Abstract
The dynamic evolution of the scorpion peptide genes in response to selective forces is poorly understood so far. This work aimed to address this issue. We identified a novel K+-channel specific toxin-like peptide with three disulfide bridges from the scorpion Androctonus bicolor, which was named as abTx1. We also cloned and sequenced the genomic genes encoding abTx1 and other 11 K+-channel specific peptides from the scorpion Mesobuthus martensii Karsch. We found that the genes of BmTx1, BmKcug2, BmTx4, BmTx2, BmKcug1a, BmP08, sKTx2 and BmTxKS3 contain two conserved introns, whereas those of BmK38, BmK39, BmKcugx and abTx1 have only one conserved intron. Based on the phylogenetic pattern of the 12 peptides and the commonly accepted view that all the scorpion peptides with three disulfide bridges had derived from a common origin, it can be concluded that the genomic genes of BmTx1, BmKcug2, BmTx4, BmTx2, BmKcug1a, BmP08, sKTx2 and BmTxKS3 gained an intron in their 5'UTRs during the scorpion evolution.
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REFERENCES
Graveley, B.R., Alternative splicing: increasing diversity in the proteomic world, Trends Genet., 2001, vol. 17, no. 2, pp. 100—107.
Keren, H., Lev-Maor, G., and Ast, G., Alternative splicing and evolution: diversification, exon definition and function, Nat. Rev. Genet., 2010, vol. 11, no. 5, pp. 345—355.
Maniatis, T. and Tasic, B., Alternative pre-mRNA splicing and proteome expansion in metazoans, Nature, 2002, vol. 418, no. 6894, pp. 236—243.
Zeng, X.C., Luo, F., and Li, W.X., Characterization of a novel cDNA encoding a short venom peptide derived from venom gland of scorpion Buthus martensii Karsch: trans-splicing may play an important role in the diversification of scorpion venom peptides, Peptides, 2006, vol. 27, no. 4, pp. 675—681.
Modrek, B., Resch, A., Grasso, C., and Lee, C., Genome-wide detection of alternative splicing in expressed sequences of human genes, Nucleic Acids Res., 2001, vol. 29, no. 13, pp. 2850—2859.
Brett, D., Pospisil, H., Valcárcel, J., et al., Alternative splicing and genome complexity, Nat. Genet., 2002, vol. 30, no. 1, pp. 29—30.
Nott, A., Meislin, S.H., and Moore, M.J., A quantitative analysis of intron effects on mammalian gene expression, RNA, 2003, vol. 9, no. 5, pp. 607—617.
Jeffares, D.C., Mourier, T., and Penny, D., The biology of intron gain and loss, Trends Genet., 2006, vol. 22, no. 1, pp. 16—22.
Wang, H.F., Feng, L., and Niu, D.K., Relationship between mRNA stability and intron presence, Biochem. Biophys. Res. Commun., 2007, vol. 354, no. 1, pp. 203—208.
Zhao, C. and Hamilton, T., Introns regulate the rate of unstable mRNA decay, J. Biol. Chem., 2007, vol. 282, no. 28, pp. 20230—20237.
Valencia, P., Dias, A.P., Reed, R., Splicing promotes rapid and efficient mRNA export in mammalian cells, Proc. Natl. Akad. Sci. U.S.A., 2008, vol. 105, no. 9, pp. 3386—3391.
Callis, J., Fromm, M., and Walbot, V., Introns increase gene expression in cultured maize cells, Genes Dev., 1987, vol. 1, no. 10, pp. 1183—1200.
Chung, B.Y., Simons, C., Firth, A.E., et al., Effect of 5'UTR introns on gene expression in Arabidopsis thaliana, BMC. Genomics, 2006, vol. 7, p. 120.
Rose, A.B., Intron-mediated regulation of gene expression, Curr. Top Microbiol. Immunol. 2008, vol. 326, pp. 277—290.
Samadder, P., Sivamani, E., Lu, J., et al., Transcriptional and post-transcriptional enhancement of gene expression by the 5' UTR intron of rice rubi3 gene in transgenic rice cells, Mol. Genet. Genomics, 2008, vol. 279, no. 4, pp. 429—439.
Cenik, C., Derti, A., Mellor, J.C., et al., Genome-wide functional analysis of human 5' untranslated region introns, Genome Biol., 2010, vol. 11, no. 3, p. R29.
Li, W., Tucker, A.E., Sung, W., et al., Extensive, recent intron gains in Daphnia populations, Science, 2009, vol. 326, no. 5957, pp. 1260—1262.
Roy, S.W. and Irimia, M., Mystery of intron gain: new data and new models, Trends Genet., 2009, vol. 25, no. 2, pp. 67—73.
Cavalier-Smith, T., Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion, Ann. Bot., 2005, vol. 95, no. 1, pp. 147—175.
Modrek, B. and Lee, C.J., Alternative splicing in the human, mouse and rat genomes is associated with an increased frequency of exon creation and/or loss, Nat. Genet., 2003, vol. 34, no. 2, pp. 177—180.
Zeng, X.C., Luo, F., and Li, W.X., Molecular dissection of venom from Chinese scorpion Mesobuthus martensii: identification and characterization of four novel disulfide-bridged venom peptides, Peptides, 2006, vol. 27, no. 7, pp. 1745—1754.
Froy, O., Sagiv, T., Poreh, M., et al., Dynamic diversification from a putative common ancestor of scorpion toxins affecting sodium, potassium, and chloride channels, J. Mol. Evol., 1999, vol. 48, no. 2, pp. 187—196.
Zhu, S., Huys, I., Dyason, K., et al., Evolutionary trace analysis of scorpion toxins specific for K-channels, Proteins, 2004, vol. 54, no. 2, pp. 361—370.
Zhijian, C., Feng, L., and Yingliang, W., et al., Genetic mechanisms of scorpion venom peptide diversification, Toxicon, 2006, vol. 47, no. 3, pp. 348—355.
Zeng, X.C., Zhang, L., Nie, Y., et al., Identification and molecular characterization of three new K+-channel specific toxins from the Chinese scorpion Mesobuthus martensii Karsch revealing intronic number polymorphism and alternative splicing in duplicated genes, Peptides, 2012, vol. 34, no. 2, pp. 311—323.
Mu, Y., Zhou, X., Liu, L., et al., Pseudominobacter arsenicus sp. nov., an arsenic-resistant bacterium isolated from arsenic-rich aquifers, Int. J. Syst. Evol. Microbiol., 2019, vol. 69, no. 3, pp. 791—797.
Schweitz, H., Bruhn, T., Guillemare, E., et al., Two different classes of sea anemone toxins for voltage sensitive K+ channels, J. Biol. Chem., 1995, vol. 270, no. 42, pp. 25121—25126.
Angsanakul, J. and Sitprija, V., Scorpion venoms, kidney and potassium, Toxicon, 2013, vol. 73, pp. 81—87.
Rodríguez de la Vega, R.C. and Possani, L.D., Current views on scorpion toxins specific for K+-channels, Toxicon, 2004, vol. 43, no. 8, pp. 865—875.
Zhao, Y., Chen, Z., Cao, Z., et al., Diverse structural features of potassium channels characterized by scorpion toxins as molecular probes, Molecules, 2019, vol. 24, no. 11, p. 2045.
Meng, L., Xie, Z., Zhang, Q., et al., Scorpion potassium channel-blocking defensin highlights a functional link with neurotoxin, J. Biol. Chem., 2016, vol. 291, no. 13, pp. 7097—7106.
Jansa, S.A. and Voss, R.S., Adaptive evolution of the venom-targeted vWF protein in opossums that eat pitvipers, PLoS One, 2011, vol. 6, no. 6. e20997.
Fishman, L., Herrmann, R., Gordon, D., et al., Insect tolerance to a neurotoxic polypeptide: pharmacokinetic and pharmacodynamic aspects, J. Exp. Biol., 1997, vol. 200, part 7, pp. 1115—1123.
Rowe, A.H. and Rowe, M.P., Physiological resistance of grasshopper mice (Onychomys spp.) to Arizona bark scorpion (Centruroides exilicauda) venom, Toxicon, 2008, vol. 52, no. 5, pp. 597—605.
Mawdsley, N. and Stork, N., Species extinctions in insects: ecological and biogeographical considerations, in Insects in a Changing Environment, London: Academic, 1995, pp. 321—369.
Samways, M.J., Insect conservation: a synthetic management approach, Annu. Rev. Entomol., 2007, vol. 52, pp. 465—487.
Barlow, A., Pook, C.E., Harrison, R.A., et al., Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution, Proc. Biol. Sci., 2009, vol. 276, no. 1666, pp. 2443—2449.
Voss, R.S. and Jansa, S.A., Snake-venom resistance as a mammalian trophic adaptation: lessons from didelphid marsupials, Biol. Rev. Camb. Philos. Soc., 2012, vol. 87, no. 4, pp. 822—837.
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X.C.Z was responsible for research designing, provided all the materials, equipment and tools; X.C.Z and W.S wrote the manuscript; Y.W and L.Z conducted all the experiments and data analysis.
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Wu, Y., Zhang, L., Zeng, XC. et al. Intronic Number Polymorphism in the Genes Encoding Potassium Channel Specific Venom Toxins from Scorpion. Russ J Genet 58, 1401–1408 (2022). https://doi.org/10.1134/S1022795422110126
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DOI: https://doi.org/10.1134/S1022795422110126