Home The complete mitogenome sequence of the coral lily (Lilium pumilum) and the Lanzhou lily (Lilium davidii) in China
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The complete mitogenome sequence of the coral lily (Lilium pumilum) and the Lanzhou lily (Lilium davidii) in China

  • Xiangying Qi EMAIL logo , Kaiqi Wang , Liping Yang , Zhenshan Deng and Zhihong Sun
Published/Copyright: December 31, 2020
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Open Life Sciences
From the journal Open Life Sciences Volume 15 Issue 1

Abstract

Background

The mitogenomes of higher plants are conserved. This study was performed to complete the mitogenome of two China Lilium species (Lilium pumilum Redouté and Lilium davidii var. unicolor (Hoog) cotton).

Methods

Genomic DNA was separately extracted from the leaves of L. pumilum and L. davidii in triplicate and used for sequencing. The mitogenome of Allium cepa was used as a reference. Genome assembly, annotation and phylogenetic tree were analyzed.

Results

The mitogenome of L. pumilum and L. davidii was 988,986 bp and 924,401 bp in length, respectively. There were 22 core protein-coding genes (including atp1, atp4, atp6, atp9, ccmB, ccmC, ccmFc, ccmFN1, ccmFN2, cob, cox3, matR, mttB, nad1, nad2, nad3, nad4, nad4L, nad5, nad6, nad7 and nad9), one open reading frame and one ribosomal protein-coding gene (rps12) in the mitogenomes. Compared with the A. cepa mitogenome, the coding sequence of the 24 genes and intergenic spacers in L. pumilum and L. davidii mitogenome contained 1,621 and 1,617 variable sites, respectively. In the phylogenetic tree, L. pumilum and L. davidii were distinct from A. cepa (NC_030100).

Conclusions

L. pumilum and L. davidii mitogenomes have far distances from other plants. This study provided additional information on the species resources of China Lilium.

Keywords: complete mitogenome sequence; Lilium species; Illumina sequencing; phylogenetic tree; variable sites

1 Introduction

The mitogenomes of higher plants are usually highly conserved and highly variable across the plant taxa [1]. Mitogenome is usually transmitted to the progeny from the maternal parent [2]. Mitogenome of higher plants ranges from 200 to 2,400 kb due to the expansion and the reduction of the intergenic region [3,4]. The constant recombination and great variation in the spacer regions in mitochondrial DNA (mtDNA) promote the evolution of higher plants. During evolution, most of the genes in plant mtDNA have been lost [5]. Compared to the chloroplast, the plant mitogenome has lower mutation rates [6]. Accordingly, the mitogenome plays a specific role in the evolution of plants. There are many studies sequencing the complete mitogenomes of higher plants and describing their genome features [3].

The genus Lilium (Liliaceae) is a very important economic plant worldwide [7,8]. Lilium species are perennial herbaceous plants with ornamental and notable medicinal value [9]. In the research and development of traditional Chinese medicine (TCM), the pharmaceutical characteristics of Lilium species, especially the extracts including polysaccharides, kaempferol and jatropham, have been widely studied [10,11]. For instance, the extract from Lilium species showed antidiabetic, antioxidant, antiapoptotic and health-protective properties [10,12,13]. These properties promoted the research and the exploration of bioactive and potential pharmaceutical activities in Lilium in the TCM field.

The genus Lilium is composed of approximately 115 species [8,14], and about 55 species are centrally distributed in China [15]. Some of the Lilium species in China have not been well identified yet. The coral lily Lilium pumilum Redouté and the Lanzhou lily Lilium davidii var. unicolor (Hoog) cotton are two Chinese species with ornamental and economic values [16,17]. Both L. pumilum and L. davidii are the important original materials of TCM [16,18]. L. pumilum, which has beautiful bright red flowers, is an endangered species in China [19]. However, the genetic evolution of these two species has not been reported until now.

This study was performed to examine the complete mitogenome of the two Lilium species. The mitogenomes of L. pumilum and L. davidii were sequenced using Illumina HiSeq X Ten sequencing platform. The variations in the mitogenomes were identified by referring to the reference mitogenome sequence of the closely related Allium cepa (GenBank: KU318712.1, NC_030100.1). The phylogenetic tree analysis was performed to identify the evolution distance of these two species from other plants with completed mitogenome sequences. This study will enrich the Chinese germplasm bank of lily.

2 Materials and methods

2.1 Plant materials and sequencing

The leaf samples of L. pumilum and L. davidii were obtained from Shaanxi Engineering and Technological Research Center for Conversation and Utilization of Regional Biological Resources, Yan’an, China. Both species were wild type and uncultivated plant genetic resources in China. Leaves were immersed into liquid nitrogen and stored at −80°C before use. Triplicate genomic DNA samples were extracted from leaves of each species using the cetyltrimethylammonium bromide (CTAB) method [20].

Following the genomic DNA quantity measurement (Qubit 3.0; Invitrogen, USA), samples were subjected to fragmentation, library construction (TruSeq™ DNA Sample Prep Kit; Illumina Inc, USA), PCR amplification and sequencing on the platform of Illumina HiSeq X Ten (pair-end 2 × 150 bp). Single-cell sequencing was performed on the PacBio RSII platform with 8–10 kb fragments.

2.2 Genome assembly and annotation

The Illumina raw data were processed using FastQC (http://www.bioinformatics.babraham.ac.uk/projects/fastqc/), followed by alignment with the PacBio RS sequencing reads using BlasR [21] and data assembly using SPAdes-3.10.1 program [22]. Long sequences assembled (>500 bp) with high alignment ratio were considered as candidates. Mt contigs were screened from these assembled candidates by blasting against the plant mitogenomes in NCBI Organelle Genome Resources (https://www.ncbi.nlm.nih.gov/genome/organelle/). The Illumina clean data were then compared back to the assembled mt contigs, followed by modification (bug fix) using GapCloser (v1.12; http://soap.genomics.org.cn/soapdenovo.html). The mitogenomic data of the two species sequenced were finally obtained.

The tRNA sequences in the obtained mitogenomes were recognized using tRNAscan-SE (http://lowelab.ucsc.edu/tRNAscan-SE/). The protein-coding genes and rRNA-coding genes in the mitogenomes were identified by aligning against the closely related A. cepa mitogenome sequence (GenBank: KU318712.1; NC_030100), with the threshold of alignment p < e value 1e−5. The exon and intron regions of genes were manually checked, and the gene sets in the mitogenome were identified. The variable sites in the coding sequence (CDS) of protein-coding genes and rRNA genes and intergenic spacers, as well as the structural variations (>100 bp) in the complete mitogenome sequence of the two Lilium species, were identified by comparison with A. cepa mitogenome (NC_030100) using the MUMmer and LASTZ alignment tools with default parameters.

2.3 Phylogenetic tree construction

The phylogenetic tree was constructed using the amino acid sequences of 29 plants with the available complete mitogenome sequences, including A. cepa (NC_030100.1), Bambusa oldhamii (EU365401.1), Lolium perenne (JX999996.1), Zea mays (DQ645536.1), Triticum aestivum (GU985444.1), Oryza sativa (NC_011033.1), Vicia faba (KC189947.1), Platycodon grandiflorus (MG775429.1), Nicotiana tabacum (NC_006581.1), Daucus carota subsp. Sativus (NC_017855.1), Arabidopsis thaliana (NC_037304.1), Gossypium harknessii (JX536494.1), Olea europaea (MG372117.1), Spirodela polyrhiza (NC_017840.1), Coleochaete scutata (MN613583.1), Chlorella vulgaris (MK948101.1), Hyoscyamus niger (NC_026515.1), Eleusine indica (NC_040989.1), Physochlaina orientalis (NC_044153.1), Sorghum bicolor (NC_008360.1), Cocos nucifera (NC_031696.1), Salix purpurea (NC_029693.1), Brassica juncea (NC_016123.1), Panax ginseng (KF735063.1), Cynodon dactylon x Cynodon transvaalensis (MK175054.1), Solanum lycopersicum (MF034192.1), Glycine max (NC_020455.1) and the two Lilium species (L. pumilum and L. davidii). The complete mitogenome sequences of these species were aligned using clustalW2 (https://www.ebi.ac.uk/Tools/msa/clustalw2/) with default parameters and manual check. The mitogenome-wide phylogenetic tree was subsequently constructed based on the concatenated amino acid sequences of 23 protein-coding genes and visualized using MEGA 5.2 Software [23] (maximum-likelihood method, n = 1,000 times, bootstrap algorithm).

3 Results and discussion

3.1 General features of the two mitogenomes

The Illumina sequencing generated 36,455,269 clean reads in L. pumilum and 59,258,050 clean reads in L. davidii with an averaged GC content of 45.06 and 44.87%, respectively. Only contigs >500 bp were included for the annotation of mitogenome. Accordingly, the mitogenome of L. pumilum was 988,986 bp in length with 45.06% GC content, and the mitogenome of L. davidii was 924,401 bp in length with 44.87% GC content (Table 1). These genomes were longer than 773,279 bp in Vitis vinifera [5], 490,520 bp in O. sativa [24], 316,363 bp in A. cepa [25], 678,653 bp in C. nucifera [26] and 452,526 bp in T. aestivum cv. Chinese Yumai [27], and smaller than 1,106,521 bp in Schisandra sphenanthera (Austrobaileyales) [28]. The obtained mitogenomes (988,986 and 924,401 bp) were of median size compared to these plants, but were relatively larger than the aforementioned monocotyledons. This difference might due to the expansion of the intergenic region [27,29]. The annotation of variable sites in the mitogenome would be of great importance.

Table 1

General features of the assembled contigs (>500 bp) from mitogenome sequencing in Lilium pumilum Redouté and Lilium davidii var. unicolor (Hoog) cotton

SpeciesL. pumilumL. davidii
Total number1717
Total length (bp)988,986924,401
Average length (bp)58,475.6554,376.53
N50 length (bp)75,22175,303
N90 length (bp)30,27636,946
Maximum length (bp)256,615159,127
Minimum length (bp)20,9121,933
GC content (%)45.0644.87
No. of variable sites1,6211,617
No. of variable sites in CDS (n (%))882 (54.41)881 (54.48)
No. of variable sites in the intergenic spacers (n (%))739 (45.59)736 (45.52)
Length of CDS and intergenic spacers (%)42.2345.18

N50 and N90, the length for which the collection of all contigs of that length or longer contains at least 50 and 90% of the total of the lengths of the contigs, respectively.

3.2 Annotation of variable sites in the mitogenomes

There were 1,621 and 1,617 variable sites in the CDS of the 23 annotated genes and the intergenic spacers between genes in the mitogenome of L. pumilum and L. davidii in comparison to A. cepa mitogenome, respectively (Table 1). The number of indels in the complete mitogenome sequence of L. pumilum (n = 45) was higher than that of L. davidii (n = 34). In addition, the variable sites in the mitogenomes in L. pumilum and L. davidii aligned onto 22 core protein-coding genes (including atp1, atp4, atp6, atp9, ccmB, ccmC, ccmFc, ccmFN1, ccmFN2, cob, cox3, matR, mttB, nad1, nad2, nad3, nad4, nad4L, nad5, nad6, nad7 and nad9), one open reading frame (ORF; orf725) and one ribosomal protein-coding gene (rps12) in A. cepa (Table 2). There were 733 and 484 variable sites in gene CDS and intergenic spacers in L. pumilum and L. davidii, respectively (Table 2). tRNA genes were not identified. The number of annotated protein-coding genes in the complete mitogenome sequence of L. pumilum and L. davidii was significantly lower than that in other reported plants, including 35 genes in T. aestivum cv. Chinese Yumai [27], 37 genes in V. vinifera [5], 41 genes in S. sphenanthera [28] and 72 genes in C. nucifera L. (coconut palm) [26], but was identical to the 23 protein-coding genes in the mitogenome of A. cepa [25]. Our previous research showed that the mitochondrial genome size of different plants is very different from others and the reference mitogenome of A. cepa due to the expansion and reduction of the intergenic region [27,29]. The narrowed gene number in L. pumilum and L. davidii might be due to the small number of known genes in the reference mitogenome in A. cepa. However, the larger mitogenome size in L. pumilum and L. davidii compared with the reference mitogenome of A. cepa might suggest that there was a large percent of mitogenomic regions with a number of unknown genes, which might be of great values for the function and evolution analysis of both L. pumilum and L. davidii species.

Table 2

Summary of the variable sites in the CDS of the 24 annotated genes and the intergenic spacers in the mitogenomes of Lilium pumilum Redouté and Lilium davidii var. unicolor (Hoog) cotton in comparison to Allium cepa mitogenome (NC_030100)

Gene_IDNumberCDSStrandNumberIntergenic spacersStrand
SynStartEndStartEnd
atp11107051,27252,795+9651,27252,795+
atp4309246,733247,296+12246,733247,296+
atp600———3582,41583,221+
atp91715103,573103,842+0———
ccmB3113278,555279,175+5278,555279,175+
ccmC00———40213,897214,712+
ccmFc391567,96368,717−566,29068,717−
ccmFN16014148,328149,374+38148,328149,374+
ccmFN22810287,429288,037−10287,429288,037−
cob267301,112302,302−2301,112302,302−
cox300———11238,167238,976−
matR893464,08466,084−864,08466,084−
mttB4015134,707135,456+0———
nad18563,26863,525−1112,51363,525−
nad214231,13931,326−691,12131,326+
nad38118,76419,120+0———
nad473168,424168,885−20159,945168,885−
nad4L109246,284246,586+13246,284246,586+
nad552121,0822,302−421,082290,301−
nad6147180,834181,802−70180,834181,802−
nad73228,13228,275−1321,41728,275−
nad92311205,033205,530−40205,033205,530−
orf7251017575,18877,365+175,18877,365+
rps12231519,16619,543+619,16619,543+
Total 733334484

Syn, synonymous.

Of the protein-coding genes, atp1, matR and ccmFN1 had the highest number of variable sites (110, 89 and 52, respectively) in the CDS regions in reference to A. cepa (Table 2). In addition, 96, 70, 42, 40 and 40 variable sites were identified in the intergenic spacers around atp1, nad6, nad5, ccmC and nad9, respectively. These results might reveal that these genes are of great value for the evolution of L. pumilum and L. davidii species [2]. By contrast, a small number of variable sites were found in the CDS of nad1, nad3, nad7 and cox3, and in the intergenic spacers around them (Table 2). These results might suggest their smaller contribution to the evolution of the two mitogenomes. The fact that there were no variable sites in the CDS of cox3, atp9 and nad3 genes showed that the CDS regions are well-conserved regions between the two species sequenced and A. cepa [30]. In addition, this conservation might govern the conservative evolution of mitogenome during the evolution of these genes [31].

3.3 Structural variations in the mitogenomes

The identified structural variations in the mitogenomes of L. pumilum and L. davidii are listed in Table 3. There were 14 variations in both mitogenomes with a length range of 100–401 bp. Most of the variations were insertion type (42.86%, 6/14), followed by deletion (35.71%, 5/14) and complex indel (21.43%, 3/14; Table 3). All the variations in L. pumilum were circular types, and half variations in L. davidii were circular types. One linear structural variation happened in ccmFc, atp1 and nad1 genes, which had a large number of variable sites (Tables 2 and 3). These variations might be of important values in the evolutionary history of L. pumilum and L. davidii [32,33].

Table 3

Summary of the total structural variations (SVs) in the mitogenome of Lilium pumilum Redouté and Lilium davidii var. unicolor (Hoog) cotton. L. davidii in comparison to Allium cepa mitogenome (NC_030100)

Target sequence (TS)Query sequence (QS)StrandSV typeL. in TS L. in QSBlock typeBlock number
L. pumilumStartEndL. davidiiStartEnd
Circle130,92738,044Circle124,3735,244+ComplexIndel7,118872400A4-4
Circle147,49447,494Circle1214,69516,655+Insertion01,9611004–4.5
Circle191,40591,685Linear1113,819113,819+Deletion2810401A11–12
Circle194,57794,826Linear1116,766116,766+Deletion250010111–12.13
Circle1217,901217,901Circle813,07214,014+Insertion094310121–23.24
Circle1218,291218,291Circle814,40514,942+Insertion053810121–24.25
Circle1244,299244,736Linear100+Deletion4380401A26–30
Circle1253,016253,016Linear18,27714,259+Insertion05,98310126–30.31
Circle124,7114,711Linear137,83038,053—Insertion022411132–37.38
Circle38,77913,019Circle18,7878,787+Deletion4,241010138–44.45
Circle55212,507Circle1110,16412,818+ComplexIndel1,9872,65510141–48.49
Circle633,52136,804Circle921,21021,210+Deletion3,284010048–56.57
Circle85,82024,748Linear246,26571,977+ComplexIndel18,92925,71310154–63.64
Circle94,5794,579Linear34,4575,644+Insertion01,18810156–66.67

Target and query length, the length of SV in the target and query sequences; L. in TS, length of corresponding SV in target sequence; L. in QS, length of corresponding SV in query sequence.

3.4 Evolutionary analysis of the two Lilium species

The phylogenetic tree was constructed based on the concatenated amino acid sequences of the 23 protein-coding genes in the two Lilium species and other 27 plants. Figure 1 shows the phylogenetic evolutionary position of L. pumilum and L. davidii. The two Lilium species had close relationships with the Brassicales and Poales clades, while A. cepa showed close relationships with Poales clades and C. nucifera (Figure 1). Both L. pumilum and L. davidii were distant from A. cepa (NC_030100; Figure 1). These distinct genetic distances between L. pumilum or L. davidii and the reference mitogenome of A. cepa might be due to a high number of variable sites in the mitogenomes of L. pumilum and L. davidii species.

Figure 1 The phylogenetic tree inferring from the concatenated amino acid sequences of 23 protein-coding genes of the 29 plants. The amino acid sequences of 23 protein-coding genes in the complete mitogenome sequences of other 27 plants were retrieved from the NCBI (https://www.ncbi.nlm.nih.gov/nuccore).
Figure 1

The phylogenetic tree inferring from the concatenated amino acid sequences of 23 protein-coding genes of the 29 plants. The amino acid sequences of 23 protein-coding genes in the complete mitogenome sequences of other 27 plants were retrieved from the NCBI (https://www.ncbi.nlm.nih.gov/nuccore).

A previous phylogenetic study based on 79 chloroplast genes showed that L. longiflorum (Liliaceae) and Alstroemeria aurea Graham (Alstroemeriaceae) were clustered into the Asparagales + Commelinids clade, showing the close genetic relationships between them [34]. İkinci et al. [35] reported that there were remote evolutionary distances among different lily species from different regions in European and other countries based on the internal transcribed spacer regions of nuclear ribosomal DNA. Similar results of Japan lily species were reported by Nishikawa et al. [36]. We suppose that the more number of the annotated protein-coding genes in the mitogenome of the two lily species, the more detailed information about lily’s evolution analysis will be obtained.

4 Conclusions

In summary, we obtained the complete mitogenome sequences of L. pumilum (988,986 bp) and L. davidii (924,401 bp) and presented the phylogenetic relationships of them for the first time. A total of 24 protein-coding genes, including one ribosomal protein-coding gene (rps12), were annotated by aligning with the reference genome in A. cepa (GenBank: KU318712.1; NC_030100). The phylogenetic tree analysis showed that these two species had distinct mitochondrial genomes from other plants including A. cepa. The large unannotated sections in the mitogenome (988,986 or 924,401 bp) in Lilium species compared with that in the A. cepa reference genome (316,363 bp) should be performed in the further research.

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Acknowledgments

The study was supported by the Serving local projects of Shaanxi Education Department (20JC036); The Basic Research and Frontier Exploration Project of Chongqing Science and Technology Bureau (cstc2019jcyj-msxmX0014); Youth Science and Technology Project of Chongqing Education Science Committee (KJQN201801428).

  1. Author contributions: Conception and design of the research: Xiangying Qi and Kaiqi Wang; acquisition, analysis and interpretation of data: Xiangying Qi, Kaiqi Wang, Liping Yang and Zhenshan Deng; plant material acquirement: Xiangying Qi and Liping Yang; drafting the manuscript: Liping Yang; manuscript revision for important intellectual content: Zhihong Sun. All the authors have read and approved the manuscript.

  2. Conflict of interest: The authors state no conflict of interest.

  3. Data availability statement: The datasets generated during and/or analyzed during the current study are available in the GenBank repository: Lilium-davidii.sqn L-Linear1 MT985331, Lilium-davidii.sqn L-Linear2 MT985332, Lilium-davidii.sqn L-Linear3 MT985333, Lilium-davidii.sqn L-Circle1 MT985334, Lilium-davidii.sqn L-Circle2 MT985335, Lilium-davidii.sqn L-Circle3 MT985336, Lilium-davidii.sqn L-Circle4 MT985337, Lilium-davidii.sqn L-Circle5 MT985338, Lilium-davidii.sqn L-Circle6 MT985339, Lilium-davidii.sqn L-Circle7 MT985340, Lilium-davidii.sqn L-Circle8 MT985341, Lilium-davidii.sqn L-Circle9 MT985342, Lilium-davidii.sqn L-Circle10 MT985343, Lilium-davidii.sqn L-Circle11 MT985344, Lilium-davidii.sqn L-Circle12 MT985345, Lilium-davidii.sqn L-Circle13 MT985346, Lilium-pumilum.sqn G-Linear1 MT985347, Lilium-pumilum.sqn G-Linear2 MT985348, Lilium-pumilum.sqn G-Linear3 MT985349, Lilium-pumilum.sqn G-Linear4 MT985350, Lilium-pumilum.sqn G-Circle1 MT985351, Lilium-pumilum.sqn G-Circle2 MT985352, Lilium-pumilum.sqn G-Circle3 MT985353, Lilium-pumilum.sqn G-Circle4 MT985354, Lilium-pumilum.sqn G-Circle5 MT985355, Lilium-pumilum.sqn G-Circle6 MT985356, Lilium-pumilum.sqn G-Circle7 MT985357, Lilium-pumilum.sqn G-Circle8 MT985358, Lilium-pumilum.sqn G-Circle9 MT985359, Lilium-pumilum.sqn G-Circle10 MT985360, Lilium-pumilum.sqn G-Circle11 MT985361, Lilium-pumilum.sqn G-Circle12 MT985362, Lilium-pumilum.sqn G-Circle13 MT985363.

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Received: 2019-11-21
Revised: 2020-07-18
Accepted: 2020-09-14
Published Online: 2020-12-31

© 2020 Xiangying Qi et al., published by De Gruyter

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

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  2. Dependence of the heterosis effect on genetic distance, determined using various molecular markers
  3. Plant Growth Promoting Rhizobacteria (PGPR) Regulated Phyto and Microbial Beneficial Protein Interactions
  4. Role of strigolactones: Signalling and crosstalk with other phytohormones
  5. An efficient protocol for regenerating shoots from paper mulberry (Broussonetia papyrifera) leaf explants
  6. Functional divergence and adaptive selection of KNOX gene family in plants
  7. In silico identification of Capsicum type III polyketide synthase genes and expression patterns in Capsicum annuum
  8. In vitro induction and characterisation of tetraploid drumstick tree (Moringa oleifera Lam.)
  9. CRISPR/Cas9 or prime editing? – It depends on…
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  14. Use of phosphatase and dehydrogenase activities in the assessment of calcium peroxide and citric acid effects in soil contaminated with petrol
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  18. Spatiotemporal dynamics of terrestrial invertebrate assemblages in the riparian zone of the Wewe river, Ashanti region, Ghana
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  117. Erratum to “MYL6B drives the capabilities of proliferation, invasion, and migration in rectal adenocarcinoma through the EMT process”
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https://doi.org/10.1515/biol-2020-0102
Keywords for this article
complete mitogenome sequence; Lilium species; Illumina sequencing; phylogenetic tree; variable sites
Creative Commons
BY 4.0

Articles in the same Issue

  1. Plant Sciences
  2. Dependence of the heterosis effect on genetic distance, determined using various molecular markers
  3. Plant Growth Promoting Rhizobacteria (PGPR) Regulated Phyto and Microbial Beneficial Protein Interactions
  4. Role of strigolactones: Signalling and crosstalk with other phytohormones
  5. An efficient protocol for regenerating shoots from paper mulberry (Broussonetia papyrifera) leaf explants
  6. Functional divergence and adaptive selection of KNOX gene family in plants
  7. In silico identification of Capsicum type III polyketide synthase genes and expression patterns in Capsicum annuum
  8. In vitro induction and characterisation of tetraploid drumstick tree (Moringa oleifera Lam.)
  9. CRISPR/Cas9 or prime editing? – It depends on…
  10. Study on the optimal antagonistic effect of a bacterial complex against Monilinia fructicola in peach
  11. Natural variation in stress response induced by low CO2 in Arabidopsis thaliana
  12. The complete mitogenome sequence of the coral lily (Lilium pumilum) and the Lanzhou lily (Lilium davidii) in China
  13. Ecology and Environmental Sciences
  14. Use of phosphatase and dehydrogenase activities in the assessment of calcium peroxide and citric acid effects in soil contaminated with petrol
  15. Analysis of ethanol dehydration using membrane separation processes
  16. Activity of Vip3Aa1 against Periplaneta americana
  17. Thermostable cellulase biosynthesis from Paenibacillus alvei and its utilization in lactic acid production by simultaneous saccharification and fermentation
  18. Spatiotemporal dynamics of terrestrial invertebrate assemblages in the riparian zone of the Wewe river, Ashanti region, Ghana
  19. Antifungal activity of selected volatile essential oils against Penicillium sp.
  20. Toxic effect of three imidazole ionic liquids on two terrestrial plants
  21. Biosurfactant production by a Bacillus megaterium strain
  22. Distribution and density of Lutraria rhynchaena Jonas, 1844 relate to sediment while reproduction shows multiple peaks per year in Cat Ba-Ha Long Bay, Vietnam
  23. Biomedical Sciences
  24. Treatment of Epilepsy Associated with Common Chromosomal Developmental Diseases
  25. A Mouse Model for Studying Stem Cell Effects on Regeneration of Hair Follicle Outer Root Sheaths
  26. Morphine modulates hippocampal neurogenesis and contextual memory extinction via miR-34c/Notch1 pathway in male ICR mice
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  33. Sevoflurane inhibits proliferation, invasion, but enhances apoptosis of lung cancer cells by Wnt/β-catenin signaling via regulating lncRNA PCAT6/ miR-326 axis
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  36. Human Dental Pulp Stem Cells Exhibit Osteogenic Differentiation Potential
  37. MiR-489-3p inhibits cell proliferation, migration, and invasion, and induces apoptosis, by targeting the BDNF-mediated PI3K/AKT pathway in glioblastoma
  38. Long non-coding RNA TUG1 knockdown hinders the tumorigenesis of multiple myeloma by regulating the microRNA-34a-5p/NOTCH1 signaling pathway
  39. Large Brunner’s gland adenoma of the duodenum for almost 10 years
  40. Neurotrophin-3 accelerates reendothelialization through inducing EPC mobilization and homing
  41. Hepatoprotective effects of chamazulene against alcohol-induced liver damage by alleviation of oxidative stress in rat models
  42. FXYD6 overexpression in HBV-related hepatocellular carcinoma with cirrhosis
  43. Risk factors for elevated serum colorectal cancer markers in patients with type 2 diabetes mellitus
  44. Effect of hepatic sympathetic nerve removal on energy metabolism in an animal model of cognitive impairment and its relationship to Glut2 expression
  45. Progress in research on the role of fibrinogen in lung cancer
  46. Advanced glycation end product levels were correlated with inflammation and carotid atherosclerosis in type 2 diabetes patients
  47. MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB
  48. Knockdown of DDX46 inhibits trophoblast cell proliferation and migration through the PI3K/Akt/mTOR signaling pathway in preeclampsia
  49. Buformin suppresses osteosarcoma via targeting AMPK signaling pathway
  50. Effect of FibroScan test in antiviral therapy for HBV-infected patients with ALT <2 upper limit of normal
  51. LncRNA SNHG15 regulates osteosarcoma progression in vitro and in vivo via sponging miR-346 and regulating TRAF4 expression
  52. LINC00202 promotes retinoblastoma progression by regulating cell proliferation, apoptosis, and aerobic glycolysis through miR-204-5p/HMGCR axis
  53. Coexisting flavonoids and administration route effect on pharmacokinetics of Puerarin in MCAO rats
  54. GeneXpert Technology for the diagnosis of HIV-associated tuberculosis: Is scale-up worth it?
  55. Circ_001569 regulates FLOT2 expression to promote the proliferation, migration, invasion and EMT of osteosarcoma cells through sponging miR-185-5p
  56. Lnc-PICSAR contributes to cisplatin resistance by miR-485-5p/REV3L axis in cutaneous squamous cell carcinoma
  57. BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells
  58. MYL6B drives the capabilities of proliferation, invasion, and migration in rectal adenocarcinoma through the EMT process
  59. Inhibition of lncRNA LINC00461/miR-216a/aquaporin 4 pathway suppresses cell proliferation, migration, invasion, and chemoresistance in glioma
  60. Upregulation of miR-150-5p alleviates LPS-induced inflammatory response and apoptosis of RAW264.7 macrophages by targeting Notch1
  61. Long non-coding RNA LINC00704 promotes cell proliferation, migration, and invasion in papillary thyroid carcinoma via miR-204-5p/HMGB1 axis
  62. Neuroanatomy of melanocortin-4 receptor pathway in the mouse brain
  63. Lipopolysaccharides promote pulmonary fibrosis in silicosis through the aggravation of apoptosis and inflammation in alveolar macrophages
  64. Influences of advanced glycosylation end products on the inner blood–retinal barrier in a co-culture cell model in vitro
  65. MiR-4328 inhibits proliferation, metastasis and induces apoptosis in keloid fibroblasts by targeting BCL2 expression
  66. Aberrant expression of microRNA-132-3p and microRNA-146a-5p in Parkinson’s disease patients
  67. Long non-coding RNA SNHG3 accelerates progression in glioma by modulating miR-384/HDGF axis
  68. Long non-coding RNA NEAT1 mediates MPTP/MPP+-induced apoptosis via regulating the miR-124/KLF4 axis in Parkinson’s disease
  69. PCR-detectable Candida DNA exists a short period in the blood of systemic candidiasis murine model
  70. CircHIPK3/miR-381-3p axis modulates proliferation, migration, and glycolysis of lung cancer cells by regulating the AKT/mTOR signaling pathway
  71. Reversine and herbal Xiang–Sha–Liu–Jun–Zi decoction ameliorate thioacetamide-induced hepatic injury by regulating the RelA/NF-κB/caspase signaling pathway
  72. Therapeutic effects of coronary granulocyte colony-stimulating factor on rats with chronic ischemic heart disease
  73. The effects of yam gruel on lowering fasted blood glucose in T2DM rats
  74. Circ_0084043 promotes cell proliferation and glycolysis but blocks cell apoptosis in melanoma via circ_0084043-miR-31-KLF3 axis
  75. CircSAMD4A contributes to cell doxorubicin resistance in osteosarcoma by regulating the miR-218-5p/KLF8 axis
  76. Relationship of FTO gene variations with NAFLD risk in Chinese men
  77. The prognostic and predictive value of platelet parameters in diabetic and nondiabetic patients with sudden sensorineural hearing loss
  78. LncRNA SNHG15 contributes to doxorubicin resistance of osteosarcoma cells through targeting the miR-381-3p/GFRA1 axis
  79. miR-339-3p regulated acute pancreatitis induced by caerulein through targeting TNF receptor-associated factor 3 in AR42J cells
  80. LncRNA RP1-85F18.6 affects osteoblast cells by regulating the cell cycle
  81. MiR-203-3p inhibits the oxidative stress, inflammatory responses and apoptosis of mice podocytes induced by high glucose through regulating Sema3A expression
  82. MiR-30c-5p/ROCK2 axis regulates cell proliferation, apoptosis and EMT via the PI3K/AKT signaling pathway in HG-induced HK-2 cells
  83. CTRP9 protects against MIA-induced inflammation and knee cartilage damage by deactivating the MAPK/NF-κB pathway in rats with osteoarthritis
  84. Relationship between hemodynamic parameters and portal venous pressure in cirrhosis patients with portal hypertension
  85. Long noncoding RNA FTX ameliorates hydrogen peroxide-induced cardiomyocyte injury by regulating the miR-150/KLF13 axis
  86. Ropivacaine inhibits proliferation, migration, and invasion while inducing apoptosis of glioma cells by regulating the SNHG16/miR-424-5p axis
  87. CD11b is involved in coxsackievirus B3-induced viral myocarditis in mice by inducing Th17 cells
  88. Decitabine shows anti-acute myeloid leukemia potential via regulating the miR-212-5p/CCNT2 axis
  89. Testosterone aggravates cerebral vascular injury by reducing plasma HDL levels
  90. Bioengineering and Biotechnology
  91. PL/Vancomycin/Nano-hydroxyapatite Sustained-release Material to Treat Infectious Bone Defect
  92. The thickness of surface grafting layer on bio-materials directly mediates the immuno-reacitivity of macrophages in vitro
  93. Silver nanoparticles: synthesis, characterisation and biomedical applications
  94. Food Science
  95. Bread making potential of Triticum aestivum and Triticum spelta species
  96. Modeling the effect of heat treatment on fatty acid composition in home-made olive oil preparations
  97. Effect of addition of dried potato pulp on selected quality characteristics of shortcrust pastry cookies
  98. Preparation of konjac oligoglucomannans with different molecular weights and their in vitro and in vivo antioxidant activities
  99. Animal Sciences
  100. Changes in the fecal microbiome of the Yangtze finless porpoise during a short-term therapeutic treatment
  101. Agriculture
  102. Influence of inoculation with Lactobacillus on fermentation, production of 1,2-propanediol and 1-propanol as well as Maize silage aerobic stability
  103. Application of extrusion-cooking technology in hatchery waste management
  104. In-field screening for host plant resistance to Delia radicum and Brevicoryne brassicae within selected rapeseed cultivars and new interspecific hybrids
  105. Studying of the promotion mechanism of Bacillus subtilis QM3 on wheat seed germination based on β-amylase
  106. Rapid visual detection of FecB gene expression in sheep
  107. Effects of Bacillus megaterium on growth performance, serum biochemical parameters, antioxidant capacity, and immune function in suckling calves
  108. Effects of center pivot sprinkler fertigation on the yield of continuously cropped soybean
  109. Special Issue On New Approach To Obtain Bioactive Compounds And New Metabolites From Agro-Industrial By-Products
  110. Technological and antioxidant properties of proteins obtained from waste potato juice
  111. The aspects of microbial biomass use in the utilization of selected waste from the agro-food industry
  112. Special Issue on Computing and Artificial Techniques for Life Science Applications - Part I
  113. Automatic detection and segmentation of adenomatous colorectal polyps during colonoscopy using Mask R-CNN
  114. The impedance analysis of small intestine fusion by pulse source
  115. Errata
  116. Erratum to “Diagnostic performance of serum CK-MB, TNF-α and hs-CRP in children with viral myocarditis”
  117. Erratum to “MYL6B drives the capabilities of proliferation, invasion, and migration in rectal adenocarcinoma through the EMT process”
  118. Erratum to “Thermostable cellulase biosynthesis from Paenibacillus alvei and its utilization in lactic acid production by simultaneous saccharification and fermentation”
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