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Genetic Consequences of Interspecific Hybridization, Its Role in Speciation and Phenotypic Diversity of Plants

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Abstract

The review focuses on the genetic consequences of interspecific hybridization and discusses its role in speciation and increasing the genetic diversity of plants, including the diversity of species and varieties of cultivated crops and garden plants. The combination of two or more genomes of different origin in the first-generation hybrids is usually accompanied by a phenomenon referred to as genomic shock, which results in different genetic and epigenetic changes. As a result, a material appears which is unique in providing multiple variants for natural selection of organisms, in different degrees adapted to new environmental conditions. In isolated plant populations with various destabilized genomes of hybrid origin under the influence of natural selection and due to genetic drift, gene and chromosomal differences will accumulate, triggering new reproductive isolating mechanisms that increase genetic isolation of a new race or species. Progressive establishment of genome stabilization at the eupolyploid stage and subsequent repeated genome and karyotype diploidization facilitate the retention of selected new genomic and epigenomic combinations. It seems likely that the evolutionary history of all agricultural crops and garden plant varieties, as well as of many invasive alien species and the components of adventive flora, was marked by interspecific crossings purposefully carried out by breeders during the creation of modern varieties and crossings between previously geographically isolated plants that were unintentionally united in apothecary and botanical gardens, in fields and backyards, and on disturbed lands around settlements. At the same time, phenotypic and genetic diversity of cultivars not only results from the combination of different alleles that already existed in the genomes of the parental species but also is a consequence of the appearance in the first-generation hybrids of new genomic and epigenomic variants that are direct or distant effects of post-hybridization genomic shock, the creative role of which we would like to emphasize.

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Notes

  1. For the first time (in translation from German into Russian language of the 18th century), the article was published under the title “Notification of Mister Professor Kölreuter on Breeding of New Tobacco with Red Flowers and the Description of the Aforesaid”—Works of the Free Economic Society for the Promotion of Agriculture and House Building in Russia, 1772. Part XX. In St. Petersburg at the Gentry Sea Cadet Corps. Pages 1–23.

REFERENCES

  1. Kel’reiter, I., A proposal of the culture of new bastard tobacco with red flowers and its description,in Kel’reiter, I., Uchenie o pole i gibridizatsii rastenii (Field Doctrine and the Plant Hybridization), Moscow: OGIZ-Sel’khozgiz 1940, pp. 61—69.

    Google Scholar 

  2. Bateson, B., William Bateson, F.R.S. Naturalist: His Essays and Addresses, Together with a Short Account of His Life, Cambridge: Cambridge Univ. Press, 1928.

    Google Scholar 

  3. Lotsy, J.P., Evolution by Means of Hybridization, The Hague: Martinus Nijhoff, 1916.

    Book  Google Scholar 

  4. Popov, M.G., Geographical and morphological method of systematics and hybridization processes in nature, Tr. Prikl. Bot., Genet. Sel., 1927, vol. 17, no. 1, pp. 221—290.

    Google Scholar 

  5. Popov, M.G., Osnovy florogenetiki (Basics of Florogenetics), Moscow: Akad. Nauk SSSR, 1963.

  6. Anderson, E., Introgressive Hybridization, New York: Hafner, 1969.

    Google Scholar 

  7. Winge, Ø., The chromosomes: their numbers and general importance, C. R. Trav. Lab. Carlsberg, 1917, vol. 13, pp. 131—275.

    Google Scholar 

  8. Rosenberg, O., Cytologische und morphologische Studien an Drosera longifolia × rotundifolia Kungliga, Sven. Vetensk.-Akad. Skr. Naturskyddsarenden Handl., 1909, vol. 43, pp. 1—64.

    Google Scholar 

  9. Federley, H., Das Verhalten der Chromosomen bei der Spermatogenese der Schmetterlinge Pygaera anachoreta, curtula und pigra sowie einiger ihrer Bastarde, Z. Indukt. Abstamm.- Vererbungsl., 1913, vol. 9, pp. 1—110.

    Google Scholar 

  10. Karpechenko, G.D., Hybrids of Raphanus sativus L. × Brassica oleracea L., J. Genet., 1924, vol. 14, pp. 375—396.

    Article  Google Scholar 

  11. De Vries, H., Species and Varieties, Their Origin by Mutation, Chicago: The Open Court, 1905.

    Google Scholar 

  12. Soltis, D.E., Visger, C.J., Marchant, D.B., and Soltis, P.S., Polyploidy: pitfalls and paths to a paradigm, Am. J. Bot., 2016, vol. 103, pp. 1146—1166. https://doi.org/10.3732/ajb.1500501

    Article  PubMed  Google Scholar 

  13. Kihara, H. and Ono, T., Chromosomenzahlen und systematische Gruppierung der Rumex-Arten, Z. Wiss. Biol., B, 1927, vol. 4, no. 3, pp. 475—481.

  14. Zelenin, A.V., Rodionov, A.V., Bol’sheva, N.L., et al., Genome: origins and evolution of the term, Mol. Biol. (Moscow), 2016, vol. 50, no. 4, pp. 542—550.

    Article  CAS  Google Scholar 

  15. Bolsheva, N.L., Melnikova, N.V., Kirov, I.V., et al., Evolution of blue-flowered species of genus Linum based on high-throughput sequencing of ribosomal RNA genes, BMC Evol. Biol., 2010, vol. 17, no. 2, p. 253. https://doi.org/10.1186/s12862-017-1105-x

    Article  CAS  Google Scholar 

  16. Oxelman, B., Brysting, A.K., Jones, G.R., et al., Phylogenetics of allopolyploids, Ann. Rev. Ecol. Evol. Syst., 2017, vol. 48, pp. 543—557.

    Article  Google Scholar 

  17. Whitney, K.D., Ahern, J.R., Campbell, L.G., et al., Patterns of hybridization in plants, Persp. Plant Ecol. Evol. Syst., 2010, vol. 12, pp. 175—182.

    Article  Google Scholar 

  18. Punina, E.O., Mordak, E.V., Timukhin, I.N., and Litvinskaya, S.A., Summary of notospecies of the genus Paeonia L. (Paeoniaceae) of the Caucasus and Crimea, Nov. Sist. Vysshikh Rast., 2011, vol. 42, pp. 120—131.

    Google Scholar 

  19. Yakimowski, S.B. and Rieseberg, L.H., The role of homoploid hybridization in evolution: a century of studies synthesizing genetics and ecology, Am. J. Bot., 2014, vol. 101, pp. 1247—1258. https://doi.org/10.3732/ajb.14002

    Article  PubMed  Google Scholar 

  20. Kamelin, R.V., Speciation in flowering plants, Tr. Zool. Inst. Russ. Akad. Nauk, 2009, suppl. 1, pp. 141—149.

  21. Mudrik, E.A., Shatokhina, A.V., Polyakova, T.A., et al., The genetic status of spruce on the northern border of its range in the European part of Russia, in Biologicheskie resursy: izuchenie, ispol’zovanie, okhrana (Biological Resources: Study, Use, Conservation), Vologda: Vologda Gos. Univ., 2016, pp. 85—88.

    Google Scholar 

  22. Orlova, L.V. and Egorov, A.A., Systematics and geographical distribution of Finnish spruce (Picea fennica (Regel) Kom., Pinaceae), Nov. Sist. Vysshikh Rast., 2011, vol. 42, pp. 5—23.

    Google Scholar 

  23. Tamayo-Ordóñez, M.C., Espinosa-Barrera, L.A., Tamayo-Ordóñez, Y.J., et al., Advances and perspectives in the generation of polyploid plant species, Euphytica, 2016, vol. 209, pp. 1—22.

    Article  Google Scholar 

  24. De Storme, N. and Mason, A., Plant speciation through chromosome instability and ploidy change: cellular mechanisms, molecular factors and evolutionary relevance, Curr. Plant Biol., 2014, vol. 1, pp. 10—33. https://doi.org/10.1016/j.cpb.2014.09.002

    Article  Google Scholar 

  25. Simanovskii, S.A. and Bogdanov, Yu.F., Genetic control of meiosis in plants, Russ. J. Genet., 2018, vol. 54, no. 4, pp. 384—402.

    Google Scholar 

  26. Satina, S. and Blakeslee, A.F., Cytological effects of a gene in Datura which causes dyad formation in sporogenesis, Bot. Gaz., 1935, vol. 96, pp. 521—532. https://doi.org/10.1086/334498

    Article  Google Scholar 

  27. Golubovskaya, I.N., Hamant, O., Timofejeva, L., et al., Alleles of afd1 dissect REC8 functions during meiotic prophase I, J. Cell Sci., 2006, vol. 119, pp. 3306—3315. https://doi.org/10.1242/jcs.03054

  28. Chelysheva, L., Diallo, S., Vezon, D., et al., AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis, J. Cell Sci., 2005, vol. 118, pp. 4621—4632.

    Article  CAS  PubMed  Google Scholar 

  29. d’Erfurth, I., Cromer, L., Jolivet, S., et al., The CYCLIN-A CYCA1;2/TAM is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition, PLoS Genet., 2010, vol. 6. e1000989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Pawlowski, W.P., Wang, C.-J.R., Golubovskaya, I.N., et al., Maize AMEIOTIC1 is essential for multiple early meiotic processes and likely required for the initiation of meiosis, Proc. Natl. Acad. Sci. U.S.A., 2009, vol. 106, pp. 3603—3608. https://doi.org/10.1073/pnas.0810115106

    Article  PubMed  PubMed Central  Google Scholar 

  31. Andreuzza, S. and Siddiqi, I., Spindle positioning, meiotic nonreduction, and polyploidy in plants, PLoS Genet., 2008, vol. 4. e1000272. https://doi.org/10.1371/journal.pgen.1000272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ramsey, J. and Schemske, D.W., Neopolyploidy in flowering plants, Annu. Rev. Ecol. Syst., 2002, vol. 33, pp. 589—639.

    Article  Google Scholar 

  33. Kreiner, J.M., Kron, P., and Husband, B.C., Frequency and maintenance of unreduced gametes in natural plant populations: associations with reproductive mode, life history and genome size, New Phytol., 2017, vol. 214, pp. 879—889. https://doi.org/10.1111/nph.14423

    Article  CAS  PubMed  Google Scholar 

  34. Müntzing, A., The evolutionary significance of autopolyploidy, Hereditas, 1936, vol. 21, pp. 263—378.

    Google Scholar 

  35. Darlington, C.D., Recent Advances in Cytology, Philadelphia: Blakiston, 1937.

    Google Scholar 

  36. Grant, V., The Origins of Adaptations, New York: Columbia Univ. Press, 1963.

    Google Scholar 

  37. Goldblatt, P., Polyploidy in angiosperms: monocotyledons,in Polyploidy: Biological Relevance, Lewis, W.H., Ed., New York: Plenum, 1980, pp. 219—239.

    Google Scholar 

  38. Wood, T.E., Takebayashi, N., Barker, M.S., et al., The frequency of polyploid speciation in vascular plants, Proc. Natl. Acad. Sci. U.S.A., 2009, vol. 106, pp. 13875—13879. https://doi.org/10.1073/pnas.0811575106

    Article  PubMed  PubMed Central  Google Scholar 

  39. Probatova, N.S., Annotated list of chromosome numbers in species of the Poaceae family from the Russian Far East, in Komarovskie chteniya (Komarov Readings), Vladivostok, 2007, issue 55, pp. 9—103.

  40. Shneer, V.S., Punina, E.O., and Rodionov, A.V., Intraspecific differences in ploidy and their taxonomic interpretation, Bot. Zh., 2018, vol. 103, no. 5, pp. 555—585.

    Article  Google Scholar 

  41. Segraves, K.A. and Anneberg, T.J., Species interactions and plant polyploidy, Am. J. Bot., 2016, vol. 103, pp. 1326—1335. https://doi.org/10.3732/ajb.1500529

    Article  PubMed  Google Scholar 

  42. Bansal, P., Kaur, P., Banga, S.K., and Banga, S.S., Augmenting genetic diversity in Brassica juncea through its resynthesis using purposely selected diploid progenitors, Int. J. Plant Breed., 2009, vol. 3, pp. 41—45.

    Google Scholar 

  43. Fu, D., Xiao, M., Hayward, A., et al., What is crop heterosis: new insights into an old topic, J. Appl. Genet., 2015, vol. 56, pp. 1—13. https://doi.org/10.1007/s13353-014-0231-z

    Article  CAS  PubMed  Google Scholar 

  44. Flagel, L.E. and Wendel, J.F., Gene duplication and evolutionary novelty in plants, New Phytol., 2009, vol. 183, pp. 557—564. https://doi.org/10.1111/j.1469-8137.2009.02923.x

    Article  PubMed  Google Scholar 

  45. Arrigo, N. and Barker, M.S., Rarely successful polyploids and their legacy in plant genomes, Curr. Opin. Plant Biol., 2012, vol. 15, pp. 140—146. https://doi.org/10.1016/j.pbi.2012.03.010

    Article  CAS  PubMed  Google Scholar 

  46. Kostoff, D., Studies on polyploid plants, J. Genet., 1938, vol. 37, pp. 129—209.

    Article  Google Scholar 

  47. Spoelhof, J.P., Soltis, P.S., and Soltis, D.E., Pure polyploidy: closing the gaps in autopolyploid research, J. Syst. Evol., 2017, vol. 55, pp. 340—352. https://doi.org/10.1111/jse.12253

    Article  Google Scholar 

  48. Van de Peer, Y., Mizrachi, E., and Marchal, K., The evolutionary significance of polyploidy, Nat. Rev. Genet., 2017, vol. 18, pp. 411—424. https://doi.org/10.1038/nrg.2017.26

    Article  CAS  PubMed  Google Scholar 

  49. Schranz, M.E., Mohammadin, S., and Edger, P.E., Ancient whole genome duplications, novelty and diversification: the WGD radiation lag-time model, Curr. Opin. Plant Biol., 2012, vol. 15, pp. 147—153. https://doi.org/10.1016/j.pbi.2012.03.011

    Article  PubMed  Google Scholar 

  50. Tank, D.C., Eastman, J.M., Pennell, M.W., et al., Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications, New Phytol., 2015, vol. 207, pp. 454—467. https://doi.org/10.1111/nph.13491

    Article  PubMed  Google Scholar 

  51. Clark, J.W. and Donoghue, P.C., Constraining the timing of whole genome duplication in plant evolutionary history, Proc. Biol. Sci., 2017, vol. 284, p. 20170912. https://doi.org/10.1098/rspb.2017.0912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Clarkson, J.J., Dodsworth, S., and Chase, M.W., Time-calibrated phylogenetic trees establish a lag between polyploidisation and diversification in Nicotiana (Solanaceae), Plant Syst. Evol., 2017, vol. 303, pp. 1001—1012. https://doi.org/10.1007/s00606-017-1416-9

    Article  Google Scholar 

  53. Leitch, A.R., Schwarzacher, T., Mosgöller, W., et al., Parental genomes are separated throughout the cell cycle in a plant hybrid, Chromosoma, 1991, vol. 101, pp. 206—213.

    Article  CAS  Google Scholar 

  54. Schwarzacher, T., Heslop-Harrison, J.S., and Anamthawat-Jónsson, K., Parental genome separation in reconstructions of somatic and premeiotic metaphases of Hordeum vulgare x H. bulbosum, J. Cell Sci., 1992, vol. 101, pp. 13—24.

    Google Scholar 

  55. Kotseruba, V., Gernand, D., Meister, A., and Houben, A., Uniparental loss of ribosomal DNA in the allotetraploid grass Zingeria trichopoda (2n = 8), Genome, 2003, vol. 46, pp. 156—163.

    Article  CAS  PubMed  Google Scholar 

  56. Rodionov, A.V., Kotseruba, V.V., Kim, E.S., et al., Grass genome and chromosome sets evolution, Tsitologiya, 2013, vol. 55, no. 4, pp. 225—229.

    CAS  Google Scholar 

  57. Tu, Y., Sun, J., Liu, Y., et al., Production and characterization of intertribal somatic hybrids of Raphanus sativus and Brassica rapa with dye and medicinal plant Isatis indigotica, Plant Cell Rep., 2008, vol. 27, pp. 873—883. https://doi.org/10.1007/s00299-008-0513-1

    Article  CAS  PubMed  Google Scholar 

  58. Ding, L., Zhao, Z.G., Ge, X.H., and Li, Z.Y., Different timing and spatial separation of parental chromosomes in intergeneric somatic hybrids between Brassica napus and Orychophragmus violaceus, Genet. Mol. Res., 2014, vol. 13, pp. 2611—2618. https://doi.org/10.4238/2014

    Article  CAS  PubMed  Google Scholar 

  59. Gernand, D., Rutten, T., Varshney, A., et al., Uniparental chromosome elimination at mitosis and interphase in wheat and pearl millet crosses involves micronucleus formation, progressive heterochromatinization, and DNA fragmentation, Plant Cell, 2005, vol. 17, pp. 2431—2438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Wang, N. and Dawe, R.K., Centromere size and its relationship to haploid formation in plants, Mol. Plant, 2018, vol. 11, pp. 398—406. https://doi.org/10.1016/j.molp.2017.12.009

    Article  CAS  PubMed  Google Scholar 

  61. Clausen, R.E. and Mann, M.C., Inheritance in Nicotiana tabacum: 5. The occurrence of haploid plants in interspecific progenies, Proc. Natl. Acad. Sci. U.S.A., 1924, vol. 10, pp. 121—124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Kasha, K.J. and Kao, K.N., High frequency haploid production in barley (Hordeum vulgare L.), Nature, 1970, vol. 225, pp. 874—876.

    Article  CAS  PubMed  Google Scholar 

  63. Golubovskaya, I.N., Cytogenetics of remote wheat hybrids and the prospects for their use in breeding, in Tsitogenetika pshenitsy i ee gibridov (Cytogenetics of Wheat and Its Hybrids), Moscow: Nauka, 1971, pp. 243—286.

  64. Golubovskaya, I.N., Shkutina, F.M., and Khvostova, V.V., Chromosome number instability found in meiosis in wheat—rye and incomplete wheat—wheatgrass amphidiploids, Genetika (Moscow), 1967, vol. 3, no. 1, pp. 25—33.

    Google Scholar 

  65. Cheng, B.F., Séguin-Swartz, G., and Somers, D.J., Cytogenetic and molecular characterization of intergeneric hybrids between Brassica napus and Orychophragmus violaceus, Genome, 2002, vol. 45, pp. 110—115.

    Article  CAS  PubMed  Google Scholar 

  66. Finch, R.A., Tissue-specific elimination of alternative whole parental genomes in one barley hybrid, Chromosoma, 1983, vol. 88, pp. 386—393.

    Article  Google Scholar 

  67. Henry, I.M., Dilkes, B.P., Tyagi, A.P., et al., Dosage and parent-of-origin effects shaping aneuploid swarms in A. thaliana, Heredity, 2009, vol. 103, pp. 458—468. https://doi.org/10.1038/hdy.2009.81

    Article  CAS  PubMed  Google Scholar 

  68. D’Hont, A., Denoeud, F., Aury, J.-M., et al., The banana (Musa acuminata) genome and the evolution of monocotyledonous plants, Nature, 2012, vol. 488, pp. 213—217. https://doi.org/10.1038/nature11241

    Article  CAS  PubMed  Google Scholar 

  69. Brenchley, R., Spannagl, M., Pfeifer, M., et al., Analysis of the bread wheat genome using whole-genome shotgun sequencing, Nature, 2012, vol. 491, pp. 705—710. https://doi.org/10.1038/nature11650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Xiong, Z., Gaeta, R.T., and Pires, J.C., Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, pp. 7908—7913. https://doi.org/10.1073/pnas.1014138108

    Article  PubMed  PubMed Central  Google Scholar 

  71. Lipman, M.J., Chester, M., Soltis, P.S., and Soltis, D.E., Natural hybrids between Tragopogon mirus and T. miscellus (Asteraceae): a new perspective on karyotypic changes following hybridization at the polyploid level, Am. J. Bot., 2013, vol. 100, pp. 2016—2022. https://doi.org/10.3732/ajb.1300036

    Article  PubMed  Google Scholar 

  72. Pagliarini, M.S., Meiotic behavior of economically important plant species: the relationship between fertility and male sterility, Genet. Mol. Biol., 2000, vol. 23, pp. 997—1002.

    Article  Google Scholar 

  73. Clausen, J., Introgression facilitated by apomixis in polyploid Poas, Euphitica, 1961, vol. 10, pp. 87—94.

    Article  Google Scholar 

  74. Shevchenko, S.V. and Zubkova, N.V., Some aspects of reproductive biology of Clematis L. (family Ranunculaceae Juss.), Tr. Nikitsk. Bot. Sada, 2008, vol. 129, pp. 6—21.

    Google Scholar 

  75. Talbert, P.B., Bryson, T.D., and Henikoff, S., Adaptive evolution of centromere proteins in plants and animals, J. Biol., 2004, vol. 3, p. 18.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Ishii, T., Karimi-Ashtiyani, R., and Houben, A., Haploidization via chromosome elimination: means and mechanisms, Annu. Rev. Plant Biol., 2016, vol. 67, pp. 421—438. https://doi.org/10.1146/annurev-arplant-043014-114714

    Article  CAS  PubMed  Google Scholar 

  77. Sanei, M., Pickering, R., Kumke, K., et al., Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, pp. 498—505. https://doi.org/10.1073/pnas.1103190108

    Article  Google Scholar 

  78. Duro, E. and Marston, A.L., From equator to pole: splitting chromosomes in mitosis and meiosis, Genes Dev., 2015, vol. 29, pp. 109—122. https://doi.org/10.1101/gad.255554.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Hamant, O., Golubovskaya, I., Meeley, R., et al., A REC8-dependent plant Shugoshin is required for maintenance of centromeric cohesion during meiosis and has no mitotic functions, Curr. Biol., 2005, vol. 15, pp. 948—954.

    Article  CAS  PubMed  Google Scholar 

  80. Zhang, H., Bian, Y., Gou, X., et al., Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat, Proc. Natl. Acad. Sci. U.S.A., 2013, vol. 110, pp. 3447—3452. https://doi.org/10.1073/pnas.1300153110

    Article  PubMed  PubMed Central  Google Scholar 

  81. Henry, I.M., Dilkes, B.P., Tyagi, A., et al., The BOY NAMED SUE quantitative trait locus confers increased meiotic stability to an adapted natural allopolyploid of Arabidopsis, Plant Cell, 2014, vol. 26, pp.181—194. https://doi.org/10.1105/tpc.113.120626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Hollister, J.D., Polyploidy: adaptation to the genomic environment, New Phytol., 2015, vol. 205, pp. 1034—1039.

    Article  PubMed  Google Scholar 

  83. Lloyd, A. and Bomblies, K., Meiosis in autopolyploid and allopolyploid Arabidopsis, Curr. Opin. Plant Biol., 2016, vol. 30, pp. 116—122. https://doi.org/10.1016/j.pbi.2016.02.004

    Article  PubMed  Google Scholar 

  84. Riley, R., Chapman, V., and Belifield, A.M., Induced mutation affecting the control of meiotic chromosome pairing in Triticum aestivum, Nature, 1966, vol. 211, pp. 368—369.

    Article  Google Scholar 

  85. Griffiths, S., Sharp, R., Foote, T.N., et al., Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat, Nature, 2006, vol. 439, pp. 749—752.

    Article  CAS  PubMed  Google Scholar 

  86. Grusz, A.L., Sigel, E.M., and Witherup, C., Homoeologous chromosome pairing across the eukaryote phylogeny, Mol. Phylogenet. Evol., 2017, vol. 117, pp. 83—94. https://doi.org/10.1016/j.ympev.2017.05.025

    Article  PubMed  Google Scholar 

  87. Nikoloudakis, N. and Katsiotis, A., Comparative molecular and cytogenetic methods can clarify meiotic incongruities in Avena allopolyploid hybrids, Caryologia, 2015, vol. 68, pp. 84—91.

    Article  Google Scholar 

  88. Cifuentes, M., Grandont, L., Moore, G., et al., Genetic regulation of meiosis in polyploid species: new insights into an old question, New Phytol., 2010, vol. 186, pp. 29—36. https://doi.org/10.1111/j.1469-8137.2009.03084.x

    Article  CAS  PubMed  Google Scholar 

  89. Chen, E.C., Najar, C.F.B.A., Zheng, C., et al., The dynamics of functional classes of plant genes in rediploidized ancient polyploids, BMC Bioinf., 2013, vol. 14, suppl. 15, p. S19. https://doi.org/10.1186/1471-2105-14-S15-S19

    Article  Google Scholar 

  90. Veitia, R.A., Gene duplicates: agents of robustness or fragility?, Trends Genet., 2017, vol. 33, pp. 377—379. https://doi.org/10.1016/j.tig.2017.03.006

    Article  CAS  PubMed  Google Scholar 

  91. Scannell, D.R., Byrne, K.P., Gordon, J.L., et al., Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts, Nature, 2006, vol. 440, pp. 341—345.

    Article  CAS  PubMed  Google Scholar 

  92. Tyupa, N.B., Kim, E.S., Loskutov, I.G., and Rodionov, A.V., To the origin of polyploids in the genus Avena L.: molecular phylogenetic research, Tr. Prikl. Bot., Genet. Sel., 2009, vol. 165, pp. 13—20.

    Google Scholar 

  93. Rodionov, A.V., Krainova, L.M., Kim, E.S., et al., The origin of few polyploid Avena species inferred from an ITS polymorphism study, Innovation for Food and Health (Proc. 10th Int. Oat Conf. “OATS 2016”), St. Petersburg, 2016, pp. 88—89.

  94. Lim, K.Y., Matyasek, R., Kovarik, A., and Leitch, A., Parental origin and genome evolution in the allopolyploid Iris versicolor, Ann. Bot., 2007, vol. 100, pp. 219—224. https://doi.org/10.1093/aob/mcm116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Sang, T., Crawford, D.J., and Stuessy, T.F., Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution, Proc. Natl. Acad. Sci. U.S.A., 1995, vol. 92, pp. 6813—6817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Punina, E.O., Machs, E.M., Krapivskaya, E.E., et al., Interspecific hybridization in the genus Paeonia (Paeoniaceae): polymorphic sites in transcribed spacers of the 45S rRNA genes as indicators of natural and artificial peony hybrids, Russ. J. Genet., 2012, vol. 48, no. 7, pp. 684—697. https://doi.org/https://doi.org/10.1134/S1022795412070113.

    Article  CAS  Google Scholar 

  97. Albalat, R. and Cañestro, C., Evolution by gene loss, Nat. Rev. Genet., 2016, vol. 17, pp. 379—391. https://doi.org/10.1038/nrg.2016.39

    Article  CAS  PubMed  Google Scholar 

  98. Muñoz-López, M. and García-Pérez, J.L., DNA transposons: nature and applications in genomics, Curr. Genomics, 2010, vol. 11, pp. 115—128. https://doi.org/10.2174/138920210790886871

    Article  PubMed  PubMed Central  Google Scholar 

  99. Wang, J., Gao, S., Mostovoy, Y., et al., Comparative genome analysis of programmed DNA elimination in nematodes, Genome Res., 2017, vol. 27, pp. 2001—2014. https://doi.org/10.1101/gr.225730.117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Qiu, G.H., Genome defense against exogenous nucleic acids in eukaryotes by non-coding DNA occurs through CRISPR-like mechanisms in the cytosol and the bodyguard protection in the nucleus, Mutat. Res. Rev. Mutat. Res., 2016, vol. 767, pp. 31—41. https://doi.org/10.1016/j.mrrev.2016.01.001

    Article  CAS  PubMed  Google Scholar 

  101. Flagel, L.E. and Wendel, J.F., Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid Cotton speciation, New Phytol., 2010, vol. 186, pp. 184—193. https://doi.org/10.1111/j.1469-8137.2009.03107.x

    Article  CAS  PubMed  Google Scholar 

  102. Schnable, J.C., Springer, N.M., and Freeling, M., Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, pp. 4069—4074. https://doi.org/10.1073/pnas.1101368108

    Article  PubMed  PubMed Central  Google Scholar 

  103. Ungerer, M.C., Strakosh, S.C., and Zhen, Y., Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation, Curr. Biol., 2006, vol. 16, pp. R872—R873.

    Article  CAS  PubMed  Google Scholar 

  104. Petit, M., Guidat, C., Daniel, J., et al., Mobilization of retrotransposons in synthetic allotetraploid tobacco, New Phytol., 2010, vol. 186, pp. 135—147. https://doi.org/10.1111/j.1469-8137.2009.03140.x

    Article  CAS  PubMed  Google Scholar 

  105. Ben-David, S., Yaakov, B., and Kashkush, K., Genome-wide analysis of short interspersed nuclear elements SINES revealed high sequence conservation, gene association and retrotranspositional activity in wheat, Plant J., 2013, vol. 76, pp. 201—210. https://doi.org/10.1111/tpj.12285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Sarilar, V., Palacios, P.M., Rousselet, A., et al., Allopolyploidy has a moderate impact on restructuring at three contrasting transposable element insertion sites in resynthesized Brassica napus allotetraploids, New Phytol., 2013, vol. 198, pp. 593—604. https://doi.org/10.1111/nph.12156

    Article  CAS  PubMed  Google Scholar 

  107. Parisod, C., Salmon, A., Zerjal, T., et al., Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina, New Phytol., 2009, vol. 184, pp. 1003—1015. https://doi.org/10.1111/j.1469-8137.2009.03029.x

    Article  CAS  PubMed  Google Scholar 

  108. Senerchia, N., Felber, F., North, B., et al., Differential introgression and reorganization of retrotransposons in hybrid zones between wild wheats, Mol. Ecol., 2016, vol. 25, pp. 2518–2528. https://doi.org/10.1111/mec.13515

    Article  PubMed  Google Scholar 

  109. Matzke, M.A. and Mosher, R.A., RNA-directed DNA methylation: an epigenetic pathway of increasing complexity, Nat. Rev. Genet., 2014, vol. 15, pp. 394—408. https://doi.org/10.1038/nrg3683

    Article  CAS  PubMed  Google Scholar 

  110. Fultz, D., Choudury, S.G., and Slotkin, R.K., Silencing of active transposable elements in plants, Curr. Opin. Plant Biol., 2015, vol. 27, pp. 67—76. https://doi.org/10.1016/j.pbi.2015.05.027

    Article  CAS  PubMed  Google Scholar 

  111. Grover, J.W., Kendall, T., Baten, A., et al., Maternal components of RNA-directed DNA methylation are required for seed development in Brassica rapa, Plant J., 2018, Mar 23. https://doi.org/10.1111/tpj.13910

  112. Gehring, M., Genomic imprinting: insights from plants, Annu. Rev. Genet., 2013, vol. 47, pp. 187—208. https://doi.org/10.1146/annurev-genet-110711-155527

    Article  CAS  PubMed  Google Scholar 

  113. Martinez, G., Panda, K., Köhler, C., and Slotkin, R.K., Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell, Nat. Plants, 2016, vol. 2, p. 16030. https://doi.org/10.1038/nplants.2016.30

    Article  CAS  PubMed  Google Scholar 

  114. Borges, F., Parent, J.S., van Ex, F., et al., Transposon-derived small RNAs triggered by miR845 mediate genome dosage response in Arabidopsis, Nat. Genet., 2018, vol. 50, pp. 186—192. https://doi.org/10.1038/s41588-017-0032-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Yoo, M.J., Liu, X., Pires, J.C., et al., Nonadditive gene expression in polyploids, Annu. Rev. Genet., 2014, vol. 48, pp. 485—517. https://doi.org/10.1146/annurev-genet-120213-092159

    Article  CAS  PubMed  Google Scholar 

  116. Navashin, M., Chromosome alterations caused by hybridisation and their bearing upon certain general genetic problems, Cytologia, 1934, vol. 5, pp. 169—203.

    Article  Google Scholar 

  117. Pikaard, C.S., Genomic change and gene silencing in polyploids, Trends Genet., 2001, vol. 17, pp. 675—677.

    Article  CAS  PubMed  Google Scholar 

  118. Rodionov, A.V., Gnutikov, A.A., Kotsinyan, A.R., et al., ITS1-5.8S rDNA-ITS2 sequence in 35S rRNA genes as a marker for reconstruction of phylogeny of grasses (Poaceae family), Biol. Bull. Rev., 2017, vol. 7, no. 2, pp. 85—102. https://doi.org/https://doi.org/10.1134/S2079086417020062.

    Article  Google Scholar 

  119. Wang, J., Tian, L., Lee, H.S., et al., Genome wide nonadditive gene regulation in Arabidopsis allotetraploids, Genetics, 2006, vol. 172, pp. 507—517. https://doi.org/10.1534/genetics.105.047894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Bottani, S., Zabet, N.R., Wendel, J.F., and Veitia, R.A., Gene expression dominance in allopolyploids: hypotheses and models, Trends Plant Sci., 2018, Feb. 9, p. S1360-1385(18)30014-1. https://doi.org/10.1016/j.tplants.2018.01.002

  121. Hollister, J.D. and Gaut, B.S., Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression, Genome Res., 2009, vol. 19, pp. 1419—1428. https://doi.org/10.1101/gr.091678.109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Zhang, C., Yang, H., and Yang, H., Evolutionary character of alternative splicing in plants, Bioinf. Biol. Insights, 2015, vol. 9, suppl. 1, pp. 47—52. https://doi.org/10.4137/BBI.S33716

    Article  Google Scholar 

  123. Zhou, R., Moshgabadi, N., and Adams, K.L., Extensive changes to alternative splicing patterns following allopolyploidy in natural and resynthesized polyploids, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, pp. 16122—16127. https://doi.org/10.1073/pnas.1109551108

    Article  PubMed  PubMed Central  Google Scholar 

  124. Soltis, D.E., Misra, B.B., Shan, S., et al., Polyploidy and the proteome, Biochim. Biophys. Acta, 2016, vol. 1864, pp. 896—890. https://doi.org/10.1016/j.bbapap.2016.03.010

    Article  CAS  PubMed  Google Scholar 

  125. Hu, G., Houston, N.L., Pathak, D., et al., Genomically biased accumulation of seed storage proteins in allopolyploid cotton, Genetics, 2011, vol. 189, pp. 1103—1115. https://doi.org/10.1534/genetics.111.132407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Islam, N., Tsujimoto, H., and Hirano, H., Proteome analysis of diploid, tetraploid and hexaploid wheat: towards understanding genome interaction in protein expression, Proteomics, 2003, vol. 3, pp. 549—557.

    Article  CAS  PubMed  Google Scholar 

  127. Koh, J., Chen, S., Zhu, N., et al., Comparative proteomics of the recently and recurrently formed natural allopolyploid Tragopogon mirus (Asteraceae) and its parents, New Phytol., 2012, vol. 196, pp. 292—305. https://doi.org/10.1111/j.1469-8137.2012.04251.x

    Article  CAS  PubMed  Google Scholar 

  128. Ng, D.W., Zhang, C., Miller, M., et al., Proteomic divergence in Arabidopsis autopolyploids and allopolyploids and their progenitors, Heredity, 2012, vol. 108, pp. 419—430. https://doi.org/10.1038/hdy.2011.92

    Article  CAS  PubMed  Google Scholar 

  129. Onda, Y., Hashimoto, K., Yoshida, T., et al., Determination of growth stages and metabolic profiles in Brachypodium distachyon for comparison of developmental context with Triticeae crops, Proc. Biol. Sci., 2015, vol. 282(1811). pii: 20150964. https://doi.org/10.1098/rspb.2015.0964

  130. Pasquet, J.-C., Chaouch, S., Macadre, C., et al., Differential gene expression and metabolomic analyses of Brachypodium distachyon infected by deoxynivalenol producing and non-producing strains of Fusarium graminearum, BMC Genomics, 2014, vol. 15, p. 629. https://doi.org/10.1186/1471-2164-15-629

    Article  PubMed  PubMed Central  Google Scholar 

  131. Rai, A., Saito, K., and Yamazaki, M., Integrated omics analysis of specialized metabolism in medicinal plants, Plant J., 2017, vol. 90, pp. 764—787. https://doi.org/10.1111/tpj.13485

    Article  CAS  PubMed  Google Scholar 

  132. Banyai, W., Sangthong, R., Karaket, N., et al., Overproduction of artemisinin in tetraploid Artemisia annua L., Plant Biotechnol., 2010, vol. 27, pp. 427—433. https://doi.org/10.5511/plantbiotechnology.10.0726a

    Article  Google Scholar 

  133. Banjanac, T., Dragićević, M., Šiler, B., et al., Chemodiversity of two closely related tetraploid Centaurium species and their hexaploid hybrid: metabolomic search for high-resolution taxonomic classifiers, Phytochemistry, 2017, vol. 140, pp. 27—44. https://doi.org/10.1016/j.phytochem.2017.04.005

    Article  CAS  PubMed  Google Scholar 

  134. López-Álvarez, D., Zubair, H., Beckmann, M., et al., Diversity and association of phenotypic and metabolomic traits in the close model grasses Brachypodium distachyon, B. stacei and B. hybridum, Ann. Bot., 2016, vol. 119, pp. 545—561. https://doi.org/10.1093/aob/mcw239

    Article  PubMed Central  Google Scholar 

  135. Xing, S.H., Guo, X.B., Wang, Q., et al., Induction and flow cytometry identification of tetraploids from seed-derived explants through colchicine treatments in Catharanthus roseus (L.) G. Don., J. Biomed. Biotechnol., 2011:793198. https://doi.org/10.1155/2011/793198

  136. Mishra, B.K., Pathak, S., Sharma, A., et al., Modulated gene expression in newly synthesized autotetraploid of Papaver somniferum L., S. Afr. J. Bot., 2010, vol. 76, pp. 447—452. https://doi.org/10.1016/j.sajb.2010.02.090.

    Article  CAS  Google Scholar 

  137. Rodionov, A.V., Nosov, N.N., Kim, E.S., et al., The origin of polyploid genomes of bluegrasses Poa L. and gene flow between northern pacific and sub-Antarctic islands, Russ. J. Genet., 2010, vol. 46, no. 12, pp. 1407—1416.

    Article  CAS  Google Scholar 

  138. Rodionov, A.V., Interspecific hybridization and polyploidy in the evolution of plants, Vavilovskii Zh. Genet. Sel., 2013, vol. 17, no. 4 (2), pp. 916—929.

  139. The International Brachypodium Initiative, Genome sequencing and analysis of the model grass Brachypodium distachyon, Nature, 2010, vol. 463, pp. 763—768. https://doi.org/10.1038/nature08747

  140. Salse, J., Deciphering the evolutionary interplay between subgenomes following polyploidy: a paleogenomics approach in grasses, Am. J. Bot., 2016, vol. 103, pp. 1167—1174. https://doi.org/10.3732/ajb.1500459

    Article  PubMed  Google Scholar 

  141. Kim E.S., Bolsheva N.L., Samatadze T.E. et al. The unique genome of two-chromosome grasses Zingeria and Colpodium, its origin, and evolution, Russ. J. Genet., 2009, vol. 45, no. 11, pp. 1329—1337.

    Article  CAS  Google Scholar 

  142. Dodsworth, S., Chase, M.W., and Leitch, A.R., Is post-polyploidization diploidization the key to the evolutionary success of angiosperms?, J. Linn. Soc. London, Bot., 2016, vol. 180, no. 1, pp. 1—5. https://doi.org/10.1111/boj.12357

    Article  Google Scholar 

  143. Ellstrand, N.C. and Schierenbeck, K.A., Hybridization as a stimulus for the evolution of invasiveness in plants?, Proc. Natl. Acad. Sci. U.S.A., 2000, vol. 97, pp. 7043—7050.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Hughes, C.E., Govindarajulu, R., Robertson, A., et al., Serendipitous backyard hybridization and the origin of crops, Proc. Natl. Acad. Sci. U.S.A., 2007, vol. 104, pp. 14389—14394.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Vavilov, N.I., Pyat’ kontinentov (Five Continents), Leningrad: Nauka, 1987.

  146. Lyubarskii, G.Yu., Rozhdenie nauki: analiticheskaya morfologiya, klassifikatsionnaya sistema, nauchnyi metod (The Birth of Science: Analytical Morphology, Classification System, Scientific Method), Moscow: Yazyki Slavyanskoi Kul’tury, 2015.

  147. Maunder, M., Hughes, C., Hawkins, J.A., and Culham, A., Hybridization in ex situ plant collections: conservation concerns, liabilities, and opportunities, in Ex situ Plant Conservation: Supporting Species Survival in the Wild, Guerrant E.O.J., Havens K., and Maunder, M., Eds., Washington: Island Press, 2004, pp. 19—438.

    Google Scholar 

  148. Hammer, K., Das Domestikationssyndrom, in Kulturpflanze, 1984, vol. 32, pp. 11—34.

    Article  Google Scholar 

  149. Negi, P., Rai, A.N., and Suprasanna, P., Moving through the stressed genome: emerging regulatory roles for transposons in plant stress response, Front. Plant Sci., 2016, vol. 7, p. 1448. https://doi.org/10.3389/fpls.2016.01448

    Article  PubMed  PubMed Central  Google Scholar 

  150. Oliver, K.R., McComb, J.A., and Greene, W.K., Transposable elements: powerful contributors to angiosperm evolution and diversity, Genome Biol. Evol., 2013, vol. 5, pp. 1886—1901. https://doi.org/10.1093/gbe/evt141

    Article  PubMed  PubMed Central  Google Scholar 

  151. Meyer, R.S. and Purugganan, M.D., Evolution of crop species: genetics of domestication and diversification, Nat. Rev. Genet., 2013, vol. 14, pp. 840—852. https://doi.org/10.1038/nrg3605

    Article  CAS  PubMed  Google Scholar 

  152. Studer, A., Zhao, Q., Ross-Ibarra, J., and Doebley, J., Identification of a functional transposon insertion in the maize domestication gene tb1, Nat. Genet., 2011, vol. 43, pp. 1160—1163. https://doi.org/10.1038/ng.942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Yao, J.-L., Xu, J., Cornille, A., et al., A microRNA allele that emerged prior to apple domestication may underlie fruit size evolution, Plant J., 2015, vol. 84, pp. 417—427. https://doi.org/10.1111/tpj.13021

    Article  CAS  PubMed  Google Scholar 

  154. Yao, J.-L., Dong, Y., and Morris, B.A., Parthenocarpic apple fruit production conferred by transposonin sertion mutations in a MADS-box transcription factor, Proc. Natl. Acad. Sci. U.S.A., 2001, vol. 98, pp. 1306—1311. https://doi.org/10.1073/pnas.983.1306

  155. Xiao, H., Jiang, N., Schaffner, E., et al., A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit, Science, 2008, vol. 319, pp. 1527—1530. https://doi.org/10.1126/science.1153040

    Article  CAS  PubMed  Google Scholar 

  156. Kobayashi, S., Goto-Yamamoto, N., and Hirochika, H., Retrotransposon-induced mutations in grape skin color, Science, 2004, vol. 304, p. 982.

    Article  PubMed  Google Scholar 

  157. Walker, A.R., Lee, E., Bogs, J., et al., White grapes arose through the mutation of two similar and adjacent regulatory genes, Plant J., 2007, vol. 49, pp. 772—785.

    Article  CAS  PubMed  Google Scholar 

  158. Kobayashi, S., Goto-Yamamoto, N., and Hirochika, H., Association of VvmybA1 gene expression with anthocyanin production in grape (Vitis vinifera) skin-color mutants, J. Jpn. Soc. Hort. Sci., 2005, vol. 74, pp. 196—203.

    Article  CAS  Google Scholar 

  159. Chiu, L.W., Zhou, X., Burke, S., et al., The purple cauliflower arises from activation of a MYB transcription factor, Plant Physiol., 2010, vol. 154, pp. 1470—1480. https://doi.org/10.1104/pp.110.164160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Salman-Minkov, A., Sabath, N., and Mayrose, I., Whole-genome duplication as a key factor in crop domestication, Nat. Plant., 2016, vol. 2, no. 8, p. 16115. https://doi.org/10.1038/nplants.2016.115

    Article  CAS  Google Scholar 

  161. Köhler, C., Scheid, O.M., and Erilova, A., The impact of the triploid block on the origin and evolution of polyploid plants, Trends Genet., 2010, vol. 26, pp. 142—148. https://doi.org/10.1016/j.tig.2009.12.006

    Article  CAS  PubMed  Google Scholar 

  162. Jenczewski, E., Chevre, A.M., and Alix, K., Chromosomal and gene expression in Brassica allopolyploids, Polyploids and Hybrid Genomics, Chen, Z.J. and Bichler, J.A., Eds., Ames: Wiley—Blackwell, 2013, pp. 171—186.

    Google Scholar 

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ACKNOWLEDGMENTS

We thank I.N. Golubovskaya for valuable comments provided in reading the first version of the paper. Some of the studies described in the paper were carried out using the equipment of the Cellular and Molecular Technologies for Studying Plants and Fungi Center for Collective Use of the Komarov Botanical Institute, Russian Academy of Sciences, St. Petersburg.

This study was supported by the Russian Foundation for Basic Research (grant nos. 17-00-00340 KOMFI (17-00-00336, 17-00-00337, 17-00-00340), 18-04-01040, 18-34-00257).

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Authors and Affiliations

  1. Komarov Botanical Institute, Russian Academy of Sciences, 197376, St. Petersburg, Russia

    A. V. Rodionov, P. M. Zhurbenko, Yu. V. Mikhailova, E. O. Punina & V. S. Shneyer

  2. Department of Cytology and Histology, St. Petersburg State University, 199034, St. Petersburg, Russia

    A. V. Rodionov, Yu. V. Mikhailova & I. G. Loskutov

  3. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991, Moscow, Russia

    A. V. Amosova & O. V. Muravenko

  4. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, 152742, Borok, Yaroslavl oblast, Russia

    E. A. Belyakov

  5. Vavilov All-Russian Institute of Plant Genetic Resources, 190000, St. Petersburg, Russia

    I. G. Loskutov

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Rodionov, A.V., Amosova, A.V., Belyakov, E.A. et al. Genetic Consequences of Interspecific Hybridization, Its Role in Speciation and Phenotypic Diversity of Plants. Russ J Genet 55, 278–294 (2019). https://doi.org/10.1134/S1022795419030141

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