Abstract
The uplift of the Tibetan Plateau significantly altered the geomorphology and climate of the Euroasia by creating large mountains and rivers. Fishes are more likely to be affected relative to other organisms, as they are largely restricted to river systems. Faced with the rapidly flowing water in the Tibetan Plateau, a group of catfish has evolved greatly enlarged pectoral fins with more numbers of fin-rays to form an adhesive apparatus. However, the genetic basis of these adaptations in Tibetan catfishes remains elusive. In this study, we performed comparative genomic analyses based on the chromosome-level genome of Glyptosternum maculatum in family Sisoridae and detected some proteins with conspicuously high evolutionary rates in particular in genes involved in skeleton development, energy metabolism, and hypoxia response. We found that the hoxd12a gene evolved faster and a loss-of-function assay of hoxd12a supports a potential role for this gene in shaping the enlarged fins of these Tibetan catfishes. Other genes with amino acid replacements and signatures of positive selection included proteins involved in low temperature (TRMU) and hypoxia (VHL) responses. Functional assays reveal that the G. maculatumTRMU allele generates more mitochondrial ATP than the ancestral allele found in low-altitude fishes. Functional assays of VHL alleles suggest that the G. maculatum allele has lower transactivation activity than the low-altitude forms. These findings provide a window into the genomic underpinnings of physiological adaptations that permit G. maculatum to survive in the harsh environment of the Tibetan Himalayas that mirror those that are convergently found in other vertebrates such as humans.
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Data availability
Raw sequencing reads have been deposited in NCBI with the BioProject accession PRJNA820898.
References
Ahn, D., and Ho, R.K. (2008). Tri-phasic expression of posterior Hox genes during development of pectoral fins in zebrafish: implications for the evolution of vertebrate paired appendages. Dev Biol 322, 220–233.
Alioto, T., Picardi, E., Guigó, R., and Pesole, G. (2013). ASPic-GeneID: a lightweight pipeline for gene prediction and alternative isoforms detection. Biomed Res Int 2013, 1–11.
Benson, G. (1999). Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27, 573–580.
Bickler, P.E., and Buck, L.T. (2007). Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69, 145–170.
Birney, E., Clamp, M., and Durbin, R. (2004). GeneWise and genomewise. Genome Res 14, 988–995.
Burton, J.N., Adey, A., Patwardhan, R.P., Qiu, R., Kitzman, J.O., and Shendure, J. (2013). Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat Biotechnol 31, 1119–1125.
Cao, L., Huang, Q., Wu, Z., Cao, D.D., Ma, Z., Xu, Q., Hu, P., Fu, Y., Shen, Y., Chan, J., et al. (2016). Neofunctionalization of zona pellucida proteins enhances freeze-prevention in the eggs of Antarctic notothenioids. Nat Commun 7, 12987.
Capella-Gutiérrez, S., Silla-Martínez, J.M., and Gabaldón, T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973.
Chu, X.L., Zheng, B.S., and Dai, D.Y. (1999). Fauna Sinica (Osteichthyes: Siluriformes) (in Chinese). Beijing: Science Press.
Conesa, A., Gotz, S., Garcia-Gomez, J.M., Terol, J., Talon, M., and Robles, M. (2005). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676.
De Bie, T., Cristianini, N., Demuth, J.P., and Hahn, M.W. (2006). CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22, 1269–1271.
Eddy, S.R. (1996). Hidden Markov models. Curr Opin Struct Biol 6, 361–365.
Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792–1797.
El Yacoubi, B., Bailly, M., and de Crécy-Lagard, V. (2012). Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu Rev Genet 46, 69–95.
Emms, D.M., and Kelly, S. (2015). OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16, 157.
Ge, R.L., Cai, Q., Shen, Y.Y., San, A., Ma, L., Zhang, Y., Yi, X., Chen, Y., Yang, L., Huang, Y., et al. (2013). Draft genome sequence of the Tibetan antelope. Nat Commun 4, 1858.
Govoni, K.E., Lee, S.K., Chadwick, R.B., Yu, H., Kasukawa, Y., Baylink, D.J., and Mohan, S. (2006). Whole genome microarray analysis of growth hormone-induced gene expression in bone: T-box3, a novel transcription factor, regulates osteoblast proliferation. Am J Physiol Endocrinol Metab 291, E128–E136.
Guo, X., He, S., and Zhang, Y. (2005). Phylogeny and biogeography of Chinese sisorid catfishes re-examined using mitochondrial cytochrome b and 16S rRNA gene sequences. Mol Phylogenet Evol 35, 344–362.
Haas, B.J., Salzberg, S.L., Zhu, W., Pertea, M., Allen, J.E., Orvis, J., White, O., Buell, C.R., and Wortman, J.R. (2008). Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol 9, R7.
Han, L., Monné, M., Okumura, H., Schwend, T., Cherry, A.L., Flot, D., Matsuda, T., and Jovine, L. (2010). Insights into egg coat assembly and egg-sperm interaction from the X-ray structure of full-length ZP3. Cell 143, 404–415.
Hao, Y., Xiong, Y., Cheng, Y., Song, G., Jia, C., Qu, Y., and Lei, F. (2019). Comparative transcriptomics of 3 high-altitude passerine birds and their low-altitude relatives. Proc Natl Acad Sci USA 116, 11851–11856.
Huang, D.W., Sherman, B.T., and Lempicki, R.A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4, 44–57.
Hui, C., and Joyner, A.L. (1993). A mouse model of Greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat Genet 3, 241–246.
Jiang, W., Lv, Y., Cheng, L., Yang, K., Bian, C., Wang, X., Li, Y., Pan, X., You, X., Zhang, Y., et al. (2019). Whole-genome sequencing of the giant devil catfish, Bagarius yarrelli. Genome Biol Evol 11, 2071–2077.
Jones, P., Binns, D., Chang, H.Y., Fraser, M., Li, W., McAnulla, C., McWilliam, H., Maslen, J., Mitchell, A., Nuka, G., et al. (2014). InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240.
Jurka, J., Kapitonov, V.V., Pavlicek, A., Klonowski, P., Kohany, O., and Walichiewicz, J. (2005). Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110, 462–467.
Kang, S., Xu, Y., You, Q., Flügel, W.A., Pepin, N., and Yao, T. (2010). Review of climate and cryospheric change in the Tibetan Plateau. Environ Res Lett 5, 015101.
Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., and Salzberg, S. L. (2013). TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14, R36.
Kolmogorov, M., Yuan, J., Lin, Y., and Pevzner, P.A. (2019). Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 37, 540–546.
Koren, S., Walenz, B.P., Berlin, K., Miller, J.R., Bergman, N.H., and Phillippy, A.M. (2017). Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 27, 722–736.
Korf, I. (2004). Gene finding in novel genomes. BMC Bioinformatics 5, 59. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10, R25.
Li, H., and Durbin, R. (2011). Inference of human population history from individual whole-genome sequences. Nature 475, 493–496.
Li, J.T., Gao, Y.D., Xie, L., Deng, C., Shi, P., Guan, M.L., Huang, S., Ren, J.L., Wu, D.D., Ding, L., et al. (2018). Comparative genomic investigation of high-elevation adaptation in ectothermic snakes. Proc Natl Acad Sci USA 115, 8406–8411.
Li, M., Tian, S., Jin, L., Zhou, G., Li, Y., Zhang, Y., Wang, T., Yeung, C.K. L., Chen, L., Ma, J., et al. (2013). Genomic analyses identify distinct patterns of selection in domesticated pigs and Tibetan wild boars. Nat Genet 45, 1431–1438.
Liu, H., Liu, Q., Chen, Z., Liu, Y., Zhou, C., Liang, Q., Ma, C., Zhou, J., Pan, Y., Chen, M., et al. (2018). Draft genome of Glyptosternon maculatum, an endemic fish from Tibet Plateau. Gigascience 7.
Liu, X.D., and Dong, B.W. (2013). Influence of the Tibetan Plateau uplift on the Asian monsoon-arid environment evolution. Chin Sci Bull 58, 4277–4291.
Luo, R., Liu, B., Xie, Y., Li, Z., Huang, W., Yuan, J., He, G., Chen, Y., Pan, Q., Liu, Y., et al. (2012). SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1, 18.
Ma, X., Kang, J., Chen, W., Zhou, C., and He, S. (2015). Biogeographic history and high-elevation adaptations inferred from the mitochondrial genome of Glyptosternoid fishes (Sisoridae, Siluriformes) from the southeastern Tibetan Plateau. BMC Evol Biol 15, 233.
Majoros, W.H., Pertea, M., and Salzberg, S.L. (2004). TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878–2879.
Maxwell, P.H., Wiesener, M.S., Chang, G.W., Clifford, S.C., Vaux, E.C., Cockman, M.E., Wykoff, C.C., Pugh, C.W., Maher, E.R., and Ratcliffe, P.J. (1999). The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271–275.
Monaghan, R.M., and Whitmarsh, A.J. (2015). Mitochondrial proteins moonlighting in the nucleus. Trends Biochem Sci 40, 728–735.
Peng, Z., He, S., and Zhang, Y. (2004). Phylogenetic relationships of glyptosternoid fishes (Siluriformes: Sisoridae) inferred from mitochondrial cytochrome b gene sequences. Mol Phylogenet Evol 31, 979–987.
Peng, Z., Ho, S.Y.W., Zhang, Y., and He, S. (2006). Uplift of the Tibetan plateau: evidence from divergence times of glyptosternoid catfishes. Mol Phylogenet Evol 39, 568–572.
Qiu, Q., Zhang, G., Ma, T., Qian, W., Wang, J., Ye, Z., Cao, C., Hu, Q., Kim, J., Larkin, D.M., et al. (2012). The yak genome and adaptation to life at high altitude. Nat Genet 44, 946–949.
Qu, Y., Chen, C., Chen, X., Hao, Y., She, H., Wang, M., Ericson, P.G.P., Lin, H., Cai, T., Song, G., et al. (2021). The evolution of ancestral and species-specific adaptations in snowfinches at the Qinghai-Tibet Plateau. Proc Natl Acad Sci USA 118, e2012398118.
Qu, Y., Zhao, H., Han, N., Zhou, G., Song, G., Gao, B., Tian, S., Zhang, J., Zhang, R., Meng, X., et al. (2013). Ground tit genome reveals avian adaptation to living at high altitudes in the Tibetan Plateau. Nat Commun 4, 2071.
Qu, Y., Chen, C., Xiong, Y., She, H., Zhang, Y.E., Cheng, Y., DuBay, S., Li, D., Ericson, P.G.P., Hao, Y., et al. (2020). Rapid phenotypic evolution with shallow genomic differentiation during early stages of high elevation adaptation in Eurasian Tree Sparrows. Natl Sci Rev 7, 113–127.
Royden, L.H., Burchfiel, B.C., and van der Hilst, R.D. (2008). The geological evolution of the Tibetan Plateau. Science 321, 1054–1058.
Schiffels, S., and Durbin, R. (2014). Inferring human population size and separation history from multiple genome sequences. Nat Genet 46, 919–925.
Spicer, R.A., Su, T., Valdes, P.J., Farnsworth, A., Wu, F.X., Shi, G., Spicer, T.E.V., and Zhou, Z. (2021). Why ‘the uplift of the Tibetan Plateau’ is a myth. Natl Sci Rev 8.
Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
Stanke, M., Diekhans, M., Baertsch, R., and Haussler, D. (2008). Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24, 637–644.
Tarailo-Graovac, M., and Chen, N. (2009). Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinformatics 25.
Thisse, C., and Thisse, B. (2008). High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc 3, 59–69.
Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L., and Pachter, L. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7, 562–578.
Vaser, R., Sović, I., Nagarajan, N., and Šikić, M. (2017). Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res 27, 737–746.
Walker, B.J., Abeel, T., Shea, T., Priest, M., Abouelliel, A., Sakthikumar, S., Cuomo, C.A., Zeng, Q., Wortman, J., Young, S.K., et al. (2014). Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963.
Wang, Y., Shen, Y., Feng, C., Zhao, K., Song, Z., Zhang, Y., Yang, L., and He, S. (2016). Mitogenomic perspectives on the origin of Tibetan loaches and their adaptation to high altitude. Sci Rep 6, 29690.
Wang, K., Shen, Y., Yang, Y., Gan, X., Liu, G., Hu, K., Li, Y., Gao, Z., Zhu, L., Yan, G., et al. (2019). Morphology and genome of a snailfish from the Mariana Trench provide insights into deep-sea adaptation. Nat Ecol Evol 3, 823–833.
Wu, Y.F., and Wu, C.Z. (1992). The Fishes of the Qinghai-Xizang Plateau (in Chinese). Chengdu: Sichuan Science and Technology Press.
Xiao, S.J., Mou, Z.B., Yang, R.B., Fan, D.D., Liu, J.Q., Zou, Y., Zhu, S.L., Zou, M., Zhou, C.W., and Liu, H.P. (2021). Genome and population evolution and environmental adaptation of Glyptosternon maculatum on the Qinghai-Tibet Plateau. Zoological Res 42, 502–513.
Xie, C., Mao, X., Huang, J., Ding, Y., Wu, J., Dong, S., Kong, L., Gao, G., Li, C.Y., and Wei, L. (2011). KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39, W316–W322.
Xiong, Y., Fan, L., Hao, Y., Cheng, Y., Chang, Y., Wang, J., Lin, H., Song, G., Qu, Y., and Lei, F. (2020). Physiological and genetic convergence supports hypoxia resistance in high-altitude songbirds. PloS Genet 16, e1009210.
Yang, L., Wang, Y., Sun, N., Chen, J., and He, S. (2021). Genomic and functional evidence reveals convergent evolution in fishes on the Tibetan Plateau. Mol Ecol 30, 5152–5164.
Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24, 1586–1591.
Yu, L., Wang, G.D., Ruan, J., Chen, Y.B., Yang, C.P., Cao, X., Wu, H., Liu, Y.H., Du, Z.L., Wang, X.P., et al. (2016). Genomic analysis of snubnosed monkeys (Rhinopithecus) identifies genes and processes related to high-altitude adaptation. Nat Genet 48, 941–952.
Yue, P.Q. (2000). Fauna Sinica: Osteichthyes Cypriniformes III (in Chinese). Beijing: Science Press.
Zhang, Z., Xu, D., Wang, L., Hao, J., Wang, J., Zhou, X., Wang, W., Qiu, Q., Huang, X., Zhou, J., et al. (2016). Convergent evolution of rumen microbiomes in high-altitude mammals. Curr Biol 26, 1813–1819.
Zhu, X., Guan, Y., Signore, A.V., Natarajan, C., DuBay, S.G., Cheng, Y., Han, N., Song, G., Qu, Y., Moriyama, H., et al. (2018). Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau. Proc Natl Acad Sci USA 115, 1865–1810.
Acknowledgements
This work was supported by the Strategic Priority Research Program of Chinese Academy of Sciences (XDB31000000), the National Natural Science Foundation of China (32170480, 31972866, 31702016, 31601858, 32022009), Chinese Academy of Sciences (Youth Innovation Promotion Association, Chinese Academy of Sciences (http://www.yicas.cn), the Pioneer Hundred Talents Program, and ZDBS-LY-SM005), the Second Tibetan Plateau Scientific Expedition and Research Program (STEP, 2019QZKK0501), State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences (GREKF21-04), and the Young Top-notch Talent Cultivation Program of Hubei Province. This work was supported by the Wuhan Branch, Supercomputing Center, Chinese Academy of Sciences, China. We are grateful to Prof. Igor Schneider from Instituto de Ciencias Biologicas, Universidade Federal do Para for help with English editing. We thank Prof. Le Kang for the comments of this paper.
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Yang, L., Sun, N., Zeng, H. et al. Enlarged fins of Tibetan catfish provide new evidence of adaptation to high plateau. Sci. China Life Sci. 66, 1554–1568 (2023). https://doi.org/10.1007/s11427-022-2253-7
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DOI: https://doi.org/10.1007/s11427-022-2253-7