Non-Additive and Asymmetric Allelic Expression of in Hybrid Tilapia ( ♀ × ♂)

Overview

Journal Animals (Basel)

Date 2024 Jan 23

PMID 38254435

Authors

Zihui Liu

Binglin Chen

Zhiying Zou

Dayu Li

Jinglin Zhu

Jie Yu

Wei Xiao

Hong Yang

Affiliations

Soon will be listed here.

Abstract

Hybridization is a widely used breeding technique in fish species that enhances desirable traits in cultured species through heterosis. However, the mechanism by which hybrids alter gene expression to form heterosis remains unclear. In this study, a group of hybrid tilapia was used to elucidate heterosis through interspecies crossing. Specifically, was analyzed to describe the regulation of gene expression variation in hybrid tilapia. Transcripts from the Nile tilapia allele were found to be significantly higher than those from the blue tilapia allele in hybrid individuals, indicating that the expression of was dominated by Nile tilapia sub-genomic alleles. The study also found a compensatory interaction of cis- and trans-acting elements of the Nile tilapia and blue tilapia sub-genomes, inducing a non-additive expression of in hybrids. Eight specific SNPs were identified in the promoter regions of Nile tilapia and blue tilapia, and were found to be promoter differences leading to differences in gene expression efficiencies between parental alleles using a dual-luciferase reporter system. This study provides insights into the non-additive expression patterns of key functional genes in fish hybrids related to growth and immunity response.

References

Xiao Q, Huang Z, Shen Y, Gan Y, Wang Y, Gong S . Transcriptome analysis reveals the molecular mechanisms of heterosis on thermal resistance in hybrid abalone. BMC Genomics. 2021; 22(1):650. PMC: 8428104. DOI: 10.1186/s12864-021-07954-y. View

Maroni P, Bendinelli P, Zuccorononno C, Schiaffonati L, Piccoletti R . Cellular signalling after in vivo heat shock in the liver. Cell Biol Int. 2000; 24(3):145-52. DOI: 10.1006/cbir.1999.0493. View

Ren P, Deng F, Wang Y, Ran J, Li J, Yin L . Genome-wide analysis of spatiotemporal allele-specific expression in F1 hybrids of meat- and egg-type chickens. Gene. 2020; 747:144671. DOI: 10.1016/j.gene.2020.144671. View

Shi X, Ng D, Zhang C, Comai L, Ye W, Chen Z . Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids. Nat Commun. 2012; 3:950. DOI: 10.1038/ncomms1954. View

Zhang G, Li J, Zhang J, Liang X, Zhang X, Wang T . Integrated Analysis of Transcriptomic, miRNA and Proteomic Changes of a Novel Hybrid Yellow Catfish Uncovers Key Roles for miRNAs in Heterosis. Mol Cell Proteomics. 2019; 18(7):1437-1453. PMC: 6601203. DOI: 10.1074/mcp.RA118.001297. View

Combes M, Hueber Y, Dereeper A, Rialle S, Herrera J, Lashermes P . Regulatory divergence between parental alleles determines gene expression patterns in hybrids. Genome Biol Evol. 2015; 7(4):1110-21. PMC: 4419803. DOI: 10.1093/gbe/evv057. View

Ren L, Cui J, Wang J, Tan H, Li W, Tang C . Analyzing homoeolog expression provides insights into the rediploidization event in gynogenetic hybrids of Carassius auratus red var. × Cyprinus carpio. Sci Rep. 2017; 7(1):13679. PMC: 5651915. DOI: 10.1038/s41598-017-14084-7. View

He F, Zhang X, Hu J, Turck F, Dong X, Goebel U . Genome-wide analysis of cis-regulatory divergence between species in the Arabidopsis genus. Mol Biol Evol. 2012; 29(11):3385-95. DOI: 10.1093/molbev/mss146. View

Zhong H, Zhang X, Xu Q, Yan J, Han Z, Zheng H . Nonadditive and Asymmetric Allelic Expression of Growth Hormone in Hybrid Tilapia. Front Genet. 2019; 10:961. PMC: 6803431. DOI: 10.3389/fgene.2019.00961. View

10.

Dana A, Tuller T . The effect of tRNA levels on decoding times of mRNA codons. Nucleic Acids Res. 2014; 42(14):9171-81. PMC: 4132755. DOI: 10.1093/nar/gku646. View

11.

Lu Y, Boswell M, Boswell W, Kneitz S, Hausmann M, Klotz B . Molecular genetic analysis of the melanoma regulatory locus in Xiphophorus interspecies hybrids. Mol Carcinog. 2017; 56(8):1935-1944. PMC: 5767473. DOI: 10.1002/mc.22651. View

12.

Pastinen T . Genome-wide allele-specific analysis: insights into regulatory variation. Nat Rev Genet. 2010; 11(8):533-8. DOI: 10.1038/nrg2815. View

13.

McManus C, Coolon J, Duff M, Eipper-Mains J, Graveley B, Wittkopp P . Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res. 2010; 20(6):816-25. PMC: 2877578. DOI: 10.1101/gr.102491.109. View

14.

Hansen T, Jorgensen J . Cloning and characterisation of p38 MAP kinase from Atlantic salmon A kinase important for regulating salmon TNF-2 and IL-1beta expression. Mol Immunol. 2007; 44(12):3137-46. DOI: 10.1016/j.molimm.2007.02.006. View

15.

Zhu F, Schlupp I, Tiedemann R . Allele-specific expression at the androgen receptor alpha gene in a hybrid unisexual fish, the Amazon molly (Poecilia formosa). PLoS One. 2017; 12(10):e0186411. PMC: 5638567. DOI: 10.1371/journal.pone.0186411. View

16.

Ren L, Li W, Tao M, Qin Q, Luo J, Chai J . Homoeologue expression insights into the basis of growth heterosis at the intersection of ploidy and hybridity in Cyprinidae. Sci Rep. 2016; 6:27040. PMC: 4893626. DOI: 10.1038/srep27040. View

17.

Hubner N, Wallace C, Zimdahl H, Petretto E, Schulz H, Maciver F . Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease. Nat Genet. 2005; 37(3):243-53. DOI: 10.1038/ng1522. View

18.

Bell G, Kane N, Rieseberg L, Adams K . RNA-seq analysis of allele-specific expression, hybrid effects, and regulatory divergence in hybrids compared with their parents from natural populations. Genome Biol Evol. 2013; 5(7):1309-23. PMC: 3730339. DOI: 10.1093/gbe/evt072. View

19.

Huang X, Huang Y, Ouyang Z, Cai J, Yan Y, Qin Q . Roles of stress-activated protein kinases in the replication of Singapore grouper iridovirus and regulation of the inflammatory responses in grouper cells. J Gen Virol. 2011; 92(Pt 6):1292-1301. DOI: 10.1099/vir.0.029173-0. View

20.

Wang Y, Qiu C, Cui Q . A Large-Scale Analysis of the Relationship of Synonymous SNPs Changing MicroRNA Regulation with Functionality and Disease. Int J Mol Sci. 2015; 16(10):23545-55. PMC: 4632712. DOI: 10.3390/ijms161023545. View