Biodiversity Science ›› 2017, Vol. 25 ›› Issue (6): 600-607.doi: 10.17520/biods.2017028

• Reviews • Previous Article     Next Article

The roles of epigenetic variation in plant hybridization and polyploidization

Linfeng Li1, 2, *(), Bao Liu2   

  1. 1 College of Life Sciences, Sun Yat-sen University, Guangzhou 510275
    2 Key Laboratory of Molecular Epigenetics of the Ministry of Education (MOE), Northeast Normal University, Changchun 130024
  • Received:2017-02-01 Accepted:2017-04-12 Online:2017-07-10
  • Li Linfeng

Hybridization and polyploidization are common phenomena in plants and play important roles in speciation and diversification of extant species. Previous studies using ecological, physiological and molecular investigations have provided a framework for understanding the underlying mechanisms of plant hybridization and polyploidization. In this review, we examine the roles of epigenetic variation in species evolution from an evolutionary perspective. We summarize recent advances in Arabidopsis thaliana, Oryza sativa and species of Brassica to elucidate the correlations between phenotypic novelty and epigenetic variation. Based on currently available observations, we propose that future studies should emphasize the roles of epigenetic variation at both the natural population and species levels, and that statistical methods need to be improved to identify causative epigenetic variations at the genome-wide level.

Key words: epigenetics, hybridization, phenotypic novelty, polyploidization, speciation

[1] Abbott R, Albach D, Ansell S, Arntzen J, Baird S, Bierne N, Boughman J, Brelsford A, Buerkle C, Buggs R (2013) Hybridization and speciation. Journal of Evolutionary Biology, 26, 229-246.
[2] Ammiraju JS, Luo M, Goicoechea JL, Wang W, Kudrna D, Mueller C, Talag J, Kim H, Sisneros NB, Blackmon B (2006) The Oryza bacterial artificial chromosome library resource: construction and analysis of 12 deep-coverage large-insert BAC libraries that represent the 10 genome types of the genus Oryza. Genome Research, 16, 140-147.
[3] Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annual Review of Ecology and Systematics, 58, 113-148.
[4] Becker C, Hagmann J, Müller J, Koenig D, Stegle O, Borgwardt K, Weigel D (2011) Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature, 480, 245-249.
[5] Bomblies K, Madlung A (2014) Polyploidy in the Arabidopsis genus. Chromosome Research, 22, 117-134.
[6] Chao DY, Dilkes B, Luo H, Douglas A, Yakubova E, Lahner B, Salt DE (2013) Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science, 341, 658-659.
[7] Chodavarapu RK, Feng S, Ding B, Simon SA, Lopez D, Jia Y, Wang GL, Meyers BC, Jacobsen SE, Pellegrini M (2012) Transcriptome and methylome interactions in rice hybrids. Proceedings of the National Academy of Sciences, USA, 109, 12040-12045.
[8] Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature, 401, 157-161.
[9] del Pozo JC, Ramirez-Parra E (2015) Whole genome duplications in plants: an overview from Arabidopsis. Journal of Experimental Botany, 66, 6991-7003.
[10] Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Annual Review of Genetics, 42, 443-461.
[11] Feinberg AP, Irizarry RA (2010) Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proceedings of the National Academy of Sciences, USA, 107, 1757-1764.
[12] Felsenfeld G (2014) A brief history of epigenetics. Cold Spring Harbor Perspectives in Biology, 6, a018200.
[13] Ge S, Sang T, Lu BR, Hong DY (1999) Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proceedings of the National Academy of Sciences, USA, 96, 14400-14405.
[14] Ge XH, Ding L, Li ZY (2013) Nucleolar dominance and different genome behaviors in hybrids and allopolyploids. Plant Cell Reports, 32, 1661-1673.
[15] Ghani MA, Li J, Rao L, Raza MA, Cao L, Yu N, Zou X, Chen L (2014) The role of small RNAs in wide hybridisation and allopolyploidisation between Brassica rapa and Brassica nigra. BMC Plant Biology, 14, 272.
[16] Gill BS, Friebe B (2002) Cytogenetics, phylogeny and evolution of cultivated wheats. In: FAO Plant Production and Protection Series No. 30: Bread Wheat: Improvement and Production (eds Curtis BC, Rajaram S, Macpherson HG), pp. 71-88. Food and Agriculture Organization of the United Nations, Rome.
[17] Goldstein DB (2009) Common genetic variation and human traits. New England Journal of Medicine, 360, 1696.
[18] Greaves IK, Groszmann M, Ying H, Taylor JM, Peacock WJ, Dennis ES (2012) Trans chromosomal methylation in Arabidopsis hybrids. Proceedings of the National Academy of Sciences, USA, 109, 3570-3575.
[19] 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. Proceedings of the National Academy of Sciences, USA, 108, 2617-2622.
[20] He G, Zhu X, Elling AA, Chen L, Wang X, Guo L, Liang M, He H, Zhang H, Chen F (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. The Plant Cell, 22, 17-33.
[21] Holliday R (2006) Epigenetics: a historical overview. Epigenetics, 1, 76-80.
[22] Jablonka E, Lamb MJ (2002) The changing concept of epigenetics. Annals of the New York Academy of Sciences, 981, 82-96.
[23] Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. The Quarterly Review of Biology, 84, 131-176.
[24] Lauss K, Wardenaar R, van Hulten MH, Guryev V, Keurentjes JJ, Stam M, Johannes F (2016) Epigenetic divergence is sufficient to trigger heterosis in Arabidopsis thaliana. bioRxiv. doi:.
[25] Li LF, Liu B, Olsen KM, Wendel JF (2015a) Multiple rounds of ancient and recent hybridizations have occurred within the Aegilops-Triticum complex. New Phytologist, 208, 11-12.
[26] Li LF, Liu B, Olsen KM, Wendel JF (2015b) A re-evaluation of the homoploid hybrid origin of Aegilops tauschii, the donor of the wheat D‐subgenome. New Phytologist, 208, 4-8.
[27] Lira-Medeiros CF, Parisod C, Fernandes RA, Mata CS, Cardoso MA, Ferreira PCG (2010) Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS ONE, 5, e10326.
[28] Mallet J (2007) Hybrid speciation. Nature, 446, 279-283.
[29] Marcussen T, Sandve SR, Heier L, Spannagl M, Pfeifer M, Jakobsen KS, Wulff BB, Steuernagel B, Mayer KF, Olsen OA (2014) Ancient hybridizations among the ancestral genomes of bread wheat. Science, 345, 1250092.
[30] Matsushita SC, Tyagi AP, Thornton GM, Pires JC, Madlung A (2012) Allopolyploidization lays the foundation for evolution of distinct populations: evidence from analysis of synthetic Arabidopsis allohexaploids. Genetics, 191, 535-547.
[31] Moghaddam AMB, Roudier F, Seifert M, Bérard C, Magniette MLM, Ashtiyani RK, Houben A, Colot V, Mette MF (2011) Additive inheritance of histone modifications in Arabidopsis thaliana intra-specific hybrids. The Plant Journal, 67, 691-700.
[32] Nagaharu U (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. The Journal of Japanese Botany 7, 389-452.
[33] Ng DW, Zhang C, Miller M, Shen Z, Briggs S, Chen Z (2012) Proteomic divergence in Arabidopsis autopolyploids and allopolyploids and their progenitors. Heredity, 108, 419-430.
[34] Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature, 457, 327-331.
[35] Otto SP (2007) The evolutionary consequences of polyploidy. Cell, 131, 452-462.
[36] Parisod C, Holderegger R, Brochmann C (2010) Evolutionary consequences of autopolyploidy. New Phytologist, 186, 5-17.
[37] Paun O, Bateman RM, Fay MF, Hedrén M, Civeyrel L, Chase MW (2010) Stable epigenetic effects impact adaptation in allopolyploid orchids (Dactylorhiza: Orchidaceae). Molecular Biology and Evolution, 27, 2465-2473.
[38] Rakyan VK, Beck S (2006) Epigenetic variation and inheritance in mammals. Current Opinion in Genetics & Development, 16, 573-577.
[39] Ramsey J (2011) Polyploidy and ecological adaptation in wild yarrow. Proceedings of the National Academy of Sciences, USA, 108, 7096-7101.
[40] Ran LP, Fang TT, Hao R, Jiang JJ, Fang YJ, Wang YP (2016) Analysis of cytosine methylation in early generations of resynthesized Brassica napus. Journal of Integrative Agriculture, 15, 1228-1238.
[41] Richards EJ (2006) Inherited epigenetic variation—revisiting soft inheritance. Nature Reviews Genetics, 7, 395-401.
[42] Rieseberg LH, Willis JH (2007) Plant speciation. Science, 317, 910-914.
[43] Riggs AD, Porter TN (1996) Overview of epigenetic mechanisms. Cold Spring Harbor Monograph Archive, 32, 29-45.
[44] Schmitz RJ, Schultz MD, Lewsey MG, O’Malley RC, Urich MA, Libiger O, Schork NJ, Ecker JR (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science, 334, 369-373.
[45] Schneeberger K, Ossowski S, Ott F, Klein JD, Wang X, Lanz C, Smith LM, Cao J, Fitz J, Warthmann N (2011) Reference-guided assembly of four diverse Arabidopsis thaliana genomes. Proceedings of the National Academy of Sciences, USA, 108, 10249-10254.
[46] Selmecki AM, Maruvka YE, Richmond PA, Guillet M, Shoresh N, Sorenson AL, De S, Kishony R, Michor F, Dowell R (2015) Polyploidy can drive rapid adaptation in yeast. Nature, 519, 349-352.
[47] Shen H, He H, Li J, Chen W, Wang X, Guo L, Peng Z, He G, Zhong S, Qi Y (2012) Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. The Plant Cell, 24, 875-892.
[48] Shi X, Zhang C, Ko DK, Chen ZJ (2015) Genome-wide dosage-dependent and -independent regulation contributes to gene expression and evolutionary novelty in plant polyploids. Molecular Biology and Evolution, 32, 2351-2366.
[49] Solhaug EM, Ihinger J, Jost M, Gamboa V, Marchant B, Bradford D, Doerge RW, Tyagi A, Replogle A, Madlung A (2016) Environmental regulation of heterosis in the allopolyploid Arabidopsis suecica. Plant Physiology, 170, 2251-2263.
[50] Soltis DE, Buggs RJ, Doyle JJ, Soltis PS (2010) What we still don’t know about polyploidy. Taxon, 59, 1387-1403.
[51] Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annual Review of Plant Biology, 60, 561-588.
[52] Song Q, Chen ZJ (2015) Epigenetic and developmental regulation in plant polyploids. Current Opinion in Plant Biology, 24, 101-109.
[53] Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature, 150, 563-565.
[54] Wang J, Tian L, Lee HS, Wei NE, Jiang H, Watson B, Madlung A, Osborn TC, Doerge R, Comai L (2006) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics, 172, 507-517.
[55] Wang X, Zhang H, Li Y, Zhang Z, Li L, Liu B (2016) Transcriptome asymmetry in synthetic and natural allotetraploid wheats, revealed by RNA‐sequencing. New Phytologist, 209, 1264-1277.
[56] Weiss KM (2004) The smallest grain in the balance. Evolutionary Anthropology: Issues, News, and Reviews, 13, 122-126.
[57] Wendel JF, Jackson SA, Meyers BC, Wing RA (2016) Evolution of plant genome architecture. Genome Biology, 17, 1.
[58] Wu W, Yi MR, Wang X, Ma L, Jiang L, Li X, Xiao H, Sun M, Li L, Liu B (2013) Genetic and epigenetic differentiation between natural Betula ermanii (Betulaceae) populations inhabiting contrasting habitats. Tree Genetics & Genomes, 9, 1321-1328.
[59] 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. Molecular Biology and Evolution, 31, 1066-1076.
[60] Xu Y, Zhong L, Wu X, Fang X, Wang J (2009) Rapid alterations of gene expression and cytosine methylation in newly synthesized Brassica napus allopolyploids. Planta, 229, 471-483.
[61] Zemach A, McDaniel IE, Silva P, Zilberman D (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science, 328, 916-919.
[62] Zhang HK, Gou XW, Zhang A, Wang XT, Zhao N, Dong YZ, Li LF, Liu B (2016) Transcriptome shock invokes disruption of parental expression-conserved genes in tetraploid wheat. Scientific Reports, 6, 26363.
[63] Zhang J, Liu Y, Xia EH, Yao QY, Liu XD, Gao LZ (2015) Autotetraploid rice methylome analysis reveals methylation variation of transposable elements and their effects on gene expression. Proceedings of the National Academy of Sciences, USA, 112, E7022-E7029.
[64] Zohary D, Feldman M (1962) Hybridization between amphidiploids and the evolution of polyploids in the wheat (Aegilops-Triticum) group. Evolution, 16, 44-61.
[1] FAN Zi-Teng, WU Yu-Ling, WANG Xin-Ju, LI Tai-Qiang, GAO Jiang-Yun. (2019) Effects of symbiotic fungi on seed germination of interspecific hybrid progenies in Orchidaceae . Chin J Plant Ecol, 43(4): 374-382.
[2] Huang Jianfeng, Xu Rui, Peng Yanqiong. (2019) Research progress of interspecific hybridization in genus Ficus . Biodiv Sci, 27(4): 457-467.
[3] Zhuang Ping. (2019) Progress on the fertility of Rhododendron . Biodiv Sci, 27(3): 327-338.
[4] Hu Ying, Wang Xi, Zhang Xinxin, Zhou Wei, Chen Xiaoyang, Hu Xinsheng. (2019) Advancing phylogeography with chloroplast DNA markers . Biodiv Sci, 27(2): 219-234.
[5] Morigengaowa , Hui Shang, Baodong Liu, Ming Kang, Yuehong Yan. (2019) One or more species? GBS sequencing and morphological traits evidence reveal species diversification of Sphaeropteris brunoniana in China . Biodiv Sci, 27(11): 1196-1204.
[6] Siqi Liang, Xianchun Zhang, Ran Wei. (2019) Integrative taxonomy resolved species delimitation in a fern complex: A case study of the Asplenium coenobiale complex . Biodiv Sci, 27(11): 1205-1220.
[7] Chenyang Xue,Yufeng Xu,Bo Qu. (2018) Comparison of morphology, photosynthesis, and growth among Xanthium strumarium, X. sibiricum and their hybrid under different nitrogen levels . Biodiv Sci, 26(6): 554-563.
[8] Jibao Jiang, Jiangping Qiu. (2018) Origin and evolution of earthworms belonging to the family Megascolecidae in China . Biodiv Sci, 26(10): 1074-1082.
[9] Daike Tian, Chun Li, Yan Xiao, Naifeng Fu, Yi Tong, Ruijuan Wu. (2017) Occurrence and characteristics of natural hybridization in Begonia in China . Biodiv Sci, 25(6): 654-674.
[10] Shuoli Zheng, Xiaoling Tian, Chengling Huang, Lingjun Wang, Yuan Feng, Jingli Zhang. (2017) Molecular and morphological evidence for natural hybridization between Rhododendron decorum and R. delavayi (Ericaceae) . Biodiv Sci, 25(6): 627-637.
[11] Yukun Wei, Yanbo Huang, Guibin Li. (2017) Reproductive isolation in sympatric Salvia species sharing a sole pollinator . Biodiv Sci, 25(6): 608-614.
[12] Yanping Xie, Jianli Zhao, Xingfu Zhu, Li Li, Qingjun Li. (2017) Asymmetric hybridization of Primula secundiflora and P. poissonii in three sympatric populations . Biodiv Sci, 25(6): 647-653.
[13] Yuguo Wang. (2017) Natural hybridization and speciation . Biodiv Sci, 25(6): 565-576.
[14] Qiujie Zhou, Yacheng Cai, Wei Lun Ng, Wei Wu, Seping Dai, Feng Wang, Renchao Zhou. (2017) Molecular evidence for natural hybridization between two Melastoma species endemic to Hainan and their widespread congeners . Biodiv Sci, 25(6): 638-646.
[15] Hui Shang, Yuehong Yan. (2017) Natural hybridization and biodiversity conservation . Biodiv Sci, 25(6): 683-688.
Full text