Point mutations of homologs as an adaptive solution to the gene loss

Guosheng Ma; Xiaojing Zhao; Xinyi Shentu; Liye Zhang

doi:10.1016/j.jgg.2023.02.012

Volume 50 Issue 7

Jul. 2023

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2023 > 50(7): 511-518

PDF( 546 KB)

Point mutations of homologs as an adaptive solution to the gene loss

doi: 10.1016/j.jgg.2023.02.012

a. School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China;
b. Shanghai Clinical Research and Trial Center, Shanghai 201210, China;
c. State Key Laboratory of Cell Biology, Shanghai Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Shanghai 200031, China

Funds:

This work was supported by the National Natural Science Foundation of China (No. 31871332). We also appreciate the linguistic assistance provided by TopEdit (www.topeditsci.com) during the preparation of this manuscript.

Received Date: 2022-10-25
Accepted Date: 2023-02-14
Rev Recd Date: 2023-02-10
Publish Date: 2023-07-28

Abstract

Abstract

Gene loss is common and influences genome evolution trajectories. Multiple adaptive strategies to compensate for gene loss have been observed, including copy number gain of paralogous genes and mutations in genes of the same pathway. By using the Ubl-specific protease 2 (ULP2) eviction model, we identify compensatory mutations in the homologous gene ULP1 by laboratory evolution and find that these mutations are capable of rescuing defects caused by the loss of ULP2. Furthermore, bioinformatics analysis of genomes of yeast gene knockout library and natural yeast isolate datasets suggests that point mutations of a homologous gene might be an additional mechanism to compensate for gene loss.
- Gene loss,
- ULP2,
- Homologous gene,
- Compensatory mutation,
- Genome evolution

FullText(HTML)

References(39)

References

[1]	Albalat, R., Canestro, C., 2016. Evolution by gene loss. Nat. Rev. Genet. 17, 379-391.
[2]	Chen, T., Chen, X., Zhang, S., Zhu, J., Tang, B., Wang, A., Dong, L., Zhang, Z., Yu, C., Sun, Y., et al., 2021. The Genome Sequence Archive family: toward explosive data growth and diverse data types. Genomics Proteomics Bioinformatics 19, 578-583.
[3]	CNCB-NGDC Members and Partners, 2022. Database resources of the National Genomics Data Center, China National Center for Bioinformation in 2023. Nucleic Acids Res. 51, D18-D28.
[4]	Clarke, M.N., Marsoner, T., Adell, M.A.Y., Ravichandran, M.C.,Campbell, C.S., 2022. Adaptation to high rates of chromosomal instability and aneuploidy through multiple pathways in budding yeast. EMBO J., e111500.
[5]	Costanzo, M., VanderSluis, B., Koch, E.N., Baryshnikova, A., Pons, C., Tan, G., Wang, W., Usaj, M., Hanchard, J., Lee, S.D., et al., 2016. A global genetic interaction network maps a wiring diagram of cellular function. Science 353, aaf1420.
[6]	Danecek, P., Bonfield, J.K., Liddle, J., Marshall, J., Ohan, V., Pollard, M.O., Whitwham, A., Keane, T., McCarthy, S.A., Davies, R.M., et al., 2021. Twelve years of samtools and bcftools. GigaScience 10, giab008.
[7]	Diss, G., Ascencio, D., DeLuna, A.,Landry, C.R., 2014. Molecular mechanisms of paralogous compensation and the robustness of cellular networks. J. Exp. Zool. B Mol. Dev. Evol. 322, 488-499.
[8]	Diss, G., Gagnon-Arsenault, I., Dion-Cote, A.M., Vignaud, H., Ascencio, D.I., Berger, C.M.,Landry, C.R., 2017. Gene duplication can impart fragility, not robustness, in the yeast protein interaction network. Science 355, 630-634.
[9]	Dragosits, M.,Mattanovich, D., 2013. Adaptive laboratory evolution -- principles and applications for biotechnology. Microb. Cell Factories 12, 64.
[10]	Giaever, G., Chu, A.M., Ni, L., Connelly, C., Riles, L., Veronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., Andre, B., et al., 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391.
[11]	Huang, C.J., Lu, M.Y., Chang, Y.W.,Li, W.H., 2018. Experimental evolution of yeast for high-temperature tolerance. Mol. Biol. Evol. 35, 1823-1839.
[12]	Hughes, T.R., Roberts, C.J., Dai, H., Jones, A.R., Meyer, M.R., Slade, D., Burchard, J., Dow, S., Ward, T.R., Kidd, M.J., et al., 2000. Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet. 25, 333-337.
[13]	Koboldt, D.C., Zhang, Q., Larson, D.E., Shen, D., McLellan, M.D., Lin, L., Miller, C.A., Mardis, E.R., Ding, L.,Wilson, R.K., 2012. Varscan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. 22, 568-576.
[14]	Kuzmin, E., VanderSluis, B., Nguyen Ba, A.N., Wang, W., Koch, E.N., Usaj, M., Khmelinskii, A., Usaj, M.M., van Leeuwen, J., Kraus, O., et al., 2020. Exploring whole-genome duplicate gene retention with complex genetic interaction analysis. Science 368.
[15]	Lewis, A., Felberbaum, R.,Hochstrasser, M., 2007. A nuclear envelope protein linking nuclear pore basket assembly, sumo protease regulation, and mrna surveillance. J. Cell Biol. 178, 813-827.
[16]	Li, H.,Durbin, R., 2009. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25, 1754-1760.
[17]	Li, S.J.,Hochstrasser, M., 2003. The ulp1 sumo isopeptidase: distinct domains required for viability, nuclear envelope localization, and substrate specificity. J. Cell Biol. 160, 1069-1081.
[18]	Livak, K.J.,Schmittgen, T.D., 2001. Analysis of relative gene expression data using real-time quantitative pcr and the 2(-delta delta c(t)) method. Methods 25, 402-408.
[19]	Lukow, D.A., Sausville, E.L., Suri, P., Chunduri, N.K., Wieland, A., Leu, J., Smith, J.C., Girish, V., Kumar, A.A., Kendall, J., et al., 2021. Chromosomal instability accelerates the evolution of resistance to anti-cancer therapies. Dev. Cell 56, 2427-2439.
[20]	MacArthur, D.G., Balasubramanian, S., Frankish, A., Huang, N., Morris, J., Walter, K., Jostins, L., Habegger, L., Pickrell, J.K., Montgomery, S.B., et al., 2012. A systematic survey of loss-of-function variants in human protein-coding genes. Science 335, 823-828.
[21]	Marchant, A., Cisneros, A.F., Dube, A.K., Gagnon-Arsenault, I., Ascencio, D., Jain, H., Aube, S., Eberlein, C., Evans-Yamamoto, D., Yachie, N., et al., 2019. The role of structural pleiotropy and regulatory evolution in the retention of heteromers of paralogs. Elife 8.
[22]	McMurray, M.A., Bertin, A., Garcia, G., 3rd, Lam, L., Nogales, E.,Thorner, J., 2011. Septin filament formation is essential in budding yeast. Dev. Cell 20, 540-549.
[23]	Ng, P.C.,Henikoff, S., 2001. Predicting deleterious amino acid substitutions. Genome Res. 11, 863-874.
[24]	Pavelka, N., Rancati, G., Zhu, J., Bradford, W.D., Saraf, A., Florens, L., Sanderson, B.W., Hattem, G.L.,Li, R., 2010. Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468, 321-325.
[25]	Peter, J., De Chiara, M., Friedrich, A., Yue, J.X., Pflieger, D., Bergstrom, A., Sigwalt, A., Barre, B., Freel, K., Llored, A., et al., 2018. Genome evolution across 1,011 saccharomyces cerevisiae isolates. Nature 556, 339-344.
[26]	Poirey, R., Despons, L., Leh, V., Lafuente, M.J., Potier, S., Souciet, J.L.,Jauniaux, J.C., 2002. Functional analysis of the saccharomyces cerevisiae dup240 multigene family reveals membrane-associated proteins that are not essential for cell viability. Microbiology (Read.) 148, 2111-2123.
[27]	Puddu, F., Herzog, M., Selivanova, A., Wang, S., Zhu, J., Klein-Lavi, S., Gordon, M., Meirman, R., Millan-Zambrano, G., Ayestaran, I., et al., 2019. Genome architecture and stability in the saccharomyces cerevisiae knockout collection. Nature 573, 416-420.
[28]	Ravichandran, M.C., Fink, S., Clarke, M.N., Hofer, F.C.,Campbell, C.S., 2018. Genetic interactions between specific chromosome copy number alterations dictate complex aneuploidy patterns. Genes Dev. 32, 1485-1498.
[29]	Ryu, H.Y., Lopez-Giraldez, F., Knight, J., Hwang, S.S., Renner, C., Kreft, S.G.,Hochstrasser, M., 2018. Distinct adaptive mechanisms drive recovery from aneuploidy caused by loss of the ulp2 sumo protease. Nat. Commun. 9, 5417.
[30]	Ryu, H.Y., Wilson, N.R., Mehta, S., Hwang, S.S.,Hochstrasser, M., 2016. Loss of the sumo protease ulp2 triggers a specific multichromosome aneuploidy. Genes Dev. 30, 1881-1894.
[31]	Schwienhorst, I., Johnson, E.S.,Dohmen, R.J., 2000. Sumo conjugation and deconjugation. Mol. Gen. Genet. 263, 771-786.
[32]	Shen, X.X., Opulente, D.A., Kominek, J., Zhou, X., Steenwyk, J.L., Buh, K.V., Haase, M.A.B., Wisecaver, J.H., Wang, M., Doering, D.T., et al., 2018. Tempo and mode of genome evolution in the budding yeast subphylum. Cell 175, 1533-1545.
[33]	Tsai, H.J.,Nelliat, A., 2019. A double-edged sword: aneuploidy is a prevalent strategy in fungal adaptation. Genes (Basel) 10.
[34]	Van der Auwera, G.A., Carneiro, M.O., Hartl, C., Poplin, R., Del Angel, G., Levy-Moonshine, A., Jordan, T., Shakir, K., Roazen, D., Thibault, J., et al., 2013. From fastq data to high confidence variant calls: the genome analysis toolkit best practices pipeline. Curr. Protoc. Bioinformatics 43, 11.10.1S1-11.10.33.
[35]	Wang, K., Li, M.,Hakonarson, H., 2010. Annovar: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38, e164.
[36]	Weems, A.D., Johnson, C.R., Argueso, J.L.,McMurray, M.A., 2014. Higher-order septin assembly is driven by gtp-promoted conformational changes: evidence from unbiased mutational analysis in saccharomyces cerevisiae. Genetics 196, 711-727.
[37]	Winzeler, E.A., Shoemaker, D.D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J.D., Bussey, H., et al., 1999. Functional characterization of the s. Cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906.
[38]	Woods, B.L.,Gladfelter, A.S., 2021. The state of the septin cytoskeleton from assembly to function. Curr. Opin. Cell Biol. 68, 105-112.
[39]	Yona, A.H., Manor, Y.S., Herbst, R.H., Romano, G.H., Mitchell, A., Kupiec, M., Pilpel, Y.,Dahan, O., 2012. Chromosomal duplication is a transient evolutionary solution to stress. Proc. Natl. Acad. Sci. U.S.A. 109, 21010-21015.