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The Complete Mitochondrial Genome and Expression Profile of Mitochondrial Protein-Coding Genes in the Bisexual and Parthenogenetic Haemaphysalis longicornis.

ABSTRACT: The tick Haemaphysalis longicornis is widely distributed in eastern Asia, New Zealand and Australia, and is well-known as a vector of multiple zoonotic pathogens. This species exhibits two reproductive strategies, bisexual and obligate parthenogenetic reproduction. Hence, in the current study, the complete mitochondrial genomes of the bisexual and parthenogenetic populations were assembled and analyzed, and the expression of the mitochondrial protein-coding genes was evaluated and compared between the two reproductive populations. The results indicated that the length of the mitochondrial genomes of the two reproductive populations is 14,694 and 14,693 bp in the bisexual and parthenogenetic populations, respectively. The AT content in the mitochondrial genome of the bisexual and obligate parthenogenetic population reached 77.22 and 77.34%, respectively. The phylogenetic tree was constructed combining 13 protein-coding genes, which showed that the genetic distance between the bisexual and parthenogenetic populations was less than that between the subspecies. The expression of the mitochondrial protein-coding genes was quantitatively analyzed at different feeding status for the bisexual and parthenogenetic populations, and the results showed significant differences in the expression patterns of these genes, suggesting that they might trigger specific energy utilization mechanisms due to their different reproductive strategies and environmental pressures.

SUBMITTER: Wang T

PROVIDER: S-EPMC6682753 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The tick Haemaphysalis longicornis has two reproductive groups: a bisexual group (HLBP) and a parthenogenetic group (HLPP). The comparative molecular regulation of ovarian development in these two groups is unexplored. We conducted transcriptome sequencing and quantitative proteomics on the ovaries of HLBP and HLPP, in different feeding stages, to evaluate the molecular function of genes associated with ovarian development. The ovarian tissues of HLBP and HLPP were divided into three feeding stages (early-fed, partially-fed and engorged). A total of 87,233 genes and 2,833 proteins were annotated in the ovary of H. longicornis in the different feeding stages. The differentially expressed genes (DEGs) of functional pathway analysis indicated that Lysosome, MAPK Signaling Pathway, Phagosome, Regulation of Actin Cytoskeleton, Endocytosis, Apoptosis, Insulin Signaling Pathway, Oxidative Phosphorylation, and Sphingolipid Metabolism were most abundant in the ovary of H. longicornis in the different feeding stages. Comparing the DEGs between HLBP and HLPP revealed that the ABC Transporter, PI3K-Akt Signaling Pathway and cAMP Signaling Pathway were the most enriched and suggested that the functions of signal transduction mechanisms may have changed during ovarian development. The functions of the annotated proteome of ovarian tissues were strongly correlated with the transcriptome annotation results, and these were further validated using quantitative polymerase chain reaction (qPCR). In the HLBP, the expression of cathepsin L, secreted proteins and glycosidase proteins was significantly up-regulated during feeding stages. In the HLPP, the lysozyme, yolk proteins, heat shock protein, glutathione S transferase, myosin and ATP synthase proteins were up-regulated during feeding stages. The significant differences of the gene expression between HLBP and HLPP indicated that variations in the genetic background and molecular function might exist in the two groups. These results provide a foundation for understanding the molecular mechanism and exploring the functions of genes in the ovarian development of different reproductive groups of H. longicornis.

Project description:BackgroundThe tick Haemaphysalis longicornis exhibits two separate reproductive populations: bisexual and parthenogenetic, which have diploid and triploid karyotypes, respectively. The parthenogenetic population can undergo engorgement without copulation and produce viable female-only offspring with a longer incubation period than the bisexual population. Three enzymes, cathepsin B, cathepsin D and acid phosphatase, were found to be involved in vitellin degradation during the embryonic development of bisexual H. longicornis. However, the expression and activity profiles of these enzymes during the embryonic development of parthenogenetic ticks remain unknown. In the present study, the transcriptional expression profile, enzyme activity and roles in embryogenesis of the three enzymes during the embryonic development of parthenogenetic H. longicornis were investigated.MethodsQuantitative real-time polymerase chain reaction (qPCR) and fluorescence detection were used to analyze the dynamic changes in the three enzymes during embryogenesis. The roles of the three enzymes during embryogenesis were also explored using RNA interference (RNAi).ResultsThe three enzymes were all expressed during embryonic development in parthenogenetic H. longicornis. The expression of cathepsin B was highest on day 15, whereas that of cathepsin D was highest on day 3 and the peak of acid phosphatase expression occurred on day 9. The activity of cathepsin B was highest on day 3 and lowest on day 5, then gradually increased and remained stable. Cathepsin D activity was highest on day 1 and showed a gradually decreasing trend, whereas acid phosphatase showed the opposite trend and reached a peak on day 23. RNA interference experiments in engorged female ticks revealed that there was no significant difference in the number of eggs laid, but the hatching rate of the eggs was significantly decreased.ConclusionThe three enzymes all play important roles in embryonic development of H. longicornis, but the expression patterns and changes in the activity of the enzymes in the bisexual and parthenogenetic populations are different. The results will help a better understanding of the similarities and differences underlying embryonic development in the bisexual and parthenogenetic populations and contribute to the future exploration of the development of the parthenogenetic population of H. longicornis.

Project description:Haemaphysalis longicornis Neumann, 1901 is one of the most well-known hard ticks because of its medical and veterinary importance. Haemaphysalis longicornis transmit a wide range of pathogens among vertebrates, affecting humans and animals in Asia and Oceania. In Japan, the tick species is a major pest of cattle because it can spread a protozoan parasite Theileria orientalis, which causes theileriosis and produces economic losses to the livestock industry (Yokoyama et al. 2012 [1]). Apart from bovine theileriosis, H. longicornis is a vector of bovine babesiosis caused by Babesia ovata, canine babesiosis caused by Babesia gibsoni, and rickettsiosis and viral diseases in humans. Its habitats are mainly Japan, Australia, New Zealand, New Caledonia, the Fiji Islands, Korea, China, and Russia (Oliver et al. 1973 [2]). In the United States, heavy H. longicornis infestations on cattle and white-tailed deer were reported in 2019, making it now one of the tick species to be an increasing threat to livestock animals and humans globally. Ticks reproduce offspring after mating with female and male ticks, however, interestingly, there are two races of H. longicornis: bisexual (diploid) and parthenogenetic (triploid) races [2]. Parthenogenetic H. longicornis is distributed throughout Japan, while the northern limit of the bisexual race is believed to be Fukushima Prefecture on Honshu Island (Fujita et al. 2013 and Kitaoka et al. 1961 [3,4]). This tick species is also considered to be of great scientific importance, and the parthenogenetic race collected in Okayama prefecture has been reared since 1961, while the bisexual race collected in Oita prefecture has been reared since 2008 under laboratory conditions in Japan (Boldbaatar et al. 2010 and Fujisaki et al. 1976 [5,6]). Namely, the "Okayama strain" and "Oita strain" of H. longicornis have been maintained for more than six decades and 15 years, respectively, stably under laboratory conditions. To obtain reference data of bisexual H. longicornis, we sequenced unfed females with haploid genomes using Illumina and MinION Q20 kit then obtained a draft genome consisting of 2.48 Gbp. The number of the contig was 98,529 and N50 was 46.5 Kb. Genome information derived from our laboratory colony of bisexual H. longicornis ticks would provide fundamental insight into understanding how different reproductive lineages occur within the same species of the tick.

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The Complete Mitochondrial Genome and Expression Profile of Mitochondrial Protein-Coding Genes in the Bisexual and Parthenogenetic Haemaphysalis longicornis.

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