Natural variation and evolutionary dynamics of transposable elements in Brassica oleracea based on next-generation sequencing data

Zhen Liu , Miao Fan , Er-Kui Yue , Yu Li , Ruo-Fu Tao , Hai-Ming Xu , Ming-Hua Duan , Jian-Hong Xu

Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) : 145

PDF (1772KB)
Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) :145 DOI: 10.1038/s41438-020-00367-0
Article
research-article
Natural variation and evolutionary dynamics of transposable elements in Brassica oleracea based on next-generation sequencing data
Author information +
History +
PDF (1772KB)

Abstract

Brassica oleracea comprises various economically important vegetables and presents extremely diverse morphological variations. They provide a rich source of nutrition for human health and have been used as a model system for studying polyploidization. Transposable elements (TEs) account for nearly 40% of the B. oleracea genome and contribute greatly to genetic diversity and genome evolution. Although the proliferation of TEs has led to a large expansion of the B. oleracea genome, little is known about the population dynamics and evolutionary activity of TEs. A comprehensive mobilome profile of 45,737 TE loci was obtained from resequencing data from 121 diverse accessions across nine B. oleracea morphotypes. Approximately 70% (32,195) of the loci showed insertion polymorphisms between or within morphotypes. In particular, up to 1221 loci were differentially fixed among morphotypes. Further analysis revealed that the distribution of the population frequency of TE loci was highly variable across different TE superfamilies and families, implying a diverse expansion history during host genome evolution. These findings provide better insight into the evolutionary dynamics and genetic diversity of B. oleracea genomes and will potentially serve as a valuable resource for molecular markers and association studies between TE-based genomic variations and morphotype-specific phenotypic differentiation.

Cite this article

Download citation ▾
Zhen Liu, Miao Fan, Er-Kui Yue, Yu Li, Ruo-Fu Tao, Hai-Ming Xu, Ming-Hua Duan, Jian-Hong Xu. Natural variation and evolutionary dynamics of transposable elements in Brassica oleracea based on next-generation sequencing data. Horticulture Research, 2020, 7 (1) : 145 DOI:10.1038/s41438-020-00367-0

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Warwick, S. I., Francis, A. & Al-Shehbaz, I. A. Brassicaceae: species checklist and database on CD-Rom. Plant Syst. Evol. 259, 249-258 (2006).

[2]

Cheng, F., Wu, J. & Wang, X. Genome triplication drove the diversification of Brassica plants. Hortic. Res. 1, 14024 (2014).

[3]

Jiao, Y., Wickett, N. J. & Ayyampalayam, S. et al. Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97-100 (2011).

[4]

Bowers, J. E., Chapman, B. A., Rong, J. & Paterson, A. H. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422, 433-438 (2003).

[5]

Lysak, M. A., Koch, M. A., Pecinka, A. & Schubert, I. Chromosome tripli-cation found across the tribe Brassiceae. Genome Res. 15, 516-525 (2005).

[6]

Wang, X., Wang, H. & Wang, J. et al. The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43, 1035-1039 (2011).

[7]

Vitte, C., Fustier, M. A., Alix, K. & Tenaillon, M. I. The bright side of transposons in crop evolution. Brief. Funct. Genomics 13, 276-295 (2014).

[8]

Liu, S., Liu, Y. & Yang, X. et al. The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat. Commun. 5, 3930 (2014).

[9]

Parkin, I. A., Koh, C. & Tang, H. et al. Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol. 15, R77 (2014).

[10]

Zhao, M., Du, J. & Lin, F. et al. Shifts in the evolutionary rate and intensity of purifying selection between two Brassica genomes revealed by analyses of orthologous transposons and relics of a whole genome triplication. Plant J. 76, 211-222. (2013).

[11]

Cheng, F., Sun, C. & Wu, J. et al. Epigenetic regulation of subgenome dom-inance following whole genome triplication in Brassica rapa. N. Phytol. 211, 288-299 (2016).

[12]

Woodhouse, M. R. et al. Origin, inheritance, and gene regulatory con-sequences of genome dominance in polyploids. Proc. Natl Acad. Sci. USA 111, 5283-5288 (2014).

[13]

Henaff, E., Vives, C. & Desvoyes, B. et al. Extensive amplification of the E2F transcription factor binding sites by transposons during evolution of Brassica species. Plant J. 77, 852-862 (2014).

[14]

Chiu, L. W. et al. The purple cauliflower arises from activation of a MYB transcription factor. Plant Physiol. 154, 1470-1480 (2010).

[15]

Gao, C., Zhou, G. & Ma, C. et al. Helitron-like transposons contributed to the mating system transition from out-crossing to self-fertilizing in polyploid Brassica napus L. Sci. Rep. 6, 33785 (2016).

[16]

Lisch, D. Epigenetic regulation of transposable elements in plants. Annu. Rev. Plant Biol. 60, 43-66 (2009).

[17]

Jiang, N., Bao, Z. & Zhang, X. et al. An active DNA transposon family in rice. Nature 421, 163-167 (2003).

[18]

Hirochika, H., Sugimoto, K., Otsuki, Y., Tsugawa, H. & Kanda, M. Retro-transposons of rice involved in mutations induced by tissue culture. Proc. Natl Acad. Sci. USA 93, 7783-7788 (1996).

[19]

Gonzalez, J., Lenkov, K., Lipatov, M., Macpherson, J. M. & Petrov, D. A. High rate of recent transposable element-induced adaptation in Drosophila melanoga-ster. PLoS Biol. 6, e251 (2008).

[20]

Dussert, Y., Remigereau, M. S. & Fontaine, M. C. et al. Polymorphism pattern at a miniature inverted-repeat transposable element locus downstream of the domestication gene Teosinte-branched1 in wild and domesticated pearl millet. Mol. Ecol. 22, 327-340 (2013).

[21]

Rishishwar, L., Tellez Villa, C. E. & Jordan, I. K. Transposable element poly-morphisms recapitulate human evolution. Mob. DNA 6, 21 (2015).

[22]

Kofler, R., Betancourt, A. J. & Schlotterer, C. Sequencing of pooled DNA sam-ples (Pool-Seq) uncovers complex dynamics of transposable element inser-tions in Drosophila melanogaster. PLoS Genet. 8, e1002487 (2012).

[23]

Nellaker, C., Keane, T. M. & Yalcin, B. et al. The genomic landscape shaped by selection on transposable elements across 18 mouse strains. Genome Biol. 13, R45 (2012).

[24]

Laricchia, K. M., Zdraljevic, S., Cook, D. E. & Andersen, E. C. Natural variation in the distribution and abundance of transposable elements across the Cae-norhabditis elegans species. Mol. Biol. Evol. 34, 2187-2202 (2017).

[25]

Ewing, A. D. Transposable element detection from whole genome sequence data. Mob. DNA 6, 24 (2015).

[26]

Goubert, C., Henri, H. & Minard, G. et al. High-throughput sequencing of transposable element insertions suggests adaptive evolution of the invasive Asian tiger mosquito towards temperate environments. Mol. Ecol. 26, 3968-3981 (2017).

[27]

Cheung, F., Trick, M. & Drou, N. et al. Comparative analysis between homoeologous genome segments of Brassica napus and its progenitor species reveals extensive sequence-level divergence. Plant Cell 21, 1912-1928 (2009).

[28]

Zhang, X. & Wessler, S. R. Genome-wide comparative analysis of the trans-posable elements in the related species Arabidopsis thaliana and Brassica oleracea. Proc. Natl Acad. Sci. USA 101, 5589-5594 (2004).

[29]

Cheng, F., Wu, J. & Cai, C. et al. Genome resequencing and comparative variome analysis in a Brassica rapa and Brassica oleracea collection. Sci. Data 3, 160119 (2016).

[30]

Hollister, J. D. & Gaut, B. S. Population and evolutionary dynamics of Helitron transposable elements in Arabidopsis thaliana. Mol. Biol. Evol. 24, 2515-2524 (2007).

[31]

Cheng, F., Sun, R. & Hou, X. et al. Subgenome parallel selection is asso-ciated with morphotype diversification and convergent crop domestica-tion in Brassica rapa and Brassica oleracea. Nat. Genet. 48, 1218-1224 (2016).

[32]

Alix, K., Joets, J. & Ryder, C. D. et al. The CACTA transposon Bot1 played a major role in Brassica genome divergence and gene proliferation. Plant J. 56, 1030-1044 (2008).

[33]

Sampath, P., Murukarthick, J. & Izzah, N. K. et al. Genome-wide comparative analysis of 20 miniature inverted-repeat transposable element families in Brassica rapa and B. oleracea. PLoS ONE 9, e94499 (2014).

[34]

Sampath, P., Lee, S. C. & Lee, J. et al. Characterization of a new high copy Stowaway family MITE, BRAMI-1 in Brassica genome. BMC Plant. Biol. 13, 56 (2013).

[35]

Alix, K., Ryder, C. D., Moore, J., King, G. J. & Pat Heslop-Harrison, J. S. The genomic organization of retrotransposons in Brassica oleracea. Plant Mol. Biol. 59, 839-851 (2005).

[36]

Stuart, T. & Eichten, S. R. Population scale mapping of transposable element diversity reveals links to gene regulation and epigenomic variation. eLife 5, 27 (2016).

[37]

Fu, Y., Kawabe, A. & Etcheverry, M. et al. Mobilization of a plant transposon by expression of the transposon-encoded anti-silencing factor. EMBO J. 32, 2407-2417 (2013).

[38]

Salmon, A., Clotault, J., Jenczewski, E., Chable, V . & Manzanares-Dauleux, M. J. Brassica oleracea displays a high level of DNA methylation polymorphism. Plant Sci. 174, 61-70 (2008).

[39]

Quadrana, L., Bortolini Silveira, A. & Mayhew, G. F. et al. The Arabidopsis thaliana mobilome and its impact at the species level. eLife 5, 25 (2016).

[40]

Quiros, C. F. & Farnham, M. W. The Genetics of Brassica oleracea (Springer, New York, 2011).

[41]

Daborn, P. J., Yen, J. L. & Bogwitz, M. R. et al. A single p450 allele associated with insecticide resistance in Drosophila. Science 297, 2253-2256 (2002).

[42]

Studer, A., Zhao, Q., Ross-Ibarra, J. & Doebley, J. Identification of a functional transposon insertion in the maize domestication gene tb1. Nat. Genet. 43, 1160-1163 (2011).

[43]

Zhou, L., Zhang, J., Yan, J. & Song, R. Two transposable element insertions are causative mutations for the major domestication gene teosinte branched 1 in modern maize. Cell Res. 21, 1267-1270 (2011).

[44]

Kaplan, N. L., Hudson, R. R. & Langley, C. H. The “hitchhiking effect” revisited. Genetics 123, 887-899 (1989).

[45]

Tam, S. M. et al. The distribution of copia-type retrotransposons and the evolutionary history of tomato and related wild species. J. Evol. Biol. 20, 1056-1072 (2007).

[46]

Gherman, A., Chen, P. E. & Teslovich, T. M. et al. Population bottlenecks as a potential major shaping force of human genome architecture. PLoS Genet. 3, e119 (2007).

[47]

Tian, Z., Zhao, M. & She, M. et al. Genome-wide characterization of non-reference transposons reveals evolutionary propensities of transposons in soybean. Plant Cell 24, 4422-4436 (2012).

[48]

Swofford, D. L. PAUP*: phylogenetic analysis using parsimony, version 4.0b10 (and other methods). Genome Res. 14, 1188-1190 (2002).

[49]

Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945-959 (2000).

[50]

Zheng, X. et al. A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28, 3326-3328 (2012).

PDF (1772KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/