Impact of Z chromosome inversions on gene expression in testis and liver tissues in the zebra finch

. 2024 Dec ; 33 (24) : e17236. [epub] 20231221

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38126688

Grantová podpora
19-22538S Czech Science Foundation
301592 Norges Forskningsråd

Chromosomal inversions have been identified in many natural populations and can be responsible for novel traits and rapid adaptation. In zebra finch, a large region on the Z chromosome has been subject to multiple inversions, which have pleiotropic effects on multiple traits but especially on sperm phenotypes, such as midpiece and flagellum length. To understand the effect, the Z inversion has on these traits, we examined testis and liver transcriptomes of young males at different maturation times. We compared gene expression differences among three inversion karyotypes: AA, B*B* and AB*, where B* denotes the inverted regions on Z with respect to A. In testis, 794 differentially expressed genes were found and most of them were located on chromosome Z. They were functionally enriched for sperm-related traits. We also identified clusters of co-expressed genes that matched with the inversion-related sperm phenotypes. In liver, there were some enriched functions and some overrepresentation on chromosome Z with similar location as in testis. In both tissues, the overrepresented genes were located near the distal end of Z but also in the middle of the chromosome. For the heterokaryotype, we observed several genes with one allele being dominantly expressed, similar to expression patterns in one or the other homokaryotype. This was confirmed with SNPs for three genes, and interestingly one gene, DMGDH, had allele-specific expression originating mainly from one inversion haplotype in the testis, yet both inversion haplotypes were expressed equally in the liver. This karyotype-specific difference in tissue-specific expression suggests a pleiotropic effect of the inversion and thus suggests a mechanism for divergent phenotypic effects resulting from an inversion.

Zobrazit více v PubMed

Aire, T. A. (2014). Spermiogenesis in birds. Spermatogenesis, 4(1), e34346. 10.4161/spmg.34346 PubMed DOI PMC

Bailey, T. L. , & Grant, C. E. (2021). SEA: Simple enrichment analysis of motifs. BioRxiv, 2021.08.23.457422 10.1101/2021.08.23.457422v1.abstract DOI

Berdan, E. L. , Mérot, C. , Pavia, H. , Johannesson, K. , Wellenreuther, M. , & Butlin, R. K. (2021). A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida). Evolution Letters, 5(6), 607–624. 10.1002/evl3.260 PubMed DOI PMC

Brionne, A. , Juanchich, A. , & Hennequet‐Antier, C. (2019). ViSEAGO: A Bioconductor package for clustering biological functions using Gene Ontology and semantic similarity. Biodata Mining, 12(1), 1–13. 10.1186/s13040-019-0204-1 PubMed DOI PMC

Buchberger, E. , Reis, M. , Lu, T. H. , & Posnien, N. (2019). Cloudy with a chance of insights: Context dependent gene regulation and implications for evolutionary studies. Genes, 10(7), 492. 10.3390/genes10070492 PubMed DOI PMC

Carreras‐Gallo, N. , Cáceres, A. , Balagué‐Dobón, L. , Ruiz‐Arenas, C. , Andrusaityte, S. , Carracedo, Á. , Casas, M. , Chatzi, L. , Grazuleviciene, R. , Gutzkow, K. B. , Lepeule, J. , Maitre, L. , Nieuwenhuijsen, M. , Slama, R. , Stratakis, N. , Thomsen, C. , Urquiza, J. , Wright, J. , Yang, T. , … González, J. R. (2022). The early‐life exposome modulates the effect of polymorphic inversions on DNA methylation. Communications Biology, 5(1), 455. 10.1038/s42003-022-03380-2 PubMed DOI PMC

Castro‐Mondragon, J. A. , Riudavets‐Puig, R. , Rauluseviciute, I. , Berhanu Lemma, R. , Turchi, L. , Blanc‐Mathieu, R. , Lucas, J. , Boddie, P. , Khan, A. , Perez, N. M. , Fornes, O. , Leung, T. Y. , Aguirre, A. , Hammal, F. , Schmelter, D. , Baranasic, D. , Ballester, B. , Sandelin, A. , Lenhard, B. , … Mathelier, A. (2022). JASPAR 2022: The 9th release of the open‐access database of transcription factor binding profiles. Nucleic Acids Research, 50(D1), D165–D173. 10.1093/nar/gkab1113 PubMed DOI PMC

Chan, Y. F. , Marks, M. E. , Jones, F. C. , Villarreal, G. , Shapiro, M. D. , Brady, S. D. , Southwick, A. M. , Absher, D. M. , Grimwood, J. , Schmutz, J. , Myers, R. M. , Petrov, D. , Jonsson, B. , Schluter, D. , Bell, M. A. , & Kingsley, D. M. (2010). Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science, 327(5963), 302–305. 10.1126/science.1182213 PubMed DOI PMC

Crow, T. , Ta, J. , Nojoomi, S. , Aguilar‐Rangel, M. R. , Rodríguez, J. V. T. , Gates, D. , Rellán‐Álvarez, R. , Sawers, R. , & Runcie, D. (2020). Gene regulatory effects of a large chromosomal inversion in highland maize. PLoS Genetics, 16, 1–28. 10.1371/journal.pgen.1009213 PubMed DOI PMC

Danecek, P. , Bonfield, J. K. , Liddle, J. , Marshall, J. , Ohan, V. , Pollard, M. O. , Whitwham, A. , Keane, T. , McCarthy, S. A. , Davies, R. M. , & Li, H. (2021). Twelve years of SAMtools and BCFtools. GigaScience, 10(2), 1–4. 10.1093/gigascience/giab008 PubMed DOI PMC

Dobin, A. , Davis, C. A. , Schlesinger, F. , Drenkow, J. , Zaleski, C. , Jha, S. , Batut, P. , Chaisson, M. , & Gingeras, T. R. (2013). STAR: Ultrafast universal RNA‐seq aligner. Bioinformatics, 29(1), 15–21. 10.1093/bioinformatics/bts635 PubMed DOI PMC

Fatica, A. , & Bozzoni, I. (2014). Long non‐coding RNAs: New players in cell differentiation and development. Nature Reviews Genetics, 15(1), 7–21. 10.1038/nrg3606 PubMed DOI

Fisher, H. S. (2017). Supergene yields super sperm. Nature Ecology & Evolution, 1(8), 1064–1065. 10.1038/s41559-017-0261-0 PubMed DOI

Forstmeier, W. , Segelbacher, G. , Mueller, J. C. , & Kempenaers, B. (2007). Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata). Molecular Ecology, 16(19), 4039–4050. 10.1111/j.1365-294X.2007.03444.x PubMed DOI

Fuller, Z. L. , Haynes, G. D. , Richards, S. , & Schaeffer, S. W. (2016). Genomics of natural populations: How differentially expressed genes shape the evolution of chromosomal inversions in Drosophila pseudoobscura . Genetics, 204(1), 287–301. 10.1534/genetics.116.191429 PubMed DOI PMC

Ge, S. X. , Jung, D. , Jung, D. , & Yao, R. (2018). ShinyGO: A graphical enrichment tool for ani‐mals and plants. BioRxiv, 36(December 2019), 315150. 10.1101/082511.Lai DOI

Guioli, S. , Lovell‐Badge, R. , & Turner, J. M. A. (2012). Error‐prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line. PLoS Genetics, 8(3), e1002560. 10.1371/journal.pgen.1002560 PubMed DOI PMC

Itoh, Y. , Kampf, K. , Balakrishnan, C. N. , & Arnold, A. P. (2011). Karyotypic polymorphism of the zebra finch Z chromosome. Chromosoma, 120(3), 255–264. 10.1007/s00412-010-0308-3 PubMed DOI PMC

Johnson, A. R. , Lao, S. , Wang, T. , Galanko, J. A. , & Zeisel, S. H. (2012). Choline dehydrogenase polymorphism rs12676 is a functional variation and is associated with changes in human sperm cell function. PLoS One, 7(4), 1–12. 10.1371/journal.pone.0036047 PubMed DOI PMC

Jumeau, F. , Chalmel, F. , Fernandez‐Gomez, F. J. , Carpentier, C. , Obriot, H. , Tardivel, M. , Caillet‐Boudin, M. L. , Rigot, J. M. , Rives, N. , Buée, L. , Sergeant, N. , & Mitchell, V. (2017). Defining the human sperm microtubulome: An integrated genomics approach. Biology of Reproduction, 96(1), 93–106. 10.1095/biolreprod.116.143479 PubMed DOI

Kahrl, A. F. , Snook, R. R. , & Fitzpatrick, J. L. (2022). Fertilization mode differentially impacts the evolution of vertebrate sperm components. Nature Communications, 13(1), 6809. 10.1038/s41467-022-34609-7 PubMed DOI PMC

Kim, K.‐W. , Bennison, C. , Hemmings, N. , Brookes, L. , Hurley, L. L. , Griffith, S. C. , Burke, T. , Birkhead, T. R. , & Slate, J. (2017). A sex‐linked supergene controls sperm morphology and swimming speed in a songbird. Nature Ecology and Evolution, 1(8), 1168–1176. 10.1038/s41559-017-0235-2 PubMed DOI

Kim, K.‐W. , Bennison, C. , Hemmings, N. , Brookes, L. , Hurley, L. L. , Griffith, S. C. , Burke, T. , Birkhead, T. R. , & Slate, J. (2018). Data from: A sex‐linked supergene controls sperm morphology and swimming speed in a songbird . Dryad. 10.5061/dryad.p4238 PubMed DOI

Kleinjan, D. A. , & van Heyningen, V. (2005). Long‐range control of gene expression: Emerging mechanisms and disruption in disease. The American Journal of Human Genetics, 76(1), 8–32. 10.1086/426833 PubMed DOI PMC

Knief, U. , Forstmeier, W. , Kempenaers, B. , & Wolf, J. B. W. (2021). A sex chromosome inversion is associated with copy number variation of mitochondrial DNA in zebra finch sperm. Royal Society Open Science, 8(9), 211025. 10.1098/rsos.211025 PubMed DOI PMC

Knief, U. , Forstmeier, W. , Pei, Y. , Ihle, M. , Wang, D. , Martin, K. , Opatová, P. , Albrechtová, J. , Wittig, M. , Franke, A. , Albrecht, T. , & Kempenaers, B. (2017). A sex‐chromosome inversion causes strong overdominance for sperm traits that affect siring success. Nature Ecology & Evolution, 1(8), 1177–1184. 10.1038/s41559-017-0236-1 PubMed DOI

Knief, U. , Hemmrich‐Stanisak, G. , Wittig, M. , Franke, A. , Griffith, S. C. , Kempenaers, B. , & Forstmeier, W. (2016). Fitness consequences of polymorphic inversions in the zebra finch genome. Genome Biology, 17(1), 199. 10.1186/s13059-016-1056-3 PubMed DOI PMC

Koch, E. L. , Morales, H. E. , Larsson, J. , Westram, A. M. , Faria, R. , Lemmon, A. R. , Lemmon, E. M. , Johannesson, K. , & Butlin, R. K. (2021). Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis . Evolution Letters, 5(3), 196–213. 10.1002/evl3.227 PubMed DOI PMC

Kosuthova, K. , & Solc, R. (2022). Inversions on human chromosomes. American Journal of Medical Genetics, Part A, 191, 672–683. 10.1002/ajmg.a.63063 PubMed DOI

Laiho, A. , Kotaja, N. , Gyenesei, A. , & Sironen, A. (2013). Transcriptome profiling of the murine testis during the first wave of spermatogenesis. PLoS One, 8(4), e61558. 10.1371/journal.pone.0061558 PubMed DOI PMC

Laskemoen, T. , Albrecht, T. , Bonisoli‐Alquati, A. , Cepak, J. , de Lope, F. , Hermosell, I. G. , Johannessen, L. E. , Kleven, O. , Marzal, A. , Mousseau, T. A. , Møller, A. P. , Robertson, R. J. , Rudolfsen, G. , Saino, N. , Vortman, Y. , & Lifjeld, J. T. (2013). Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations. Behavioral Ecology and Sociobiology, 67(2), 301–309. 10.1007/s00265-012-1450-0 DOI

Lavington, E. , & Kern, A. D. (2017). The effect of common inversion polymorphisms in(2L)t and in(3R)Mo on patterns of transcriptional variation in Drosophila melanogaster. G3: Genes, Genomes, Genetics, 7(11), 3659–3668. 10.1534/g3.117.1133 PubMed DOI PMC

Law, C. W. , Chen, Y. , Shi, W. , & Smyth, G. K. (2014). Voom: Precision weights unlock linear model analysis tools for RNA‐seq read counts. Genome Biology, 15(2), R29. 10.1186/gb-2014-15-2-r29 PubMed DOI PMC

Lifjeld, J. T. , Laskemoen, T. , Kleven, O. , Albrecht, T. , & Robertson, R. J. (2010). Sperm length variation as a predictor of extrapair paternity in passerine birds. PLoS One, 5(10), e13456. 10.1371/journal.pone.0013456 PubMed DOI PMC

Martin, M. (2011). Cutadapt removes adapter sequences from high‐throughput sequencing reads. EMBnet Journal, 17(1), 10. 10.14806/ej.17.1.200 DOI

Míčková, K. , Tomášek, O. , Jelínek, V. , Šulc, M. , Pazdera, L. , Albrechtová, J. , & Albrecht, T. (2023). Age‐related changes in sperm traits and evidence for aging costs of sperm production in a sexually promiscuous passerine. Frontiers in Ecology and Evolution, 11, 1–9. 10.3389/fevo.2023.1105596 PubMed DOI

Pei, Y. (2021). Evolutionary genetics of reproductive performance in the zebra finch (Issue August) .

Pigozzi, M. I. (2022). A bird's‐eye view of chromosomes during meiotic prophase I. Journal of Basic and Applied Genetics, 33(1), 27–41. 10.35407/bag.2022.33.01.02 DOI

Pitnick, S. , Hosken, D. J. , & Birkhead, T. R. (2009). Sperm morphological diversity. In Birkhead T. R., Hosken D. J., & Pitnick S. (Eds.), Sperm biology: An evolutionary perspective (1st ed., pp. 69–149). Elsevier.

Prichard, M. R. , Grogan, K. E. , Merritt, J. R. , Root, J. , & Maney, D. L. (2022). Allele‐specific cis‐regulatory methylation of the gene for vasoactive intestinal peptide in white‐throated sparrows. Genes, Brain and Behavior, 21(8), 1–12. 10.1111/gbb.12831 PubMed DOI PMC

Puig, M. , Casillas, S. , Villatoro, S. , & Cáceres, M. (2015). Human inversions and their functional consequences. Briefings in Functional Genomics, 14(5), 369–379. 10.1093/bfgp/elv020 PubMed DOI PMC

R Core Team . (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r‐project.org/

Robinson, M. D. , McCarthy, D. J. , & Smyth, G. K. (2009). edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26(1), 139–140. 10.1093/bioinformatics/btp616 PubMed DOI PMC

Sabarís, G. , Laiker, I. , Preger‐Ben Noon, E. , & Frankel, N. (2019). Actors with multiple roles: Pleiotropic enhancers and the paradigm of enhancer modularity. Trends in Genetics, 35(6), 423–433. 10.1016/j.tig.2019.03.006 PubMed DOI

Segami, J. C. , Semon, M. , Cunha, C. , Bergin, C. , Mugal, C. F. , & Qvarnström, A. (2022). Single‐Cell Transcriptomics reveals relaxed evolutionary constraint of spermatogenesis in two passerine birds as compared to mammals. BioRxiv Pre‐Print, 1–40. 10.14341/Conf7-8.09.22-98-99 DOI

Smyth, G. K. (2005). Limma: Linear models for microarray data. In Gentleman R., Carey V. J., Huber W., Irizarry R. A., & Dudoit S. (Eds.), Bioinformatics and computational biology solutions using R and Bioconductor (pp. 397–420). Springer‐Verlag. 10.1007/0-387-29362-0_23 DOI

van der Heijden, G. W. , Eijpe, M. , & Baarends, W. M. (2011). The X and y chromosome in meiosis: How and why they keep silent. Asian Journal of Andrology, 13(6), 779–780. 10.1038/aja.2011.93 PubMed DOI PMC

Wei, J. W. , Huang, K. , Yang, C. , & Kang, C. S. (2017). Non‐coding RNAs as regulators in epigenetics (Review). Oncology Reports, 37(1), 3–9. 10.3892/or.2016.5236 PubMed DOI

Wellenreuther, M. , Mérot, C. , Berdan, E. , & Bernatchez, L. (2019). Going beyond SNPs: The role of structural genomic variants in adaptive evolution and species diversification. Molecular Ecology, 28(6), 1203–1209. 10.1111/mec.15066 PubMed DOI

Whiting, J. R. (2022). JimWhiting91/genotype_plot: Genotype Plot . 10.5281/zenodo.5913504 DOI

Zhang, X. , Zhang, P. , Song, D. , Xiong, S. , Zhang, H. , Fu, J. , Gao, F. , Chen, H. , & Zeng, X. (2019). Expression profiles and characteristics of human lncRNA in normal and asthenozoospermia sperm. Biology of Reproduction, 100(4), 982–993. 10.1093/biolre/ioy253 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...