Asymmetric expression patterns reveal a strong maternal effect and dosage compensation in polyploid hybrid fish

BMC Genomics

Volumn 19, Issue 1, 2018, Pages

  Li, Wuhui ^a   Liu, Junmei ^a   Tan, Hui ^a   Luo, Lingling ^a   Cui, Jialin ^a   Hu, Jie ^a   Wang, Shi ^a   Liu, Qingfeng ^a   Hu, Fangzhou ^a   Tang, Chenchen ^a   Ren, Li ^a   Yang, Conghui ^a   Zhao, Rurong ^a   Tao, Min ^a   Zhang, Chun ^a   Qin, Qinbo ^a   Liu, Shaojun ^a  

^a HUNAN NORMAL UNIVERSITY   (China)

Author keywords

Dosage compensation; Duplicated genes; Hybridization; Maternal effect; Transcriptome

Indexed keywords

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; FISH; GENE DOSAGE; GENE DUPLICATION; GENE EXPRESSION; HYBRIDIZATION; MALE; MEGALOBRAMA AMBLYCEPHALA; NONHUMAN; PLOIDY; POLYPLOIDY; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; SANGER SEQUENCING; TRANSCRIPTOMICS; XENOCYPRI DAVIDI; ANIMAL; CHEMISTRY; CHIMERA; CYPRINIDAE; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; MATERNAL INHERITANCE; METABOLISM; SEQUENCE ANALYSIS; TESTIS;

RNA; TRANSCRIPTOME;

ANIMALS; CHIMERA; CYPRINIDAE; DOSAGE COMPENSATION, GENETIC; FEMALE; MALE; MATERNAL INHERITANCE; POLYPLOIDY; RNA; SEQUENCE ANALYSIS, RNA; TESTIS; TRANSCRIPTOME;

EID: 85049454386     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-018-4883-7     Document Type: Article

References (70)

1. Rieseberg LH, Willis JH. Plant speciation. Science. 2007;317(5840):910-4.
2. Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF. Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet. 2008;42:443.
3. Mallet J. Hybridization as an invasion of the genome. Trends Ecol Evol. 2005;20:229-37.
4. Sumpter JP, Lincoln RF, Bye VJ, Carragher JF, Bail PYL. Plasma growth hormone levels during sexual maturation in diploid and triploid rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol. 1991;83(1):103.
5. Hu J, Liu S, Xiao J, Zhou Y, You C, He W, Zhao R, Song C, Liu Y. Characteristics of diploid and triploid hybrids derived from female Megalobrama amblycephala Yih × male Xenocypris davidi Bleeker. Aquaculture. 2012;364:157-64.
6. He W, Xie L, Li T, Liu S, Xiao J, Hu J, Wang J, Qin Q, Liu Y. The formation of diploid and triploid hybrids of female grass carp x male blunt snout bream and their 5S rDNA analysis. BMC Genet. 2013;14(1):110.
7. Xiao J, Kang X, Xie L, Qin Q, He Z, Hu F, Zhang C, Zhao R, Wang J, Luo K, et al. The fertility of the hybrid lineage derived from female Megalobrama amblycephala × male Culter alburnus. Anim Reprod Sci. 2014;151(1-2):61-70.
8. Huang S, Cao X, Wang W, Nasr M. Fertility and ploidy of gametes of allodiploid and allotriploid loaches produced by diploid Misgurnus anguillicaudatus females and Paramisgurnus dabryanus males. Fish Physiol Biochem. 2018;44(1):13-20.
9. Soltis PS, Soltis DE. The role of hybridization in plant speciation. Annu Rev Plant Biol. 2009;60:561-88.
10. Jiang B, Lou Q, Wu Z, Zhang W, Wang D, Mbira KG, Weng Y, Chen J. Retrotransposon- and microsatellite sequence-associated genomic changes in early generations of a newly synthesized allotetraploid Cucumis × hytivus Chen & Kirkbride. Plant Mol Biol. 2011;77(3):225.
11. Feldman M, Liu B, Segal G, Abbo S, Levy AA, Vega JM. Rapid elimination of low-copy DNA sequences in polyploid wheat: a possible mechanism for differentiation of homoeologous chromosomes. Genetics. 1997;147(3):1381-7.
12. Livingstone K, Rieseberg L. Chromosomal evolution and speciation: a recombination-based approach. New Phytol. 2004;161(1):107-12.
13. Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J, Luo D. Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell. 2006;18(3):676-87.
14. Wang H, Jiang J, Chen S, Qi X, Fang W, Guan Z, Teng N, Liao Y, Chen F. Rapid genetic and epigenetic alterations under intergeneric genomic shock in newly synthesized Chrysanthemum morifolium x Leucanthemum paludosum hybrids (Asteraceae). Genome Biol Evol. 2014;6(1):247-59.
15. Chen ZJ. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol. 2007;58(1):377.
16. Madlung A, Tyagi AP, Watson B, Jiang H, Kagochi T, Doerge RW, Martienssen R, Comai L. Genomic changes in synthetic Arabidopsis polyploids. Plant J. 2005;41(2):221-30.
17. Kraitshtein Z, Yaakov B, Khasdan V, Kashkush K. Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics. 2010;186(3):801-12.
18. Szadkowski E, Eber F, Huteau V, Lode M, Huneau C, Belcram H, Coriton O, Manzanares-Dauleux M, Delourme R, King GJ. The first meiosis of resynthesized Brassica napus, a genome blender. New Phytol. 2010;186(1):102-12.
19. Salmon A, Flagel L, Ying B, Udall JA, Wendel JF. Homoeologous nonreciprocal recombination in polyploid cotton. New Phytol. 2010;186(1):123-34.
20. Wang S, Ye X, Wang Y, Chen Y, Lin B, Yi Z, Mao Z, Hu F, Zhao R, Wang J, et al. A new type of homodiploid fish derived from the interspecific hybridization of female common carp × male blunt snout bream. Sci Rep. 2017;7(1):4189.
21. Comai L. The advantages and disadvantages of being polyploid. Nat Rev Genet. 2005;6(11):836.
22. Wang J, Tian L, Lee HS, Chen ZJ. Nonadditive regulation of FRI and FLC loci mediates flowering-time variation in Arabidopsis allopolyploids. Genetics. 2006;173(2):965-74.
23. Yang J, Liu D, Wang X, Ji C, Cheng F, Liu B, Hu Z, Chen S, Pental D, Ju Y. The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection. Nat Genet. 2016;48(10):1225.
24. Qian L, Qian W, Snowdon RJ. Sub-genomic selection patterns as a signature of breeding in the allopolyploid Brassica napus genome. BMC Genomics. 2014;15(1):1170.
25. Wang M, Tu L, Lin M, Lin Z, Wang P, Yang Q, Ye Z, Shen C, Li J, Zhang L. Asymmetric subgenome selection and cis-regulatory divergence during cotton domestication. Nat Genet. 2017;49(4):579.
26. Birchler JA. Understanding mechanisms of novel gene expression in polyploids. Trends Genet. 2003;19(3):141.
27. Adams KL. Evolution of duplicate gene expression in polyploid and hybrid plants. J Hered. 2007;98(2):136.
28. Wu Y, Sun Y, Wang X, Lin X, Sun S, Shen K, Wang J, Jiang T, Zhong S, Xu C, et al. Transcriptome shock in an interspecific F1 triploid hybrid of Oryza revealed by RNA sequencing. J Integ Plant Biol. 2016;58(2):150-64.
29. Yoo MJ, Szadkowski E, Wendel JF. Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity. 2013;110(2):171-80.
30. Grover CE, Gallagher JP, Szadkowski EP, Yoo MJ, Flagel LE, Wendel JF. Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol. 2012;196(4):966-71.
31. Cox MP, Dong T, Shen GG, Dalvi Y, Scott DB, Ganley ARD. An interspecific fungal hybrid reveals cross-kingdom rules for allopolyploid gene expression patterns. PLoS Genet. 2014;10(3):e1004180.
32. Ren L, Li W, Tao M, Qin Q, Luo J, Chai J, Tang C, Xiao J, Tang X, Lin G, et al. Homoeologue expression insights into the basis of growth heterosis at the intersection of ploidy and hybridity in Cyprinidae. Sci Rep. 2016;6:27040.
33. Ren L, Cui J, Wang J, Tan H, Li W, Tang C, Qin Q, Liu S. 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.
34. Powell JJ, Fitzgerald TL, Stiller J, Berkman PJ, Gardiner DM, Manners JM, Henry RJ, Kazan K. The defence-associated transcriptome of hexaploid wheat displays homoeolog expression and induction bias. Plant Biotechnol J. 2017;15(4):533-43.
35. Videvall E, Sletvold N, Hagenblad J, Agren J, Hansson B. Strong maternal effects on gene expression in Arabidopsis lyrata hybrids. Mol Biol Evol. 2016;33(4):984-94.
36. Alves MJ, Coelho MM, Collarespereira MJ. Evolution in action through hybridisation and polyploidy in an Iberian freshwater fish: a genetic review. Genetica. 2001;111(1-3):375-85.
37. Ching B, Jamieson S, Heath JW, Heath DD, Hubberstey A. Transcriptional differences between triploid and diploid Chinook salmon (Oncorhynchus tshawytscha) during live Vibrio anguillarum challenge. Heredity. 2010;104(2):224-34.
38. Ren L, Tang C, Li W, Cui J, Tan X, Xiong Y, Chen J, Wang J, Xiao J, Zhou Y, et al. Determination of dosage compensation and comparison of gene expression in a triploid hybrid fish. BMC Genomics. 2017;18(1):38.
39. Bomblies K, Doebley JF. Pleiotropic effects of the duplicate maize FLORICAULA/LEAFY genes zfl1 and zfl2 on traits under selection during maize domestication. Genetics. 2006;172(1):519-31.
40. Gottlieb L. Conservation and duplication of isozymes in plants. Science. 1982;216(4544):373-80.
41. Gaeta RT, Chris PJ. Homoeologous recombination in allopolyploids: the polyploid ratchet. New Phytol. 2010;186(1):18-28.
42. Buggs RJ, Zhang L, Miles N, Tate JA, Gao L, Wei W, Schnable PS, Barbazuk WB, Soltis PS, Soltis DE. Transcriptomic shock generates evolutionary novelty in a newly formed, natural allopolyploid plant. Curr Biol. 2011;21(7):551-6.
43. Otto SP, Lenormand T. Resolving the paradox of sex and recombination. Nat Rev Genet. 2002;3(4):252.
44. Liu S, Luo J, Chai J, Ren L, Zhou Y, Huang F, Liu X, Chen Y, Zhang C, Tao M, et al. Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross. PNAS. 2016;113(5):1327-32.
45. Flagel LE, Wendel JF. Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol. 2010;186(1):184-93.
46. Hegarty MJ, Barker GL, Wilson ID, Abbott RJ, Edwards KJ, Hiscock SJ. Transcriptome shock after interspecific hybridization in senecio is ameliorated by genome duplication. Curr Biol. 2006;16(16):1652.
47. Gaeta RT, Yoo SY, Pires JC, Doerge RW, Chen ZJ, Osborn TC. Analysis of gene expression in resynthesized Brassica napus allopolyploids using Arabidopsis 70mer oligo microarrays. PLoS One. 2009;4(3):e4760.
48. Adams KL, Cronn R, Percifield R, Wendel JF. Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. PNAS. 2003;100(8):4649-54.
49. Duarte JM, Cui L, Wall PK, Zhang Q, Zhang X, Leebens-Mack J, Ma H, Altman N, Depamphilis CW. Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol. 2006;23(2):469-78.
50. Rapp RA, Udall JA, Wendel JF. Genomic expression dominance in allopolyploids. BMC Biol. 2009;7(1):1-10.
51. Xu C, Bai Y, Lin X, Zhao N, Hu L, Gong Z, Wendel JF, Liu B. Genome-wide disruption of gene expression in allopolyploids but not hybrids of rice subspecies. Mol Biol Evol. 2014;31(5):1066.
52. Bougas B, Granier S, Audet C, Bernatchez L. The transcriptional landscape of cross-specific hybrids and its possible link with growth in brook charr (Salvelinus fontinalis Mitchill). Genetics. 2010;186(1):97-107.
53. White SL, Sakhrani D, Danzmann RG, Devlin RH. Influence of developmental stage and genotype on liver mRNA levels among wild, domesticated, and hybrid rainbow trout (Oncorhynchus mykiss). BMC Genomics. 2013;14(1):673.
54. Renaut S, Nolte A, Bernatchez L. Gene expression divergence and hybrid misexpression between lake whitefish species pairs (Coregonus spp. Salmonidae). Mol Biol Evol. 2009;26(4):925.
55. Pea G, Ferron S, Gianfranceschi L, Krajewski P, Pe ME. Gene expression non-additivity in immature ears of a heterotic F1 maize hybrid. Plant Sci. 2008;174(1):17-24.
56. Meyer S, Pospisil H, Scholten S. Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant pattern. Plant Mol Biol. 2007;63(3):381-91.
57. Hochholdinger F, Hoecker N. Towards the molecular basis of heterosis. Trends Plant Sci. 2007;12(9):427-32.
58. Zhou Y, Zhong H, Liu S, Yu F, Hu J, Zhang C, Tao M, Liu Y. Elevated expression of Piwi and piRNAs in ovaries of triploid crucian carp. Mol Cell Endocrinol. 2014;383(1-2):1-9.
59. Pala I, Coelho MM, Schartl M. Dosage compensation by gene-copy silencing in a triploid hybrid fish. Curr Biol. 2008;18(17):1344.
60. Donohue K. Completing the cycle: maternal effects as the missing link in plant life histories. Philos T R Soc B. 2009;364(1520):1059-74.
61. Johnson RM, Shrimpton JM, Cho GK, Heath DD. Dosage effects on heritability and maternal effects in diploid and triploid Chinook salmon (Oncorhynchus tshawytscha). Heredity. 2007;98(5):303-10.
62. Yao H, Gray AD, Auger DL, Birchler JA. Genomic dosage effects on heterosis in triploid maize. PNAS. 2013;110(7):2665.
63. Liu S, Liu Y, Zhou G, Zhang X, Luo C, Feng H, He X, Zhu G, Yang H. The formation of tetraploid stocks of red crucian carp × common carp hybrids as an effect of interspecific hybridization. Aquaculture. 2001;192(2):171-86.
64. Andrews S. FastQC: A quality control tool for high throughput sequence data. 2010.
65. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29(7):644.
66. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21(18):3674.
67. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22(13):1658-9.
68. Mortazavi A, Williams B, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5(7):621.
69. Wang L, Feng Z, Wang X, Wang X, Zhang X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics. 2010;26(1):136.
70. Robinson MD, Mccarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009;26(1):139.