Homoeolog Expression Is Modulated Differently by Different Subgenomes in Brassica napus Hybrids and Allotetraploids

Original Paper
  • 23 Downloads

Abstract

Synthetic and natural allotetraploid Brassica napus (2n = 38, AACC) have been widely used as a model to study the genetic changes associated with allopolyploidization; however, there has been little research on the homoeolog expression patterns and the roles of cis and trans regulation. Herein, homoeolog expression patterns were assessed by using RNA-seq for two interspecific hybrids (AnCo with the extracted A subgenome from natural B. napus, and ArCo with the A subgenome from extant B. rapa), synthetic and natural allopolyploids (CoCoArAr and AnAnCnCn), and the diploid parents. The ranges of homoeolog expression bias decreased after hybridization, whereas the extents of homoeolog expression bias and non-conserved expression, especially transgressive expression, increased over evolutionary time. Despite sharing the same C subgenome parent, these two hybrids showed different homolog expression patterns in many respects. In AnCo, the trans-regulatory factors from Co subgenome tended to cause downregulation of An subgenome homoeologs, but trans-regulatory factors from the An subgenome acted as both activators and repressors, and such asymmetric effects of trans-regulatory factors might explain why the homoeolog expression was biased toward the C subgenome after genome merger. No significant asymmetric effects of trans-regulatory factors were found in ArCo, which was consistent with the overall balanced expression of homoeologs. These results suggested that A subgenomes with different regulatory systems might act differently in modulating homoeolog expression after merger with the C subgenome, resulting in either balanced or unbalanced homoeolog expression biases.

Keywords

Brassica napus Synthetic hybrids Homoeolog expression bias cis and trans regulation Allopolyploidization 

Notes

Acknowledgements

This work was funded by National Key Research and Development Program of China (Grant No. 2016YFD0100202), National Natural Science Foundation of China (Grant No. 31701462), The Hunan Provincial Natural Science Foundation of China (Grant No. 2016JJ1010), and Foundation of Hunan University of Science and Technology (Grant No. E51760).

Authors’ Contributions

ZYL and YML conceived the study. CT, XHG, and LLL participated in sample preparations for RNA-seq. DWZ and QP analyzed the data and wrote the manuscript. All the authors have read and approved the final manuscript.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

Supplementary material

11105_2018_1087_Fig6_ESM.gif (8 kb)
Fig. S1

(GIF 8 kb)

11105_2018_1087_MOESM1_ESM.tif (94 kb)
High resolution image (TIF 94 kb)
11105_2018_1087_Fig7_ESM.gif (180 kb)
Fig. S2

(GIF 180 kb)

11105_2018_1087_MOESM2_ESM.tif (1013 kb)
High resolution image (TIF 1013 kb)
11105_2018_1087_MOESM3_ESM.doc (36 kb)
Table S1 (DOC 35 kb)

References

  1. Bell GD, Kane NC, Rieseberg LH, Adams KL (2013) RNA-seq analysis of allele-specific expression, hybrid effects, and regulatory divergence in hybrids compared with their parents from natural populations. Genome Biol Evol 5:1309–1323CrossRefPubMedPubMedCentralGoogle Scholar
  2. Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H et al (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953CrossRefPubMedGoogle Scholar
  3. Combes MC, Hueber Y, Dereeper A, Rialle S, Herrera JC, Lashermes P (2015) Regulatory divergence between parental alleles determines gene expression patterns in hybrids. Genome Biol Evol 7:1110–1121CrossRefPubMedPubMedCentralGoogle Scholar
  4. Cui C, Ge X, Gautam M, Kang L, Li Z (2012) Cytoplasmic and genomic effects on meiotic pairing in Brassica hybrids and allotetraploids from pair crosses of three cultivated diploids. Genetics 191:725–738CrossRefPubMedPubMedCentralGoogle Scholar
  5. Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42:443–461CrossRefPubMedGoogle Scholar
  6. Flagel LE, Wendel JF (2010) Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol 186:184–193Google Scholar
  7. Gaeta RT, Yoo SY, Pires J, Doerge RW, Chen ZJ, Osborn TC (2009) Analysis of gene expression in resynthesized Brassica napus allopolyploids using Arabidopsis 70mer oligo microarrays. PloS One 4:e4760Google Scholar
  8. Ge XH, Ding L, Li ZY (2013) Nucleolar dominance and different genome behaviors in hybrids and allopolyploids. Plant Cell Rep 2:1661–1673Google Scholar
  9. Groszmann M, Greaves IK, Albertyn ZI, Scofield GN, Peacock WJ, Dennis ES (2011) Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proc Natl Acad Sci U S A 108:2617–2622CrossRefPubMedPubMedCentralGoogle Scholar
  10. Grover C, Gallagher J, Szadkowski E, Yoo M, Flagel L et al (2012) Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol 196:966–971CrossRefPubMedGoogle Scholar
  11. Jiang J, Shao Y, Du K, Ran L, Fang X et al (2013) Use of digital gene expression to discriminate gene expression differences in early generations of resynthesized Brassica napus and its diploid progenitors. BMC Genomics 14:72CrossRefPubMedPubMedCentralGoogle Scholar
  12. Jiao W, Yuan J, Jiang S, Liu Y, Wang L, et al (2018) Asymmetrical changes of gene expression, small RNAs and chromatin in two resynthesized wheat allotetraploids. Plant J 93(5):828–842Google Scholar
  13. Li A, Liu D, Wu J, Zhao X, Hao M, Geng S, Yan J, Jiang X, Zhang L, Wu J, Yin L, Zhang R, Wu L, Zheng Y, Mao L (2014) mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. Plant Cell 26:1878–1900CrossRefPubMedPubMedCentralGoogle Scholar
  14. Liu S, Liu Y, Yang X, Tong C, Edwards D et al (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930PubMedPubMedCentralGoogle Scholar
  15. McManus CJ, Coolon JD, Duff MO, Eipper-Mains J, Graveley BR et al (2010) Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res 20:816–825CrossRefPubMedPubMedCentralGoogle Scholar
  16. Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–462CrossRefPubMedGoogle Scholar
  17. Shen Y, Sun S, Hua S, Shen E, Ye CY, Cai D, Timko MP, Zhu QH, Fan L (2017) Analysis of transcriptional and epigenetic changes in hybrid vigor of allopolyploid Brassica napus uncovers key roles for small RNAs. Plant J 91:874–893CrossRefPubMedGoogle Scholar
  18. Shi X, Ng DW, Zhang C, Comai L, Ye W et al (2012) Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids. Nat Commun 3:950CrossRefPubMedGoogle Scholar
  19. Soltis DE, Visger CJ, Marchant DB, Soltis PS (2016) Polyploidy: Pitfalls and paths to a paradigm. Am J Bot 103 (7):1146–1166Google Scholar
  20. Song K, Lu P, Tang K, Osborn TC (1995) Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc Nati Acad Sci USA 92:7719–7723Google Scholar
  21. Tan C, Pan Q, Cui C, Xiang Y, Ge X et al (2016) Genome-wide gene/genome dosage imbalance regulates gene expressions in synthetic Brassica napus and derivatives (AC, AAC, CCA, CCAA). Front Plant Sci 7:1432PubMedPubMedCentralGoogle Scholar
  22. Tu YQ, Sun J, Ge XH, Li ZY (2010) Production and genetic analysis of partial hybrids from intertribal sexual crosses between Brassica napus and Isatis indigotica and progenies. Genome 53:146–156CrossRefPubMedGoogle Scholar
  23. Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138Google Scholar
  24. Wang X, Wang H, Wang J, Sun R, Wu J et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039CrossRefPubMedGoogle Scholar
  25. Wang Z, Sun X, Zhao Y, Guo X, Jiang H, Li H, Gu Z (2015) Evolution of gene regulation during transcription and translation. Genome Biol Evol 7:1155–1167CrossRefPubMedPubMedCentralGoogle Scholar
  26. Wendel JF, Jackson SA, Meyers BC, Wing RA (2016) Evolution of plant genome architecture. Genome Biol 17:37CrossRefPubMedPubMedCentralGoogle Scholar
  27. Wendel JF, Lisch D, Hu G, Mason AS (2018) The long and short of doubling down: polyploidy, epigenetics, and the temporal dynamics of genome fractionation. Curr Opin Genet Dev 49:1–7CrossRefPubMedGoogle Scholar
  28. Woodhouse MR, Cheng F, Pires JC, Lisch D, Freeling M, Wang X (2014) Origin, inheritance, and gene regulatory consequences of genome dominance in polyploids. Proc Natl Acad Sci U S A 111:5283–5288CrossRefPubMedPubMedCentralGoogle Scholar
  29. Xiong Z, Gaeta RT, Pires JC (2011) Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc Natl Acad Sci U S A 108:7908–7913CrossRefPubMedPubMedCentralGoogle Scholar
  30. Xu C, Bai Y, Lin X, Zhao N, Hu L, Gong Z, Wendel JF, Liu B (2014) Genome-wide disruption of gene expression in allopolyploids but not hybrids of rice subspecies. Mol Biol Evol 31:1066–1076CrossRefPubMedPubMedCentralGoogle Scholar
  31. Yang J, Liu D, Wang X, Ji C, Cheng F, Liu B, Hu Z, Chen S, Pental D, Ju Y, Yao P, Li X, Xie K, Zhang J, Wang J, Liu F, Ma W, Shopan J, Zheng H, Mackenzie SA, Zhang M (2016a) The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection. Nat Genet 48:1225–1232CrossRefPubMedGoogle Scholar
  32. Yang M, Wang X, Huang H, Ren D, Su Y et al (2016b) Natural variation of H3K27me3 modification in two Arabidopsis accessions and their hybrid. J Integr Plant Biol 58(5):466–474CrossRefPubMedGoogle Scholar
  33. Yoo MJ, Szadkowski E, Wendel JF (2013) Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity 110:171–180CrossRefPubMedGoogle Scholar
  34. Yoo MJ, Liu X, Pires JC, Soltis PS, Soltis DE (2014) Nonadditive gene expression in polyploids. Annu Rev Genet 48:485–517CrossRefPubMedGoogle Scholar
  35. Zhang D, Pan Q, Cui C, Tan C, Ge X et al (2015) Genome-specific differential gene expressions in resynthesized Brassica allotetraploids from pair-wise crosses of three cultivated diploids revealed by RNA-seq. Front Plant Sci 6:957PubMedPubMedCentralGoogle Scholar
  36. Zhang D, Pan Q, Tan C, Zhu B, Ge X et al (2016) Genome-wide gene expressions respond differently to A-subgenome origins in Brassica napus synthetic hybrids and natural allotetraploid. Front Plant Sci 7:1508PubMedPubMedCentralGoogle Scholar
  37. Zhu B, Tu Y, Zeng P, Ge X, Li Z (2016) Extraction of the constituent subgenomes of the natural allopolyploid rapeseed (Brassica napus L.). Genetics 204:1015–1027CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Life ScienceHunan University of Science and TechnologyXiangtanPeople’s Republic of China
  2. 2.National Key Lab of Crop Genetic Improvement, National Center of Crop Molecular Breeding Technology, National Center of Oil Crop Improvement (Wuhan), College of Plant Science and TechnologyHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  3. 3.Key Laboratory of Ecological Remediation and Safe Utilization of Heavy Metal-Polluted SoilsCollege of Hunan ProvinceXiangtanPeople’s Republic of China

Personalised recommendations