Genomic and transcriptomic alterations following intergeneric hybridization and polyploidization in the Chrysanthemum nankingense×Tanacetum vulgare hybrid and allopolyploid (Asteraceae)

Xiangyu Qi , Haibin Wang , Aiping Song , Jiafu Jiang , Sumei Chen , Fadi Chen

Horticulture Research ›› 2018, Vol. 5 ›› Issue (1) : 5

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Horticulture Research ›› 2018, Vol. 5 ›› Issue (1) :5 DOI: 10.1038/s41438-017-0003-0
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Genomic and transcriptomic alterations following intergeneric hybridization and polyploidization in the Chrysanthemum nankingense×Tanacetum vulgare hybrid and allopolyploid (Asteraceae)
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Abstract

Allopolyploid formation involves two major events: interspecific hybridization and polyploidization. A number of species in the Asteraceae family are polyploids because of frequent hybridization. The effects of hybridization on genomics and transcriptomics in Chrysanthemum nankingense×Tanacetum vulgare hybrids have been reported. In this study, we obtained allopolyploids by applying a colchicine treatment to a synthesized C. nankingense×T. vulgare hybrid. Sequence-related amplified polymorphism (SRAP), methylation-sensitive amplification polymorphism (MSAP), and high-throughput RNA sequencing (RNA-Seq) technologies were used to investigate the genomic, epigenetic, and transcriptomic alterations in both the hybrid and allopolyploids. The genomic alterations in the hybrid and allopolyploids mainly involved the loss of parental fragments and the gain of novel fragments. The DNA methylation level of the hybrid was reduced by hybridization but was restored somewhat after polyploidization. There were more significant differences in gene expression between the hybrid/allopolyploid and the paternal parent than between the hybrid/allopolyploid and the maternal parent. Most differentially expressed genes (DEGs) showed down-regulation in the hybrid/allopolyploid relative to the parents. Among the non-additive genes, transgressive patterns appeared to be dominant, especially repression patterns. Maternal expression dominance was observed specifically for down-regulated genes. Many methylase and methyltransferase genes showed differential expression between the hybrid and parents and between the allopolyploid and parents. Our data indicate that hybridization may be a major factor affecting genomic and transcriptomic changes in newly formed allopolyploids. The formation of allopolyploids may not simply be the sum of hybridization and polyploidization changes but also may be influenced by the interaction between these processes.

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Xiangyu Qi, Haibin Wang, Aiping Song, Jiafu Jiang, Sumei Chen, Fadi Chen. Genomic and transcriptomic alterations following intergeneric hybridization and polyploidization in the Chrysanthemum nankingense×Tanacetum vulgare hybrid and allopolyploid (Asteraceae). Horticulture Research, 2018, 5 (1) : 5 DOI:10.1038/s41438-017-0003-0

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References

[1]

Paun, O., Fay, M. F., Soltis, D. E. & Chase, M. W. Genetic and epigenetic alterations after hybridization and genome doubling. Taxon 56, 649-656 (2007).

[2]

Chen, Z. J. Genomic and epigenetic insights into the molecular bases of heterosis. Nat. Rev. Genet. 14, 471-482 (2013).

[3]

Hegarty, M. J. & Hiscock, S. J. Genomic clues to the evolutionary success of polyploid plants. Curr. Biol. 18, R435-R444 (2008).

[4]

Ozkan, H. & Feldman, M. Allopolyploidy-induced rapid genome evolution in the wheat (Aegilops-Triticum) group. Plant Cell 13, 1735-1747 (2001).

[5]

Zhang, S. Z., Wang, Y. L., Zi-Can, H. E. & Ejder, E. Genome differentiation in Magonoliaceae as revealed from meiotic pairing in interspecific and intergeneric hybrids. J. Syst. Evol. 49, 518-527 (2011).

[6]

Soltis, D. E., Albert, V. A., Leebensmack, J., Bell, C. D., Paterson, A. H. & Zheng, C. et al. Polyploidy and angiosperm diversification. Am. J. Bot. 96, 336-348 (2009).

[7]

Jiao, Y., Wickett, N. J., Ayyampalayam, S., Chanderbali, A. S., Landherr, L. & Ralph, P. E. et al. Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97-100 (2011).

[8]

Soltis, P. S., Marchant, D. B., Van de Peer, Y. & Soltis, D. E. Polyploidy and genome evolution in plants. Curr. Opin. Genet. Dev. 35, 119-125 (2015).

[9]

Chen, Z. J. Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant. Sci. 15, 57-71 (2010).

[10]

Chelaifa, H., Monnier, A., Ainouche, M., Ainouche, M. L. & Jenczewski, E. Transcriptomic changes following recent natural hybridization and allopolyploidy in the salt marsh species Spartina×townsendii and Spartina anglica (Poaceae). N. Phytol. 186, 161-174 (2010).

[11]

Wang, H., Jiang, J., Chen, S., Qi, X., Fang, W. & Guan, Z. et al. Rapid genetic and epigenetic alterations under intergeneric genomic shock in newly synthesized Chrysanthemum morifolium×Leucanthemum paludosum hybrids (Asteraceae). Genome Biol. Evol. 6, 247-259 (2014).

[12]

Hegarty, M. J., Barker, G. L., Wilson, I. D., Abbott, R. J., Edwards, K. J. & Hiscock, S. J. Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr. Biol. 16, 1652-1659 (2006).

[13]

Zhao, Q., Zou, J., Meng, J., Mei, S. & Wang, J. Tracing the transcriptomic changes in synthetic trigenomic allohexaploids of Brassica using an RNA-Seq approach. PLoS ONE 8, 191-195 (2013).

[14]

Cheng, S., Huang, Z., Suo, Y., Wang, J. & Kang, X. Gene expression differences associated with growth vigor in Populus full-sib allotriploid progeny following manipulated first division restitution of the diploid maternal parent. Euphytica 203, 683-700 (2015).

[15]

Soltis, D. E., Soltis, P. S. & Tate, J. A. Advances in the study of polyploidy since plant speciation. N. Phytol. 161, 173-191 (2004).

[16]

Xiong, Z., Gaeta, R. T. & Pires, J. C. Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc. Natl Acad. Sci. USA 108, 7908-7913 (2011).

[17]

Hegarty, M. J., Barker, G. L., Brennan, A. C., Edwards, K. J., Abbott, R. J. & Hiscock, S. J. Changes to gene expression associated with hybrid speciation in plants: further insights from transcriptomic studies in Senecio. Philos. Trans. R. Soc. Lond. 363, 3055-3069 (2008).

[18]

Shaked, H., Kashkush, K., Ozkan, H., Feldman, M. & Levy, A. A. Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13, 1749-1759 (2001).

[19]

Kashkush, K., Feldman, M. & Levy, A. A. Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160, 1651-1659 (2002).

[20]

Gaeta, R. T., Pires, J. C., Iniguezluy, F., Leon, E. & Osborn, T. C. Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19, 3403-3417 (2007).

[21]

Kashkush, K., Feldman, M. & Levy, A. A. Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat. Genet. 33, 102-106 (2003).

[22]

Zenoni, S., Ferrarini, A., Giacomelli, E., Xumerle, L., Fasoli, M. & Malerba, G. et al. Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-seq. Plant Physiol. 152, 1787-1795 (2010).

[23]

Miguel, B., H. Sofia, P., Margarida, R., Perry, G., Wanda, V. & Manuela, S. Polyploidization as a retraction force in plant genome evolution: sequence rearrangements in triticale. PLoS ONE 3, e1402 (2008).

[24]

Adams, K. L., Percifield, R. & Wendel, J. F. Organ-specific silencing of duplicated genes in a newly synthesized cotton allotetraploid. Genetics 168, 2217-2226 (2004).

[25]

Adams, K. L. & Wendel, J. F. Novel patterns of gene expression in polyploid plants. Trends Genet. 21, 539-543 (2005).

[26]

Wang, J., Tian, L., Lee, H. S., Wei, N. E., Jiang, H. & Watson, B. et al. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172, 507-517 (2006).

[27]

Wang, H., Qi, X., Chen, S., Fang, W., Guan, Z. & Teng, N. et al. Limited DNA methylation variation and the transcription of MET1 and DDM1 in the genus Chrysanthemum (Asteraceae): following the track of polyploidy. Front Plant Sci. 6, 668 (2015).

[28]

Guo, Y. P., Wang, S. Z., Vogl, C. & Ehrendorfer, F. Nuclear and plastid haplotypes suggest rapid diploid and polyploid speciation in the N hemisphere Achillea millefolium complex (Asteraceae). BMC Evol. Biol. 12, 2 (2012).

[29]

Tang, F., Wang, H., Chen, S., Chen, F., Liu, Z. & Fang, W. Intergeneric hybridization between Dendranthema nankingense and Tanacetum vulgare. Sci. Hortic. 132, 1-6 (2011).

[30]

Wang, H., Jiang, J., Chen, S., Fang, W., Guan, Z. & Liao, Y. et al. Rapid genomic and transcriptomic alterations induced by wide hybridization: Chrysanthemum nankingense×Tanacetum vulgare and C. crassum×Crossostephium chinense (Asteraceae). BMC Genome 14, 902 (2013).

[31]

Liu, S., Chen, S., Chen, Y., Guan, Z., Yin, D. & Chen, F. In vitro induced tetraploid of Dendranthema nankingense (Nakai) Tzvel. shows an improved level of abiotic stress tolerance. Sci. Hortic. 127, 411-419 (2011).

[32]

Hanania, U., Velcheva, M., Sahar, N. & Perl, A. An improved method for isolating high-quality DNA from Vitis vinifera nuclei. Plant Mol. Biol. Rep. 22, 173-177 (2004).

[33]

Li, G. & Quiros, C. F. Sequence-related amplified polymorphism (SRAP), a new marker system based on a simple PCR reaction: its application to mapping and gene tagging in Brassica. Theor. Appl. Genet. 103, 455-461 (2001).

[34]

Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).

[35]

Conesa, A., Götz, S., García-Gómez, J. M., Terol, J., Talón, M. & Robles, M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676 (2005).

[36]

Quevillon, E., Silventoinen, V., Pillai, S., Harte, N., Mulder, N. & Apweiler, R. et al InterProScan: protein domains identifier. Nucleic Acids Res. 33, W116-W120 (2005).

[37]

Audic, S. & Claverie, J.-M. The significance of digital gene expression profiles. Genome Res. 7, 986-995 (1997).

[38]

Richards, A. Apomixis in flowering plants: an overview. Philos. Trans. R. Soc. B 358, 1085-1093 (2003).

[39]

Bell, G. D., 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).

[40]

Xu, Y., Zhao, Q., Mei, S. & Wang, J. Genomic and transcriptomic alterations following hybridisation and genome doubling in trigenomic allohexaploid Brassica carinata×Brassica rapa. Plant Biol. 14, 734-744 (2012).

[41]

Szadkowski, E., Eber, F., Huteau, V., Lodé, M., Huneau, C. & Belcram, H. et al. The first meiosis of resynthesized Brassica napus, a genome blender. N. Phytol. 186, 102-112 (2010).

[42]

Xu, Y., Zhong, L., Wu, X., Fang, X. & Wang, J. Rapid alterations of gene expression and cytosine methylation in newly synthesized Brassica napus allopolyploids. Planta 229, 471-483 (2009).

[43]

Beaulieu, J., Jean, M. & Belzile, F. The allotetraploid Arabidopsis thaliana-Arabidopsis lyrata subsp. petraea as an alternative model system for the study of polyploidy in plants. Mol. Genet. Genome 281, 421-435 (2009).

[44]

Hegarty, M. J., Batstone, T., Barker, G. L., Edwards, K. J., Abbott, R. J. & Hiscock, S. J. Non-additive changes to cytosine methylation as a consequence of hybridization and genome duplication in Senecio (Asteraceae). Mol. Ecol. 20, 105-113 (2011).

[45]

Chen, L. & Chen, J. Changes of cytosine methylation induced by wide hybridization and allopolyploidy in Cucumis. Genome 51, 789-799 (2008).

[46]

Parisod, C., Salmon, A., Zerjal, T., Tenaillon, M., Grandbastien, M. A. & Ainouche, M. Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina. N. Phytol. 184, 1003-1015 (2009).

[47]

Rambani, A., Page, J. T. & Udall, J. A. Polyploidy and the petal transcriptome of Gossypium. BMC Plant Biol. 14, 3 (2014).

[48]

Ren, L., Sun, J., Chen, S., Gao, J., Dong, B. & Liu, Y. et al. A transcriptomic analysis of Chrysanthemum nankingense provides insights into the basis of low temperature tolerance. BMC Genome 15, 844 (2014).

[49]

Dai, F., Wang, Z., Luo, G. & Tang, C. Phenotypic and transcriptomic analyses of autotetraploid and diploid mulberry (Morus alba L.). Int. J. Mol. Sci. 16, 22938-22956 (2015).

[50]

Jiang, J., Yue, W., Bao, Z., Fang, T., Fang, Y. & Wang, Y. Digital gene expression analysis of gene expression differences within Brassica diploids and allopolyploids. BMC Plant Biol. 15, 22 (2015).

[51]

Powell, J. J., Fitzgerald, T. L., Stiller, J., Berkman, P. J., Gardiner, D. M. & Manners, J. M. et al. The defence-associated transcriptome of hexaploid wheat displays homoeolog expression and induction bias. Plant Biotechnol. J. 15, 1-11 (2016).

[52]

Rapp, R. A., Udall, J. A. & Wendel, J. F. Genomic expression dominance in allopolyploids. BMC Biol. 7, 18 (2009).

[53]

Zhang, H., Gou, X., Zhang, A., Wang, X., Zhao, N. & Dong, Y. et al. Transcriptome shock invokes disruption of parental expression-conserved genes in tetraploid wheat. Sci. Rep. 6, 26363 (2016).

[54]

Albertin, W., Balliau, T., Brabant, P., Chèvre, A. M., Eber, F. & Malosse, C. et al. Numerous and rapid nonstochastic modifications of gene products in newly synthesized Brassica napus allotetraploids. Genetics 173, 1101-1113 (2006).

[55]

Barbash, D. A., Siino, D. F., Tarone, A. M. & Roote, J. A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc. Natl Acad. Sci. USA 100, 5302-5307 (2003).

[56]

Birchler, J. A., Auger, D. L. & Riddle, N. C. In search of the molecular basis of heterosis. Plant Cell 15, 2236-2239 (2003).

[57]

Wang, J., Tian, L., Madlung, A., Lee, H.-S., Chen, M. & Lee, J. J. et al. Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics 167, 1961-1973 (2004).

[58]

Stupar, R. M. & Springer, N. M. Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics 173, 2199-2210 (2006).

[59]

Stupar, R. M., Hermanson, P. J. & Springer, N. M. Nonadditive expression and parent-of-origin effects identified by microarray and allele-specific expression profiling of maize endosperm. Plant Physiol. 145, 411-425 (2007).

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