Interspecific hybridization represents one of the main mechanisms of plant speciation. Merging of two genomes from different subspecies, species, or even genera is frequently accompanied by whole-genome duplication (WGD). Besides its evolutionary role, interspecific hybridization has also been successfully implemented in multiple breeding programs. Interspecific hybrids combine agronomic traits of two crop species or can be used to introgress specific loci of interests, such as those for resistance against abiotic or biotic stresses. The genomes of newly established interspecific hybrids (both allopolyploids and homoploids) undergo dramatic changes, including chromosome rearrangements, amplifications of tandem repeats, activation of mobile repetitive elements, and gene expression modifications. To ensure genome stability and proper transmission of chromosomes from both parental genomes into subsequent generations, allopolyploids often evolve mechanisms regulating chromosome pairing. Such regulatory systems allow only pairing of homologous chromosomes and hamper pairing of homoeologs. Despite such regulatory systems, several hybrid examples with frequent homoeologous chromosome pairing have been reported. These reports open a way for the replacement of one parental genome by the other. In this review, we provide an overview of the current knowledge of genomic changes in interspecific homoploid and allopolyploid hybrids, with strictly homologous pairing and with relaxed pairing of homoeologs.

Department of Plant Developmental Genetics Institute of Biophysics of the Czech Academy of Sciences Brno Czechia

Institute of Experimental Botany Czech Academy of Sciences Centre of the Region Hana for Biotechnological and Agricultural Research Olomouc Czechia

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Akera T., Chmatal L., Trimm E., Yang K., Aonbangkhen C., Chenoweth D. M., et al. (2017). Spindle asymmetry drives non-Mendelian chromosome segregation. Science 358 668–672. 10.1126/science.aan0092 PubMed DOI PMC

Bardil A., de Almeida J. D., Combes M. C., Lashermes P., Bertrand B. (2011). Genomic expression dominance in the natural allopolyploid Coffea arabica is massively affected by growth temperature. New Phytol. 192 760–774. 10.1111/j.1469-8137.2011.03833.x PubMed DOI

Bartel D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 281–297. 10.1016/S0092-8674(04)00045-5 PubMed DOI

Bennetzen J. L., Wang H. (2014). The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu. Rev. Plant Biol. 65 505–530. 10.1146/annurev-arplant-050213-035811 PubMed DOI

Bertrand B., Bardil A., Baraille H., Dussert S., Doulbeau S., Dubois E., et al. (2015). The greater phenotypic homeostasis of the allopolyploid Coffea arabica improved the transcriptional homeostasis over that of both diploid parents. Plant Cell Physiol. 56 2035–2051. 10.1093/pcp/pcv117 PubMed DOI PMC

Bird K. A., VanBuren R., Puzey J. R., Edger P. P. (2018). The causes and consequences of subgenome dominance in hybrids and recent polyploids. New Phytol. 220 87–93. 10.1111/nph.15256 PubMed DOI

Borowska-Zuchowska N., Kwasniewski M., Hasterok R. (2016). Cytomolecular analysis of ribosomal DNA evolution in a natural allotetraploid Brachypodium hybridum and its putative ancestors - dissecting complex repetitive structure of intergenic spacers. Front. Plant Sci. 7:1499. 10.3389/fpls.2016.01499 PubMed DOI PMC

Bottani S., Zabet N. R., Wendel J. F., Veitia R. A. (2018). Gene expression dominance in allopolyploids: hypotheses and models. Trends Plant Sci. 23 393–402. 10.1016/j.tplants.2018.01.002 PubMed DOI

Brandvain Y., Haig D. (2005). Divergent mating systems and parental conflict as a barrier to hybridization in flowering plants. Am. Nat. 166 330–338. 10.1086/432036 PubMed DOI

Chalhoub B., Denoeud F., Liu S. Y., Parkin I. A. P., Tang H. B., Wang X. Y., et al. (2014). Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345 950–953. 10.1126/science.1253435 PubMed DOI

Chandrasekhara C., Mohannath G., Blevins T., Pontvianne F., Pikaard C. S. (2016). Chromosome-specific NOR inactivation explains selective rRNA gene silencing and dosage control in Arabidopsis. Gene. Dev. 30 177–190. 10.1101/gad.273755.115 PubMed DOI PMC

Chelaifa H., Chague V., Chalabi S., Mestiri I., Arnaud D., Deffains D., et al. (2013). Prevalence of gene expression additivity in genetically stable wheat allohexaploids. New Phytol. 197 730–736. 10.1111/nph.12108 PubMed DOI

Chen Z. J. (2010). Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci. 15 57–71. 10.1016/j.tplants.2009.12.003 PubMed DOI PMC

Chen Z. J., Comai L., Pikaard C. S. (1998). Gene dosage and stochastic effects determine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids. Proc. Natl. Acad. Sci. U.S.A. 95 14891–14896. 10.1073/pnas.95.25.14891 PubMed DOI PMC

Cheng F., Wu J., Fang L., Sun S. L., Liu B., Lin K., et al. (2012). Biased gene fractionation and dominant gene expression among the subgenomes of Brassica rapa. PLoS One 7:e36442. 10.1371/journal.pone.0036442 PubMed DOI PMC

Chmatal L., Gabriel S. I., Mitsainas G. P., Martinez-Vargas J., Ventura J., Searle J. B., et al. (2014). Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in Mice. Curr. Biol. 24 2295–2300. 10.1016/j.cub.2014.08.017 PubMed DOI PMC

Comai L. (2005). The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6 836–846. 10.1038/nrg1711 PubMed DOI

Combes M. C., Hueber Y., Dereeper A., Rialle S., Herrera J. C., Lashermes P. (2015). Regulatory divergence between parental alleles determines gene expression patterns in hybrids. Genome Biol. Evol. 7 1110–1121. 10.1093/gbe/evv057 PubMed DOI PMC

Costa-Nunes P., Pontes O. (2013). “Chromatin and small RNA regulation of nucleolar dominance,” in Polyploid and Hybrid Genomics, eds Chen Z. J., Birchler J. A. (Hoboken, NJ: Wiley; ), 10.1002/9781118552872.ch18 DOI

Dobesova E., Malinska H., Matyasek R., Leitch A. R., Soltis D. E., Soltis P. S., et al. (2015). Silenced rRNA genes are activated and substitute for partially eliminated active homeologs in the recently formed allotetraploid, Tragopogon mirus (Asteraceae). Heredity 114 356–365. 10.1038/hdy.2014.111 PubMed DOI PMC

Dobzhansky T. (1936). Studies on Hybrid Sterility. II. Localization of sterility factors in Rosophila pseudoobscura hybrids. Genetics 21 113–135. PubMed PMC

Edger P. P., Smith R., McKain M. R., Cooley A. M., Vallejo-Marin M., Yuan Y. W., et al. (2017). Subgenome dominance in an interspecific hybrid, synthetic allopolyploid, and a 140-year-old naturally established neo-allopolyploid Monkeyflower. Plant Cell 29 2150–2167. 10.1105/tpc.17.00010 PubMed DOI PMC

Eilam T., Anikster Y., Millet E., Manisterski J., Feldman M. (2010). Genome size in diploids, allopolyploids, and autopolyploids of mediterranean triticeae. J. Bot. 2010:341380 10.1155/2010/341380 DOI

Emery M., Willis M. M. S., Hao Y., Barry K., Oakgrove K., Peng Y., et al. (2018). Preferential retention of genes from one parental genome after polyploidy illustrates the nature and scope of the genomic conflicts induced by hybridization. PLoS Genet. 14:e1007267. 10.1371/journal.pgen.1007267 PubMed DOI PMC

Freeling M., Woodhouse M. R., Subramaniam S., Turco G., Lisch D., Schnable J. C. (2012). Fractionation mutagenesis and similar consequences of mechanisms removing dispensable or less-expressed DNA in plants. Curr. Opin. Plant Biol. 15 131–139. 10.1016/j.pbi.2012.01.015 PubMed DOI

French S. L., Osheim Y. N., Cioci F., Nomura M., Beyer A. L. (2003). In exponentially growing Saccharomyces cerevisiae cells, rRNA synthesis is determined by the summed RNA polymerase I loading rate rather than by the number of active genes. Mol. Cell. Biol. 23 1558–1568. 10.1128/MCB.23.5.1558-1568.2003 PubMed DOI PMC

Fuchs J., Schubert I. (2012). “Chromosomal distribution and functional interpretation of epigenetic histone marks in plants,” in Plant Cytogenetics: Genome structure and chromosome function, Vol. 4 eds Bass H., Birchler J. (New York, NY: Springer; ), 231–253. 10.1007/978-0-387-70869-0_9 DOI

Gaeta R. T., Pires J. C. (2010). Homoeologous recombination in allopolyploids: the polyploid ratchet. New Phytol. 186 18–28. 10.1111/j.1469-8137.2009.03089.x PubMed DOI

Garsmeur O., Schnable J. C., Almeida A., Jourda C., D’Hont A., Freeling M. (2014). Two evolutionarily distinct classes of paleopolyploidy. Mol. Biol. Evol. 31 448–454. 10.1093/molbev/mst230 PubMed DOI

Gonzalez-Sandoval A., Gasser S. M. (2016). On TADs and LADs: spatial control over gene expression. Trends Genet. 32 485–495. 10.1016/j.tig.2016.05.004 PubMed DOI

Greaves I. K., Gonzalez-Bayon R., Wang L., Zhu A. Y., Liu P. C., Groszmann M., et al. (2015). Epigenetic changes in hybrids. Plant Physiol. 168 1197–1205. 10.1104/pp.15.00231 PubMed DOI PMC

Greer E., Martin A. C., Pendle A., Colas I., Jones A. M. E., Moore G., et al. (2012). The Ph1 locus suppresses Cdk2-type activity during premeiosis and meiosis in wheat. Plant Cell 24 152–162. 10.1105/tpc.111.094771 PubMed DOI PMC

Groszmann M., Greaves I. K., Fujimoto R., Peacock W. J., Dennis E. S. (2013). The role of epigenetics in hybrid vigour. Trends Genet. 29 684–690. 10.1016/j.tig.2013.07.004 PubMed DOI

Grover C. E., Gallagher J. P., Szadkowski E. P., Yoo M. J., Flagel L. E., Wendel J. F. (2012). Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol. 196 966–971. 10.1111/j.1469-8137.2012.04365.x PubMed DOI

Guo X., Han F. P. (2014). Asymmetric epigenetic modification and elimination of rDNA sequences by polyploidization in wheat. Plant Cell 26 4311–4327. 10.1105/tpc.114.129841 PubMed DOI PMC

Ha M., Lu J., Tian L., Ramachandran V., Kasschau K. D., Chapman E. J., et al. (2009). Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc. Natl. Acad. Sci. U.S.A. 106 17835–17840. 10.1073/pnas.0907003106 PubMed DOI PMC

Haag J. R., Pikaard C. S. (2011). Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat. Rev. Mol. Cell Biol. 12 483–492. 10.1038/nrm3152 PubMed DOI

Harper A. L., Trick M., He Z. S., Clissold L., Fellgett A., Griffiths S., et al. (2016). Genome distribution of differential homoeologue contributions to leaf gene expression in bread wheat. Plant Biotechnol. J. 14 1207–1214. 10.1111/pbi.12486 PubMed DOI PMC

He G., Deng X.-W. (2013). “Chromatin and gene expression mechanisms in hybrids,” in Polyploid and Hybrid Genomics, eds Chen Z. J., Birchler J. A. (Alexandria, VA: NSF; ), 10.1002/9781118552872.ch20 DOI

Herklotz V., Kovarik A., Lunerova J., Lippitsch S., Groth M., Ritz C. M. (2018). The fate of ribosomal RNA genes in spontaneous polyploid dogrose hybrids Rosa L. sect. Caninae (DC.) Ser. exhibiting non-symmetrical meiosis. Plant J. 94 77–90. 10.1111/tpj.13843 PubMed DOI

Hu G. J., Wendel J. F. (2019). Cis-trans controls and regulatory novelty accompanying allopolyploidization. New Phytol. 221 1691–1700. 10.1111/nph.15515 PubMed DOI

Idziak D., Hasterok R. (2008). Cytogenetic evidence of nucleolar dominance in allotetraploid species of Brachypodium. Genome 51 387–391. 10.1139/G08-017 PubMed DOI

Jenczewski E., Alix K. (2004). From diploids to allopolyploids: the emergence of efficient pairing control genes in plants. Crit. Rev. Plant Sci. 23 21–45. 10.1080/07352680490273239 DOI

Jiao Y. N., Wickett N. J., Ayyampalayam S., Chanderbali A. S., Landherr L., Ralph P. E., et al. (2011). Ancestral polyploidy in seed plants and angiosperms. Nature 473 97–100. 10.1038/nature09916 PubMed DOI

Josefsson C., Dilkes B., Comai L. (2006). Parent-dependent loss of gene silencing during interspecies hybridization. Curr. Biol. 16 1322–1328. 10.1016/j.cub.2006.05.045 PubMed DOI

Kamstra S. A., Kuipers A. G. J., De Jeu M. J., Ramanna M. S., Jacobsen E. (1999). The extent and position of homoeologous recombination in a distant hybrid of Alstroemeria: a molecular cytogenetic assessment of first generation backcross progenies. Chromosoma 108 52–63. 10.1007/s004120050351 PubMed DOI

Karlov G. I., Khrustaleva L. I., Lim K. B., van Tuyl J. M. (1999). Homoeologous recombination in 2n-gametes producing interspecific hybrids of Lilium (Liliaceae) studied by genomic in situ hybridization (GISH). Genome 42 681–686. 10.1139/g98-167 DOI

Kashkush K., Feldman M., Levy A. A. (2003). Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat. Genet. 33 102–106. 10.1038/ng1063 PubMed DOI

Khaitová L., Werlemark G., Nybom H., Kovarik A. (2010). Frequent silencing of rDNA loci on the univalent-forming genomes contrasts with their stable expression on the bivalent-forming genomes in polyploid dogroses (Rosa sect. Caninae). Heredity 104 113–120. 10.1038/hdy.2009.94 PubMed DOI

Khan N., Barba-Gonzalez R., Ramanna M. S., Visser R. G. F., Van Tuyl J. M. (2009). Construction of chromosomal recombination maps of three genomes of lilies (Lilium) based on GISH analysis. Genome 52 238–251. 10.1139/G08-122 PubMed DOI

Kim M. Y., Zilberman D. (2014). DNA methylation as a system of plant genomic immunity. Trends Plant Sci. 19 320–326. 10.1016/j.tplants.2014.01.014 PubMed DOI

Knight E., Greer E., Draeger T., Thole V., Reader S., Shaw P., et al. (2010). Inducing chromosome pairing through premature condensation: analysis of wheat interspecific hybrids. Funct. Integr. Genomics 10 603–608. 10.1007/s10142-010-0185-0 PubMed DOI PMC

Kopecky D., Bartos J., Zwierzykowski Z., Dolezel J. (2009). Chromosome pairing of individual genomes in tall fescue (Festuca arundinacea Schreb.), its progenitors, and hybrids with Italian ryegrass (Lolium multiflorum Lam.). Cytogenet. Genome Res. 124 170–178. 10.1159/000207525 PubMed DOI

Kopecky D., Loureiro J., Zwierzykowski Z., Ghesquiere M., Dolezel J. (2006). Genome constitution and evolution in Lolium x Festuca hybrid cultivars (Festulolium). Theor. Appl. Genet. 113 731–742. 10.1007/s00122-006-0341-z PubMed DOI

Kraitshtein Z., Yaakov B., Khasdan V., Kashkush K. (2010). Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics 186 801–812. 10.1534/genetics.110.120790 PubMed DOI PMC

Kryvokhyzha D., Milesi P., Duan T. L., Orsucci M., Wright S. I., Glemin S., et al. (2019). Towards the new normal: transcriptomic convergence and genomic legacy of the two subgenomes of an allopolyploid weed (Capsella bursa-pastoris). PLoS Genet. 15:e1008131. 10.1371/journal.pgen.1008131 PubMed DOI PMC

Ksiazczyk T., Kovarik A., Eber F., Huteau V., Khaitova L., Tesarikova Z., et al. (2011). Immediate unidirectional epigenetic reprogramming of NORs occurs independently of rDNA rearrangements in synthetic and natural forms of a polyploid species Brassica napus. Chromosoma 120 557–571. 10.1007/s00412-011-0331-z PubMed DOI

Kubota A., Akiyama Y., Fujimori M. (2019). The relationship between f ratio and seed yield-related traits in Festulolium. Crop Sci. 59 1992–1996. 10.2135/cropsci2019.02.0092 DOI

Lanctot C., Cheutin T., Cremer M., Cavalli G., Cremer T. (2007). Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat. Rev. Genet. 8 104–115. 10.1038/nrg2041 PubMed DOI

Lawrence R. J., Earley K., Pontes O., Silva M., Chen Z. J., Neves N., et al. (2004). A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol. Cell 13 599–609. 10.1016/S1097-2765(04)00064-4 PubMed DOI

Li A. L., Liu D. C., Wu J., Zhao X. B., Hao M., Geng S. F., et al. (2014). mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. Plant Cell 26 1878–1900. 10.1105/tpc.114.124388 PubMed DOI PMC

Li N., Xu C., Zhang A., Lv R., Meng X., Lin X., et al. (2019). DNA methylation repatterning accompanying hybridization, whole genome doubling and homoeolog exchange in nascent segmental rice allotetraploids. New Phytol. 223 979–992. 10.1111/nph.15820 PubMed DOI

Lim K. Y., Matyasek R., Kovarik A., Leitch A. (2004). Genome evolution in allotetraploid Nicotiana. Biol. J. Linn. Soc. 82 599–606. 10.1111/j.1095-8312.2004.00344.x DOI

Lindroth A. M., Shultis D., Jasencakova Z., Fuchs J., Johnson L., Schubert D., et al. (2004). Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J. 23 4146–4155. 10.1038/sj.emboj.7600430 PubMed DOI PMC

Liu Z. Q., Adamczyk K., Manzanares-Dauleux M., Eber F., Lucas M. O., Delourme R., et al. (2006). Mapping PrBn and other quantitative trait loci responsible for the control of homeologous chromosome pairing in oilseed rape (Brassica napus L.) haploids. Genetics 174 1583–1596. 10.1534/genetics.106.064071 PubMed DOI PMC

Lu F. H., McKenzie N., Gardiner L. J., Luo M., Hall A., Bevan M. W. (2019). Reduced chromatin accessibility underlies gene expression differences in homologous chromosome arms of hexaploid wheat and diploid Aegilops tauschii. bioRxiv [Preprint]. 10.1101/571133 PubMed DOI PMC

Lu J., Zhang C. Q., Baulcombe D. C., Chen Z. J. (2012). Maternal siRNAs as regulators of parental genome imbalance and gene expression in endosperm of Arabidopsis seeds. Proc. Natl. Acad. Sci. U.S.A. 109 5529–5534. 10.1073/pnas.1203094109 PubMed DOI PMC

Lukaszewski A. J., Apolinarska B., Gustafson J. P., Krolow K. D. (1987). Chromosome pairing and aneuploidy in tetraploid triticale. I. Stabilized karyotypes. Genome 29 554–561. 10.1139/g87-093 DOI

Lukaszewski A. J., Kopecky D. (2010). The Ph1 locus from wheat controls meiotic chromosome pairing in autotetraploid rye (Secale cereale L.). Cytogenet. Genome Res. 129 117–123. 10.1159/000314279 PubMed DOI

Ma X. F., Gustafson J. P. (2005). Genome evolution of allopolyploids: a process of cytological and genetic diploidization. Cytogenet. Genome Res. 109 236–249. 10.1159/000082406 PubMed DOI

Madlung A. (2013). Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110 99–104. 10.1038/hdy.2012.79 PubMed DOI PMC

Mallet J. (2005). Hybridization as an invasion of the genome. Trends Ecol. Evol. 20 229–237. 10.1016/j.tree.2005.02.010 PubMed DOI

Martin A. C., Rey M. D., Shaw P., Moore G. (2017). Dual effect of the wheat Ph1 locus on chromosome synapsis and crossover. Chromosoma 126 669–680. 10.1007/s00412-017-0630-0 PubMed DOI PMC

Martin A. C., Shaw P., Phillips D., Reader S., Moore G. (2014). Licensing MLH1 sites for crossover during meiosis. Nat. Commun. 5:4580. 10.1038/ncomms5580 PubMed DOI PMC

Masterson J. (1994). Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264 421–424. 10.1126/science.264.5157.421 PubMed DOI

McClintock B. (1984). The significance of responses of the genome to challenge. Science 226 792–801. 10.1126/science.15739260 PubMed DOI

Mhiri C., Parisod C., Daniel J., Petit M., Lim K. Y., Dorlhac de Borne F., et al. (2019). Parental transposable element loads influence their dynamics in young Nicotiana hybrids and allotetraploids. New Phytol. 221 1619–1633. 10.1111/nph.15484 PubMed DOI

Mohannath G., Pontvianne F., Pikaard C. S. (2016). Selective nucleolus organizer inactivation in Arabidopsis is a chromosome position-effect phenomenon. Proc. Natl. Acad. Sci. U.S.A. 113 13426–13431. 10.1073/pnas.1608140113 PubMed DOI PMC

Naranjo T. (2014). Dynamics of rye telomeres in a wheat background during early meiosis. Cytogenet. Genome Res. 143 60–68. 10.1159/000363524 PubMed DOI

Navashin M. (1934). Chromosomal alterations caused by hybridization and their bearing upon certain general genetic problems. Cytologia 5 169–203. 10.1508/cytologia.5.169 DOI

Neves N., Silva M., HeslopHarrison J. S., Viegas W. (1997). Nucleolar dominance in triticales: control by unlinked genes. Chromosome Res. 5 125–131. 10.1023/A:1018470208730 PubMed DOI

Novikova P. Y., Tsuchimatsu T., Simon S., Nizhynska V., Voronin V., Burns R., et al. (2017). Genome sequencing reveals the origin of the allotetraploid Arabidopsis suecica. Mol. Biol. Evol. 34 957–968. 10.1093/molbev/msw299 PubMed DOI PMC

Orellana J., Cermeno M. C., Lacadena J. R. (1984). Meiotic pairing in wheat-rye addition and substitution lines. Can. J. Genet. Cytol. 26 25–33. 10.1139/g84-005 DOI

Pandit M. K., Pocock M. J. O., Kunin W. E. (2011). Ploidy influences rarity and invasiveness in plants. J. Ecol. 99 1108–1115. 10.1111/j.1365-2745.2011.01838.x DOI

Parisod C., Alix K., Just J., Petit M., Sarilar V., Mhiri C., et al. (2010a). Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol. 186 37–45. 10.1111/j.1469-8137.2009.03096.x PubMed DOI

Parisod C., Holderegger R., Brochmann C. (2010b). Evolutionary consequences of autopolyploidy. New Phytol. 186 5–17. 10.1111/j.1469-8137.2009.03142.x PubMed DOI

Parisod C., Mhiri C., Lim K. Y., Clarkson J. J., Chase M. W., Leitch A. R., et al. (2012). Differential dynamics of transposable elements during long-term diploidization of Nicotiana section Repandae (Solanaceae) allopolyploid genomes. PLoS One 7:e50352. 10.1371/journal.pone.0050352 PubMed DOI PMC

Pernickova K., Kolackova V., Lukaszewski A. J., Fan C. L., Vrana J., Duchoslav M., et al. (2019a). Instability of alien chromosome introgressions in wheat associated with improper positioning in the nucleus. Int. J. Mol. Sci 20:E1448. 10.3390/ijms20061448 PubMed DOI PMC

Pernickova K., Linc G., Gaal E., Kopecky D., Samajova O., Lukaszewski A. J. (2019b). Out-of-position telomeres in meiotic leptotene appear responsible for chiasmate pairing in an inversion heterozygote in wheat (Triticum aestivum L.). Chromosoma 128 31–39. 10.1007/s00412-018-0686-5 PubMed DOI

Pfeifer M., Kugler K. G., Sandve S. R., Zhan B. J., Rudi H., Hvidsten T. R., et al. (2014). Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345:1250091. 10.1126/science.1250091 PubMed DOI

Ramirez-Gonzalez R. H., Borrill P., Lang D., Harrington S. A., Brinton J., Venturini L., et al. (2018). The transcriptional landscape of polyploid wheat. Science 361:eaar6089. 10.1126/science.aar6089 PubMed DOI

Rando O. J. (2012). Combinatorial complexity in chromatin structure and function: revisiting the histone code. Curr. Opin. Genet. Dev. 22 148–155. 10.1016/j.gde.2012.02.013 PubMed DOI PMC

Rao D. D., Vorhies J. S., Senzer N., Nemunaitis J. (2009). siRNA vs. shRNA: similarities and differences. Adv. Drug Deliv. Rev. 61 746–759. 10.1016/j.addr.2009.04.004 PubMed DOI

Rawale K. S., Khan M. A., Gill K. S. (2019). The novel function of the Ph1 gene to differentiate homologs from homoeologs evolved in Triticum turgidum ssp. dicoccoides via a dramatic meiosis-specific increase in the expression of the 5B copy of the C-Ph1 gene. Chromosoma 128 561–570. 10.1007/s00412-019-00724-6 PubMed DOI

Renny-Byfield S., Chester M., Kovaøík A., Le Comber S. C., Grandbastien M. A., Deloger M., et al. (2011). Next generation sequencing reveals genome downsizing in allotetraploid Nicotiana tabacum, predominantly through the elimination of paternally derived repetitive DNAs. Mol. Biol. Evol. 28 2843–2854. 10.1093/molbev/msr112 PubMed DOI

Rey M. D., Martin A. C., Higgins J., Swarbreck D., Uauy C., Shaw P., et al. (2017). Exploiting the ZIP4 homologue within the wheat Ph1 locus has identified two lines exhibiting homoeologous crossover in wheat-wild relative hybrids. Mol. Breed. 37:95. 10.1007/s11032-017-0700-2 PubMed DOI PMC

Rey M. D., Martin A. C., Smedley M., Hayta S., Harwood W., Shaw P., et al. (2018). Magnesium increases homoeologous crossover frequency during meiosis in ZIP4 (Ph1 Gene) mutant wheat-wild relative hybrids. Front. Plant Sci. 9:509. 10.3389/fpls.2018.00509 PubMed DOI PMC

Rieseberg L. H., Kim S., Randell R. A., Whitney K. D., Gross B. L., Lexer C., et al. (2007). Hybridization and the colonization of novel habitats by annual sunflowers. Genetica 129 149–165. 10.1007/s10709-006-9011-y PubMed DOI PMC

Rodrigues J. A., Zilberman D. (2015). Evolution and function of genomic imprinting in plants. Genes Dev. 29 2517–2531. 10.1101/gad.269902.115 PubMed DOI PMC

Ruprecht C., Proost S., Hernandez-Coronado M., Ortiz-Ramirez C., Lang D., Rensing S. A., et al. (2017). Phylogenomic analysis of gene co-expression networks reveals the evolution of functional modules. Plant J. 90 447–465. 10.1111/tpj.13502 PubMed DOI

Schnable J. C., Springer N. M., Freeling M. (2011). Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc. Natl. Acad. Sci. U.S.A. 108 4069–4074. 10.1073/pnas.1101368108 PubMed DOI PMC

Schubert I., Lysak M. A. (2011). Interpretation of karyotype evolution should consider chromosome structural constraints. Trends Genet. 27 207–216. 10.1016/j.tig.2011.03.004 PubMed DOI

Sears E. R., Okamoto M. (1958). “Intergenomic chromosome relationships in hexaploid wheat,” in Proceedings of the Xth International Congress of Genetics, ed. Boyes J. W. (Toronto: University of Toronto Press; ), 258–259. 10.1093/aob/mcm331 DOI

Sedel’nikova T. S., Muratova E. N., Pimenov A. V. (2011). Variability of chromosome numbers in gymnosperms. Biol. Bull. Rev. 1 100–109. 10.1134/S2079086411020083 DOI

Shi X. L., Ng D. W. K., Zhang C. Q., Comai L., Ye W. X., Chen Z. J. (2012). Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids. Nat. Commun. 3:950. 10.1038/ncomms1954 PubMed DOI

Soltis P. S., Soltis D. E. (2009). The role of hybridization in plant speciation. Annu. Rev. Plant Biol. 60 561–588. 10.1146/annurev.arplant.043008.092039 PubMed DOI

Soltis P. S., Soltis D. E. (2012). Polyploidy and Genome Evolution. Berlin: Springer, 10.1007/978-3-642-31442-1 DOI

Song Q. X., Chen Z. J. (2015). Epigenetic and developmental regulation in plant polyploids. Curr. Opin. Plant Biol. 24 101–109. 10.1016/j.pbi.2015.02.007 PubMed DOI PMC

Stoces S., Ruttink T., Bartos J., Studer B., Yates S., Zwierzykowski Z., et al. (2016). Orthology guided transcriptome assembly of Italian ryegrass and meadow fescue for single-ncleotide polymorphism discovery. Plant Genome 9 1–14. 10.3835/plantgenome2016.02.0017 PubMed DOI

Takahashi C., Leitch I. J., Ryan A., Bennett M. D., Brandham P. E. (1997). The use of genomic in situ hybridization (GISH) to show transmission of recombinant chromosomes by a partially fertile bigeneric hybrid, Gasteria lutzii x Aloe aristata (Aloaceae), to its progeny. Chromosoma 105 342–348. 10.1007/s004120050193 PubMed DOI

Talbert P. B., Masuelli R., Tyagi A. P., Comai L., Henikoff S. (2002). Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14 1053–1066. 10.1105/tpc.010425 PubMed DOI PMC

te Beest M., Le Roux J. J., Richardson D. M., Brysting A. K., Suda J., Kubesova M., et al. (2012). The more the better? The role of polyploidy in facilitating plant invasions. Ann. Bot. 109 19–45. 10.1093/aob/mcr277 PubMed DOI PMC

Thomas B. C., Pedersen B., Freeling M. (2006). Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Res. 16 934–946. 10.1101/gr.4708406 PubMed DOI PMC

Tsunewaki K. (1964). Genetic studies of 6X-derivative from an 8x Triticale. Can. J. Genet. Cytol. 6 1–11. 10.1139/g64-001 PubMed DOI

van Heusden A. W., van Ooijen J. W., Vrielink-van Ginkel R., Verbeek W. H. J., Wietsma W. A., Kik C. (2000). A genetic map of an interspecific cross in Allium based on amplified fragment length polymorphism (AFLP (TM)) markers. Theor. Appl. Genet. 100 118–126. 10.1007/s001220050017 DOI

Vieira R., Queiroz A., Morais L., Barao A., Mello-Sampayo T., Viegas W. (1990). Genetic control of 1R nucleolus organizer region expression in the presence of wheat genomes. Genome 33 713–718. 10.1139/g90-107 DOI

Wang M. J., Wang P. C., Lin M., Ye Z. X., Li G. L., Tu L. L., et al. (2018). Evolutionary dynamics of 3D genome architecture following polyploidization in cotton. Nat. Plants 4 90–97. 10.1038/s41477-017-0096-3 PubMed DOI

Wicker T., Sabot F., Hua-Van A., Bennetzen J. L., Capy P., Chalhoub B., et al. (2007). A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8 973–982. 10.1038/nrg2165 PubMed DOI

Woodhouse M. R., Cheng F., Pires J. C., 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 5283–5288. 10.1073/pnas.1402475111 PubMed DOI PMC

Wu J., Lin L., Xu M. L., Chen P. P., Liu D. X., Sun Q. F., et al. (2018). Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus. BMC Genomics 19:586. 10.1186/s12864-018-4966-5 PubMed DOI PMC

Xiong Z. Y., Gaeta R. T., Pires J. C. (2011). Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc. Natl. Acad. Sci. U.S.A. 108 7908–7913. 10.1073/pnas.1014138108 PubMed DOI PMC

Yaakov B., Kashkush K. (2012). Mobilization of Stowaway-like MITEs in newly formed allohexaploid wheat species. Plant Mol. Biol. 80 419–427. 10.1007/s11103-012-9957-3 PubMed DOI

Yakimowski S. B., Rieseberg L. H. (2014). The role of homoploid hybridization in evolution: a century of studies synthesizing genetics and ecology. Am. J. Bot. 101 1247–1258. 10.3732/ajb.1400201 PubMed DOI

Yoo M. J., Szadkowski E., Wendel J. F. (2013). Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity 110 171–180. 10.1038/hdy.2012.94 PubMed DOI PMC

Zhao N., Zhu B., Li M. J., Wang L., Xu L. Y., Zhang H. K., et al. (2011). Extensive and heritable epigenetic remodeling and genetic stability accompany allohexaploidization of wheat. Genetics 188 499–510. 10.1534/genetics.111.127688 PubMed DOI PMC

Zhu W. S., Hu B., Becker C., Dogan E. S., Berendzen K. W., Weigel D., et al. (2017). Altered chromatin compaction and histone methylation drive non-additive gene expression in an interspecific Arabidopsis hybrid. Genome Biol. 18:157. 10.1186/s13059-017-1281-4 PubMed DOI PMC

Zwierzykowski Z., Kosmala A., Zwierzykowska E., Jones N., Joks W., Bocianowski J. (2006). Genome balance in six successive generations of the allotetraploid Festuca pratensis x Lolium perenne. Theor. Appl. Genet. 113 539–547. 10.1007/s00122-006-0322-2 PubMed DOI

Zwierzykowski Z., Zwierzykowska E., Taciak M., Jones N., Kosmala A., Krajewski P. (2008). Chromosome pairing in allotetraploid hybrids of Festuca pratensis x Lolium perenne revealed by genomic in situ hybridization (GISH). Chromosome Res. 16 575–585. 10.1007/s10577-008-1198-6 PubMed DOI

Zwierzykowski Z., Zwierzykowska E., Taciak M., Kosmala A., Jones R. N., Zwierzykowski W., et al. (2011). Genomic structure and fertility in advanced breeding populations derived from an allotetraploid Festuca pratensis x Lolium perenne cross. Plant Breed. 130 476–480. 10.1111/j.1439-0523.2010.01839.x DOI

Uniparental expression of ribosomal RNA in ×Festulolium grasses: a link between the genome and nucleolar dominance

Genome Dominance in Allium Hybrids (A. cepa × A. roylei)

Reciprocal allopolyploid grasses (Festuca × Lolium) display stable patterns of genome dominance