chenopodiaceae), an annual desert plant. Mitochondrial DNA B Resour. 2022, 7, 426–427. [Google Scholar] [CrossRef] [PubMed]
  50. Gao, M.Z.; Dong, Y.H.; Valcárcel, V.; Ren, Z.M.; Li, Y.L. Complete chloroplast genome of the grain Chenopodium quinoa Willed., an important economical and dietary plant. Mitochondrial DNA B Resour. 2021, 6, 40–42. [Google Scholar] [CrossRef]
  51. Wariss, H.M.; Qu, X.J. The complete chloroplast genome of Chenopodium acuminatum Willd. (Amaranthaceae). Mitochondrial DNA B Resour. 2021, 6, 174–175. [Google Scholar] [CrossRef]
  52. Li, F.Z.; Zhang, X.L.; Zhu, L.L.; Lu, H.F.; Song, D.L. Characterization of the complete chloroplast genome of an annual herb, Chenopodium album (Amaranthaceae). Mitochondrial DNA B Resour. 2021, 6, 2107–2108. [Google Scholar] [CrossRef] [PubMed]
  53. Li, B.; Zheng, Y. Dynamic evolution and phylogenomic analysis of the chloroplast genome in Schisandraceae. Sci. Rep. 2018, 8, 9285. [Google Scholar] [CrossRef] [PubMed]
  54. Bao, G.Y.; Wang, Y.Q.; Li, W.X. Comparative analysis of chloroplast genome repeats of betavulgaris and its related groups. Seed 2023, 42, 36–44. [Google Scholar]
  55. Yang, T.; Aishan, S.; Zhu, J.; Qin, Y.; Liu, J.; Liu, H.; Tie, J.; Wang, J.; Qin, R. Chloroplast genomes and phylogenetic analysis of three Carthamus (Asteraceae) species. Int. J. Mol. Sci. 2023, 24, 15634. [Google Scholar] [CrossRef]
  56. Saha, D.; Rana, R.S.; Das, S.; Datta, S.; Mitra, J.; Cloutier, S.J.; You, F.M. Genome-wide regulatory gene-derived SSRs reveal genetic differentiation and population structure in fiber flax genotypes. J. Appl. Genet. 2019, 60, 13–25. [Google Scholar] [CrossRef] [PubMed]
  57. Hebert, P.D.; Cywinska, A.; Ball, S.L.; de Waard, J.R. Biological identifications through DNA barcodes. Proc. Biol. Sci. 2003, 270, 313–321. [Google Scholar] [CrossRef] [PubMed]
  58. Hajibabaei, M.; Singer, G.A.; Hebert, P.D.; Hickey, D.A. DNA barcoding: How it complements taxonomy, molecular phylogenetics and population genetics. Trends Genet. 2007, 23, 167–172. [Google Scholar] [CrossRef] [PubMed]
  59. Yao, H.; Song, J.Y.; Ma, X.Y.; Liu, C.; Li, Y.; Xu, H.X.; Han, J.P.; Duan, L.S.; Chen, S.L. Identification of Dendrobium species by a candidate DNA barcode sequence: The chloroplast psbA-trnH intergenic region. Planta Med. 2009, 75, 667–669. [Google Scholar] [CrossRef]
  60. Fuentes-Bazan, S.; Uotila, P.; Borsch, T. A novel phylogeny-based generic classification for Chenopodium sensu lato, and a tribal rearrangement of Chenopodioideae (Chenopodiaceae). Willdenowia 2012, 42, 5–24. [Google Scholar] [CrossRef]
Genes 15 00546 g001
Figure 1. Map of the chloroplast genome structure of K. ewersmanniana. Genes drawn in circles are transcribed clockwise, whereas genes outside the circle are transcribed counterclockwise. Different colors are annotated according to the different functions of the genes.
Figure 1. Map of the chloroplast genome structure of K. ewersmanniana. Genes drawn in circles are transcribed clockwise, whereas genes outside the circle are transcribed counterclockwise. Different colors are annotated according to the different functions of the genes.
Genes 15 00546 g001
Genes 15 00546 g002
Figure 2. Relative synonymous codon usage of amino acids of K. ewersmanniana. The blocks underneath stand for different codon encoding amino acids. The columns on the top depict the sums of RSCU values of the 20 amino acids.
Figure 2. Relative synonymous codon usage of amino acids of K. ewersmanniana. The blocks underneath stand for different codon encoding amino acids. The columns on the top depict the sums of RSCU values of the 20 amino acids.
Genes 15 00546 g002
Genes 15 00546 g003
Figure 3. Analysis of tandem repeat sequences in the plastomes of two Krascheninnikovia plants. (A) type of scattered repeats; (B) length of scattered repeats.
Figure 3. Analysis of tandem repeat sequences in the plastomes of two Krascheninnikovia plants. (A) type of scattered repeats; (B) length of scattered repeats.
Genes 15 00546 g003
Genes 15 00546 g004
Figure 4. Analysis of SSRs in the chloroplast genome of two Krascheninnikovia plants. (A) Frequency of identified SSR motifs; (B) location distribution of all SSR motifs.
Figure 4. Analysis of SSRs in the chloroplast genome of two Krascheninnikovia plants. (A) Frequency of identified SSR motifs; (B) location distribution of all SSR motifs.
Genes 15 00546 g004
Genes 15 00546 g005
Figure 5. Comparative analysis of four boundary regions in the chloroplast genomes of seven Amaranthaceae plants.
Figure 5. Comparative analysis of four boundary regions in the chloroplast genomes of seven Amaranthaceae plants.
Genes 15 00546 g005
Genes 15 00546 g006
Figure 6. Global alignment of seven chloroplast genomes using C. quinoa as a reference. Horizontal axis represents coordinates in the chloroplast genome; vertical axis indicates the average percentage sequence similarity in the aligned regions from 50% to 100%.
Figure 6. Global alignment of seven chloroplast genomes using C. quinoa as a reference. Horizontal axis represents coordinates in the chloroplast genome; vertical axis indicates the average percentage sequence similarity in the aligned regions from 50% to 100%.
Genes 15 00546 g006
Genes 15 00546 g007
Figure 7. Nucleotide polymorphisms in chloroplast genome of two Krascheninnikovia plants. Horizontal and vertical axes show the name of the gene and Pi value, respectively.
Figure 7. Nucleotide polymorphisms in chloroplast genome of two Krascheninnikovia plants. Horizontal and vertical axes show the name of the gene and Pi value, respectively.
Genes 15 00546 g007
Genes 15 00546 g008
Figure 8. Phylogenetic tree of K. ewersmanniana with 34 other representative Amaranthaceae species. A. thaliana and O. sativa were selected as outgroups. The maximum likelihood and Bayesian tree were determined based on shared protein-coding genes. Maximum likelihood bootstrap support values/Bayesian posterior probabilities are shown for each node.
Figure 8. Phylogenetic tree of K. ewersmanniana with 34 other representative Amaranthaceae species. A. thaliana and O. sativa were selected as outgroups. The maximum likelihood and Bayesian tree were determined based on shared protein-coding genes. Maximum likelihood bootstrap support values/Bayesian posterior probabilities are shown for each node.
Genes 15 00546 g008
Table 1. Gene functional classification and composition of the K. ewersmanniana chloroplast genome.
Table 1. Gene functional classification and composition of the K. ewersmanniana chloroplast genome.
Gene CategoryGene GroupGene Name
PhotosynthesisPhotosystem IIpsbZ, psbA, psbT, psbB, psbN, psbC, psbM, psbD, psbL, psbE, psbJ, psbK, psbF, psbI, psbH
Photosystem IpsaJ, psaB, psaI, psaC, psaA
RubiscorbcL
Cytochrome b/f complexpetD *, petB *, petL, petA, petN, petG
ATP synthaseatpF *, atpI, atpA, atpE, atpB, atpH
NADH-dehydrogenasendhB *(2), ndhA *, ndhI, ndhD, ndhC, ndhE, ndhG, ndhF ndhH, ndhK, ndhJ
Self-replicationrRNA genesrrn4.5S(2), rrn23S(2), rrn5S(2), rrn16S(2)
Large subunit of ribosomerpl16 *, rpl14, rpl2(2), rpl22, rpl36, rpl20, rpl33, rpl32
DNA-dependent RNA polymeraserpoC1 *, rpoB, rpoC2, rpoA
tRNA genestrnA-UGC *(2), trnI-GAU *(2), trnV-UAC *, trnL-UAA *, trnR-UCU *, trnK-UUU *, trnI-CAU(2), trnfM-CAU, trnL-CAA(2), trnW-CCA, trnN-GUU(2), trnT-GGU, trnS-GGA,
trnR-ACG(2), trnS-UGA, trnV-GAC(2), trnC-GCA, trnS-GCU, trnD-GUC, trnQ-UUG, trnY-GUA, trnT-UGU, trnM-CAU, trnP-UGG, trnL-UAG, trnF-GAA, trnG-UCC, trnG-GCC, trnE-UUC
Small subunit of ribosomerps12 *(2), rps16 *, rps8, rps4, rps19, rps14, rps7(2), rps15, rps11, rps2, rps18, rps3, rps12
Other genesTranslation initiation factorinfA
C-type cytochrome synthesis geneccsA
ProteaseclpP **
Acetyl-CoA carboxylaseaccD
MaturasematK
Envelope membrane proteincemA
UnknownConserved open reading framesycf3 **, ycf2(2), ycf4, ycf1
Note: * only one intron gene; ** two intron genes; gene (2): indicates the presence of two copies of the gene.
Table 2. Length of exons and introns of split genes in the chloroplast genome of K. ewersmanniana.
Table 2. Length of exons and introns of split genes in the chloroplast genome of K. ewersmanniana.
GeneStrandStartEndExon I (bp)Intron I (bp)Exon II (bp)Intron II (bp)Exon III (bp)
ycf3−41,85843,88512477923080590
clpP−69,73271,73371811292603225
trnK-UUU−1470403437249335
rpl16−80,99682,45891055399
ndhA+118,491120,536552954540
petB+74,65576,1376835642
rps12−139,808140,60823254326
ndhB+92,77194,970777667756
rps12+95,77896,57823254326
trnA-UGC−134,254135,1533782736+
ndhB−141,416143,615777667756
petD+76,35977,5608719475
trnI-GAU−135,224136,2273793235
rps16−47135913100907194
trnV-UAC−51,06051,7513861638
trnI-GAU+100,159101,1623793235
atpF−11,20012,593145839410
trnL-UAA+46,70947,4363963950
trnA-UGC+101,233102,1323882735
Note: + positive strand; − negative strand.
Table 3. Codon numbers for K. ewersmanniana chloroplast PCGs.
Table 3. Codon numbers for K. ewersmanniana chloroplast PCGs.
CodonCountCodonCountCodonCountCodonCount
UAA40GGC168AUG501AGU353
UAG19GGG280AAC253UCA340
UGA19GGU492AAU796UCC224
GCA363CAC132CCA265UCG157
GCC211CAU392CCC169UCU472
GCG160AUA626CCG140ACA381
GCU544AUC320CCU374ACC205
UGC63AUU982CAA655ACG124
UGU190AAA978CAG162ACU476
GAC181AAG280AGA338GUA462
GAU736CUA344AGG141GUC140
GAA1033CUC144CGA331GUG160
GAG260CUG128CGC88GUU486
UUC409CUU490CGG99UGG381
UUU933UUA827CGU300UAC155
GGA598UUG462AGC104UAU660
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Wei, P.; Li, Y.; Ke, M.; Hou, Y.; Aikebaier, A.; Wu, Z. Complete Chloroplast Genome of Krascheninnikovia ewersmanniana: Comparative and Phylogenetic Analysis. Genes 2024, 15, 546. https://doi.org/10.3390/genes15050546

AMA Style

Wei P, Li Y, Ke M, Hou Y, Aikebaier A, Wu Z. Complete Chloroplast Genome of Krascheninnikovia ewersmanniana: Comparative and Phylogenetic Analysis. Genes. 2024; 15(5):546. https://doi.org/10.3390/genes15050546

Chicago/Turabian Style

Wei, Peng, Youzheng Li, Mei Ke, Yurong Hou, Abudureyimu Aikebaier, and Zinian Wu. 2024. "Complete Chloroplast Genome of Krascheninnikovia ewersmanniana: Comparative and Phylogenetic Analysis" Genes 15, no. 5: 546. https://doi.org/10.3390/genes15050546

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