Unifying framework explaining how parental regulatory divergence can drive gene expression in hybrids and allopolyploids.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
08 Oct 2024
Historique:
received: 20 07 2023
accepted: 12 09 2024
medline: 9 10 2024
pubmed: 9 10 2024
entrez: 8 10 2024
Statut: epublish

Résumé

Hybridization and polyploidy are powerful evolutionary forces, inducing a range of phenotypic outcomes, including non-additive expression, subgenome dominance, deviations in genomic dosage, and transcriptome downsizing. The reasons for these patterns and whether they are universal adaptive responses to genome merging and doubling remain debated. To address this, we develop a thermodynamic model of gene expression based on transcription factor (TF)-promoter binding. Applied to hybridization between species with divergent gene expression levels, cell volumes, or euchromatic ratios, this model distinguishes the effects of hybridization from those of polyploidy. Our results align with empirical observations, suggesting that gene regulation patterns in hybrids and polyploids often stem from the constrained interplay between inherited diverged regulatory networks rather than from subsequent adaptive evolution. In addition, occurrence of certain phenotypic traits depend on specific assumptions about promoter-TF coevolution and their distribution within the hybrid's nucleoplasm, offering new research avenues to understand the underlying mechanisms. In summary, our model explains how the legacy of divergent species directly influences the phenotypic traits of hybrids and allopolyploids.

Identifiants

pubmed: 39379366
doi: 10.1038/s41467-024-52546-5
pii: 10.1038/s41467-024-52546-5
doi:

Substances chimiques

Transcription Factors 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

8714

Subventions

Organisme : Grantová Agentura České Republiky (Grant Agency of the Czech Republic)
ID : 21-25185S
Organisme : Grantová Agentura České Republiky (Grant Agency of the Czech Republic)
ID : 21-25185S
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy (Ministry of Education, Youth and Sports)
ID : e-INFRA 90254
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy (Ministry of Education, Youth and Sports)
ID : CZ.02.1.01/0.0/0.0/16_025/0007370

Informations de copyright

© 2024. The Author(s).

Références

Veitia, R. A., Bottani, S. & Birchler, J. A. Gene dosage effects: nonlinearities, genetic interactions, and dosage compensation. Trends Genet. 29, 385–393 (2013).
pubmed: 23684842 doi: 10.1016/j.tig.2013.04.004
Yoo, M.-J., Liu, X., Pires, J. C., Soltis, P. S. & Soltis, D. E. Nonadditive gene expression in polyploids. Annu. Rev. Genet. 48, 485–517 (2014).
pubmed: 25421600 doi: 10.1146/annurev-genet-120213-092159
Comeault, A. A. & Matute, D. R. Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation. Proc. Natl Acad. Sci. USA 115, 9761–9766 (2018).
pubmed: 30209213 pmcid: 6166845 doi: 10.1073/pnas.1809685115
Stöck, M. et al. Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum’. Philos. Trans. R. Soc. Lond. B Biol. Sci. 376, 20200103 (2021).
pubmed: 34304588 pmcid: 8310718 doi: 10.1098/rstb.2020.0103
Bartoš, O. et al. The legacy of sexual ancestors in phenotypic variability, gene expression, and homoeolog regulation of asexual hybrids and polyploids. Mol. Biol. Evol. 36, 1902–1920 (2019).
pubmed: 31077330 pmcid: 6735777 doi: 10.1093/molbev/msz114
Li, M., Wang, R., Wu, X. & Wang, J. Homoeolog expression bias and expression level dominance (ELD) in four tissues of natural allotetraploid Brassica napus. BMC Genom. 21, 330 (2020).
doi: 10.1186/s12864-020-6747-1
Gianinetti, A. A criticism of the value of midparent in polyploidization. J. Exp. Bot. 64, 4119–4129 (2013).
pubmed: 24006422 doi: 10.1093/jxb/ert263
Matos, I., Machado, M. P., Schartl, M. & Coelho, M. M. Gene expression dosage regulation in an allopolyploid fish. PLoS ONE 10, e0116309 (2015).
pubmed: 25789776 pmcid: 4366067 doi: 10.1371/journal.pone.0116309
Zhang, M. et al. Effects of parental genetic divergence on gene expression patterns in interspecific hybrids of Camellia. BMC Genom. 20, 828 (2019).
doi: 10.1186/s12864-019-6222-z
Wang, X., Morton, J. A., Pellicer, J., Leitch, I. J. & Leitch, A. R. Genome downsizing after polyploidy: mechanisms, rates and selection pressures. Plant J. 107, 1003–1015 (2021).
pubmed: 34077584 doi: 10.1111/tpj.15363
Goncalves, A. et al. Extensive compensatory cis-trans regulation in the evolution of mouse gene expression. Genome Res. 22, 2376–2384 (2012).
pubmed: 22919075 pmcid: 3514667 doi: 10.1101/gr.142281.112
Hu, G. & Wendel, J. F. Cis–trans controls and regulatory novelty accompanying allopolyploidization. N. Phytol. 221, 1691–1700 (2019).
doi: 10.1111/nph.15515
Mattioli, K. et al. Cis and trans effects differentially contribute to the evolution of promoters and enhancers. Genome Biol. 21, 210 (2020).
pubmed: 32819422 pmcid: 7439725 doi: 10.1186/s13059-020-02110-3
Ren, L. et al. The subgenomes show asymmetric expression of alleles in hybrid lineages of Megalobrama amblycephala × Culter alburnus. Genome Res. 29, 1805–1815 (2019).
pubmed: 31649058 pmcid: 6836732 doi: 10.1101/gr.249805.119
Hollister, J. D. & Gaut, B. S. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 19, 1419–1428 (2009).
pubmed: 19478138 pmcid: 2720190 doi: 10.1101/gr.091678.109
Tulchinsky, A. Y., Johnson, N. A., Watt, W. B. & Porter, A. H. Hybrid incompatibility arises in a sequence-based bioenergetic model of transcription factor binding. Genetics 198, 1155–1166 (2014).
pubmed: 25173845 pmcid: 4224158 doi: 10.1534/genetics.114.168112
Botet, R. & Keurentjes, J. J. B. The role of transcriptional regulation in hybrid vigor. Front. Plant Sci. 11, 410 (2020).
pubmed: 32351526 pmcid: 7174566 doi: 10.3389/fpls.2020.00410
McClintock, B. The significance of responses of the genome to challenge. Science 226, 792–801 (1984).
pubmed: 15739260 doi: 10.1126/science.15739260
GTEx Consortium et al. Genetic effects on gene expression across human tissues. Nature 550, 204–213 (2017).
pmcid: 5776756 doi: 10.1038/nature24277
Wittkopp, P. J., Haerum, B. K. & Clark, A. G. Evolutionary changes in cis and trans gene regulation. Nature 430, 85–88 (2004).
pubmed: 15229602 doi: 10.1038/nature02698
Wittkopp, P. J., Haerum, B. K. & Clark, A. G. Regulatory changes underlying expression differences within and between Drosophila species. Nat. Genet. 40, 346–350 (2008).
pubmed: 18278046 doi: 10.1038/ng.77
Tirosh, I., Reikhav, S., Levy, A. A. & Barkai, N. A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324, 659–662 (2009).
pubmed: 19407207 doi: 10.1126/science.1169766
Emerson, J. J. et al. Natural selection on cis and trans regulation in yeasts. Genome Res. 20, 826–836 (2010).
pubmed: 20445163 pmcid: 2877579 doi: 10.1101/gr.101576.109
Shi, X. et al. Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids. Nat. Commun. 3, 950 (2012).
pubmed: 22805557 doi: 10.1038/ncomms1954
Osada, N., Miyagi, R. & Takahashi, A. Cis- and trans-regulatory effects on gene expression in a natural population of drosophila melanogaster. Genetics 206, 2139–2148 (2017).
pubmed: 28615283 pmcid: 5560811 doi: 10.1534/genetics.117.201459
Chu, D., Zabet, N. R. & Mitavskiy, B. Models of transcription factor binding: sensitivity of activation functions to model assumptions. J. Theor. Biol. 257, 419–429 (2009).
pubmed: 19121637 doi: 10.1016/j.jtbi.2008.11.026
Mueller, F., Stasevich, T. J., Mazza, D. & McNally, J. G. Quantifying transcription factor kinetics: at work or at play? Crit. Rev. Biochem. Mol. Biol. 48, 492–514 (2013).
pubmed: 24025032 doi: 10.3109/10409238.2013.833891
Porter, A. H., Johnson, N. A. & Tulchinsky, A. Y. A new mechanism for mendelian dominance in regulatory genetic pathways: competitive binding by transcription factors. Genetics 205, 101–112 (2017).
pubmed: 27866169 doi: 10.1534/genetics.116.195255
Okubo, K. & Kaneko, K. Evolution of dominance in gene expression pattern associated with phenotypic robustness. BMC Ecol. Evol. 21, 110 (2021).
pubmed: 34092214 pmcid: 8182915 doi: 10.1186/s12862-021-01841-6
Bottani, S., Zabet, N. R., Wendel, J. F. & Veitia, R. A. Gene expression dominance in allopolyploids: hypotheses and models. Trends Plant Sci. 23, 393–402 (2018).
pubmed: 29433919 doi: 10.1016/j.tplants.2018.01.002
Spivakov, M. Spurious transcription factor binding: non-functional or genetically redundant? Bioessays 36, 798–806 (2014).
pubmed: 24888900 pmcid: 4230394 doi: 10.1002/bies.201400036
An, H., Pires, J. C. & Conant, G. C. Gene expression bias between the subgenomes of allopolyploid hybrids is an emergent property of the kinetics of expression. PLOS Computat. Biol. 20, e1011803 (2024).
doi: 10.1371/journal.pcbi.1011803
Coate, J. E. & Doyle, J. J. Quantifying whole transcriptome size, a prerequisite for understanding transcriptome evolution across species: an example from a plant allopolyploid. Genome Biol. Evol. 2, 534–546 (2010).
pubmed: 20671102 pmcid: 2997557 doi: 10.1093/gbe/evq038
Coate, J. E. & Doyle, J. J. Variation in transcriptome size: are we getting the message? Chromosoma 124, 27–43 (2015).
pubmed: 25421950 doi: 10.1007/s00412-014-0496-3
Yoo, M.-J., Szadkowski, E. & Wendel, J. F. Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity 110, 171 (2013).
pubmed: 23169565 doi: 10.1038/hdy.2012.94
Combes, M.-C. et al. Regulatory divergence between parental alleles determines gene expression patterns in hybrids. Genome Biol. Evol. 7, 1110–1121 (2015).
pubmed: 25819221 pmcid: 4419803 doi: 10.1093/gbe/evv057
Bell, G. D. M., Kane, N. C., Rieseberg, L. H. & Adams, K. L. RNA-seq analysis of allele-specific expression, hybrid effects, and regulatory divergence in hybrids compared with their parents from natural populations. Genome Biol. Evol. 5, 1309–1323 (2013).
pubmed: 23677938 pmcid: 3730339 doi: 10.1093/gbe/evt072
Ren, L. et al. Determination of dosage compensation and comparison of gene expression in a triploid hybrid fish. BMC Genom. 18, 38 (2017).
doi: 10.1186/s12864-016-3424-5
Zhang, X., Fang, B. & Huang, Y.-F. Transcription factor binding sites are frequently under accelerated evolution in primates. Nat. Commun. 14, 783 (2023).
pubmed: 36774380 pmcid: 9922303 doi: 10.1038/s41467-023-36421-3
Wunderlich, Z. & Mirny, L. A. Spatial effects on the speed and reliability of protein-DNA search. Nucleic Acids Res. 36, 3570–3578 (2008).
pubmed: 18453629 pmcid: 2441786 doi: 10.1093/nar/gkn173
Stoof, R., Wood, A. & Goñi-Moreno, Á. A model for the spatiotemporal design of gene regulatory circuits †. ACS Synth. Biol. 8, 2007–2016 (2019).
pubmed: 31429541 doi: 10.1021/acssynbio.9b00022
Bottani, S. & Veitia, R. A. Hill function-based models of transcriptional switches: impact of specific, nonspecific, functional and nonfunctional binding. Biol. Rev. Camb. Philos. Soc. 92, 953–963 (2017).
pubmed: 27061969 doi: 10.1111/brv.12262
Tsong, A. E., Tuch, B. B., Li, H. & Johnson, A. D. Evolution of alternative transcriptional circuits with identical logic. Nature 443, 415–420 (2006).
pubmed: 17006507 doi: 10.1038/nature05099
Metzger, B. P. H., Wittkopp, P. J. & Coolon Joseph. D. Evolutionary dynamics of regulatory changes underlying gene expression divergence among saccharomyces species. Genome Biol. Evol. 9, 843–854 (2017).
pubmed: 28338820 pmcid: 5604594 doi: 10.1093/gbe/evx035
Wickham, H. Ggplot2: Elegant Graphics for Data Analysis 1st edn, Vol. 213 (Springer, New York, NY, 2009).

Auteurs

Karel Janko (K)

Laboratory of Non-Mendelian Evolution, Institute of Animal Physiology and Genetics of the Czech Aacademy of Sciences, Rumburská 89, 277 21, Liběchov, Czech Republic. k_janko@yahoo.com.

Jan Eisner (J)

Department of Mathematics, Faculty of Science, University of South Bohemia in České Budějovice, Branišovská 1760, 370 05, České Budějovice, Czech Republic.
Department of Biology and Ecology, Faculty of Natural Sciences, University of Ostrava, Chittussiho 10, Ostrava, Czech Republic.

Petr Cigler (P)

Institute of Organic Chemistry and Biochemistry of the CAS, 166 10, Prague, Czech Republic. petr.cigler@uochb.cas.cz.

Tomáš Tichopád (T)

Department of Biology and Ecology, Faculty of Natural Sciences, University of Ostrava, Chittussiho 10, Ostrava, Czech Republic.
University of South Bohemia in České Budějovice, Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Zátiší 728/II, 389 25, Vodňany, Czech Republic.

Articles similaires

Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family
Animals Natural Killer T-Cells Mice Adipose Tissue Lipid Metabolism

Classifications MeSH