Startseite Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
Artikel Open Access

Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua

  • Jiaqiang Zhang , Huichun Liu , Wenting Xu , Xiao Wan und Kaiyuan Zhu EMAIL logo
Veröffentlicht/Copyright: 11. November 2024
Artikel downloaden (PDF)
Open Life Sciences
Aus der Zeitschrift Open Life Sciences Band 19 Heft 1

Abstract

Lonicera japonica is a well-known medicinal plant, and the Damaohua cultivar is one of the oldest known honeysuckle cultivars in China. The 155,151 bp chloroplast genome of this cultivar was obtained through Illumina sequencing. The genome includes a pair of inverted repeats (IRa and IRb; 23,789 bp each), a large single-copy region (88,924 bp), and a small single-copy (SSC) region (18,649 bp). In total, 127 unique genes were identified: 80 protein-coding, 39 tRNA, and 8 rRNA genes. Only ycf3 contained two introns. Eighty-nine large repetitive sequences and 54 simple sequence repeats were detected. Fifty potential RNA editing sites were predicted. Adaptive evolution analysis revealed that infA, matK, petB, petD, rbcL, rpl16, rpl2, rps3, ycf1, and ycf2 were positively selected, possibly reflecting the specific environmental adaptations of this cultivar. Sequence alignment and analysis revealed several candidate fragments for Lonicera species identification, such as the intergenic regions rpoB-petN, rbcL-accD, and psaA-ycf3. The IR region boundary and phylogenetic analysis revealed that the L. japonica cv. Damaohua chloroplast genome was most closely related to the L. japonica genome, but there were five distinct differences between the two. There are four sites with high variability between L. japonica and L. japonica cv. Damaohua with nucleotide variability (Pi) greater than 0.002, including rps2-rpoC2, atpB-rbcL, ycf1, and ycf1-trnN GUU. The differences between L. japonica and L. japonica cv. Damaohua were further confirmed by the single nucleotide polymorphism sites between these two species. Therefore, this study revealed that the chloroplast genome can serve as a universal super barcode for plant identification, which can identify differences and help distinguish Lonicera japonica from related species. An understanding of Lonicera japonica cv. Damaohua chloroplast genomics and a comparative analysis of Lonicera species will provide a scientific basis for breeding, species identification, systematic evolution analysis, and chloroplast genetic engineering research on medicinal honeysuckle plants.

Graphical abstract

Keywords: Lonicera japonica, chloroplast genome, evolution, phylogenetic analysis

1 Introduction

Lonicera japonica Thunb. (Caprifoliaceae) is a commonly used herb that grows widely in China, Japan, Korea, and Southeast Asian countries [1]. Flower buds, known as Lonicerae japonicae, are the most important medicinal part of the plant [2,3], with more than 3,000 years of medical history. Lonicerae japonicae flos was first identified in one of the earliest pharmacopoeias in the world, “Shen Nong’s Material Medica,” Modern pharmacological studies have revealed that its extracts contain numerous bioactive compounds for treating various diseases, such as antibacterial, antiviral, anti-inflammatory, and antioxidative compounds [3]. In recent years, Lonicerae japonicae flos have also become the main raw material for “cooling” beverages in China.

Since the 2005 edition of the Chinese Pharmacopoeia, Lonicerae japonicae flos (called Jinyinhua, JYH in Chinese) and Lonicerae flos (called Shanyinhua, SYH in Chinese) have been documented as two herbs. Lonicera japonica Thunb. has been identified as the only botanical source of Lonicerae japonicae flos [4]. During the long-term cultivation process, when coupled with artificial introduction, domestication, and screening, L. japonicae species have undergone obvious differentiation, resulting in many intraspecific variations, such as “Damaohua,” “Xiaomaohua,” “Lanhan,” “Jiufengyihao,” “Sijihua,” and other varieties [5]. These findings indicate that the source of Lonicerae japonicae flos was more complicated. Among these varieties, L. japonica cv. Damaohua is one of the oldest known varieties of L. japonicae and is produced primarily in Shandong and Henan Provinces in China. The most prominent characteristic of this variety is its high yield; its high content of active elements (chlorogenic acid, luteoloside, flavonoids, and iridoids) is another notable feature. This variety can be considered as an excellent parental candidate [6]. Examples of its derivatives include L. japonica cv. Jiufengyihao and L. japonica cv. Beihuayihao [7,8]. There are also significant differences in the yield and quality of L. japonica compared with the different original species [9]. At present, there are two prominent problems associated with the application of L. japonica. First, the source of L. japonica flos on the market is complex, and it is difficult to identify the source plant based on morphological characteristics alone; thus, it is necessary to develop a more effective species identification method. Second, few studies have investigated the population inheritance of L. japonica, especially the intraspecific variation of the original species of traditional Chinese medicines. Therefore, research on the intraspecific variation of the original medicinal plant materials is not only helpful for understanding the process and reasons for the intraspecific differentiation of medicinal plants but also provides a theoretical basis for screening excellent germplasm resources and improving new medicinal varieties. Therefore, the accurate identification of the original botanical source is the first step in ensuring the quality of the resulting herbal medicines [10].

The identification of the original species of traditional Chinese medicines has always been a popular topic in the field of medicinal plant research. The conventional morphological characteristics and commonly used DNA barcode fragments are insufficient for identifying honeysuckle species accurately, especially for the identification of closely related species. Difficulties in species identification have led to uneven quality among medicinal honeysuckle compounds [2,11,12,13]. Genetic analysis is a reliable strategy for elucidating the evolutionary relationships among species at various taxonomic levels. Owing to the existence of functional genes that play important roles in plant cells, the chloroplast genome contains enough genetic information for comparative analysis and species diversification studies [14]. Although honeysuckle nuclear genome sequencing has been completed [15], the chloroplast genome is less common than the plant nuclear genome and has a relatively conserved structure. Chloroplast genomes have become ideal models for evolution and comparative genomic research [16]. The entire chloroplast genome can be used as a “super barcode” for species identification [17,18], which provides an essential basis for determining the evolutionary and phylogenetic relationships of medicinal plants in Caprifoliaceae (the honeysuckle family).

The chloroplast is an important organelle of green plants and plays a key role in autotrophic photosynthesis [19,20,21]. Among the three genomes present in plants, the chloroplast genome is the most conserved. The chloroplast genome is maternally inherited in most plants, and its composition and sequence are highly conserved. The chloroplast genome is a typical circular multicopy DNA molecule in cells that can be generally divided into four fragments: a large single-copy (LSC) region, a small single-copy (SSC) region, and two inverted repeat (IR) regions. The genome size usually ranges from 120 to 170 kb and includes 120–130 genes [22]. The different sizes of chloroplast genomes among different species are attributable primarily to the contraction or expansion of the IR region. Compared with the chloroplast genomes of other plants [23,24], the L. japonica chloroplast genome has a unique rearrangement between trnI-CAU and trnN-GUU. In the L. japonica chloroplast genome, rps19, rpl2, and rpl23 are moved from the IR region to the LSC region. The ycf1 pseudogene is lost from the IR region, and only one copy is present in SSC region2. These changes lead to sequence differences between species and can be used to study plant taxonomy, phylogeny, and evolutionary relationships. Genomic data, including organelle genomic data, can provide a molecular basis for research on the original species of traditional Chinese medicines [11,25].

With the increase in the number of available chloroplast genomes for Loniceraceae plants, the chloroplast genome sequences of Loniceraceae species have become easier to splice [1,2,8,26,27]. He et al. first reported the chloroplast genome sequence of Lonicera japonica [2]. Only the differences between plant families were compared and analyzed. Liu et al. compared the chloroplast genome sequence variation in seven Lonicera species [8], which was not the source of the original L. japonica Thunb. species specified in the Chinese Pharmacopoeia. Therefore, the phylogenetic evolution of the original species Lonicera japonica Thunb. is still poorly understood. There have been few reports on the chloroplast genome of L. japonica cv. Damaohua, which is one of the main varieties of honeysuckle in China. In general, there have been few studies on the genetics of L. japonica cv. Damaohua, especially the molecular genetics of this variety, which has severely restricted the protection, development and use of L. japonica cv. Damaohua resources.

In this study, the complete chloroplast genome of L. japonica cv. Damaohua was obtained using Illumina sequencing assembly. Here we not only described the whole chloroplast genome sequence of L. japonica cv. Damaohua and the characteristics of its long repeats and simple sequence repeats (SSRs) but also analyzed the chloroplast genome and compared it with those of other members of the original species of L. japonica Thunb. This study revealed that the L. japonica cv. Damaohua chloroplast genome was the most closely related to that of L. japonica from a previous report, but there were five distinct differences between the two. These results suggest that the chloroplast genome can be used to discriminate among Lonicera species effectively at the species level. Comprehensive chloroplast genome analysis of L. japonica cv. Damaohua will facilitate the identification of Lonicera species and provide a further basis for elucidating the evolutionary origins of this species.

2 Materials and methods

2.1 DNA sequencing, genome assembly, and annotation

Fresh leaves of L. japonica cv. Damaohua were collected from Hangzhou in Zhejiang Province, China (N30°06′, E120°22′) (Figure 1a and b), and total genomic DNA was extracted by cetyltrimethylammonium bromide method [28]. The DNA quality was tested (> 50 ng μL−1), and the DNA was then sequenced with an Illumina HiSeq 2500 platform (Illumina, San Diego, CA, USA) at Genesky Biotechnologies Inc. (Shanghai, China).

Figure 1 Images of Lonicera japonica cv. Damaohua. (a) Phenotypic characteristics of Lonicera japonica cv. Damaohua at the bud stage. (b) Flower buds and flowers of Lonicera japonica cv. Damaohua. Photographs by Jiaqiang Zhang.
Figure 1

Images of Lonicera japonica cv. Damaohua. (a) Phenotypic characteristics of Lonicera japonica cv. Damaohua at the bud stage. (b) Flower buds and flowers of Lonicera japonica cv. Damaohua. Photographs by Jiaqiang Zhang.

The quality of the Illumina paired-end raw reads was evaluated with FastQC software [29], and low-quality and short (L < 60 bp) reads were filtered. The remaining clean reads were assembled using NOVOPlasty (https://github.com/ndierckx/NOVOPlasty) [30] with the chloroplast genome sequence of L. japonica (NC_026839) being used as the reference sequence. The chloroplast genome was annotated using CPGAVAS2 [31]. Protein-coding genes, tRNA genes, and rRNA genes were predicted using the default parameters and were then functionally annotated in combination with the Kyoto Encyclopedia of Genes and Genomes [32,33,34], Clusters of Orthologous Groups, Nonredundant, Swiss-Prot, and Gene Ontology databases.

The chloroplast genome sequence of L. japonica cv. Damaohua has been submitted to GenBank (accession number: MZ779026). The associated BioProject, sequence read archive, and Bio-Sample numbers are PRJNA780957, SRR16980190, and SAMN23258802, respectively.

2.2 Genome structure and comparative analysis

The online tool MISA (http://pgrc.ipk gatersleben.de/misa/misa.html) [35] was used to identify SSRs in the chloroplast genome of L. japonica cv. Damaohua. There were ten mononucleotide repeats; five dinucleotide repeats; four trinucleotide repeats; and three tetranucleotide, pentanucleotide, and hexanucleotide repeats. Repetitive sequences, including palindromic, forward, reverse, and complement sequences, were analyzed with the REPuter program [36] with the following parameter settings: a minimal repeat size of 30 bp, a Hamming distance of 3, and a maximum number of computed repeats of 90. The relative synonymous codon usage (RSCU) value was calculated using MEGA6 [37]. RNA editing sites were predicted using the PREP-Cp web server (http://prep.unl.edu/cgi-bin/cp-input.pl) with a cutoff value of 0.8 [38]. The IR regions were examined and plotted using the online program IRscope (https://irscope.shinyapps.io/irapp/) [39]. The complete chloroplast genomes of the six Lonicera species were compared with the mVISTA online program using the annotation of L. insularis as a reference in shuffle-LAGAN mode [40]. We analyzed nonsynonymous (Ka) and synonymous (Ks) substitution rates, and the chloroplast genome sequence of L. japonica cv. Damaohua was compared with those of six Lonicera species. The coding sequences (CDSs) were subsequently translated into protein sequences. We identified 74 shared protein-coding genes that were shared between them. Ka/Ks ratio was calculated with TBtools according to the coding sequence [41]. Ka/Ks ratios > 1 indicate positive selection, Ka/Ks ratios = 1 indicate neutral selection, and Ka/Ks ratios < 1 indicate negative selection (purifying selection) [42].

We compared the chloroplast genome of L. japonica cv. Damaohua (MZ779026) with the chloroplast genomes of L. macranthoides (NC_040959), L. confusa (NC_045045), L. japonica (NC_026839), L. maackii (NC_039636), and L. insularis (MH028739).

2.3 Phylogenetic analysis

A total of 15 complete chloroplast genome sequences were downloaded from the NCBI database, namely, those of L. japonica cv. Damaohua (MZ779026), L. macranthoides (NC_040959), L. confusa (NC_045045), L. japonica (NC_026839), L. maackii (NC_039636), L. insularis (MH028739), L. ferdinandi (NC_040963), L. hispida (NC_040962), L. nervosa (NC_040961), L. praeflorens (NC_039635), L. sachalinensis (MH028742), L. vesicaria (NC_039638), L. tatarica (MW340876), T. pinnatifidum (NC_037952) and C. boreale (NC_037388). With C. boreale as the outgroup, the complete chloroplast genomes were aligned using MAFFT version 7 [43], and then the phylogenetic analysis was subsequently conducted using maximum likelihood (ML) and Bayesian inference (BI) methods. ML analysis was performed using the program RAxML v7.2.6 [44], BI analysis was implemented using the program MrBayes v3.1.2 [45], and visualization was performed using FigTree 1.4.4 (http://tree.bio.ed.ac.uk/software/figtree/). In addition, DnaSP v5.10 was used to evaluate the nucleotide diversity (Pi) between the L. japonica and L. japonica cv. Damaohua chloroplast genomes with a window length of 600 bp and step length of 200 bp [46].

3 Results

3.1 Chloroplast genome features of L. japonica cv. Damaohua

The chloroplast genome sequence of L. japonica cv. Damaohua was found to be 155,151 bp in length, with a typical tetragonal structure consisting of an LSC region (88,924 bp), an SSC region (18,649 bp), and two IRs (IRA and IRB, 23,789 bp) (Figure 2). The chloroplast genome of L. japonica cv. Damaohua has 127 functional genes, consisting of 80 protein-coding genes, 8 ribosomal RNA (rRNA) genes, and 39 transfer RNA (tRNA) genes. The overall nucleotide composition of L. japonica cv. Damaohua was 30.2% A, 31.2% T, 19.6% C, and 19.0% G, and the total guanine (G) and cytosine (C) content was 38.6% (Table 1). A total of 16 genes were found to be repeated in the IR region, with 10 protein-coding genes (atpF, ndhA, ndhB, rps12, rps16, rps18, rpl2, rpoC1, ycf2, and ycf3) and 6 tRNA genes (trnA-UGC, trnG-GCC, trnI-GAU, trnK-UUU, trnL-UAA, and trnV-UAC). Gene structure analysis revealed that 16 genes contained introns, of which 15 (9 protein-coding genes and 6 tRNA genes) had one intron, whereas only one (ycf3) had two introns. The intron of trnK-UUU was the longest, whereas the intron of rps12 was the shortest (Table 2 and Table S1).

Figure 2 Gene map of the L. japonica cv. Damaohua chloroplast genome. LSC indicates large single-copy; SSC indicates small single-copy; and IR indicates inverted repeat.
Figure 2

Gene map of the L. japonica cv. Damaohua chloroplast genome. LSC indicates large single-copy; SSC indicates small single-copy; and IR indicates inverted repeat.

Table 1

Base composition of the L. japonica cv. Damaohua chloroplast genome

Region Length T(U) (%) C (%) A (%) G (%)
Genome 155,151 31.2 19.6 30.2 19
LSC 88,924 32.1 19.0 30.8 18.1
SSC 18,649 34.3 16.9 32.3 16.5
Ira 23,789 28.7 23.1 27.9 20.4
IRb 23,789 27.9 20.4 28.7 23.1
CDS 74,214 31.3 18.1 30.0 20.6
CDS, 1 position 24,738 23.7 19.3 29.7 27.3
CDS, 2 position 24,738 32.5 20.6 28.9 18.0
CDS, 3 position 24,738 37.7 14.4 31.4 16.5
Table 2

Introns in the genes of the L. japonica cv. Damaohua chloroplast genome

GeneID Gene Exon Ⅰ (bp) Intron Ⅰ (bp) Exon Ⅱ (bp) Intron Ⅱ (bp) Exon Ⅲ (bp)
1 atpF 144 735 409
2 ndhA 552 1,092 538
3 ndhB 776 678 755
4 rpl2 386 671 428
5 rpoC1 431 776 1,607
6 rps12 113 231 535 — 31
7 rps16 39 868 229
8 rps18 160 307 30
9 trnA-UGC 37 808 34
10 trnG-GCC 22 716 46
11 trnI-GAU 36 946 34
12 trnK-UUU 36 2,534 34
13 trnL-UAA 35 512 48
14 trnV-UAC 39 564 35
15 ycf2 6,118 248 483
16 ycf3 123 731 229 759 152

We assessed the basic characteristics of the chloroplast genomes of Loniceraceae and compared them with those of the L. japonica cv. Damaohua chloroplast genome. The L. japonica cv. Damaohua genome was slightly larger than the L. japonica (155,078 bp), L. insularis (155,124 bp), and L. macranthoides (154,897 bp) genomes but smaller than the L. maackii (155,318 bp) and L. confusa (155,346 bp) genomes (Table 3). Among the Loniceraceae chloroplast genomes, L. macranthoides, L. maackii, L. japonica, and L. insularis presented the greatest number of chloroplast genes (131), followed by L. confusa (129) and L. japonica cv. Damaohua, which presented the fewest (127). In addition, the GC contents of the chloroplast genomes from the six Lonicera species were similar, ranging from 38.3 to 38.6%.

Table 3

Comparison of the general features of the chloroplast genomes from six Lonicera species

Species GenBank accession numbers All length (bp) LSC length (bp) SSC length (bp) IR length (bp) Protein coding tRNA LSC rRNA IRA Total GC (%)
L. japonica cv. Damaohua MZ779026 155,151 88,924 18,675 23,776 80 39 8 38.6
L. macranthoides NC_040959 154,897 88,692 18,623 23,791 84 39 8 38.5
L. confusa NC_045045 155,346 89,122 18,634 23,795 84 37 8 38.6
L. japonica NC_026839 155,078 88,858 18,672 23,774 84 39 8 38.6
L. maackii NC_039636 155,318 89,202 18,680 23,718 86 37 8 38.5
L. insularis MH028739 155,124 88,230 18,774 24,060 86 37 8 38.3

3.2 Characterization of SSRs and repeat sequences

A total of 54 SSRs were detected in the chloroplast genome of L. japonica cv. Damaohua, of which 36 were mononucleotide, 4 were dinucleotide, 2 were trinucleotide, 9 were tetranucleotide, and 3 were hexanucleotide repeats, with pentanucleotide deletions (Table 4). In addition, we compared the SSR distribution pattern and number of L. japonica cv. Damaohua with those of the five other chloroplast genomes in the Loniceraceae family (Tables S2 and S3). Among the six Lonicera species, there were more mononucleotide repeats than all the other types combined, and most of the SSRs were composed of mononucleotide and tetranucleotide repeats. The numbers and types of chloroplast SSRs vary in different species. Among the species, L. japonica cv. Damaohua, L. confusa, L. maackii, and L. insularis all lacked pentanucleotide repeats, whereas L. macranthoides lacked hexanucleotide repeats. L. japonica cv. Damaohua (54 SSRs) and L. confusa (54 SSRs) presented the greatest number of SSRs, whereas L. japonica (47 SSRs) presented the fewest SSRs. In addition, the chloroplast genomes of L. insularis, L. macranthoides, and L. maackii contained 52, 51, and 48 SSRs, respectively. The main type of SSR was a mononucleotide repeat, and most of the mononucleotide repeats were A/T-type SSRs.

Table 4

Number of different SSR types in the chloroplast genomes of six Lonicera species

SSR types L. japonica cv. Damaohua L. macranthoides L. confusa L. japonica L. maackii L. insularis
Mononucleotide 36 33 37 29 29 33
Dinucleotide 4 6 4 4 7 6
Trinucleotide 2 4 2 2 1 2
Tetranucleotide 9 7 8 9 10 9
Pentanucleotide — 1 — — — —
Hexanucleotide 3 — 3 3 1 2
Total 54 51 54 47 48 52

A total of 89 large repeats were identified in the chloroplast genome of L. japonica cv. Damaohua using REPuter, including 68 forward repeats and 21 palindrome repeats (Figure 3). Among them, the largest repeat was a forward repeat with a size of 83 bp. The repetitive sequences of the chloroplast genomes from the six Lonicera species were compared and analyzed. L. macranthoides had palindrome, forward, and reverse repeats, whereas L. japonica cv. Damaohua, L. confusa, L. japonica, L. maackii, and L. insularis presented palindrome and forward repeats. L. japonica cv. Damaohua and L. maackii presented the highest number of forward repeats (68), whereas L. insularis presented the fewest forward repeats (49). L. insularis had the most palindrome repeats (40), whereas L. japonica cv. Damaohua and L. maackii had the same number of palindrome repeats (21 each) (Table S4).

Figure 3 The number of different repeats in the four chloroplast genomes of the six Lonicera species. P = palindromic, F = forward, R = reverse, and C = complement.
Figure 3

The number of different repeats in the four chloroplast genomes of the six Lonicera species. P = palindromic, F = forward, R = reverse, and C = complement.

3.3 Codon usage analysis

The chloroplast genome of L. japonica cv. Damaohua consisted of 51,717 analyzed codons. Among these codons, the most commonly used was UUU (2,132), encoding Phe, and the least commonly used was CGC (254), encoding Arg. There were 31 codons with RSCU values greater than 1 that all ended in A/U, indicating codon usage bias (Figure 4). The RSCU values of the chloroplast genomes of the six Lonicera species slightly differed. The six Loniceraceae species presented the highest frequency of UUU (encoding Phe) in the genome. L. japonica and L. insularis presented the lowest frequency of GCGs (encoding Ala), and L. japonica cv. Damaohua, L. macranthoides, and L. confusa. The least commonly used codon in the L. maackii genome was CGC (encoding Arg). Except Met, all the amino acids are encoded by multiple codons. Leu, Arg, and Ser have six synonymous codons; Ala, Gly, Pro, Thr, and Val have four synonymous codons; Ile, Trp, and stop codons have three synonymous codons; and Cys, Asp, Glu, Phe, His, Lys, Asn, and Gln all have two synonymous codons. In the codon usage bias analysis, L. insularis had 35 codons with RSCU values greater than 1, and L. japonica cv. Damaohua, L. confusa, L. japonica, and L. maackii had 33 codons with RSCU values greater than 1. L. macranthoides had 32 codons with RSCU values greater than 1, and most of the synonymous codons ended in A and U (Table S5).

Figure 4 Codon contents of 20 amino acids and stop codons in all protein-coding genes of the L. japonica cv. Damaohua chloroplast genome. The color in the histogram corresponds to the color of the codons.
Figure 4

Codon contents of 20 amino acids and stop codons in all protein-coding genes of the L. japonica cv. Damaohua chloroplast genome. The color in the histogram corresponds to the color of the codons.

Fifty potential RNA editing sites were found in the chloroplast genome of L. japonica cv. Damaohua (Table S6). The ndhD gene contained the greatest number of RNA editing sites (ten), followed by ndhB with eight editing sites; rpoB with seven editing sites; matK with four editing sites; and ndhA, petB, rpl2, and rps2 with two editing sites. The following genes had one editing site (the lowest number): atpA, atpF, atpI, ccsA, clpP, ndhF, ndhG, psaI, psbE, psbF, rpl20, rpoC2, and rps8. Among the 50 potential RNA editing sites, 10 were observed at the first position of the codon, and 40 were observed at the second position. No potential RNA editing sites were found in the third position, and the base conversion types were all C-to-T. This result is similar to those reported in other land plants. The amino acid conversion from Ser to Leu was the most frequent, whereas the conversion from Leu to Phe was the least frequent.

The RNA editing sites of the chloroplast genomes from the six Lonicera species were different. Among the species, L. insularis had the greatest number of RNA editing sites with 61, followed by L. maackii with 59; and L. japonica with the fewest 48. The accD gene is a potential RNA editing site that was not detected in L. japonica cv. Damaohua, L. vesicaria, or L. macranthoides, and the clpP gene was a potential RNA editing site not detected in L. maackii or L. confusa. The rpoA gene was a potential RNA editing site not detected in L. japonica cv. Damaohua, L. macranthoides, or L. confusa, and rpoC1 was the only potential RNA editing site detected in L. confusa. There were ten genes with no potential RNA editing sites detected, including atpB, petD, petG, petL, psaB, psbB, rpl23, ycf14, ycf16, and ycf3. Among the six potential RNA editing sites in Loniceraceae, most were located in the second position of the codon; no potential RNA editing sites were found in the third position. The base conversion types ranged from C to T, and Ser-to-Leu was the most frequent amino acid conversion.

3.4 Comparison of complete chloroplast genomes among Lonicera species

To characterize the genomic differences, we used the program mVISTA to align the sequences of the six Lonicera species and used the annotations of L. insularis as a reference. The comparison revealed that the chloroplast genomes of the six Lonicera species were highly similar, with very few differences (Figure 5). Compared with the LSC and SSC regions, the IR region presented fewer differences. In addition, the divergent coding regions were smaller than the noncoding regions. Among the coding genes were genes in highly conserved regions, including matK, rpoC2, rpoB, ycf1, and ycf2. In addition, several highly differentiated regions, such as the rpoB-petN, rbcL-accD, and psaA-ycf3 intergenic regions, were identified.

Figure 5 Comparison of the chloroplast genomes of six Lonicera species using the mVISTA program.
Figure 5

Comparison of the chloroplast genomes of six Lonicera species using the mVISTA program.

3.5 Expansion and contraction of the IR region

The IR-LSC and IR-SSC boundaries of the chloroplast genome of L. japonica were compared with those of five reported Lonicera species (Figure 6). The chloroplast genomes of the six Lonicera species were relatively conserved, and the six boundaries of L. japonica cv. Damaohua and L. japonica were similar. The chloroplast genomes of the six Lonicera species were located in the coding region of rpl23 at the LSC/IRa junction. The IRb/SSC connection between IRb and the SSC region (junction of the SSC and IRB [JSB]) was located between the ycf2 and ndhF genes in four species (L. insularis, L. maackii, L. confusa, and L. macranthoides), whereas it was located in the coding area of ndhF in L. japonica cv. Damaohua and L. japonica. The ycf1 gene was located on the IRa/SSC boundary in the six Lonicera species, but the length of the IRa/SSC junction of ycf1 in the SSC and IRa regions was different (L. insularis: 231 bp; L. maackii: 261 bp; L. japonica cv. Damaohua: 220 bp; L. confusa: 195 bp; L. macranthoides: 196 bp; and L. japonica: 220 bp).

Figure 6 Comparison of the borders of the LSC, SSC, and IR regions among the six chloroplast genomes of Lonicera species. (JLB: junction of the LSC and IRB; JSB: junction of the SSC and IRB; JSA: junction of the SSC and IRA; and JLA: junction of the LSC and IRA).
Figure 6

Comparison of the borders of the LSC, SSC, and IR regions among the six chloroplast genomes of Lonicera species. (JLB: junction of the LSC and IRB; JSB: junction of the SSC and IRB; JSA: junction of the SSC and IRA; and JLA: junction of the LSC and IRA).

3.6 Adaptive evolution analysis

TBtools was used to calculate the synonymous (Ks) and nonsynonymous (Ka) substitution rates and Ka/Ks ratios in the chloroplast genomes of the six Lonicera species to detect whether the 74 shared protein-coding genes were under selection pressure (Figure 7). The results revealed that the majority of genes presented Ka/Ks ratios < 1, indicating that the chloroplast genes of Loniceraceae species were subjected to purifying selection during long-term evolution (Table S7). A total of ten positively selected genes (Ka/Ks > 1) were detected in this study. Among them, the infA gene was positively selected in L. japonica cv. Damaohua vs L. insularis; the matK gene was positively selected in L. japonica cv. Damaohua vs L. macranthoides; the petB gene was positively selected in L. japonica cv. Damaohua vs L. confusa; the petD gene was positively selected in L. japonica cv. Damaohua vs L. insularis, and L. japonica cv. Damaohua vs L. maackii; the rbcL gene was positively selected in L. japonica cv. Damaohua vs L. macranthoides; the rpl16 gene was positively selected in L. japonica cv. Damaohua vs L. confusa; the rpl2 gene was positively selected in L. japonica cv. Damaohua vs L. confusa; the rps3 gene was positively selected in L. japonica cv. Damaohua vs L. insularis and L. japonica cv. Damaohua vs L. maackii; the ycf1 gene was positively selected in L. japonica cv. Damaohua vs L. japonica; and the ycf2 gene was positively selected in L. japonica cv. Damaohua vs L. japonica, L. japonica cv. Damaohua vs L. macranthoides and L. japonica cv. Damaohua vs L. maackii. These findings indicate that these genes may have undergone positive selection during evolution.

Figure 7 The Ka/Ks ratios of 74 protein-coding genes from the chloroplast genomes of the six Lonicera species.
Figure 7

The Ka/Ks ratios of 74 protein-coding genes from the chloroplast genomes of the six Lonicera species.

3.7 Phylogenetic analysis

To clarify the phylogenetic positions and evolutionary relationships of Caprifoliaceae, the whole chloroplast genome sequences of 14 species of Caprifoliaceae were selected, and Chrysanthemum boreale was used as the outgroup to construct phylogenetic tree using the ML and BI methods (Figure 8). The ML and BI analysis results show that these two methods are consistent with one another. The chloroplast genome sequences of the 15 plant species were divided into 2 groups. The outgroup C. boreale was a separate group. Triosteum pinnatifidum and 13 Lonicera species were grouped. In Caprifoliaceae, Triosteum and Lonicera were divided into two subgroups. In Lonicera, the chloroplast genome sequence of L. japonica cv. Damaohua had the closest relationship with that of L. japonica, followed by L. confusa and L. macranthoides. The three phylogenetic trees of these 14 chloroplast genome sequences were consistent with traditional taxonomy, indicating that the chloroplast genome can be used to effectively analyze the phylogenetic positions and relationships of species effectively.

Figure 8 Phylogenetic analysis of Lonicera species based on the complete chloroplast genome with (a) ML and (b) BI analysis methods.
Figure 8

Phylogenetic analysis of Lonicera species based on the complete chloroplast genome with (a) ML and (b) BI analysis methods.

3.8 Analysis of variant loci

To further analyze the chloroplast genome differences between L. japonica and L. japonica cv. Damaohua, we used L. japonica as a control to compare the single nucleotide polymorphisms (SNPs) and small insertions/deletions (InDels) among the chloroplast genomes of the six Lonicera species (Table 5). Table 5 shows that there are 2,204 variant sites between L. japonica and L. maackii, including 1,957 SNPs and 247 InDels; there are 2,196 variant sites between L. japonica and L. insularis, including 1,931 SNPs and 265 InDels; and L. japonica and L. japonica cv. Damaohua have extremely high sequence similarity, with only 41 variant sites between them, consisting of 14 SNPs and 27 InDels.

Table 5

SNPs and InDels among the chloroplast genomes of the six Lonicera species

Species L. japonica
LSC SSC IR Total
SNP InDel SNP InDel SNP InDel SNP InDel
L. japonica cv. Damaohua 7 20 7 5 0 2 14 27
L. macranthoides 419 93 105 20 106 8 630 121
L. confusa 49 37 9 9 7 4 65 50
L. maackii 1,187 170 346 38 424 39 1,957 247
L. insularis 1,095 181 406 34 430 50 1,931 265

3.9 Nucleotide diversity analysis

The coding gene regions of L. japonica and L. japonica cv. Damaohua were compared, and different hotspot regions were analyzed by nucleotide variation (Pi) values (Figure 9). We obtained eight different loci (five of these regions were located in the LSC regions and three of these regions were located in the SSC regions) in the chloroplast genomes of L. japonica and L. japonica cv. Damaohua (Pi > 0.001), namely, atpA-atpF, atpF-atpH, rps2-rpoC2, rpoC2-rpoC1, atpB-rbcL, ndhD-ndhE, ycf1, and ycf1-trnN GUU. Four variable sites (Pi > 0.002) were detected between the chloroplast genomes of L. japonica and L. japonica cv. Damaohua, namely, rps2-rpoC2, atpB-rbcL, ycf1, and ycf1-trnN GUU. This finding shows that the IR region is more conserved.

Figure 9 Comparison of the nucleotide variability (Pi) values between L. japonica and L. japonica cv. Damaohua.
Figure 9

Comparison of the nucleotide variability (Pi) values between L. japonica and L. japonica cv. Damaohua.

4 Discussion

Accurate identification of the original species is the first stage in ensuring the quality of herbal medicines [11,12,13]. Owing to the variety of Lonicera japonica Thunb. and the complex original species, the identification of the original Lonicera japonica Thunb. species has not been effectively solved, which makes the protection of Lonicera japonica Thunb. germplasm resources and the safe use of medicinal materials inconvenient. DNA barcoding technology is stable and objective because it is not affected by environmental factors, tissue types, or developmental stages. However, DNA barcoding is often unable to distinguish among closely related species, which limits its application in species identification. The chloroplast genome contains more variation and the phylogenetic resolution is significantly greater, which is valuable for revealing phylogenetic relationships between closely related species [17,18]. In this study, the feasibility of a plant identification method based on the chloroplast genome was validated. There were some differences in the genome size and LSC, SSC, and IR regions among the six chloroplast genomes of Loniceraceae, and the number of genes and GC content were similar, reflecting the high degree of conservation of angiosperm chloroplast genomes to some extent [47,48,49]. The GC contents of the chloroplast genomes of the six Lonicera species were similar, ranging from 38.3 to 38.6%, and the genome size and IR, LSC, and SSC region lengths and gene contents were highly similar across the chloroplast genomes, indicating that the gene structure of Lonicera was highly conserved.

Introns play important roles in RNA stability, gene expression regulation, and alternative splicing, which have been reported in many other species [50]. He et al. reported that the ycf3 gene and the rps18 gene contained two introns in L. japonica [2]. In this study, the ycf3 gene included two introns and rps18 had only one intron in the chloroplast genome of L. japonica cv. Damaohua. The ycf3 gene is necessary for the accumulation of the photosystem I (PSI) complex and acts as a chaperone that interacts with the PSI subunit at the posttranslational level [51]. This finding revealed a large amount of intron gain and/or intron loss during the evolution of Loniceraceae [52].

Comparative analysis of chloroplast genomes is an important method for deep investigation of complex evolutionary [53,54]. The mVISTA program was used to analyze the differences in the chloroplast genomes of the six Lonicera species. The comparison revealed that the chloroplast genomes of Lonicera species were highly conserved, but there was a certain degree of variation. The coding region was more conserved than the noncoding region, the IR region was more conserved than the LSC and SSC regions, and there were more variations in the latter two regions than in other regions. Similar findings have been reported in the chloroplast genomes of certain genera in previous studies [11,55,56]. The mutation levels of the matK, rpoC2, rpoB, ycf1, and ycf2 genes were slightly lower, while the mutation levels of the rpoB-petN, rbcL-accD, and psaA-ycf3 gene regions were quite different. These regions are sources of potential barcodes for the identification of Lonicera species. Owing to its standardization, minimization, and scalability, DNA barcoding has become an extremely widely used technique in molecular marker-based species identification. At present, DNA barcoding technology has also made some progress in the identification of honeysuckle medicinal plants. These six divergence hotspot regions (trnH-GUG-psbA, rps2-rpoC2, rbcL-psaI, trnN-GUU-ndhF, rps15-ycf1, and infA) should be applied to the development of molecular markers in Lonicera species. Studies have shown that the species identification efficiency of DNA barcoding was closely related to the species selected and the quantity. In this study, rpoB-petN, rbcL-accD, and psaA-ycf3 gene regions were highly obvious. These markers were potential barcode candidate gene. And these DNA barcoding candidate genes have also been identified in other species. The rpoB-petN can be used as DNA barcode for the identification of Sanicula L. [57]. The rbcL-accD was used for the identification of the Fritillaria germplasm resources [58]. Several studies have verified the use of hotspot regions of the chloroplast genome for identifying species. Sequencing results proved that psaA-ycf3 can be used as a specific DNA barcode to accurately identify Zizania spp. [59], Fosbergia [60], Streptocarpus ionanthus [61], and Fertile Lycoris [62]. The divergent regions of rbcL-accD and psaA-ycf3 were highly obvious, which could be used as DNA barcodes for the taxonomic evidence of Stellaria dichotoma [63]. In this study, these potential barcodes require further experimental validation.

Ka/Ks analysis is an effective method for assessing whether the functions of protein-coding genes have evolved. Synonymous nucleotide substitutions occur more frequently than nonsynonymous substitutions for most genes, so the Ka/Ks value is usually less than 1 [64,65,66]. A total of ten positively selected genes (including infA, matK, petB, petD, rbcL, rpl16, rpl2, rps3, ycf1, and ycf2) were detected in this study. This finding indicates that most of the Lonicera genes are under negative selection and that only ten genes have undergone positive selection. These ten genes included two subunits of cytochrome b/f complex genes (petB and petD), two large subunit of ribosome genes (rpl16 and rpl2), subunit of rubisco gene (rbcL), translational initiation factor gene (infA), maturase gene (matK), and ycf1 and ycf2. The petB encodes a protein containing S1 domain in photosynthetic electron transfer B, which is associated with in the stability and translation of chloroplast mRNAs [67]. The petD constitutes a subunit of cytochrome b/f complex, which is critical to electron flow. It is useful to noting that in the response of plants to drought stress, half of the chloroplasts revealed a decrease in petD [68]. The rpl16 and rpl2 genes encode ribosomal proteins, which are indispensable for chloroplast translation devices [69]. The rbcL gene encodes the Rubisco subunit. Rubisco catalyzes the assimilation of carbon dioxide in the atmosphere during photosynthesis. Positive selection of rbcL is quite common in terrestrial plants [70]. The positive selection of rbcL in Lonicera species is linked to adaptation to low carbon dioxide concentrations in high-altitude environments. The infA are genes involved in photosynthesis, responsible for encoding and translating starting factors. The infA gene was absent in the chloroplast genome of some plant, which may be involved in the transfer of functional genes to the nuclear genome, leading to their replacement by nuclear-encoded proteins [69,71,72]. The saturation enzyme K protein, encoded by the matK gene, is the only recognized group II intrinsic maturation enzyme in chloroplast genome. The mature enzyme matK is required to split its own and other group II introns and plays a role in photosynthesis and plant development. The products encoded by the genes ycf1 and ycf2, which are essential in the chloroplast genome of higher plants, are indispensable for cell survival [70]. Among these genes, ycf2 presented Ka/Ks values > 1 in three of the species, indicating that this gene has recently undergone evolution. Ycf2 is a gene with a coding region in the chloroplast genome. The function of its encoded product is still unclear. The ycf2 gene is positively selected in many plants. It has been speculated that this gene plays an important role in the adaptation of terrestrial plants to environmental changes. Therefore, this positively selected gene in L. japonica cv. Damaohua may help this cultivar to adapt its specific environment.

The phylogenetic tree constructed based on the complete chloroplast genome has greater support and discrimination ability. The use of the complete chloroplast genome as a super-barcode to accurately identify closely related species in an accurate manner is therefore proposed [17,18]. In this study, we found that the L. japonica cv. Damaohua chloroplast genome was most closely related to that of the previously reported L. japonica, but there were some clear differences between them. The first difference was the chloroplast genome size and the number of encoded proteins. The L. japonica chloroplast genome is 155,078 bp in length and contains 84 protein-coding genes. The chloroplast genome of L. japonica cv. Damaohua is 155,151 bp in length and includes 80 protein-coding genes. The second difference was the number of genes that had two introns. L. japonica cv. Damaohua contains only one gene (ycf3), whereas L. japonica contains two genes (rps18 and ycf3). The third difference was the difference in the number of SSRs. L. japonica cv. Damaohua found 54 SSRs. In L. japonica, 47 SSRs were found. The fourth difference was that the ycf1 and ycf2 genes were positively selected in L. japonica cv. Damaohua vs L. japonica. The fifth difference was that there were 14 SNPs and 27 InDels that differed between L. japonica and L. japonica cv. Damaohua. The chloroplast genome is characterized by maternal inheritance and is highly conserved in composition and sequence. These results suggest that L. japonica cv. Damaohua and L. japonica are different, and that they may be related species. The chloroplast genome can be used to effectively discriminate among intraspecific variations effectively in L. japonica from related species. The super-barcode is a useful complement to current molecular identification methods. These findings provide an important basis for determining the evolutionary and phylogenetic relationships of medicinal plants in the Lonicera species.

The chloroplast genome contains a large amount of genetic information and has become a powerful tool for species identification and phylogenetic research on medicinal plants [48,49,52,53,54]. Compared with the commonly used DNA barcode fragments, the chloroplast genome can provide more informative loci [61,62,63]. In this study, the complete chloroplast genome of L. japonica cv. Damaohua was obtained using Illumina sequencing assembly and those of five other species of honeysuckle SNP sites were screened and identified SNP sites, and further established molecular identification methods for related species were established. Among them, four different mutation hotspots (rps2-rpoC2, atpB-rbcL, ycf1, and ycf1-trnN GUU) with high nucleotide variability (Pi > 0.002) could serve as a new and unique DNA barcode for honeysuckle and its related species. Because of the increasing demands for Lonicera japonica in the herbal market, quality control has become an important issue for this variety [1,11,18]. Thus, an authentic DNA marker to identify these species could be utilized to prevent adulteration or abuse other Lonicera species. Therefore, we hope to develop more DNA markers and establish a practical Lonicera species authentication system. Based on the results of this study, the next step is to develop a DNA barcoding method for the identification of Lonicera and its related species.

The availability of the complete L. japonica cv. Damaohua chloroplast genome provides sequence information that can be used to confirm the phylogenetic location of L. japonica cv. Damaohua and understand phylogenetic relationships between Loniceraceae species. However, since we used only a few species in the Loniceraceae family, we should further study other chloroplast genomes and nuclear genome sequences of Lonicera species to provide more sufficient evidence to explain the evolutionary process of Caprifoliaceae accurately.

5 Conclusion

In this study, the chloroplast genome of L. japonica cv. Damaohua was sequenced and assembled, providing a valuable genome resource for Lonicera. A comparative analysis of L. japonica cv. Damaohua and its relatives revealed that the chloroplast genomes of the six Lonicera species were highly similar, with very few differences. Compared with the LSC and SSC regions, the IR region presented fewer differences. In addition, the divergent coding regions were smaller than the noncoding regions. Phylogenetic analysis of the chloroplast genome revealed that L. japonica cv. Damaohua and L. japonica had a close intra-genus relationship, but there were five distinct differences between the two. Four sites with high variability with a nucleotide variability (Pi) greater than 0.002 between L. japonica and L. japonica cv. Damaohua, including rps2-rpoC2, atpB-rbcL, ycf1, and ycf1-trnN GUU were located. These different SNP sites between these two species further confirmed the differences between the species. These results suggest that the chloroplast genome can be used to discriminate intraspecific variation in L. japonica from related species effectively. This finding also verifies the feasibility of using the chloroplast genome as a super-barcode to identify L. japonica and related species. These findings provide a basis for future research on the genetic resource development, species identification and conservation biology of Lonicera.

  1. Funding information: This work was supported by the Demonstration and Promotion Project of New Scientific and Technological Achievements from Zhejiang Academy of Agricultural Sciences in 2021 (No. tg2021009), the Program of Cooperation between Zhejiang Academy of Agricultural Sciences and Pujiang County (No. PJ202104), the Program of Cooperation between Zhejiang Academy of Agricultural Sciences and Wuyi County (No. 2023R25A77C01), and Major Science and Technology Program of Xiaoshan District (No. 2020219).

  2. Author contributions: Jiaqiang Zhang and Kaiyuan Zhu conceived and designed the experiments; Jiaqiang Zhang and Huichun Liu performed the experiments; Wenting Xu and Xiao Wan performed the data analysis; Jiaqiang Zhang prepared the manuscript; Wenting Xu and Kaiyuan Zhu performed the proofreading. All the authors approved the manuscript.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

  5. Supplementary information: Supplementary Table S1. Genes present in the chloroplast genome of Lonicera japonica cv. Damaohua. Supplementary Table S2. The total number of perfect simple sequence repeats (SSRs) identified within the chloroplast genomes of the six Lonicera species. Supplementary Table S3. Distribution pattern and the number of simple sequence repeats (SSRs) identified within the Lonicera chloroplast genome. Supplementary Table S4. Long repeat sequences in the chloroplast genomes of the six Lonicera species. Supplementary Table S5. Codon usage for the chloroplast genomes of the six Lonicera species. Supplementary Table S6. RNA editing sites of the chloroplast genomes of the six Lonicera species. Supplementary Table S7. Ka/Ks ratios of protein-coding sequences between pairs of species among the six Lonicera species.

References

[1] Kang KB, Kang SJ, Kim MS, Lee DY, Han SI, Kim TB, et al. Chemical and genomic diversity of six Lonicera species occurring in Korea. Phytochemistry. 2018;155:126–35.10.1016/j.phytochem.2018.07.012Suche in Google Scholar PubMed

[2] He L, Qian J, Li X, Sun Z, Xu X, Chen S. Complete chloroplast genome of medicinal plant Lonicera japonica: genome rearrangement, intron gain and loss, and implications for phylogenetic studies. Molecules. 2017;22:249.10.3390/molecules22020249Suche in Google Scholar PubMed PubMed Central

[3] Shang XF, Pan H, Li MX, Miao XL, Ding H. Lonicera japonica Thunb.: ethnopharmacology, phytochemistry and pharmacology of an important traditional Chinese medicine. J Ethnopharmacol. 2011;138:1–21.10.1016/j.jep.2011.08.016Suche in Google Scholar PubMed PubMed Central

[4] Chinese Pharmacopoeia Commission. Pharmacopoeia of the People’s Republic of China. 32, 230 (China Medical Science Press: Beijing, China, 2020).Suche in Google Scholar

[5] Li Y, Li W, Fu C, Song Y, Fu Q. Lonicerae japonicae flos and Lonicerae flos: a systematic review of ethnopharmacology, phytochemistry and pharmacology. Phytochem Rev. 2020;22:1–61.10.1007/s11101-019-09655-7Suche in Google Scholar PubMed PubMed Central

[6] Cai Z, Wang C, Chen C, Zou L, Chai C, Chen J, et al. Quality evaluation of Lonicerae Japonicae Flos and Lonicerae Flos based on simultaneous determination of multiple bioactive constituents combined with multivariate statistical analysis. Phytochem Anal. 2021;32(2):129–40.10.1002/pca.2882Suche in Google Scholar PubMed PubMed Central

[7] Yan R, Chen JB, Sun SQ, Guo BL. Rapid identification of Lonicerae japonicae Flos and Lonicerae Flos by Fourier transform infrared (FT-IR) spectroscopy and two-dimensional correlation analysis. J Mol Struct. 2016;1124:110–6.10.1016/j.molstruc.2016.03.039Suche in Google Scholar

[8] Liu ML, Fan WB, Wang N, Dong PB, Zhang TT, Yue M, et al. Evolutionary analysis of plastid genomes of seven Lonicera L. Species: implications for sequence divergence and phylogenetic relationships. Int J Mol Sci. 2018;19(12):4039.10.3390/ijms19124039Suche in Google Scholar PubMed PubMed Central

[9] Xiong L, Zhao H, Wang Y, Liu Y, Jin Y, Zhang L, et al. Study on phenolic acids of Lonicerae japonicae Flos based on ultrahigh performance liquid chromatography-tandem mass spectrometry combined with multivariate statistical analysis. J Sep Sci. 2022;45(13):2239–51.10.1002/jssc.202100973Suche in Google Scholar PubMed

[10] Li JJ, Lian XY, Ye CL, Wang L. Analysis of flower color variations at different developmental stages in two honeysuckle (Lonicera Japonica Thunb.) cultivars. Hortscience. 2019;54:779–82.10.21273/HORTSCI13819-18Suche in Google Scholar

[11] Liang C, Wang L, Lei J, Duan B, Ma W, Xiao S, et al. A comparative analysis of the chloroplast genomes of four salvia medicinal plants. Engineering. 2019;5:907–15.10.1016/j.eng.2019.01.017Suche in Google Scholar

[12] Gao C, Wu C, Zhang Q, Zhao X, Wu M, Chen R, et al. Characterization of chloroplast genomes from two salvia medicinal plants and gene transfer among their mitochondrial and chloroplast genomes. Front Genet. 2020;11:574962.10.3389/fgene.2020.574962Suche in Google Scholar PubMed PubMed Central

[13] Yik MH, Kong BL, Siu TY, Lau DT, Cao H, Shaw PC. Differentiation of Hedyotis diffusa and Common adulterants based on chloroplast genome sequencing and DNA barcoding markers. Plants. 2021;10:161.10.3390/plants10010161Suche in Google Scholar PubMed PubMed Central

[14] GuisingerTimothy MM, Chumley TW, Kuehl JV, Boore JL, Jansen RK. Implications of the plastid genome sequence of typha (Typhaceae, Poales) for understanding genome evolution in Poaceae. J Mol Evol. 2010;70:149–66.10.1007/s00239-009-9317-3Suche in Google Scholar PubMed PubMed Central

[15] Pu X, Li Z, Tian Y, Gao R, Hao L, Hu Y, et al. The honeysuckle genome provides insight into the molecular mechanism of carotenoid metabolism underlying dynamic flower coloration. N Phytol. 2020;227:930–43.10.1111/nph.16552Suche in Google Scholar PubMed PubMed Central

[16] Huang DI, Hefer CA, Kolosova N, Douglas CJ, Cronk QC. Whole plastome sequencing reveals deep plastid divergence and cytonuclear discordance between closely related balsam poplars, Populus balsamifera and P. trichocarpa (Salicaceae). N Phytol. 2014;204:693–703.10.1111/nph.12956Suche in Google Scholar PubMed

[17] Li X, Yang Y, Henry RJ, Rossetto M, Wang Y, Chen S. Plant DNA barcoding: From gene to genome. Biol Rev. 2015;90:157–66.10.1111/brv.12104Suche in Google Scholar PubMed

[18] Chen X, Li W, Lu X, Tran LSP, Alolga RN, Yin X. Research progress on the biosynthesis, metabolic engineering, and pharmacology of bioactive compounds from the Lonicera genus. Med Plant Biol. 2024;3:e008.10.48130/mpb-0024-0008Suche in Google Scholar

[19] Martin AE, Gisby MF, Day A. Seamless editing of the chloroplast genome in plants. BMC Plant Biol. 2016;16:168.10.1186/s12870-016-0857-6Suche in Google Scholar PubMed PubMed Central

[20] Dobrogojski J, Adamiec M, Luciński R. The chloroplast genome: a review. Acta Physiol Plant. 2020;42:98.10.1007/s11738-020-03089-xSuche in Google Scholar

[21] Freudenthal JA, Pfaff S, Terhoeven N, Korte A, Ankenbrand MJ, Förster F. A systematic comparison of chloroplast genome assembly tools. Genome Biol. 2020;21:254.10.1186/s13059-020-02153-6Suche in Google Scholar PubMed PubMed Central

[22] Jansen RK, Wojciechowski MF, Sanniyasi E, Lee SB, Daniell H. Complete plastid genome sequence of the chickpea (Cicer arietinum) and the phylogenetic distribution of rps12 and clpP intron losses among legumes (Leguminosae). Mol Phylogenet Evol. 2008;48:1204–17.10.1016/j.ympev.2008.06.013Suche in Google Scholar PubMed PubMed Central

[23] Dhafer AA, Samaila SY, Enas JA, Abidina A. Complete chloroplast genome sequence of Barleria prionitis, Comparative chloroplast genomics and phylogenetic relationships among Acanthoideae. BMC Genom. 2020;21:393.10.1186/s12864-020-06798-2Suche in Google Scholar PubMed PubMed Central

[24] Alzahrani DA. Complete chloroplast genome of abutilon fruticosum: genome structure, comparative and phylogenetic analysis. Plants. 2021;10:270.10.3390/plants10020270Suche in Google Scholar PubMed PubMed Central

[25] Jiang W, Tan W, Gao H, Yu X, Zhang H, Bian Y, et al. Transcriptome and complete chloroplast genome of Glycyrrhiza inflata and comparative analysis with the other two licorice species. Genomics. 2020;112:4179–88.10.1016/j.ygeno.2020.07.007Suche in Google Scholar PubMed

[26] Jia G, Wang H, Yu P, Li P. The complete chloroplast genome of the Lonicera maackii (Caprifoliaceae), an ornamental plant. Mitochondrial DNA B Resour. 2020;5:560–1.10.1080/23802359.2019.1710288Suche in Google Scholar PubMed PubMed Central

[27] Luo J. Characterization of the complete chloroplast genome of Lonicera japonica (Caprifoliaceae), a long history herb species plant from China. Mitochondrial DNA B Resour. 2019;4:3936–7.10.1080/23802359.2019.1687353Suche in Google Scholar PubMed PubMed Central

[28] Porebski S, Bailey LG, Baum BR. Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Rep. 1997;15:8–15.10.1007/BF02772108Suche in Google Scholar

[29] Sena D, Brandine G, Smith AD. Falco: high-speed FastQC emulation for quality control of sequencing data. F1000Research. 2019;8:1874.10.12688/f1000research.21142.1Suche in Google Scholar

[30] Dierckxsens N, Mardulyn P, Smits G. NOVOPlasty: De novo assembly of organelle genomes from whole genome data. Nucleic Acids Res. 2016;45:e18.10.1093/nar/gkw955Suche in Google Scholar PubMed PubMed Central

[31] Shi L, Chen H, Jiang M, Wang L, Wu X, Huang L, et al., CPGAVAS2, an integrated plastome sequence annotator and analyzer. Nucleic Acids Res. 2019;47:W65–73.10.1093/nar/gkz345Suche in Google Scholar PubMed PubMed Central

[32] Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28(1):27–30.10.1093/nar/28.1.27Suche in Google Scholar PubMed PubMed Central

[33] Kanehisa M. Toward understanding the origin and evolution of cellular organisms. Protein Sci. 2019;28(11):1947–51.10.1002/pro.3715Suche in Google Scholar PubMed PubMed Central

[34] Kanehisa M, Furumichi M, Sato Y, Ishiguro-Watanabe M, Tanabe M. KEGG: integrating viruses and cellular organisms. Nucleic Acids Res. 2021;49(D1):D545–51.10.1093/nar/gkaa970Suche in Google Scholar PubMed PubMed Central

[35] Beier S, Thiel T, Munch T, Scholz U, Mascher M. MISA-web: A web server for microsatellite prediction. Bioinformatics. 2017;33:2583–5.10.1093/bioinformatics/btx198Suche in Google Scholar PubMed PubMed Central

[36] Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R. REPuter: The manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 2001;29:4633–42.10.1093/nar/29.22.4633Suche in Google Scholar PubMed PubMed Central

[37] Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–9.10.1093/molbev/mst197Suche in Google Scholar PubMed PubMed Central

[38] Mower JP. The PREP suite: Predictive RNA editors for plant mitochondrial genes, chloroplast genes and user-defined alignments. Nucleic Acids Res. 2009;37:253–9.10.1093/nar/gkp337Suche in Google Scholar PubMed PubMed Central

[39] Amiryousefi A, Hyvonen J, Poczai P. IRscope: An online program to visualize the junction sites of chloroplast genomes. Bioinformatics. 2018;34:3030–1.10.1093/bioinformatics/bty220Suche in Google Scholar PubMed

[40] Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: Computational tools for comparative genomics. Nucleic Acids Res. 2004;32:273–9.10.1093/nar/gkh458Suche in Google Scholar PubMed PubMed Central

[41] Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, et al. TBtools: An integrative toolkit developed for interactive analysis of big biological data. Mol Plant. 2020;13:1194–202.10.1016/j.molp.2020.06.009Suche in Google Scholar PubMed

[42] Yang Z, Nielsen R. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol. 2002;19(6):908–17.10.1093/oxfordjournals.molbev.a004148Suche in Google Scholar PubMed

[43] Katoh K, Rozewicki J, Yamada KD. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2017;20:1160–6.10.1093/bib/bbx108Suche in Google Scholar PubMed PubMed Central

[44] Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12):1572–4.10.1093/bioinformatics/btg180Suche in Google Scholar PubMed

[45] Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analysis with thousands of taxa and mixed models. Bioinformatics. 2006;22(21):2688–90.10.1093/bioinformatics/btl446Suche in Google Scholar PubMed

[46] Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25(11):1451–2.10.1093/bioinformatics/btp187Suche in Google Scholar PubMed

[47] Greiner S, Sobanski J, Bock R. Why are most organelle genomes transmitted maternally? BioEssays. 2015;37:80–94.10.1002/bies.201400110Suche in Google Scholar PubMed PubMed Central

[48] WickeGerald S, Schneeweiss GM, Depamphilis CW, Müller KF, Quandt D. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol. 2011;76:273–97.10.1007/s11103-011-9762-4Suche in Google Scholar PubMed PubMed Central

[49] Li Y, Dong Y, Liu Y, Yu X, Yang M, Huang Y. Comparative analysis of euonymus chloroplast genomes: genetic structure, screening for loci with suitable polymorphism, positive selection genes, and phylogenetic relationships within celastrineae. Front Plant Sci. 2021;11:593984.10.3389/fpls.2020.593984Suche in Google Scholar PubMed PubMed Central

[50] Nguyen Dinh S, Sai TZT, Nawaz G, Lee K, Kang H. Abiotic stresses affect differently the intron splicing and expression of chloroplast genes in coffee plants (Coffea arabica) and rice (Oryza sativa). J Plant Physiol. 2016;201:85–94.10.1016/j.jplph.2016.07.004Suche in Google Scholar PubMed

[51] Naver H, Boudreau E, Rochaix JD. Functional studies of YCF3: Its role in assembly of photosystem I and Interactions with some of its subunits. Plant Cell. 2002;13:2731–45.10.1105/tpc.010253Suche in Google Scholar PubMed PubMed Central

[52] Fan WB, Wu Y, Yang J, Shahzad K, Li ZH. Comparative chloroplast genomics of dipsacales species: insights into sequence variation, adaptive evolution, and phylogenetic relationships. Front Plant Sci. 2018;9:689.10.3389/fpls.2018.00689Suche in Google Scholar PubMed PubMed Central

[53] Dong F, Lin Z, Lin J, Ming R, Zhang W. Chloroplast genome of rambutan and comparative analysis in Sapindaceae. Plants. 2021;10:283.10.3390/plants10020283Suche in Google Scholar PubMed PubMed Central

[54] Jiang D, Zhao Z, Zhang T, Zhong W, Liu C, Yuan Q, et al. The chloroplast genome sequence of scutellaria baicalensis provides insight into intraspecific and interspecific chloroplast genome diversity in scutellaria. Genes. 2017;8:227.10.3390/genes8090227Suche in Google Scholar PubMed PubMed Central

[55] Zhao K, Li L, Quan H, Yang J, Zhang Z, Liao Z, et al. Comparative analysis of chloroplast genomes from 14 Zanthoxylum species: identification of variable DNA markers and phylogenetic relationships within the Genus. Front Plant Sci. 2021;11:605793.10.3389/fpls.2020.605793Suche in Google Scholar PubMed PubMed Central

[56] Liu H, Su Z, Yu S, Liu J, Yin X, Zhang G, et al. Genome comparison reveals mutation hotspots in the chloroplast genome and phylogenetic relationships of Ormosia Species. Biomed Res Int. 2019;2019:7265030.10.1155/2019/7265030Suche in Google Scholar PubMed PubMed Central

[57] Song W, Ji C, Chen Z, Cai H, Wu X, Shi C, et al. Comparative analysis the complete chloroplast genomes of nine musa species: genomic features, comparative analysis, and phylogenetic implications. Front Plant Sci. 2022;13:832884.10.3389/fpls.2022.832884Suche in Google Scholar PubMed PubMed Central

[58] Huang J, Yu Y, Liu YM, Xie DF, He XJ, Zhou SD. Comparative chloroplast genomics of fritillaria (Liliaceae), inferences for phylogenetic relationships between fritillaria and lilium and plastome evolution. Plants. 2020;9:133.10.3390/plants9020133Suche in Google Scholar PubMed PubMed Central

[59] Lu R, Chen M, Feng Y, Yuan N, Zhang Y, Cao M. Comparative plastome analyses and genomic resource development in wild rice (Zizania spp., Poaceae) using genome skimming data. Ind Crop Prod. 2022;186:115244.10.1016/j.indcrop.2022.115244Suche in Google Scholar

[60] Chen L, Zhu W, Song Y, Zhou Q, Li H. Complete chloroplast genome sequences of endangered tropical fosbergia species (Family: Rubiaceae). Forests. 2024;15:1150.10.3390/f15071150Suche in Google Scholar

[61] Kyalo CM, Li ZZ, Mkala EM, Malombe I, Hu GW, Wang QF. The first glimpse of streptocarpus ionanthus (Gesneriaceae) phylogenomics: analysis of five subspecies’ chloroplast genomes. Plants. 2020;9:456.10.3390/plants9040456Suche in Google Scholar PubMed PubMed Central

[62] Liu K, Sun L, Meng W, Zhu H, Zhang D, Wang J. Comparative genomics and phylogenetic perspectives of six fertile Lycoris species endemic to East Asia based on plastome characterization. Nord J Bot. 2022;4:e03412.10.1111/njb.03412Suche in Google Scholar

[63] Liu W, Qiu K, Huang Y, Li Y, Zhang S. Molecular organization of the chloroplast genome and taxonomic position of Stellaria dichotoma var. lanceolate. Cytol Genet. 2023;57:174–85.10.3103/S0095452723020081Suche in Google Scholar

[64] Guo X, Liu J, Hao G, Zhang L, Mao K, Wang X, et al. Plastome phylogeny and early diversification of Brassicaceae. BMC Genom. 2017;18:176.10.1186/s12864-017-3555-3Suche in Google Scholar PubMed PubMed Central

[65] Yang Z, Nielsen R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol. 2000;17:32–43.10.1093/oxfordjournals.molbev.a026236Suche in Google Scholar PubMed

[66] Yin K, Zhang Y, Li Y, Du FK. Different natural selection pressures on the atpF gene in evergreen sclerophyllous and deciduous oak species: evidence from comparative analysis of the complete chloroplast genome of quercus aquifolioides with other Oak species. Int J Mol Sci. 2018;19(4):1042.10.3390/ijms19041042Suche in Google Scholar PubMed PubMed Central

[67] Li DM, Pan YG, Liu HL, Yu B, Huang D, Zhu GF. Thirteen complete chloroplast genomes of the costaceae family: insights into genome structure, selective pressure and phylogenetic relationships. BMC Genom. 2024;25(1):68.10.1186/s12864-024-09996-4Suche in Google Scholar PubMed PubMed Central

[68] Lee K. Relocation of chloroplast proteins from cytosols into chloroplasts. Plant Signal Behav. 2023;18(1):2258321.10.1080/15592324.2023.2258321Suche in Google Scholar PubMed PubMed Central

[69] Liu X, Bai Y, Wang Y, Chen Y, Dong W, Zhang Z. Complete chloroplast genome of hypericum perforatum and dynamic evolution in Hypericum (Hypericaceae). Int J Mol Sci. 2023;24:16130.10.3390/ijms242216130Suche in Google Scholar PubMed PubMed Central

[70] Li QQ, Zhang ZP, Aogan, Wen J. Comparative chloroplast genomes of argentina species: genome evolution and phylogenomic implications. Front Plant Sci. 2024;15:1349358.10.3389/fpls.2024.1349358Suche in Google Scholar PubMed PubMed Central

[71] Yan M, Dong S, Gong Q, Xu Q, Ge Y. Comparative chloroplast genome analysis of four polygonatum species insights into DNA barcoding, evolution, and phylogeny. Sci Rep. 2023;13(1):16495.10.1038/s41598-023-43638-1Suche in Google Scholar PubMed PubMed Central

[72] Wang Y, Xie Y, Jin J, Li J, Qiu X, Tong Y, et al. Comparison of the chloroplast genomes and phylogenomic analysis of Elaeocarpaceae. PeerJ. 2023;11:e15322.10.7717/peerj.15322Suche in Google Scholar PubMed PubMed Central

Received: 2024-05-24
Revised: 2024-09-13
Accepted: 2024-09-18
Published Online: 2024-11-11

© 2024 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

Artikel in diesem Heft

  1. Biomedical Sciences
  2. Constitutive and evoked release of ATP in adult mouse olfactory epithelium
  3. LARP1 knockdown inhibits cultured gastric carcinoma cell cycle progression and metastatic behavior
  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
  5. Research progress on ocular complications caused by type 2 diabetes mellitus and the function of tears and blepharons
  6. The role and mechanism of esketamine in preventing and treating remifentanil-induced hyperalgesia based on the NMDA receptor–CaMKII pathway
  7. Brucella infection combined with Nocardia infection: A case report and literature review
  8. Detection of serum interleukin-18 level and neutrophil/lymphocyte ratio in patients with antineutrophil cytoplasmic antibody-associated vasculitis and its clinical significance
  9. Ang-1, Ang-2, and Tie2 are diagnostic biomarkers for Henoch-Schönlein purpura and pediatric-onset systemic lupus erythematous
  10. PTTG1 induces pancreatic cancer cell proliferation and promotes aerobic glycolysis by regulating c-myc
  11. Role of serum B-cell-activating factor and interleukin-17 as biomarkers in the classification of interstitial pneumonia with autoimmune features
  12. Effectiveness and safety of a mumps containing vaccine in preventing laboratory-confirmed mumps cases from 2002 to 2017: A meta-analysis
  13. Low levels of sex hormone-binding globulin predict an increased breast cancer risk and its underlying molecular mechanisms
  14. A case of Trousseau syndrome: Screening, detection and complication
  15. Application of the integrated airway humidification device enhances the humidification effect of the rabbit tracheotomy model
  16. Preparation of Cu2+/TA/HAP composite coating with anti-bacterial and osteogenic potential on 3D-printed porous Ti alloy scaffolds for orthopedic applications
  17. Aquaporin-8 promotes human dermal fibroblasts to counteract hydrogen peroxide-induced oxidative damage: A novel target for management of skin aging
  18. Current research and evidence gaps on placental development in iron deficiency anemia
  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
  22. Sirtuin 5 regulates acute myeloid leukemia cell viability and apoptosis by succinylation modification of glycine decarboxylase
  23. Apigenin 7-glucoside impedes hypoxia-induced malignant phenotypes of cervical cancer cells in a p16-dependent manner
  24. KAT2A changes the function of endometrial stromal cells via regulating the succinylation of ENO1
  25. Current state of research on copper complexes in the treatment of breast cancer
  26. Exploring antioxidant strategies in the pathogenesis of ALS
  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
  28. IL-33/soluble ST2 axis is associated with radiation-induced cardiac injury
  29. The predictive value of serum NLR, SII, and OPNI for lymph node metastasis in breast cancer patients with internal mammary lymph nodes after thoracoscopic surgery
  30. Carrying SNP rs17506395 (T > G) in TP63 gene and CCR5Δ32 mutation associated with the occurrence of breast cancer in Burkina Faso
  31. P2X7 receptor: A receptor closely linked with sepsis-associated encephalopathy
  32. Probiotics for inflammatory bowel disease: Is there sufficient evidence?
  33. Identification of KDM4C as a gene conferring drug resistance in multiple myeloma
  34. Microbial perspective on the skin–gut axis and atopic dermatitis
  35. Thymosin α1 combined with XELOX improves immune function and reduces serum tumor markers in colorectal cancer patients after radical surgery
  36. Highly specific vaginal microbiome signature for gynecological cancers
  37. Sample size estimation for AQP4-IgG seropositive optic neuritis: Retinal damage detection by optical coherence tomography
  38. The effects of SDF-1 combined application with VEGF on femoral distraction osteogenesis in rats
  39. Fabrication and characterization of gold nanoparticles using alginate: In vitro and in vivo assessment of its administration effects with swimming exercise on diabetic rats
  40. Mitigating digestive disorders: Action mechanisms of Mediterranean herbal active compounds
  41. Distribution of CYP2D6 and CYP2C19 gene polymorphisms in Han and Uygur populations with breast cancer in Xinjiang, China
  42. VSP-2 attenuates secretion of inflammatory cytokines induced by LPS in BV2 cells by mediating the PPARγ/NF-κB signaling pathway
  43. Factors influencing spontaneous hypothermia after emergency trauma and the construction of a predictive model
  44. Long-term administration of morphine specifically alters the level of protein expression in different brain regions and affects the redox state
  45. Application of metagenomic next-generation sequencing technology in the etiological diagnosis of peritoneal dialysis-associated peritonitis
  46. Clinical diagnosis, prevention, and treatment of neurodyspepsia syndrome using intelligent medicine
  47. Case report: Successful bronchoscopic interventional treatment of endobronchial leiomyomas
  48. Preliminary investigation into the genetic etiology of short stature in children through whole exon sequencing of the core family
  49. Cystic adenomyoma of the uterus: Case report and literature review
  50. Mesoporous silica nanoparticles as a drug delivery mechanism
  51. Dynamic changes in autophagy activity in different degrees of pulmonary fibrosis in mice
  52. Vitamin D deficiency and inflammatory markers in type 2 diabetes: Big data insights
  53. Lactate-induced IGF1R protein lactylation promotes proliferation and metabolic reprogramming of lung cancer cells
  54. Meta-analysis on the efficacy of allogeneic hematopoietic stem cell transplantation to treat malignant lymphoma
  55. Mitochondrial DNA drives neuroinflammation through the cGAS-IFN signaling pathway in the spinal cord of neuropathic pain mice
  56. Application value of artificial intelligence algorithm-based magnetic resonance multi-sequence imaging in staging diagnosis of cervical cancer
  57. Embedded monitoring system and teaching of artificial intelligence online drug component recognition
  58. Investigation into the association of FNDC1 and ADAMTS12 gene expression with plumage coloration in Muscovy ducks
  59. Yak meat content in feed and its impact on the growth of rats
  60. A rare case of Richter transformation with breast involvement: A case report and literature review
  61. First report of Nocardia wallacei infection in an immunocompetent patient in Zhejiang province
  62. Rhodococcus equi and Brucella pulmonary mass in immunocompetent: A case report and literature review
  63. Downregulation of RIP3 ameliorates the left ventricular mechanics and function after myocardial infarction via modulating NF-κB/NLRP3 pathway
  64. Evaluation of the role of some non-enzymatic antioxidants among Iraqi patients with non-alcoholic fatty liver disease
  65. The role of Phafin proteins in cell signaling pathways and diseases
  66. Ten-year anemia as initial manifestation of Castleman disease in the abdominal cavity: A case report
  67. Coexistence of hereditary spherocytosis with SPTB P.Trp1150 gene variant and Gilbert syndrome: A case report and literature review
  68. Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells
  69. Exploratory evaluation supported by experimental and modeling approaches of Inula viscosa root extract as a potent corrosion inhibitor for mild steel in a 1 M HCl solution
  70. Imaging manifestations of ductal adenoma of the breast: A case report
  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
  72. Isomangiferin promotes the migration and osteogenic differentiation of rat bone marrow mesenchymal stem cells
  73. Prognostic value and microenvironmental crosstalk of exosome-related signatures in human epidermal growth factor receptor 2 positive breast cancer
  74. Circular RNAs as potential biomarkers for male severe sepsis
  75. Knockdown of Stanniocalcin-1 inhibits growth and glycolysis in oral squamous cell carcinoma cells
  76. The expression and biological role of complement C1s in esophageal squamous cell carcinoma
  77. A novel GNAS mutation in pseudohypoparathyroidism type 1a with articular flexion deformity: A case report
  78. Predictive value of serum magnesium levels for prognosis in patients with non-small cell lung cancer undergoing EGFR-TKI therapy
  79. HSPB1 alleviates acute-on-chronic liver failure via the P53/Bax pathway
  80. IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report
  81. Baculovirus-mediated endostatin and angiostatin activation of autophagy through the AMPK/AKT/mTOR pathway inhibits angiogenesis in hepatocellular carcinoma
  82. Metformin mitigates osteoarthritis progression by modulating the PI3K/AKT/mTOR signaling pathway and enhancing chondrocyte autophagy
  83. Evaluation of the activity of antimicrobial peptides against bacterial vaginosis
  84. Atypical presentation of γ/δ mycosis fungoides with an unusual phenotype and SOCS1 mutation
  85. Analysis of the microecological mechanism of diabetic kidney disease based on the theory of “gut–kidney axis”: A systematic review
  86. Omega-3 fatty acids prevent gestational diabetes mellitus via modulation of lipid metabolism
  87. Refractory hypertension complicated with Turner syndrome: A case report
  88. Interaction of ncRNAs and the PI3K/AKT/mTOR pathway: Implications for osteosarcoma
  89. Association of low attenuation area scores with pulmonary function and clinical prognosis in patients with chronic obstructive pulmonary disease
  90. Long non-coding RNAs in bone formation: Key regulators and therapeutic prospects
  91. The deubiquitinating enzyme USP35 regulates the stability of NRF2 protein
  92. Neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as potential diagnostic markers for rebleeding in patients with esophagogastric variceal bleeding
  93. G protein-coupled receptor 1 participating in the mechanism of mediating gestational diabetes mellitus by phosphorylating the AKT pathway
  94. LL37-mtDNA regulates viability, apoptosis, inflammation, and autophagy in lipopolysaccharide-treated RLE-6TN cells by targeting Hsp90aa1
  95. The analgesic effect of paeoniflorin: A focused review
  96. Chemical composition’s effect on Solanum nigrum Linn.’s antioxidant capacity and erythrocyte protection: Bioactive components and molecular docking analysis
  97. Knockdown of HCK promotes HREC cell viability and inner blood–retinal barrier integrity by regulating the AMPK signaling pathway
  98. The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes
  99. Laryngeal non-Hodgkin lymphoma: Report of four cases and review of the literature
  100. Clinical value of macrogenome next-generation sequencing on infections
  101. Overview of dendritic cells and related pathways in autoimmune uveitis
  102. TAK-242 alleviates diabetic cardiomyopathy via inhibiting pyroptosis and TLR4/CaMKII/NLRP3 pathway
  103. Hypomethylation in promoters of PGC-1α involved in exercise-driven skeletal muscular alterations in old age
  104. Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals
  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
  106. A histomorphometric study to evaluate the therapeutic effects of biosynthesized silver nanoparticles on the kidneys infected with Plasmodium chabaudi
  107. PGRMC1 and PAQR4 are promising molecular targets for a rare subtype of ovarian cancer
  108. Analysis of MDA, SOD, TAOC, MNCV, SNCV, and TSS scores in patients with diabetes peripheral neuropathy
  109. SLIT3 deficiency promotes non-small cell lung cancer progression by modulating UBE2C/WNT signaling
  110. The relationship between TMCO1 and CALR in the pathological characteristics of prostate cancer and its effect on the metastasis of prostate cancer cells
  111. Heterogeneous nuclear ribonucleoprotein K is a potential target for enhancing the chemosensitivity of nasopharyngeal carcinoma
  112. PHB2 alleviates retinal pigment epithelium cell fibrosis by suppressing the AGE–RAGE pathway
  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
  114. Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
  123. Myriad factors and pathways influencing tumor radiotherapy resistance
  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
  144. Screening of different growth conditions of Bacillus subtilis isolated from membrane-less microbial fuel cell toward antimicrobial activity profiling
  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
  182. Role of Embinin in the reabsorption of nucleus pulposus in lumbar disc herniation: Promotion of nucleus pulposus neovascularization and apoptosis of nucleus pulposus cells
  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
  194. An optimization method for measuring the stomata in cassava (Manihot esculenta Crantz) under multiple abiotic stresses
  195. Fosinopril inhibits Ang II-induced VSMC proliferation, phenotype transformation, migration, and oxidative stress through the TGF-β1/Smad signaling pathway
  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
https://doi.org/10.1515/biol-2022-0984
Schlagwörter für diesen Artikel
Lonicera japonica, chloroplast genome, evolution, phylogenetic analysis
Creative Commons
BY 4.0

Artikel in diesem Heft

  1. Biomedical Sciences
  2. Constitutive and evoked release of ATP in adult mouse olfactory epithelium
  3. LARP1 knockdown inhibits cultured gastric carcinoma cell cycle progression and metastatic behavior
  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
  5. Research progress on ocular complications caused by type 2 diabetes mellitus and the function of tears and blepharons
  6. The role and mechanism of esketamine in preventing and treating remifentanil-induced hyperalgesia based on the NMDA receptor–CaMKII pathway
  7. Brucella infection combined with Nocardia infection: A case report and literature review
  8. Detection of serum interleukin-18 level and neutrophil/lymphocyte ratio in patients with antineutrophil cytoplasmic antibody-associated vasculitis and its clinical significance
  9. Ang-1, Ang-2, and Tie2 are diagnostic biomarkers for Henoch-Schönlein purpura and pediatric-onset systemic lupus erythematous
  10. PTTG1 induces pancreatic cancer cell proliferation and promotes aerobic glycolysis by regulating c-myc
  11. Role of serum B-cell-activating factor and interleukin-17 as biomarkers in the classification of interstitial pneumonia with autoimmune features
  12. Effectiveness and safety of a mumps containing vaccine in preventing laboratory-confirmed mumps cases from 2002 to 2017: A meta-analysis
  13. Low levels of sex hormone-binding globulin predict an increased breast cancer risk and its underlying molecular mechanisms
  14. A case of Trousseau syndrome: Screening, detection and complication
  15. Application of the integrated airway humidification device enhances the humidification effect of the rabbit tracheotomy model
  16. Preparation of Cu2+/TA/HAP composite coating with anti-bacterial and osteogenic potential on 3D-printed porous Ti alloy scaffolds for orthopedic applications
  17. Aquaporin-8 promotes human dermal fibroblasts to counteract hydrogen peroxide-induced oxidative damage: A novel target for management of skin aging
  18. Current research and evidence gaps on placental development in iron deficiency anemia
  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
  22. Sirtuin 5 regulates acute myeloid leukemia cell viability and apoptosis by succinylation modification of glycine decarboxylase
  23. Apigenin 7-glucoside impedes hypoxia-induced malignant phenotypes of cervical cancer cells in a p16-dependent manner
  24. KAT2A changes the function of endometrial stromal cells via regulating the succinylation of ENO1
  25. Current state of research on copper complexes in the treatment of breast cancer
  26. Exploring antioxidant strategies in the pathogenesis of ALS
  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
  28. IL-33/soluble ST2 axis is associated with radiation-induced cardiac injury
  29. The predictive value of serum NLR, SII, and OPNI for lymph node metastasis in breast cancer patients with internal mammary lymph nodes after thoracoscopic surgery
  30. Carrying SNP rs17506395 (T > G) in TP63 gene and CCR5Δ32 mutation associated with the occurrence of breast cancer in Burkina Faso
  31. P2X7 receptor: A receptor closely linked with sepsis-associated encephalopathy
  32. Probiotics for inflammatory bowel disease: Is there sufficient evidence?
  33. Identification of KDM4C as a gene conferring drug resistance in multiple myeloma
  34. Microbial perspective on the skin–gut axis and atopic dermatitis
  35. Thymosin α1 combined with XELOX improves immune function and reduces serum tumor markers in colorectal cancer patients after radical surgery
  36. Highly specific vaginal microbiome signature for gynecological cancers
  37. Sample size estimation for AQP4-IgG seropositive optic neuritis: Retinal damage detection by optical coherence tomography
  38. The effects of SDF-1 combined application with VEGF on femoral distraction osteogenesis in rats
  39. Fabrication and characterization of gold nanoparticles using alginate: In vitro and in vivo assessment of its administration effects with swimming exercise on diabetic rats
  40. Mitigating digestive disorders: Action mechanisms of Mediterranean herbal active compounds
  41. Distribution of CYP2D6 and CYP2C19 gene polymorphisms in Han and Uygur populations with breast cancer in Xinjiang, China
  42. VSP-2 attenuates secretion of inflammatory cytokines induced by LPS in BV2 cells by mediating the PPARγ/NF-κB signaling pathway
  43. Factors influencing spontaneous hypothermia after emergency trauma and the construction of a predictive model
  44. Long-term administration of morphine specifically alters the level of protein expression in different brain regions and affects the redox state
  45. Application of metagenomic next-generation sequencing technology in the etiological diagnosis of peritoneal dialysis-associated peritonitis
  46. Clinical diagnosis, prevention, and treatment of neurodyspepsia syndrome using intelligent medicine
  47. Case report: Successful bronchoscopic interventional treatment of endobronchial leiomyomas
  48. Preliminary investigation into the genetic etiology of short stature in children through whole exon sequencing of the core family
  49. Cystic adenomyoma of the uterus: Case report and literature review
  50. Mesoporous silica nanoparticles as a drug delivery mechanism
  51. Dynamic changes in autophagy activity in different degrees of pulmonary fibrosis in mice
  52. Vitamin D deficiency and inflammatory markers in type 2 diabetes: Big data insights
  53. Lactate-induced IGF1R protein lactylation promotes proliferation and metabolic reprogramming of lung cancer cells
  54. Meta-analysis on the efficacy of allogeneic hematopoietic stem cell transplantation to treat malignant lymphoma
  55. Mitochondrial DNA drives neuroinflammation through the cGAS-IFN signaling pathway in the spinal cord of neuropathic pain mice
  56. Application value of artificial intelligence algorithm-based magnetic resonance multi-sequence imaging in staging diagnosis of cervical cancer
  57. Embedded monitoring system and teaching of artificial intelligence online drug component recognition
  58. Investigation into the association of FNDC1 and ADAMTS12 gene expression with plumage coloration in Muscovy ducks
  59. Yak meat content in feed and its impact on the growth of rats
  60. A rare case of Richter transformation with breast involvement: A case report and literature review
  61. First report of Nocardia wallacei infection in an immunocompetent patient in Zhejiang province
  62. Rhodococcus equi and Brucella pulmonary mass in immunocompetent: A case report and literature review
  63. Downregulation of RIP3 ameliorates the left ventricular mechanics and function after myocardial infarction via modulating NF-κB/NLRP3 pathway
  64. Evaluation of the role of some non-enzymatic antioxidants among Iraqi patients with non-alcoholic fatty liver disease
  65. The role of Phafin proteins in cell signaling pathways and diseases
  66. Ten-year anemia as initial manifestation of Castleman disease in the abdominal cavity: A case report
  67. Coexistence of hereditary spherocytosis with SPTB P.Trp1150 gene variant and Gilbert syndrome: A case report and literature review
  68. Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells
  69. Exploratory evaluation supported by experimental and modeling approaches of Inula viscosa root extract as a potent corrosion inhibitor for mild steel in a 1 M HCl solution
  70. Imaging manifestations of ductal adenoma of the breast: A case report
  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
  72. Isomangiferin promotes the migration and osteogenic differentiation of rat bone marrow mesenchymal stem cells
  73. Prognostic value and microenvironmental crosstalk of exosome-related signatures in human epidermal growth factor receptor 2 positive breast cancer
  74. Circular RNAs as potential biomarkers for male severe sepsis
  75. Knockdown of Stanniocalcin-1 inhibits growth and glycolysis in oral squamous cell carcinoma cells
  76. The expression and biological role of complement C1s in esophageal squamous cell carcinoma
  77. A novel GNAS mutation in pseudohypoparathyroidism type 1a with articular flexion deformity: A case report
  78. Predictive value of serum magnesium levels for prognosis in patients with non-small cell lung cancer undergoing EGFR-TKI therapy
  79. HSPB1 alleviates acute-on-chronic liver failure via the P53/Bax pathway
  80. IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report
  81. Baculovirus-mediated endostatin and angiostatin activation of autophagy through the AMPK/AKT/mTOR pathway inhibits angiogenesis in hepatocellular carcinoma
  82. Metformin mitigates osteoarthritis progression by modulating the PI3K/AKT/mTOR signaling pathway and enhancing chondrocyte autophagy
  83. Evaluation of the activity of antimicrobial peptides against bacterial vaginosis
  84. Atypical presentation of γ/δ mycosis fungoides with an unusual phenotype and SOCS1 mutation
  85. Analysis of the microecological mechanism of diabetic kidney disease based on the theory of “gut–kidney axis”: A systematic review
  86. Omega-3 fatty acids prevent gestational diabetes mellitus via modulation of lipid metabolism
  87. Refractory hypertension complicated with Turner syndrome: A case report
  88. Interaction of ncRNAs and the PI3K/AKT/mTOR pathway: Implications for osteosarcoma
  89. Association of low attenuation area scores with pulmonary function and clinical prognosis in patients with chronic obstructive pulmonary disease
  90. Long non-coding RNAs in bone formation: Key regulators and therapeutic prospects
  91. The deubiquitinating enzyme USP35 regulates the stability of NRF2 protein
  92. Neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as potential diagnostic markers for rebleeding in patients with esophagogastric variceal bleeding
  93. G protein-coupled receptor 1 participating in the mechanism of mediating gestational diabetes mellitus by phosphorylating the AKT pathway
  94. LL37-mtDNA regulates viability, apoptosis, inflammation, and autophagy in lipopolysaccharide-treated RLE-6TN cells by targeting Hsp90aa1
  95. The analgesic effect of paeoniflorin: A focused review
  96. Chemical composition’s effect on Solanum nigrum Linn.’s antioxidant capacity and erythrocyte protection: Bioactive components and molecular docking analysis
  97. Knockdown of HCK promotes HREC cell viability and inner blood–retinal barrier integrity by regulating the AMPK signaling pathway
  98. The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes
  99. Laryngeal non-Hodgkin lymphoma: Report of four cases and review of the literature
  100. Clinical value of macrogenome next-generation sequencing on infections
  101. Overview of dendritic cells and related pathways in autoimmune uveitis
  102. TAK-242 alleviates diabetic cardiomyopathy via inhibiting pyroptosis and TLR4/CaMKII/NLRP3 pathway
  103. Hypomethylation in promoters of PGC-1α involved in exercise-driven skeletal muscular alterations in old age
  104. Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals
  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
  106. A histomorphometric study to evaluate the therapeutic effects of biosynthesized silver nanoparticles on the kidneys infected with Plasmodium chabaudi
  107. PGRMC1 and PAQR4 are promising molecular targets for a rare subtype of ovarian cancer
  108. Analysis of MDA, SOD, TAOC, MNCV, SNCV, and TSS scores in patients with diabetes peripheral neuropathy
  109. SLIT3 deficiency promotes non-small cell lung cancer progression by modulating UBE2C/WNT signaling
  110. The relationship between TMCO1 and CALR in the pathological characteristics of prostate cancer and its effect on the metastasis of prostate cancer cells
  111. Heterogeneous nuclear ribonucleoprotein K is a potential target for enhancing the chemosensitivity of nasopharyngeal carcinoma
  112. PHB2 alleviates retinal pigment epithelium cell fibrosis by suppressing the AGE–RAGE pathway
  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
  114. Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
  123. Myriad factors and pathways influencing tumor radiotherapy resistance
  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
  144. Screening of different growth conditions of Bacillus subtilis isolated from membrane-less microbial fuel cell toward antimicrobial activity profiling
  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
  182. Role of Embinin in the reabsorption of nucleus pulposus in lumbar disc herniation: Promotion of nucleus pulposus neovascularization and apoptosis of nucleus pulposus cells
  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
  194. An optimization method for measuring the stomata in cassava (Manihot esculenta Crantz) under multiple abiotic stresses
  195. Fosinopril inhibits Ang II-induced VSMC proliferation, phenotype transformation, migration, and oxidative stress through the TGF-β1/Smad signaling pathway
  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
Jetzt anmelden und 20% sparen
Institutioneller Zugang
Wie funktioniert Authentifizierung?
Haben Sie eine Idee, wie wir unsere Website verbessern können?
Bitte schreiben Sie uns.
© 2025 De Gruyter Brill
Heruntergeladen am 27.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biol-2022-0984/html
Button zum nach oben scrollen