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Comparative transcriptome and adaptive evolution analysis on the main liver and attaching liver of Pareuchiloglanis macrotrema

  • Animal Genetics • Original Paper
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Abstract

Pareuchiloglanis macrotrema is a glyptosternoid fish belonging to the Siluriform family and is endemic to the Qinghai-Tibet Plateau tributaries. P. macrotrema is an ideal model for studying the adaptive evolution of fish at high altitudes. P. macrotrema has two attaching livers connected to the main liver, a common feature in most Sisoridae fishes but is a special phenomenon relative to other vertebrates. Using RNA-Seq, 42 differentially expressed genes were found between the main liver and attaching liver, of which 31 were upregulated and 11 were downregulated in the main liver. The major differentially expressed genes between the main liver and attaching liver of P. macrotrema are related to metabolism, immunity, and digestive processes. Meanwhile, a comparative transcriptome analysis was carried out on P. macrotrema fish and six non-plateau Siluriformes fishes. We found 268 positively selected genes in P. macrotrema that are related to energy metabolism, immunity, and hypoxic responses. The findings of this study highlight the gene expression differences between the main liver and attaching livers of Sisoridae fishes and provide greater insight into the evolution of Tibetan fishes.

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Data availability

The sequencing reads were deposited in the Sequence Read Archive (SRA) of GenBank (https://www.ncbi.nlm.nih.gov/genbank) under the BioProject number PRJNA751452, and the Python scripts available on the GitHub (https://github.com/byemaxx/callCodeml).

References

  • Amos B, Rolf A (1996) The SWISS-PROT protein sequence data bank and its new supplement TREMBL. Nucleic Acids Res 1:21

    Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Cherry JM (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium Nature Genetics 25:25–29

    Article  CAS  PubMed  Google Scholar 

  • Bakewell MA, Shi P, Zhang J (2007) More genes underwent positive selection in chimpanzee evolution than in human evolution. Proc Natl Acad Sci 104:7489–7494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrett AJ, Woessner JF, Rawlings ND (2012) Handbook of proteolytic enzymes. Elsevier, Miami

    Google Scholar 

  • Becker L et al (2014) MTO1-deficient mouse model mirrors the human phenotype showing complex I defect and cardiomyopathy. PLoS ONE 9:e114918

    Article  PubMed  PubMed Central  Google Scholar 

  • Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60

    Article  CAS  PubMed  Google Scholar 

  • Chen X (2013) Checklist of fishes of Yunnan. Zool Res 34:281–343

    Google Scholar 

  • Chu X (1990) The fishes of Yunnan. China Science Publishing & Media, China

    Google Scholar 

  • Dao W, Li X, Yang HF, Zhou W (2020) Pareuchiloglanis (Teleostei: Sisoridae) from the Pearl River, China with description of three new species. J Fish Biol 96:23–36

    Article  PubMed  Google Scholar 

  • Deng YY, Li JQ, Wu SF, Zhu YP, He FC (2006) Integrated nr database in protein annotation system and its localization. Comput Eng 32:71–72

    Google Scholar 

  • El-Bakary N, El-Gammal HL (2010) Comparative histological, histochemical and ultrastructural studies on the liver of flathead grey mullet (Mugil cephalus) and sea bream (Sparus aurata). Global Veterinaria 4:548–553

    Google Scholar 

  • Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:157

    Article  PubMed  PubMed Central  Google Scholar 

  • Geng L-n, Hu C-j, Li Y-w (2008) Purification and characterization of two kinds of trypsins from the hepatopancreas of grass carp (Ctenopharyngodon Idellus). JOURNAL-CHONGQING NORMAL UNIVERSITY NATURAL SCIENCE EDITION 25:19

    Google Scholar 

  • Gould DB et al (2005) Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly. Science 308:1167–1171

    Article  CAS  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Amit I (2013) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29:644

    Article  Google Scholar 

  • Guo X, He S, Zhang Y (2007) Phylogenetic relationships of the Chinese sisorid catfishes: a nuclear intron versus mitochondrial gene approach. Hydrobiologia 579:55–68

    Article  CAS  Google Scholar 

  • He S (1996) The phylogeny of the glyptosternoid fishes (Teleostei: Siluriformes, Sisoridae). Cybium 20:115–159

    Google Scholar 

  • He S, Cao W, Chen Y (2001) The uplift of Qinghai-Xizang (Tibet) Plateau and the vicariance speciation of glyptosternoid fishes (Siluriformes: Sisoridae). Sci China, Ser C Life Sci 44:644–651

    Article  CAS  Google Scholar 

  • Hightower LE (1991) Heat shock, stress proteins, chaperones, and proteotoxicity. Cell 66:191–197

    Article  CAS  PubMed  Google Scholar 

  • Kang J, Ma X, He S (2017) Evidence of high-altitude adaptation in the glyptosternoid fish, Creteuchiloglanis macropterus from the Nujiang River obtained through transcriptome analysis. BMC Evol Biol 17:1–12

    Article  Google Scholar 

  • Kazutaka, et al (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 12:128–134

    Google Scholar 

  • Kingeter LM, Paul S, Maynard SK, Cartwright NG, Schaefer BC (2010) Cutting edge: TCR ligation triggers digital activation of NF-κB. J Immunol 185:4520–4524

    Article  CAS  PubMed  Google Scholar 

  • Lam-Tung N, Schmidt HA, Arndt VH, Quang MB (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 3:268–274

    Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lecellier CH et al (2005) A cellular microRNA mediates antiviral defense in human cells. Science 308:557–560

    Article  CAS  PubMed  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang Y, Huang T, Li F (1998) Analysis of variants of the angiotensinogen gene in essential hypertension (in Chinese). Chinese Journal of Hypertensi 2:102–105

    Google Scholar 

  • Liu Y-C, Penninger J, Karin M (2005) Immunity by ubiquitylation: a reversible process of modification. Nat Rev Immunol 5:941–952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma X, Dai W, Kang J, Yang L, He S (2016) Comprehensive transcriptome analysis of six catfish species from an altitude gradient reveals adaptive evolution in Tibetan fishes. G3: Genes. Genomes, Genetics 6:141–148

    CAS  Google Scholar 

  • MacDonald MJ, Marshall LK (2000) Mouse lacking NAD+-linked glycerol phosphate dehydrogenase has normal pancreatic beta cell function but abnormal metabolite pattern in skeletal muscle. Arch Biochem Biophys 384:143–153

    Article  CAS  PubMed  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet Journal 17:10–12

    Article  Google Scholar 

  • Minoru K, Susumu G, Shuichi K, Yasushi O, Masahiro H (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277

    Article  Google Scholar 

  • Morimoto RI (1993) Cells in stress: transcriptional activation of heat shock genes. SCIENCE-NEW YORK THEN WASHINGTON- 259:1409–1409

    Article  CAS  Google Scholar 

  • Nair V, Zavolan M (2006) Virus-encoded microRNAs: novel regulators of gene expression. Trends Microbiol 14:169–175

    Article  CAS  PubMed  Google Scholar 

  • Neri LM et al (1997) Changes of nuclear PI-PLC γ1 during rat liver regeneration. Cell Signal 9:353–362

    Article  CAS  PubMed  Google Scholar 

  • Ng HH, Vidthayanon C (2014) A review of the glyptosternine catfish genus Exostoma Blyth 1860 from Thailand, with descriptions of two new species (Teleostei: Siluriformes). Zootaxa 3869:420–434

    Article  PubMed  Google Scholar 

  • Pan Q, Guo G, Fang Z, Li Z (1996) The comparative anatomy studies on digestive system of 6 fish species of stomach-containing teleost in freshwater. Journal Huazhong (Central China) Agricultural University 15:13–17

    CAS  Google Scholar 

  • Peng Z, He S, Zhang Y (2004) Phylogenetic relationships of glyptosternoid fishes (Siluriformes: Sisoridae) inferred from mitochondrial cytochrome b gene sequences. Mol Phylogenet Evol 31:979–987

    Article  CAS  PubMed  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    Article  CAS  PubMed  Google Scholar 

  • Smith DBGJKMOVSRS, John SWM (2007) Col4a1 mutation causes endoplasmic reticulum stress and genetically modifiable ocular dysgenesis. Hum Mol Genet 16:798–807

    Article  PubMed  Google Scholar 

  • Stenmark H (2009) Stenmark, H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10: 513–525. Nat Rev Mol Cell Biol 10:513–525

    Article  CAS  PubMed  Google Scholar 

  • Takle H, Baeverfjord G, Lunde M, Kolstad K, Andersen Ø (2005) The effect of heat and cold exposure on HSP70 expression and development of deformities during embryogenesis of Atlantic salmon (Salmo salar). Aquaculture 249:515–524

    Article  CAS  Google Scholar 

  • Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tom VA et al (2005) Dominant mutations of Col4a1 result in basement membrane defects which lead to anterior segment dysgenesis and glomerulopathy. Hum Mol Genet 23:3161–3168

    Google Scholar 

  • vor F, et al (2007) Type IV procollagen missense mutations associated with defects of the eye, vascular stability, the brain, kidney function and embryonic or postnatal viability in the mouse, Mus musculus: an extension of the Col4a1 allelic series and the identification. Genetics 175:725–736

    Article  Google Scholar 

  • Wang Y et al (2015) Evidence for adaptation to the Tibetan Plateau inferred from Tibetan loach transcriptomes. Genome Biol Evol 7:2970–2982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Knowlton AA, Christensen TG, Shih T, Borkan SC (1999) Prior heat stress inhibits apoptosis in adenosine triphosphate-depleted renal tubular cells. Kidney Int 55:2224–2235

    Article  CAS  PubMed  Google Scholar 

  • Weizhong Li, andAdam, Godzik, (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 12:12–15

    Google Scholar 

  • Wickham H (2011) ggplot2. Wiley Interdisciplinary Reviews: Computational Statistics 3:180–185

    Article  Google Scholar 

  • Xiao S-J et al (2021) Genome and population evolution and environmental adaptation of Glyptosternon maculatum on the Qinghai-Tibet Plateau. Zool Res 42:502

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie C et al (2007) A special organ of Glyptosternum maculatum-extraperitoneal liver (in Chinese). Prog Nat Sci 17:683–686

    Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Wang Y, Zhang Z, He S (2015) Comprehensive transcriptome analysis reveals accelerated genic evolution in a Tibet fish, Gymnodiptychus pachycheilus. Genome Biol Evol 7:251–261

    Article  Google Scholar 

  • Zhang W et al (2014) Hypoxia adaptations in the grey wolf (Canis lupus chanco) from Qinghai-Tibet Plateau. PLoS Genet 10:e1004466

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Hu C, Li Y (2006) Research progress on trypsin from fish in countries (in Chinese). Feed Industry 27:20–22

    Google Scholar 

  • Zhang Y, Han F, Liu L, Wang Z (2016b) Cloning and expression of rab11 gene in large yellow croaker larimichthys crocea (in Chinese). Journal of Jimei University (natural Science) 3:167–174

    Google Scholar 

  • De Pinna MC (1996). A phylogenetic analysis of the Asian catfish families Sisoridae, Akysidae and Amblycipitidae, with a hypothesis on the relationships of the neotropical Aspredinidae (Teleostei, Ostariophysi). Fieldiana Zool (New Ser) 84

  • Ebersberger I, Strauss S, Haeseler AV (2009) HaMStR: profile hidden markov model based search for orthologs in ESTs. BMC Evolutionary Biology,9,1(2009–07–08) 9: 157–157

  • Fricke R (2020) Eschmeyer’s catalog of fishes: genera, species, references. In: California

  • Kottelat M 2013. The fishes of the inland waters of Southeast Asia: a catalogue and core bibliography of the fishes known to occur in freshwaters, mangroves and estuaries. Raffles Bulletin of Zoology

  • Li M (2015) PLCG2 promotes hepatocyte proliferation via NF-kB and ERK pathways during rat liver regeneration (in Chinese). [[Xinxiang]: Henan Normal University

  • Luo J et al (2020) From asymmetrical to balanced genomic diversification during rediploidization: Subgenomic evolution in allotetraploid fish. Science advances 6: eaaz7677

  • Thomson AW, Page LM (2006) Genera of the Asian catfish families Sisoridae and Erethistidae (Teleostei: Siluriformes). Zootaxa 1345: 1–96–91–96

  • Zhang C, Zhao Y, Xing Y, Zhou W, Tang W (2016). Species diversity and distribution of inland fishes in China (pp. 130–148). In: Beijing: Science Press (in Chinese)

  • Zhang H (2011) Study on the occurrence and biological adaptation of liver of Glyptosternum maculatum (in Chinese). [[Wuhan]: Huazhong Agricultural University

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Funding

The study was supported by the 14th Five-Year Aquaculture Breeding Project of Sichuan Province, China (2021YFYZ0015), the Sichuan Science and Technology Program (2021JDRC0135), and the Research project of main economic fish and conservation fish population dynamics in the Yalong River (YLDC-ZBA-2019104).

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Authors and Affiliations

  1. College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, 611130, China

    Qing Wu, Xiaoyang Zhang, Dongjie Wang, Min Liao, Xiaoli Huang, Defang Chen, Yan Wang, Shiyong Yang, Zongjun Du & Wei Luo

  2. Sichuan Runjie Hongda Aquatic Products Technology Co. Ltd, Chengdu, China

    Jie Li

  3. Yalong River Hydropower Development Co. Ltd, Chengdu, China

    Longjun Deng

  4. Agriculture and Rural Bureau of Chongzhou City, Chongzhou, China

    Zhonggang Guo

Authors
  1. Qing Wu
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  2. Xiaoyang Zhang
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Contributions

Conceptualization, Qing Wu, Xiaoyang Zhang, Zongjun Du, and Wei Luo; data curation, Qing Wu and Xiaoyang Zhang; formal analysis, Qing Wu and Xiaoyang Zhang; methodology, Qing Wu, Xiaoli Huang, Defang Chen, Yan Wang, and Shiyong Yang; project administration, Longjun Deng, Zongjun Du, and Wei Luo; resources, Jie Li and Zhonggang Guo; validation, Xiaoyang Zhang, Dongjie Wang and Min Liao; writing — original draft, Qing Wu; writing — review & editing, Qing Wu and Wei Luo.

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Correspondence to Zongjun Du or Wei Luo.

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Communicated by Maciej Szydlowski.

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Wu, Q., Zhang, X., Li, J. et al. Comparative transcriptome and adaptive evolution analysis on the main liver and attaching liver of Pareuchiloglanis macrotrema. J Appl Genetics 63, 743–761 (2022). https://doi.org/10.1007/s13353-022-00712-0

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