Startseite Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
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Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan

  • Amber Khalid EMAIL logo , Amjad Rashid Kayani , Muhammad Sajid Nadeem , Muhammad Mushtaq und Mirza Azhar Beg
Veröffentlicht/Copyright: 15. Juni 2022
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Aus der Zeitschrift Open Life Sciences Band 17 Heft 1

Abstract

Genus Tatera is comprised of 12 species, but only one species, Tatera indica, exists in Asia. T. indica is considered an agricultural pest and host of a few zoonotic diseases. However, the data on morphological characteristics are published, but the aspect of molecular characterization is lacking to confirm the status of subspecies in most of the Asian countries including Pakistan. Therefore, the present study is the first study on morphological and molecular characterization of T. indica to get a phylogenetic relationship with the population of T. indica in Pakistan. Almost all the morphometric, cranial, and dental values of T. indica were lower in the present study as compared to the specimen from Iran, Syria, and Turkey. The molecular analysis indicated the presence of sub-species of T. indica. Interestingly, the cytochrome b gene sequence showed more resemblance to the Iranian rat than the previously reported sequence of a Pakistani T. indica. Iran shares a border with Pakistan, and migration between the two countries could be a possible reason. The resembling morphometric data on Iranian rats also explain this phenomenon. The present study found, although minor, evidence of the presence of sub-species even within Pakistan. Unfortunately, the previously submitted sequence from Pakistan was not supplemented with morphometric data and the exact capturing site of the rat. Therefore, further molecular and morphometric data from other regions are required to confirm the presence of sub-species.

Keywords: Tatera indica ; genetics; cytochrome b ; molecular DNA; morphometry

1 Introduction

The members of the genus Tatera are common in the cultivated areas. Out of 12 species, 11 are found in Africa and only one (Tatera indica) in Asia [1,2]. T. indica is distributed in Pakistan, Afghanistan, Iraq, Nepal, India, Kuwait, Sri Lanka, Syria, and Turkey [3,4,5,6,7,8,9]. The distribution of T. indica in Pakistan is known poorly. In Pakistan, its presence has been reported throughout Punjab except for the foothills of Murree, parts of Khyber Pakhtunkhwa province, and Sindh and Baluchistan provinces [6,10].

Chevret and Dobigny declared Tatera a polyphyletic taxon based on the genomic DNA [11]. They proposed that the migration occurs from Asia to Africa, unlike other gerbiline rodents. Ancestors of T. indica belonged to Africa, and they voyaged to Asia by some land bridges. The subspecies status of T. indica is still controversial. In Iran, four different subspecies, namely T. indica persica, T. indica scansa, T. indica monticola, and T. indica bailwardi, were reported earlier [12]. However, later on, only two subspecies T. indica and T. indica teaniura were recognized in Iran [13]. Furthermore, Mirshamsi et al. found that there is no discrimination between the southern and northern populations of T. indica in Iran [14]. Mohammadi and Pervaizi found that two phenotypically different T. indica, i.e., buff-black and buff-brown, are not subspecies molecularly [9]. However, in Pakistan, only buff-browns were reported to exist. No record of any subspecies of T. indica was found in Pakistan.

Although morphometry is a useful, cheaper, and robust tool for identifying and classifying animals, molecular analysis is needed to confirm species identification and determine intraspecific variation. The proper identification and estimation of the diversity of T. indica are pre-requisite for the control of this agricultural pest and a host of leishmaniasis. Therefore, the present study was designed to perform morphometric and molecular characterization of T. indica from Pothwar, a subtropical area in the province of Punjab, Pakistan.

2 Materials and methods

2.1 Study site and sample collection

A total of 120 samples of T. indica were collected from different active colonies of rats in Pothwar, a semi-arid subtropical plateau in the north of Punjab province of Pakistan. It covers a 23,160 sq km area and stretches from latitude 32°10 to 34°9N and longitude 71°10–73°55E with an altitude of 305–610 m above sea levels. The specimens were collected using snap traps from dusk to dawn by baiting them with bread dipped in vegetable oil. Collected rats were brought to the Laboratory of Ecology and Wildlife PirMehr Ali Shah, Arid Agriculture University, Rawalpindi.

  1. Ethical approval: The research related to animal use has complied with all the relevant national regulations and institutional policies for the care and use of animals and was approved by the Ethical Committee of PirMehr Ali Shah, Arid Agriculture University, Rawalpindi.

2.2 Morphological study

2.2.1 Body measurements

A total of 85 specimens were subjected to morphometric analysis. Each specimen was weighed using a digital balance (Model: TX323L, MedigeneSdn. Bhd., Malaysia). Standard methods of measurement were used to measure six external morphological features, namely total body length (TBL), head and body length (HBL), tail length (TL) from the rump, ear length (EL) from basal notch to the distal tip of the head and left hindfoot length (HFL) without claw using a ruler, compass, and/or an analog vernier caliper and recorded in a tabulated form [6].

2.2.2 Skull measurements

The skull was prepared by detaching the ligaments of the head from the neck using scissors and forceps. The detached head was cleaned by removing the flesh and eyes from the eye socket. It was then placed in the 2% sodium hydroxide (NaOH) solution. When all the remaining flesh was separated, the cleaned skull was preserved in airtight bags or the small boxes containing cotton pads. Each skull was tagged with the original field number and other specific information for identification. Eight measurements of skull bones, including nasal length (NL), zygomatic breadth (ZB), greatest skull length (GSL), mandible length (ML), upper molar tooth row length (UMRL), lower molar tooth row length (LMRL), and least interorbital breadth, were measured using the standard methods mentioned above.

2.3 Genomic and phylogenetic analysis

The phenol-chloroform (Organic) method was used to extract DNA from ∼0.25 g of tail tissue of each specimen (n = 13). Extracted DNA was evaluated for quality and quantity by using standard methods, and pellets were stored at 4°C. DNA was amplified for the mitochondrial cytochrome b (Cyt-b) gene with the forward primer UNFOR403 (5′-TGAGGACAAATATCATTCTGAGG-3′) and the reverse primer UNREV1025 (5′-GGTTGTCCTCCAATTCATGTTA-3′) through specific conditions optimized for the polymerase chain reaction (PCR) (Model: 865061CL, Galaxy XP ClearLine Thermal Cycler, China). The primers were selected as described in Kent and Norris [15]. Amplification of PCR product was confirmed on ethidium bromide-stained 2% agarose gel visualized under UV.

The purified PCR products of the Cyt-b gene were sequenced directly, and the sequences were aligned by using Mesquite and MEGA X 10.1 Software. The sequences were blasted in GenBank, and a phylogenetic tree was constructed using MOLE-BLAST to find out the closest database neighbors (https://blast.ncbi.nlm.nih.gov/moleblast/moleblast.cgi). The aligned sequences were also compared with already published sequenced mitochondrial Cyt-b of T. indica (GenBank Accession No.: KP001566 and AJ430563). Tajima’s Neutrality test was conducted using MEGA X 10.1 software. Estimation of nucleotide composition and the maximum likelihood were also calculated using the above-mentioned software.

3 Results

3.1 Physical appearance

The dorsal side body color is reddish-brown to fawnish, while the ventral side of the body is creamy white in color. Feet are naked and are hairless. The forefoot has four toes with a thumb. The hindfoot has five digits. Female individuals have four pairs of mammae. The animal’s tail is approximately half of the length of the body. The tail has a tuft of black hairs at the end, and a brown band is present on the sides of the tail. Ears are also naked and elongated.

3.2 Dietary habits

T. indica is an omnivorous species. It predominately consumed plant matter in its diet along with animal matter. When the supply of insects increases during the rainy season, they feed on insects.

3.3 Habitat and predation

T. indica is successfully adopted in different habitats. They can occupy habitats if there is an abundant supply of food and frequent through irrigation canals. However, they avoid cold temperatures. They primarily preyed on by birds of prey, especially owls.

3.4 Morphological diversity

3.4.1 Body measurements

The body color of all the samples was brown. The body weight (BW) of rats ranged from 55.4 to 154.9 g (118.3 ± 25.4 g). The TBL of the adult animal was 240–350 mm (350.1 ± 24.5 mm). HBL was 110–180 mm (142.3 ± 19.1 mm). TL was 120–200 mm (164.2 ± 16. mm5). The EL was 10–25 mm (20.2 ± 2.8 mm). HFL was 30–40 mm (35.8 ± 2.1 mm) (Table 1). TBL, HFL, HBL, TL, and EL were used as distinguishing features of T. indica from other rat species in the area (Table 1)

Table 1

Morphometric measurements of T. indica (n = 85)

Character Mean ± SD Min Max
BW (g) 118.3 ± 25.4 55.4 154.9
TBL (mm) 350.1 ± 24.5 240 350
HBL (mm) 142.3 ± 19.1 110 180
TL (mm) 164.2 ± 16.5 120 200
HFL (mm) 35.8 ± 2.1 30 40
EL (mm) 20.2 ± 2.8 10 25

BW: body weight; TBL: total body length; TL: tail length; HBL: head and body length; HFL: hindfoot length; EL: ear length.

3.4.2 Cranial measurements

The GSL of rats ranged from 36.5 to 97.2 mm (39.6 ± 3.1 mm). The diameter of the auditory bulla was 3.4–5.9 mm (5.1 ± 1.1 mm). Depth of braincase and breadth of braincase were 12.2–14.2 mm (13.4 ± 1.0 mm) and 14.6–18.8 mm (17.3 ± 2.3 mm), respectively. ZB was 22.0–22.1 mm (27.9 ± 0.01 mm). The EL was 10.0–25.0 mm (20.2 ± 2.8 mm), while NL was 14.9–17.5 mm (16.3 ± 1.0 mm). LMR and UMRL were 5.2–6.0 mm (5.8 ± 0.3 mm) and 5.8–6.4 mm (6.1 ± 0.2 mm), respectively. The ML was 19.33–20.81 mm (19.9 ± 0.6 mm), while the first molar length was 3.19–3.7 mm (3.4 ± 0.2 mm) (Table 2).

Table 2

Cranial measurements of T. indica

Measurements (mm) N Mean ± SD Min Max
GSL 65 39.6 ± 0.3 36.4 97.2
BBC 64 17.3 ± 2.3 14.6 18.8
DBC 68 13.4 ± 1.0 12.2 14.2
ZB 61 27.9 ± 0.01 22.0 22.1
NL 66 16.3 ± 0.9 14.9 17.5
ABD 66 5.1 ± 1.1 3.4 5.9
IFL 65 7.5 ± 0.1 7.4 7.5
UMRL 66 6.1 ± 0.2 5.8 6.4
MIL 66 3.4 ± 0.2 3.2 3.7
IOB 66 6.7 ± 0.2 5.5 6.7
ML 66 19.9 ± 0.6 19.3 20.8
LMRL 66 5.8 ± 0.3 5.2 6.0

GSL: greatest skull length, BBC: breadth of braincase, DBC, depth of braincase, ZB, zygomatic breadth, NL, nasal length, ABD, auditory bulla diameter, FL, incisive foramen length, UMRL, upper molar tooth row length, MIL, first molar length, IOB, interorbital breadth, ML, mandible length LMRL lower molar tooth row length.

3.5 Genetic diversity

To determine the genetic diversity between the two populations, nucleotide sequences were compared using BLAST, Clustal W, and MEGA software. The sequences from all 13 samples were almost similar. All the sequences were submitted to the GenBank (Accession numbers: BankIt2492881 AK9789-13 MZ852449 to BankIt2492881 AK9789-1 MZ852461). Supplementary files 1 and 2 are attached as sequence alignment data and individual sequences of samples.

3.5.1 Nucleotide sequence BLAST analysis

The obtained sequence of the Cyt-b gene from the selected rat species was subjected to BLAST (https://blast.ncbi.nlm.nih.gov/Blast.cgi). It brought two matched sequences of T. indica from Iran (KP001566) and Pakistan (AJ430563). Our sequences had more similarities with the Iranian (97.11%) sample than Pakistani (96.43%).

3.5.2 Phylogenetic tree based on nucleotide sequence

The phylogenetic tree was also constructed using MOLE-BLAST (https://blast.ncbi.nlm.nih.gov/moleblast/moleblast.cgi). The phylogram has shown 0.05 genetic diversity indicating a close relationship with the Cyt-b of already published sequences of the Cyt-b gene of T. indica. The present molecular analysis showed a relationship with Gerbilliscus (Figure 1).

Figure 1 Phylogenetic tree constructed by MOLE-BLAST where ICII Query_10001 was resulted in the sequence of Cyt-b gene.
Figure 1

Phylogenetic tree constructed by MOLE-BLAST where ICII Query_10001 was resulted in the sequence of Cyt-b gene.

3.5.3 Maximum likelihood estimate of substitution matrix

The substitution rates and patterns were estimated using Tamura-Nei (1993) model [16]. The rates of different substitutions are shown in Table 3. The analysis involved 15 nucleotide sequences of the Cyt-b gene, 13 sequences from the present study, and 2 already published sequences. The estimated nucleotide frequencies were A = 30.42%, T/U = 30.77%, C = 27.49%, and G = 11.31%. The maximum Log-likelihood for this computation was −979.044.

Table 3

Maximum likelihood estimate of substitution matrix

A T/U C G
A — 2.74 2.45 7.34
T/U 2.71 — 26.01 1.01
C 2.71 29.11 — 1.01
G 19.73 2.74 2.45 —

A: adenine, T: thymine, U: uracil, G: guanine, C: cytosine.

The bold values represent the rates of different transitional substitutions, and the italics represent the transversions substitutions.

3.5.4 Tajima’s neutrality test

Tajima’s neutrality test was conducted using MEGA X10.1 software for 15 nucleotide sequences of the Cyt-b gene of T. indica. The nucleotide diversity was investigated for the nucleotide sequences of the Cyt-b gene had given 26 segregating sites, including nucleotide diversity of 0.009370 (Table 4).

Table 4

Tajima’s neutrality test based on Cyt-b gene of Tatera indica using MEGA X 10.1

No. sequences “m” No. segregating sites “S” ps = S/n Θ = ps/a1 Nucleotide diversity (π) Tajima’s test statistic “D”
15 26 0.041868 0.012876 0.009370 −1.136164

m: number of sequences, n: total number of sites, S: number of segregating sites.

4 Discussion

Almost all research studies on morphometry of T. indica were of Iranian origin [9,14,17]. However, only two studies reported molecular characterization of T. indica in Iran and Pakistan [9,11]. In Pakistan, most of the studies on T. indica reported its status, habits, and susceptibility as a disease vector. Except for the BW of T. indica, the published morphometric data were not available from Pakistan [18].

Most of the studies worldwide distinguished the coloration of T. indica as brown and black but did not report morphometrics separately. All the specimens captured in the present study were brown. Almost all the morphometric values of T. indica were lower in the present study as compared to the previous studies [8,9,19]. The most closed measurements were reported from Iranian T. indica that was captured from southeastern Iran and adjoining areas of Pakistan [16,20]. Although the mean values of BW corresponded to the previous studies, the minimum BW of rats in the present study was lower (55.42 g) than in all previous reports [8,9,19]. However, all studies found that T. indica from Syria was the heaviest (196–356 g) [19]. The minimum and maximum TBL (240–350 mm) in the present study were the lowest compared to the previous studies. The values of TBL of the Turkish rats were the highest (368–480 mm) among all studies [8]. The values of HBL were also lower in the present study (110–180 mm) as compared to those reported in Iranian (160–300 mm) and Syrian (171–215 mm) studies [9,19]. TL, HFL, and ER were also the lowest in the present study compared to the previous reports from Iran, Syria, and Turkey [8,9,19]. Similarly, almost all the cranial and dental measurements were measured least in the present study compared to the previous reports [8,9,19]. The cranial and dental measurements being positively correlated with body size have been used traditionally for the estimation of body size in rodents [21]. The smaller body size in the present study well explained the lowest cranial and dental measurements.

Body size in small mammals is determined by season, climate, latitude, and food availability and may fluctuate with these factors [17,18,20]. The T. indica captured from northeastern Iran at a higher altitude and cold climate had increased body size than from southeastern regions [20,22,23]. The temperature has a negative association with the body size of these mammals to retain heat in cold climates and emit heat in hot climates. Syria and Turkey are at a higher latitude than the Pothwar region and experience lower temperatures than the Pothwar. The Pothwar region is a sub-tropical plateau exhibiting seasonal temperature fluctuation, but the temperature rarely goes near or below freezing point, especially in areas at lower altitudes. Furthermore, the temperature in summer reaches 45°C or above. Along with these climatic factors, food availability in the area is an important covariate to consider for the variable body size of rodents [20].

The molecular analysis of the Cyt-b gene showed single-nucleotide polymorphisms compared with already published literature submitted in GENBANK. BLAST analysis showed that the sequence of the Cyt-b gene showed more resemblance to the Iranian sample (Accession No. KP001566) than the previously reported sequence of a Pakistani T. indica (Genbank Accession No. AJ430563). Iran shares a border with Pakistan, and migration between the two countries could be a possible reason. The resembling morphometric data on Iranian rats also explain this phenomenon. The present study found, less evidence of presence of sub-species within Pakistan. However, morphometric data along with molecular characterization is novel information reported here. The subspecies status of T. indica is still controversial. In Iran, four different subspecies, namely T. indica persica, T. indica scansa, T. indica monticola, and T. indica bailwardi, were reported earlier (Ellerman 1948). However, later on, only two subspecies namely T. indica indica and T. indica teaniura were recognized in Iran [13]. Furthermore, Mirshamsi et al. found that there is no discrimination between the southern and northern populations of T. indica in Iran [14]. Mohammadi and Pervaizi found two phenotypically different T. indica, i.e., buff-black and buff-brown, but molecularly these are not subspecies [9]. It is also not possible to explain great morphometric variations in the T. indica from other Asian regions (Syria and Turkey) due to the unavailability of genetic data in those studies. The morphometric variations alone could be explained only due to climatic pressure. Molecular approaches are now often used to complement morphological taxonomic methods for the identification of the species, as species identification is the first step in any kind of biological research. Thus, molecular data including numerous new genes yield true biological diversity. The results thus proved that conventional methods of identification by morphometry should be accomplished with molecular techniques to find out the original intraspecific diversity that could be helpful for the species-specific pest management.

5 Conclusion

Almost all the morphometric, cranial, and dental values of T. indica were lower in the present study compared to the previous studies. The molecular analysis indicates the presence of sub-species of T. indica. However, further molecular and morphometric data from other regions are required to validate the presence of sub-species.

  1. Funding information: This research is conducted under the financial assistance of the Pakistan Science Foundation through Grant No. PSF/Res/P-PMAS.AAUR/Bio.446.

  2. Author contributions: Amber Khalid collected samples, performed analysis, and wrote the manuscript. Amjad Rashid Kayani supervised research and revised the manuscript. Mirza Azher Beg conceived the idea and designed the study, supervised research, and reviewed the manuscript. Muhammad Sajid Nadeem provided laboratory facilities and technical support, supervised, and reviewed. Muhammad Mushtaq helped in the sampling and identification of rats, supervised, and reviewed.

  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.

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Received: 2021-12-03
Revised: 2022-04-08
Accepted: 2022-04-15
Published Online: 2022-06-15

© 2022 Amber Khalid et al., published by De Gruyter

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

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  55. Correlation between peripheral blood lymphocyte subpopulations and primary systemic lupus erythematosus
  56. A novel SLC8A1-ALK fusion in lung adenocarcinoma confers sensitivity to alectinib: A case report
  57. β-Hydroxybutyrate upregulates FGF21 expression through inhibition of histone deacetylases in hepatocytes
  58. Identification of metabolic genes for the prediction of prognosis and tumor microenvironment infiltration in early-stage non-small cell lung cancer
  59. BTBD10 inhibits glioma tumorigenesis by downregulating cyclin D1 and p-Akt
  60. Mucormycosis co-infection in COVID-19 patients: An update
  61. Metagenomic next-generation sequencing in diagnosing Pneumocystis jirovecii pneumonia: A case report
  62. Long non-coding RNA HOXB-AS1 is a prognostic marker and promotes hepatocellular carcinoma cells’ proliferation and invasion
  63. Preparation and evaluation of LA-PEG-SPION, a targeted MRI contrast agent for liver cancer
  64. Proteomic analysis of the liver regulating lipid metabolism in Chaohu ducks using two-dimensional electrophoresis
  65. Nasopharyngeal tuberculosis: A case report
  66. Characterization and evaluation of anti-Salmonella enteritidis activity of indigenous probiotic lactobacilli in mice
  67. Aberrant pulmonary immune response of obese mice to periodontal infection
  68. Bacteriospermia – A formidable player in male subfertility
  69. In silico and in vivo analysis of TIPE1 expression in diffuse large B cell lymphoma
  70. Effects of KCa channels on biological behavior of trophoblasts
  71. Interleukin-17A influences the vulnerability rather than the size of established atherosclerotic plaques in apolipoprotein E-deficient mice
  72. Multiple organ failure and death caused by Staphylococcus aureus hip infection: A case report
  73. Prognostic signature related to the immune environment of oral squamous cell carcinoma
  74. Primary and metastatic squamous cell carcinoma of the thyroid gland: Two case reports
  75. Neuroprotective effects of crocin and crocin-loaded niosomes against the paraquat-induced oxidative brain damage in rats
  76. Role of MMP-2 and CD147 in kidney fibrosis
  77. Geometric basis of action potential of skeletal muscle cells and neurons
  78. Babesia microti-induced fulminant sepsis in an immunocompromised host: A case report and the case-specific literature review
  79. Role of cerebellar cortex in associative learning and memory in guinea pigs
  80. Application of metagenomic next-generation sequencing technique for diagnosing a specific case of necrotizing meningoencephalitis caused by human herpesvirus 2
  81. Case report: Quadruple primary malignant neoplasms including esophageal, ureteral, and lung in an elderly male
  82. Long non-coding RNA NEAT1 promotes angiogenesis in hepatoma carcinoma via the miR-125a-5p/VEGF pathway
  83. Osteogenic differentiation of periodontal membrane stem cells in inflammatory environments
  84. Knockdown of SHMT2 enhances the sensitivity of gastric cancer cells to radiotherapy through the Wnt/β-catenin pathway
  85. Continuous renal replacement therapy combined with double filtration plasmapheresis in the treatment of severe lupus complicated by serious bacterial infections in children: A case report
  86. Simultaneous triple primary malignancies, including bladder cancer, lymphoma, and lung cancer, in an elderly male: A case report
  87. Preclinical immunogenicity assessment of a cell-based inactivated whole-virion H5N1 influenza vaccine
  88. One case of iodine-125 therapy – A new minimally invasive treatment of intrahepatic cholangiocarcinoma
  89. S1P promotes corneal trigeminal neuron differentiation and corneal nerve repair via upregulating nerve growth factor expression in a mouse model
  90. Early cancer detection by a targeted methylation assay of circulating tumor DNA in plasma
  91. Calcifying nanoparticles initiate the calcification process of mesenchymal stem cells in vitro through the activation of the TGF-β1/Smad signaling pathway and promote the decay of echinococcosis
  92. Evaluation of prognostic markers in patients infected with SARS-CoV-2
  93. N6-Methyladenosine-related alternative splicing events play a role in bladder cancer
  94. Characterization of the structural, oxidative, and immunological features of testis tissue from Zucker diabetic fatty rats
  95. Effects of glucose and osmotic pressure on the proliferation and cell cycle of human chorionic trophoblast cells
  96. Investigation of genotype diversity of 7,804 norovirus sequences in humans and animals of China
  97. Characteristics and karyotype analysis of a patient with turner syndrome complicated with multiple-site tumors: A case report
  98. Aggravated renal fibrosis is positively associated with the activation of HMGB1-TLR2/4 signaling in STZ-induced diabetic mice
  99. Distribution characteristics of SARS-CoV-2 IgM/IgG in false-positive results detected by chemiluminescent immunoassay
  100. SRPX2 attenuated oxygen–glucose deprivation and reperfusion-induced injury in cardiomyocytes via alleviating endoplasmic reticulum stress-induced apoptosis through targeting PI3K/Akt/mTOR axis
  101. Aquaporin-8 overexpression is involved in vascular structure and function changes in placentas of gestational diabetes mellitus patients
  102. Relationship between CRP gene polymorphisms and ischemic stroke risk: A systematic review and meta-analysis
  103. Effects of growth hormone on lipid metabolism and sexual development in pubertal obese male rats
  104. Cloning and identification of the CTLA-4IgV gene and functional application of vaccine in Xinjiang sheep
  105. Antitumor activity of RUNX3: Upregulation of E-cadherin and downregulation of the epithelial–mesenchymal transition in clear-cell renal cell carcinoma
  106. PHF8 promotes osteogenic differentiation of BMSCs in old rat with osteoporosis by regulating Wnt/β-catenin pathway
  107. A review of the current state of the computer-aided diagnosis (CAD) systems for breast cancer diagnosis
  108. Bilateral dacryoadenitis in adult-onset Still’s disease: A case report
  109. A novel association between Bmi-1 protein expression and the SUVmax obtained by 18F-FDG PET/CT in patients with gastric adenocarcinoma
  110. The role of erythrocytes and erythroid progenitor cells in tumors
  111. Relationship between platelet activation markers and spontaneous abortion: A meta-analysis
  112. Abnormal methylation caused by folic acid deficiency in neural tube defects
  113. Silencing TLR4 using an ultrasound-targeted microbubble destruction-based shRNA system reduces ischemia-induced seizures in hyperglycemic rats
  114. Plant Sciences
  115. Seasonal succession of bacterial communities in cultured Caulerpa lentillifera detected by high-throughput sequencing
  116. Cloning and prokaryotic expression of WRKY48 from Caragana intermedia
  117. Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
  118. Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)
  119. Phytoremediation of pollutants from wastewater: A concise review
  120. Genome-wide identification and characterization of NBS-encoding genes in the sweet potato wild ancestor Ipomoea trifida (H.B.K.)
  121. Alleviative effects of magnetic Fe3O4 nanoparticles on the physiological toxicity of 3-nitrophenol to rice (Oryza sativa L.) seedlings
  122. Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
  123. Study on pecan seed germination influenced by seed endocarp
  124. Identification of active compounds in Ophiopogonis Radix from different geographical origins by UPLC-Q/TOF-MS combined with GC-MS approaches
  125. The entire chloroplast genome sequence of Asparagus cochinchinensis and genetic comparison to Asparagus species
  126. Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant (Camellia sinensis)
  127. Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
  128. Cloning and expression analysis of SERK1 gene in Diospyros lotus
  129. Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
  130. A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
  131. Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
  132. The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
  133. Food Science
  134. Dietary food additive monosodium glutamate with or without high-lipid diet induces spleen anomaly: A mechanistic approach on rat model
  135. Binge eating disorder during COVID-19
  136. Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
  137. FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
  138. Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
  139. Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
  140. Functional constituents of plant-based foods boost immunity against acute and chronic disorders
  141. Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
  142. Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
  143. Ecology and Environmental Sciences
  144. Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
  145. Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
  146. Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
  147. Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
  148. Plant volatile organic compounds attractive to Lygus pratensis
  149. Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
  150. Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
  151. Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
  152. Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
  153. Bioengineering and Biotechnology
  154. Poly-l-lysine-caused cell adhesion induces pyroptosis in THP-1 monocytes
  155. Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
  156. Development and validation of a predictive model for immune-related genes in patients with tongue squamous cell carcinoma
  157. Agriculture
  158. Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
  159. Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions
  160. Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
  161. Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
  162. Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse
  163. Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
  164. Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
  165. Animal Sciences
  166. Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
  167. Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
  168. SI: A Scientific Memoir
  169. Suggestions on leading an academic research laboratory group
  170. My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
  171. Erratum
  172. Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
https://doi.org/10.1515/biol-2022-0063
Schlagwörter für diesen Artikel
Tatera indica; genetics; cytochrome b; molecular DNA; morphometry
Creative Commons
BY 4.0

Artikel in diesem Heft

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  50. Effects of the interaction of Notch and TLR4 pathways on inflammation and heart function in septic heart
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  53. Rapid death due to pulmonary epithelioid haemangioendothelioma in several weeks: A case report
  54. Hepatoprotective role of peroxisome proliferator-activated receptor-α in non-cancerous hepatic tissues following transcatheter arterial embolization
  55. Correlation between peripheral blood lymphocyte subpopulations and primary systemic lupus erythematosus
  56. A novel SLC8A1-ALK fusion in lung adenocarcinoma confers sensitivity to alectinib: A case report
  57. β-Hydroxybutyrate upregulates FGF21 expression through inhibition of histone deacetylases in hepatocytes
  58. Identification of metabolic genes for the prediction of prognosis and tumor microenvironment infiltration in early-stage non-small cell lung cancer
  59. BTBD10 inhibits glioma tumorigenesis by downregulating cyclin D1 and p-Akt
  60. Mucormycosis co-infection in COVID-19 patients: An update
  61. Metagenomic next-generation sequencing in diagnosing Pneumocystis jirovecii pneumonia: A case report
  62. Long non-coding RNA HOXB-AS1 is a prognostic marker and promotes hepatocellular carcinoma cells’ proliferation and invasion
  63. Preparation and evaluation of LA-PEG-SPION, a targeted MRI contrast agent for liver cancer
  64. Proteomic analysis of the liver regulating lipid metabolism in Chaohu ducks using two-dimensional electrophoresis
  65. Nasopharyngeal tuberculosis: A case report
  66. Characterization and evaluation of anti-Salmonella enteritidis activity of indigenous probiotic lactobacilli in mice
  67. Aberrant pulmonary immune response of obese mice to periodontal infection
  68. Bacteriospermia – A formidable player in male subfertility
  69. In silico and in vivo analysis of TIPE1 expression in diffuse large B cell lymphoma
  70. Effects of KCa channels on biological behavior of trophoblasts
  71. Interleukin-17A influences the vulnerability rather than the size of established atherosclerotic plaques in apolipoprotein E-deficient mice
  72. Multiple organ failure and death caused by Staphylococcus aureus hip infection: A case report
  73. Prognostic signature related to the immune environment of oral squamous cell carcinoma
  74. Primary and metastatic squamous cell carcinoma of the thyroid gland: Two case reports
  75. Neuroprotective effects of crocin and crocin-loaded niosomes against the paraquat-induced oxidative brain damage in rats
  76. Role of MMP-2 and CD147 in kidney fibrosis
  77. Geometric basis of action potential of skeletal muscle cells and neurons
  78. Babesia microti-induced fulminant sepsis in an immunocompromised host: A case report and the case-specific literature review
  79. Role of cerebellar cortex in associative learning and memory in guinea pigs
  80. Application of metagenomic next-generation sequencing technique for diagnosing a specific case of necrotizing meningoencephalitis caused by human herpesvirus 2
  81. Case report: Quadruple primary malignant neoplasms including esophageal, ureteral, and lung in an elderly male
  82. Long non-coding RNA NEAT1 promotes angiogenesis in hepatoma carcinoma via the miR-125a-5p/VEGF pathway
  83. Osteogenic differentiation of periodontal membrane stem cells in inflammatory environments
  84. Knockdown of SHMT2 enhances the sensitivity of gastric cancer cells to radiotherapy through the Wnt/β-catenin pathway
  85. Continuous renal replacement therapy combined with double filtration plasmapheresis in the treatment of severe lupus complicated by serious bacterial infections in children: A case report
  86. Simultaneous triple primary malignancies, including bladder cancer, lymphoma, and lung cancer, in an elderly male: A case report
  87. Preclinical immunogenicity assessment of a cell-based inactivated whole-virion H5N1 influenza vaccine
  88. One case of iodine-125 therapy – A new minimally invasive treatment of intrahepatic cholangiocarcinoma
  89. S1P promotes corneal trigeminal neuron differentiation and corneal nerve repair via upregulating nerve growth factor expression in a mouse model
  90. Early cancer detection by a targeted methylation assay of circulating tumor DNA in plasma
  91. Calcifying nanoparticles initiate the calcification process of mesenchymal stem cells in vitro through the activation of the TGF-β1/Smad signaling pathway and promote the decay of echinococcosis
  92. Evaluation of prognostic markers in patients infected with SARS-CoV-2
  93. N6-Methyladenosine-related alternative splicing events play a role in bladder cancer
  94. Characterization of the structural, oxidative, and immunological features of testis tissue from Zucker diabetic fatty rats
  95. Effects of glucose and osmotic pressure on the proliferation and cell cycle of human chorionic trophoblast cells
  96. Investigation of genotype diversity of 7,804 norovirus sequences in humans and animals of China
  97. Characteristics and karyotype analysis of a patient with turner syndrome complicated with multiple-site tumors: A case report
  98. Aggravated renal fibrosis is positively associated with the activation of HMGB1-TLR2/4 signaling in STZ-induced diabetic mice
  99. Distribution characteristics of SARS-CoV-2 IgM/IgG in false-positive results detected by chemiluminescent immunoassay
  100. SRPX2 attenuated oxygen–glucose deprivation and reperfusion-induced injury in cardiomyocytes via alleviating endoplasmic reticulum stress-induced apoptosis through targeting PI3K/Akt/mTOR axis
  101. Aquaporin-8 overexpression is involved in vascular structure and function changes in placentas of gestational diabetes mellitus patients
  102. Relationship between CRP gene polymorphisms and ischemic stroke risk: A systematic review and meta-analysis
  103. Effects of growth hormone on lipid metabolism and sexual development in pubertal obese male rats
  104. Cloning and identification of the CTLA-4IgV gene and functional application of vaccine in Xinjiang sheep
  105. Antitumor activity of RUNX3: Upregulation of E-cadherin and downregulation of the epithelial–mesenchymal transition in clear-cell renal cell carcinoma
  106. PHF8 promotes osteogenic differentiation of BMSCs in old rat with osteoporosis by regulating Wnt/β-catenin pathway
  107. A review of the current state of the computer-aided diagnosis (CAD) systems for breast cancer diagnosis
  108. Bilateral dacryoadenitis in adult-onset Still’s disease: A case report
  109. A novel association between Bmi-1 protein expression and the SUVmax obtained by 18F-FDG PET/CT in patients with gastric adenocarcinoma
  110. The role of erythrocytes and erythroid progenitor cells in tumors
  111. Relationship between platelet activation markers and spontaneous abortion: A meta-analysis
  112. Abnormal methylation caused by folic acid deficiency in neural tube defects
  113. Silencing TLR4 using an ultrasound-targeted microbubble destruction-based shRNA system reduces ischemia-induced seizures in hyperglycemic rats
  114. Plant Sciences
  115. Seasonal succession of bacterial communities in cultured Caulerpa lentillifera detected by high-throughput sequencing
  116. Cloning and prokaryotic expression of WRKY48 from Caragana intermedia
  117. Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
  118. Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)
  119. Phytoremediation of pollutants from wastewater: A concise review
  120. Genome-wide identification and characterization of NBS-encoding genes in the sweet potato wild ancestor Ipomoea trifida (H.B.K.)
  121. Alleviative effects of magnetic Fe3O4 nanoparticles on the physiological toxicity of 3-nitrophenol to rice (Oryza sativa L.) seedlings
  122. Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
  123. Study on pecan seed germination influenced by seed endocarp
  124. Identification of active compounds in Ophiopogonis Radix from different geographical origins by UPLC-Q/TOF-MS combined with GC-MS approaches
  125. The entire chloroplast genome sequence of Asparagus cochinchinensis and genetic comparison to Asparagus species
  126. Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant (Camellia sinensis)
  127. Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
  128. Cloning and expression analysis of SERK1 gene in Diospyros lotus
  129. Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
  130. A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
  131. Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
  132. The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
  133. Food Science
  134. Dietary food additive monosodium glutamate with or without high-lipid diet induces spleen anomaly: A mechanistic approach on rat model
  135. Binge eating disorder during COVID-19
  136. Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
  137. FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
  138. Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
  139. Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
  140. Functional constituents of plant-based foods boost immunity against acute and chronic disorders
  141. Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
  142. Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
  143. Ecology and Environmental Sciences
  144. Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
  145. Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
  146. Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
  147. Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
  148. Plant volatile organic compounds attractive to Lygus pratensis
  149. Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
  150. Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
  151. Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
  152. Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
  153. Bioengineering and Biotechnology
  154. Poly-l-lysine-caused cell adhesion induces pyroptosis in THP-1 monocytes
  155. Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
  156. Development and validation of a predictive model for immune-related genes in patients with tongue squamous cell carcinoma
  157. Agriculture
  158. Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
  159. Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions
  160. Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
  161. Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
  162. Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse
  163. Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
  164. Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
  165. Animal Sciences
  166. Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
  167. Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
  168. SI: A Scientific Memoir
  169. Suggestions on leading an academic research laboratory group
  170. My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
  171. Erratum
  172. Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
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