ISSN 1022-7954, Russian Journal of Genetics, 2019, Vol. 55, No. 3, pp. 278–294. © Pleiades Publishing, Inc., 2019.

Russian Text © A.V. Rodionov, A.V. Amosova, E.A. Belyakov, P.M. Zhurbenko, Yu.V. Mikhailova, E.O. Punina, V.S. Shneyer, I.G. Loskutov, O.V. Muravenko, 2019, published
in Genetika, 2019, Vol. 55, No. 3, pp. 255–272.

REVIEWS
AND THEORETICAL ARTICLES

Genetic Consequences of Interspecific Hybridization,

Its Role in Speciation and Phenotypic Diversity of Plants
A. V. Rodionova, b, *, A. V. Amosovac, E. A. Belyakovd, P. M. Zhurbenkoa, Yu. V. Mikhailovaa, b,
E. O. Puninaa, V. S. Shneyera, I. G. Loskutovb, e, and O. V. Muravenkoc
aKomarov
Botanical Institute, Russian Academy of Sciences, St. Petersburg, 197376 Russia
b
Department of Cytology and Histology, St. Petersburg State University, St. Petersburg, 199034 Russia
c
Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, 119991 Russia
d
Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Yaroslavl oblast, 152742 Russia
e
Vavilov All-Russian Institute of Plant Genetic Resources, St. Petersburg, 190000 Russia
*e-mail: avrodionov@mail.ru
Received April 16, 2018; revised September 3, 2018; accepted September 17, 2018

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 cul-
tivated crops and garden plants. The combination of two or more genomes of different origin in the first-gener-
ation 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 mech-
anisms 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 agri-
cultural crops and garden plant varieties, as well as of many invasive alien species and the components of adven-
tive flora, was marked by interspecific crossings purposefully carried out by breeders during the creation of mod-
ern 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-hybrid-
ization genomic shock, the creative role of which we would like to emphasize.

Keywords: evolution, interspecific hybridization, cryptic aneuploidy, genome and karyotype evolution, trans-
posons, transcriptome, proteome, metabolome
DOI: 10.1134/S1022795419030141

INTRODUCTION
For the first time, the possibility of the appearance
of new morphological forms of plants as a result of
interspecific hybridization, moreover, plants that not
only combine the traits of parental species but also
possess “several other good properties that distinguish
it from all other species,” was demonstrated almost
250 years ago. Interspecific tobacco hybrids were pur-
posefully obtained and investigated by Joseph Kölreu-
ter, associate professor of the Botanical Garden of the
Imperial Academy of Sciences at St. Petersburg. He
wrote: “Each century has its own new discoveries, and
there is no country in the world that, having science
and art in a flourishing state and a genius, not
oppressed by coercion and shortcomings, could not
manifest them. The discoveries of the modern century
are bastard plants, the establishment of the genuine
structure of pollen, …, the existence of plant pollina-
tion only by insects, etc., and the most surprising among
them, perhaps even more unexpected, is the complete
transformation of one natural plant species into another,
which I rightfully dare to ascribe to myself (italics is
ours). And if the academic world creates pleasure or
benefit for the people over time, this should be
attributed to the Russian Academy of Sciences, in the
service of which I had the honor to do this study”
(quoted from the translation of Kölreuter’s article into
the modern language, published in 19401 [1]).
1 For the first time (in translation from German into Russian lan-
guage 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 Pro-
motion of Agriculture and House Building in Russia, 1772. Part
XX. In St. Petersburg at the Gentry Sea Cadet Corps. Pages 1–23.

278
 GENETIC CONSEQUENCES OF INTERSPECIFIC HYBRIDIZATION
Later, the problem of interspecific hybridization
and its role in morphogenesis/speciation and progres-
sive evolution in plants was repeatedly discussed. This
discussion went through several key steps:
(1) Investigation of interspecific and interlineage
hybridization phenomenon in plants by G. Mendel,
G. de Vries, K.E. Correns, and W. Bateson showed
that hybridization was the path to reveal the hereditar-
ily determined plant diversity, which, in fact, led to the
emergence of genetics. At the Third International
Conference on Hybridization and Plant Breeding,
London, July 1906, W. Bateson, president of the con-
ference, in his address to the participants, entitled
“The Progress of Genetic Research,” declared that
research on plant hybridization had already led to the
emergence of a new research area, the subject of which
was the study of the heredity and variability; a new sci-
ence had appeared, which had no short and clear
name. Batson suggested calling it “Genetics” (from
the adjective genetic, “referring to the basics of being”
[2], which in turn is from Genesis, the title of the First
Book of Moses). Bateson’s report was so vivid and
convincing that W. Wilks, preparing the proceedings
of the conference for publication, gave it the title
“Report of the Third International Conference 1906
on Genetics: Hybridization (the Cross-Breeding of
Genera or Species), the Cross-Breeding of Varieties,
and General Plant-Breeding.” It should be noted that
the true name of the conference was the Third Confer-
ence on Hybridization and Plant Breeding.
(2) Lotsy’s formulation of the principle that evolu-
tion was possible only by means hybridization; only in
this way could a new combination of traits arise [3].
Evolution by means of hybridization is an impressive
and catchy formulation, but it is important to consider
that this is not about distant hybridization. Lotsy, in
the spirit of the time, understands species in a narrow
sense, like a jordanon; as we would say now, a pure
line, a group of morphologically similar plants which
do not demonstrate the segregation of traits upon
crossing. The main idea of Lotsy about the role of
hybridogenesis in the evolution of plants was
expanded and developed by M.G. Popov [4, 5] and
E. Anderson [6], who thought that hybridogenesis
played the main role in the genesis of the Eurasian
flora and in the appearance of angiosperms.
(3) Winge’s hypothesis [7] on the possibility of the
emergence of new species as a result of distant hybrid-
ization provided that polyploidization of the hybrid
karyotype occurs. Winge’s speculations were based on
observations by Rosenberg [8] and Federley [9].
Rosenberg studied the behavior of chromosomes in
meiosis in two sundew species, Drosera longifolia and
D. rotundifolia, and in their hybrid. The diploid karyo-
type of D. longifolia had 40 chromosomes, while the
karyotype of D. rotundifolia consisted of 20 chromo-
somes. In the first meiotic division, 20 bivalents were
formed in the first species, and in the second species,
RUSSIAN JOURNAL OF GENETICS Vol. 55 No. 3
279
10 bivalents were formed. In hybrids, chromosome
pairing in meiosis was disturbed, and hybrids were
almost sterile. Federley observed a similar phenome-
non in moth species of the genus Pygaera. The hybrids
between P. anachoreta, P. curtula, and P. pigra were
sterile, and their chromosome conjugation in meiosis
was disturbed. On the basis of these observations,
Winge [7] hypothesized that chromosome pairing in
meiosis I was the most important stage in the life of
sexually reproducing organisms. He suggested that,
during the somatic life, chromosomes accumulated
mutations, and some of the genetic material was lost.
However, during pairwise chromosome conjugation,
due to the interaction of homologs, mutations were
repaired according to a normal copy. This speculation,
on one hand, explained the fertility dysfunctions in the
case of inbreeding (the repair is impossible owing to
the fact that homologs carry the same defects) and dis-
tant crossings (the chromosomes are different and
cannot conjugate, and therefore, reparation does not
occur). From this, it was possible to conclude that, if
chromosomal doubling (polyploidization) occurs in a
distant hybrid, the conjugation of homologs in meiosis I
will be restored, and the possibility for mutation repair
will appear; therefore, the distant hybrid will become
fertile, leading to the emergence of a new species.
Winge’s hypothesis that polyploidization was the way
to overcome distant hybrid sterility was brilliantly con-
firmed in the studies of G.D. Karpechenko, who
obtained fertile intergeneric polyploid Raphanobras-
sica hybrid [10].
(4) A new stage in understanding the meaning and
place of interspecific hybridization in the progressive
evolution of plants is associated with the development
of whole-genome sequencing and molecular cytoge-
netics methods. It became clear that representatives of
all extant phylogenetic branches of flowering plants
passed through the stages of interspecific hybridiza-
tion and whole-genome duplication. The phenomena
of saltational speciation in terms of the G. de Vries
mutation theory [11, 12] and many unusual phenom-
ena caused by mutational and epigenetic modification
of genomes [12] are associated with these stages.
HOW OFTEN ARE HYBRIDOGENIC TAXA
FOUND IN NATURE?
The origin of a new species via distant hybridiza-
tion can be determined using the time-consuming but
effective method of genome analysis proposed by
Kihara [13] or using the methods of karyogenomics
(GISH and FISH) [14, 15], or by next-generation
sequencing techniques [16]. Within each of these
labor-intensive studies, it is possible to validate the
hybrid origin of only one, two, or several species.
Therefore, when answering the question, we will try to
rely on the opinion of experienced florists who estab-
lish the hybrid origin of a particular species according
to its morphological characters. A summary of this
2019
280 RODIONOV et al.
kind of data was made in [17]. In particular, among
37000 species from the flora of Europe, North Amer-
ica, and part of Australia belonging to 3212 genera
from 282 families of vascular plants, species of hybrid
origin were observed in 40% of families and 16% of
genera with an average frequency of 9 hybridogenic
species per 100 non-hybrid species. Most of the pre-
sumptive hybrids are interspecific hybrids within the
same genus; intergeneric hybrids are also not uncom-
mon, constituting 3.5%. Most often, botanists
observed hybrids in the families Poaceae, Asteraceae,
and Orchidaceae.
Speaking of hybrids, the homoploid hybrids, i.e.,
hybrids that retain the ploidy level characteristic of
parental species, and allopolyploid hybrids (amphidip-
loids) should be distinguished. In the case where
parental karyotypes of viable homoploid hybrid were
considerably different, in meiosis, such hybrids can
have problems with conjugation and segregation of
homologous chromosomes. These hybrids will pro-
duce gametes with unbalanced chromosome sets, but
they can also give rise to a long-existing clone, differ-
ing from the parents in morphology, having its own
range, and reproducing vegetatively or apomictically.
If the parental karyotypes of are almost the same, then
homoploid hybrids can be fertile and retain the ability
to backcross with parental species. An example can be
the peony endemic to Georgia, Paeonia × chamaeleon,
which is a species of hybrid origin producing germi-
nating seeds both in self-pollination and in crossings
with the parental species P. caucasica and P. mlokose-
witschii [18]. This type of hybridization is called intro-
gressive hybridization [6] because, as a rule, it is
accompanied by the inclusion of some of the genes of
one parental species in the genome of another, which
leads to the increase in genetic diversity and the
appearance of new features in parental species. In the
case where parental karyotypes are considerably dif-
ferent, F1 hybrids will be almost completely sterile, as
is observed, for example, in Elymus glaucus × E. mul-
tisetus hybrids. However, single gametes with balanced
chromosome sets, occasionally produced by such
hybrids, can participate in backcrosses. As a result,
more or less fertile introgressive hybrids with restored
fertility arise [19]. Those of them that will have a special
range and appearance (set of characters), different from
those of the parents, can be recognized by taxonomists as
a new species, subspecies, or form [20]. This type of spe-
ciation is called recombinational speciation [19].
Sometimes, introgressive hybridization zones
cover vast areas. For instance, in Eastern Europe and
Western Siberia, after the retreat of the glacier, the
ranges of the European spruce (Picea abies) and the
Siberian spruce (P. obovata), which were previously
separated by the glacier, approached each other and
partially overlapped. According to morphological and
nuclear DNA (allozymes, microsatellites) data, natu-
ral hybrids between these two species bias either
toward one or toward the other ancestor and are dis-
RUSSIAN JOURNAL OF GENETICS
tributed in a band extending from northwest to south-
east from Murmansk oblast to Perm oblast and Bash-
kiria [21, 22]. Hybrid races are called Finnish spruce
(P. fennica), which is considered a young, not fully
formed hybridogenic species [22]. The true distribu-
tion of P. abies × P. obovata hybrids is probably even
wider than that revealed by morphological analysis,
since mitochondrial DNA haplotypes characteristic of
Northern European populations are distributed among
phenotypically typical Siberian spruce to the left bank
of the Ob River [21].
HOW OFTEN ARE POLYPLOIDS
FOUND IN NATURE?
According to Winge and Karpechenko, promising
interspecific hybridization events should be accompa-
nied by polyploidization of the genome. Polyploids
can result, for example, from fusion of unreduced
gametes. Doubling of the number of chromosomes in
the gametes may be associated with the processes tak-
ing place at both premeotic and meiotic stages of the
formation of germ cells [23–25]. The frequency of the
gametes produced with doubled chromosome number
is under genetic control and can be changed by natural
selection [24, 25]. The first mutation affecting the fre-
quency of unreduced gametes, named dy (dyad), was
discovered by S. Horowitz in 1931 (see [26]) and was
studied in detail by Satina and Blakeslee [26]. Among
the accessions obtained from the irradiated pollen of
the Datura starmonium jimsonweed (2n = 24), there
were those in which normal chromosome segregation
in megasporogenesis and microsporogenesis took
place only in the first meiotic division, the second
division was absent, and the chromatids did not segre-
gate. The mutant megagametophyte had 8 nuclei,
each with 24 chromosomes. In microsporogenesis,
interkinesis, apparently, was replaced by true inter-
phase, since after one of the products of the first divi-
sion was eliminated, the second underwent three suc-
cessive mitotic divisions, and each microspore con-
tained 12 chromosome pairs [26].
Further studies have shown that the frequency of
unreduced gametes was first of all determined by the
genes and gene combinations whose products were
associated with the synthesis and activity of cyclin-
dependent kinases (CDKs) and cyclins (CYCs), as
well as by the genes responsible for the synthesis of
meiosis-specific cohesins, such as the afd1 (“absence
of first division1”) and rec8 genes [27], especially in
the combination of mutations for these genes with
gene mutations that blocked the appearance of double-
stranded breaks (e.g., spo 11-1, “sporulation 11-1”) and
led to the replacement of the second meiotic division
by the mitotic division (the osd1 gene, omission of sec-
ond division 1) [28, 29]. It seems likely that the emer-
gence of germ cells with nonreduced chromosome
number can be induced by some alleles of the ameiot-
ic1 (am1) gene, mutations of which disrupt the transi-
Vol. 55 No. 3 2019
 GENETIC CONSEQUENCES OF INTERSPECIFIC HYBRIDIZATION
tion from mitotic to meiotic cell division, affecting
such key stages of meiosis as the attachment of telo-
meres to the nuclear envelope, the formation of char-
acteristic chromosome arrangement in the meiotic
prophase (“bouquet”), homologous synapsis, and
assembly of meiosis-specific cohesin complexes on
bivalents [24, 25, 30]. For instance, homozygous loss
of the tam genes (synthesis of CYCA1 and CYCA2
proteins) leads to the appearance of 30% of unreduced
gametes; the loss of the osd1 genes results in that the
number of gametes with an unreduced chromosome
number reaches 85–100% [24, 29]. In the AtPS1
mutants of Arabidopsis (Arabidopsis thaliana PARAL-
LEL SPINDLES), improper spindle orientation in
meiosis II is observed, which results in the formation
of dyads with diploid chromosome sets instead of tet-
rads [31].
Calculations show that, in diploids, the frequency
of unreduced gametes is relatively high, constituting
about 0.6% [32]. In wild Brassicaceae, 96% of plants
belonging to different species produced unreduced
gametes. Usually, their frequency is less than 1%;
however, in approximately 7% of individuals, the pro-
portion of unreduced gametes was higher than 5%
[33]. For interspecific hybrids, this proportion
increases, on average, to 27.5% [32].
Let us try to evaluate, how often are polyploids
found in nature? Cariologists Müntzing [34] and Dar-
lington [35] thought that about half of flowering plants
were polyploids. Grant [36] considered all plants with
2n = 28 or more in the karyotype to be polyploids.
This calculation gave 47% of polyploids. Later, Gold-
blatt [37] proposed to consider all plants in the karyo-
types of which there were more than 18 chromosomes
as polyploids (about 70%). Obviously, these estimates
of the frequency of polyploids among plants were
based on assumptions that are difficult to validate.
Wood et al. proposed a rational criterion [38]. They
calculated the proportion of polyploid species only in
those genera where polyploid rows were observed and
the species with the smallest chromosome number
could be considered a diploid. This calculation
showed that 15% of flowering plant species were poly-
ploids. In ferns, the proportion of polyploids is higher
and reaches 31%. In angiosperm genera with low base
chromosome number (x = 2–7), the proportion of
polyploid species increased to 50%.
SPECULATIONS ON THE ROLE
OF POLYPLOIDS IN PROGRESSIVE
EVOLUTION OF PLANTS
The widespread occurrence of polyploids, espe-
cially among plants living in extreme conditions and at
the periphery of ranges, may mean that progressive
evolution of plants and the development of new eco-
logical niches are associated with polyploids [37–40].
This opinion is popular due to a number of circum-
stances. First of all, in accordance with the synthetic
RUSSIAN JOURNAL OF GENETICS Vol. 55 No. 3
281
theory of evolution, reproductive isolation is critical to
the divergence of genomes, and polyploids are often
reproductively isolated from parents [41]. In poly-
ploids of hybrid origin (allopolyploids), the allelic
diversity should theoretically be higher than that of
each of the parental forms, and therefore, there is
more material for natural selection [42]. Allopolyploid
hybrids are characterized by heterosis [43]. Finally, the
presence of several alleles of a single gene in the allo-
polyploid genome forms the conditions for the gene
divergence and acquisition of new functions, which is
essential in terms of progressive evolution [12, 44].
On the other hand, the large number of polyploids
in nature does not mean that they play a prominent
role in the evolution of plants. It is possible that there
are many of them because they easily arise during
interspecific hybridization, but do not give anything
fundamentally new, being terminal branches, so-
called evolutionary dead ends, on a phylogenetic tree
[45]. This opinion is supported by the characteristics
of synthetic allo- and autopolyploids obtained in the
experiment. In most cases, these polyploids are not
fundamentally different from their diploid ancestors
and do not have advantages over them [12]. The pres-
ence of several gene copies in one genome should lead
to the fact that mutations in the genomes of polyploids
will be “buffered” and not checked by selection.
Therefore, polyploids should have limited evolution-
ary potential. Autopolyploids seem to be especially
unpromising in terms of evolutionary success, since
they have serious problems with the correct chromo-
some segregation in meiosis I owing to the high num-
ber of multivalents [46].
WHOLE-GENOME DUPLICATIONS (WGD)
IN PLANT EVOLUTION ACCORDING
TO THE RESULTS
OF WHOLE-GENOME SEQUENCING
The results of genome sequencing of representa-
tives of all main branches of flowering plants provide
an answer to the question on the role of whole-genome
duplications in the progressive evolution of flowering
plants. All flowering plants were found to pass through
one or several rounds of the genome polyploidization
(whole-genome duplication) [47, 48]. The time of
occurrence of many recorded WGD events in different
phylogenetic branches of plants roughly corresponds
to the boundary between the Cretaceous and Paleo-
gene and the boundaries of other geological eras. It is
tempting to think that these were WGDs that gave the
plants more chances to survive in the changed envi-
ronment [48].
Schranz et al. [49] drew attention to an important
fact. They showed (and further calculations [50–52]
supported their conclusion) that the time of WGD
occurring in phylogenetic branches, as a rule, was sev-
eral tens of millions of years away from the stage of sal-
tational speciation (diversification).
2019
282 RODIONOV et al.
GENOMIC SHOCK STATE IN HYBRIDS
AND NEOPOLYPLOIDS:
GENOMIC AND EPIGENETIC VARIATIONS
Let us run through the genetic processes that
accompany cases of interspecific hybridization and
whole-genome duplication (polyploidization) of plant
genomes and the processes that precede and/or facili-
tate speciation in plants. First of all, it should be noted
that, in the interphase nuclei of hybrid plants, parental
genomes occupy different positions. This was demon-
strated for the experimentally obtained hybrid crops
Hordeum chilense × Secale africanum, Hordeum vul-
gare × Secale africanum, and Hordeum vulgare ×
H. bulbosum [53, 54]; for the allopolyploid genome of
Zingeria pisidica [55, 56]; and for the hybrids Brassica
carinata × Orychophragmus violaceus and Brassica
rapa × Isatis indigotica [57, 58]. When one of the
alloploid subgenomes is heterochromatized, its chro-
mosomes are mostly associated with lamina [59], but
in the interphase of Z. pisidica cereal, each of its 2-chro-
mosomal subgenomes occupies half of the nucleus, its
hemisphere, and no traces of heterochromatization of
one of the subgenomes are visible [55, 56]. Cellular
mechanisms of such division of subgenomic territories
are unknown.
The emergence of a hybrid karyotype is often
accompanied by problems with chromosome segrega-
tion in mitosis and meiosis, as well as gradual elimina-
tion of the chromosomes of one of the parents, to the
extent that the offspring would receive only the hap-
loid chromosome set [59, 60]. This phenomenon was
described first by Clausen and Mann [61], who stud-
ied the karyotypes of the Nicotiana tabacum × N. syl-
vestris hybrid, and later by Kasha and Kao [62], who
studied the Hordeum vulgare × H. bulbosum hybrids.
The loss of the chromosomes of one of the parents was
especially frequently observed in intergeneric hybrids,
such as Triticum × Agropyron [58–60], Triticum ×
Secale [63, 64], and Brassica × Orychophragmus [65].
More frequently, paternal chromosomes are lost.
Since the loss of chromosomes occurs gradually and a
specific chromosome can be lost in different somatic
cell divisions, in a hybrid plant, different cell clones
may have different sets of chromosomes; sometimes
the loss of chromosomes is tissue-specific. For
instance, in the Hordeum marinum × H. vulgare cv.
Tuleen 346 F1 hybrids, chromosomes of H. vulgare are
eliminated in the endosperm, while chromosomes of
H. marinum are gradually lost in embryonic tissues [66].
Aneuploids, even in highly polyploid plants, are
often inferior in viability to polyploids with balanced
karyotypes. The most important selection factor here
is the necessity to retain the correct gene dosage [67,
68], and an unbalanced loss of only one of the
homeologous chromosomes should lead to the dosage
alteration at many hundreds and thousands of genes
simultaneously. For example, in Triticum aestivum
wheat (2n = 42), there is on average about 4500 genes
RUSSIAN JOURNAL OF GENETICS
per chromosome [69]. One of the ways to maintain the
correct gene dosage is the phenomenon of compensa-
tion or cryptic aneuploidy, i.e., the replacement of a
lost chromosome/pair of chromosomes from a subge-
nome of one of the parents with an additional chro-
mosome/additional pair of homeologous chromo-
somes from another subgenome [24, 70, 71]. The
mechanism of this phenomenon is unknown. We
think that the “two minus = plus” model should work
here (Fig. 1). The main point of the hypothesis is that
the incorrect segregation of one of the homologous
chromosome pairs in meiosis I or sister chromatid
nondisjunction of one of the chromosomes in meiosis II
can be compensated by an incorrect segregation of
homeologous chromosomes or chromatids in the
same meiosis. Then, probably stabilizing selection
comes into play at the stage of micro- or macrospores;
i.e., gametes with unbalanced chromosome sets may
be less successful in fertilization than cryptic aneu-
ploid gametes.
In our opinion, this model is supported by a well-
known but hardly trivial fact. Meiosis in plants often
occurs with various kinds of aberrations. The low chi-
asma frequency and premature segregation or, on the
contrary, sister chromatid nondisjunction in meiosis II
leads to disruption of regular segregation, to polyso-
mies and aneuploidies, and to the fact that some chro-
mosomes or chromatids get into the micronuclei and
are eliminated. This irregular chromosome behavior
during meiosis is also observed in inbred lines and,
most often, in hybrids and allopolyploids (for a review
of many similar cases, see [72]). For example, the Poa
juncifolia (=P. ampla) bluegrass, common from Yukon
to California, reproduces apomictically in 90–95% of
cases and under apomictic reproduction has a rela-
tively stable karyotype with 2n = 63. However, 5–9%
of accessions of this species, sexual generation that
passed through meiosis, receive diverse and not very
balanced karyotypes with 2n = 56, 60–63, 66, 70, 82–
84, 90–93, 98–102, 126, 147 and are noticeably infe-
rior to apomictic generation in viability [73].
A natural consequence of the unstable chromo-
some segregation is that, even in diploid plants, for
example, in good Clematis species with 2n = 16, only
28–80% of the set seeds are fully developed in inter-
specific hybrids in different combinations, this pro-
portion is even lower, constituting 1–13% [74].
In hybrids, problems with chromosome segregation
in mitosis and meiosis are associated with the fact that
during species divergence in plants, both the centro-
meric DNA sequences and domains of the centro-
meric CENH3 and CENP-C proteins, interacting
with this DNA, change very quickly [60, 75, 76]. It is
suggested that rapid evolution of the centromeric
DNA and that of centromeric protein domains inter-
acting with the DNA are associated events. It seems
likely that the complementary combination of species-
specific centromeric DNA and species-specific cen-
Vol. 55 No. 3 2019
 GENETIC CONSEQUENCES OF INTERSPECIFIC HYBRIDIZATION
Diakinesis
Interkinesis (telophase I + prophase II)
Telophase II
Fig. 1. Improper chromosome and chromatid segregation
at anaphase I and anaphase II in allopolyploid can lead to
cryptic aneuploidy, as well as karyotype polyploidization
and haploidization. Top, tetraploid, 2n = 4, x = 1 at diak-
inesis. Homologs are paired with chiasmata. Center, inter-
kinesis, to the left, after proper segregation of the homo-
logs; to the right, one pair of homologs segregated improp-
erly. Bottom, chromosomal composition of cells at
telophase II. To the left, the two upper cells, cryptic aneu-
ploidy; the two bottom ones, proper chromosome set.
Right from top to bottom: cryptic aneuploidy in the
nucleus with doubled chromosome set; below, norm;
below, two cells with haploid chromosome sets.
tromeric proteins facilitates rapid chromosome segre-
gation in meiosis, with the result that the best quality
centromeres more likely enter the macrospore cells
and are transmitted to the offspring [75]. On the other
hand, kinetochores, in which centromeric DNA and
centromeric proteins are not very suitable for each
other, will not function well enough or kinetochores
will not be formed at all [60], as is the case with inter-
specific Hordeum vulgare × H. bulbosum hybrids [76]
or in hybrids derived from crossing of cereals that
diverged 50–60 million years ago, such as Triticum ×
Pennisetum [59] or Avena × Pennisetum [77].
Correct segregation of homologous chromosomes
in meiosis I requires pairing of homologous chromo-
somes in prophase; this pairwise arrangement will be
retained up to anaphase I. In the majority of cases,
homologs are attached to each other at chiasmata,
which in turn are retained until anaphase due to the
fact that sister chromatids of each homolog remain
connected to each other due to cohesins. When homo-
logs in anaphase I begin to segregate, the segregation
is possible only if the cohesion between sister chroma-
tids terminally from chiasmata is removed, which is
realized with the participation of separase. However, at
the centromeric region of each chromosome, the cohe-
sion between chromatids should be maintained until
anaphase II [78]. The latter is necessary for the forma-
RUSSIAN JOURNAL OF GENETICS Vol. 55 No. 3
283
tion of a bidirectional spindle and the correct chromatid
segregation in the second division of meiosis and is pro-
vided by a special protein, shugoshin [25, 79].
The issue is that, in polyploid genomes in meiosis,
not only homologs but also homeologs can form a syn-
apse, resulting in the formation of multivalents. Sev-
eral crossingovers that occurred in a multivalent, in
which exchanges took place between homologs and
homeologs, differing in inversions, can lead to the
appearance of acentric and polycentric chromosomes,
incapable of correct segregation. Consequently, mei-
otic products with unbalanced chromosome sets
appear. It was demonstrated that, in resynthesized
neopoliploids, the frequency of multivalents and
abnormal chromosome segregation, as well as the fre-
quency of aborted pollen, was noticeably higher than
that in stabilized eupolyploids [80–83]. One of the
ways of polyploid karyotype stabilization is to suppress
homeologous pairing. This activity is regulated by
many genes (pairing control genes, PCGs), of which
the dominant Ph1 (Pairing homoeologous 1) locus
from wheat is best studied [84]. This locus is a cluster
of genes encoding cyclin-dependent kinases homolo-
gous to the mammalian Cdk2 cluster, which affects
chromosome condensation, homologous conjugation,
and recombination [25, 85, 86]. In wheat, the Ph1
deletion leads to synapsis and recombination of
homeologous chromosomes. On the contrary, the
introduction of additional copies of this locus into the
genome reduces the frequency of homeologous pair-
ing, but sometimes, redundant copies can have the
opposite effect [86]. The high frequency of multiva-
lents and exchanges of regions between homeologous
chromosomes in meiosis I in allohexaploid Avena
sativa is explained by the loss of the Ph1 locus by the
Avena genome [87].
Ph1 is not the only locus affecting the homeolo-
gous pairing frequency in wheat; the Ph2 locus and
other loci mapped to chromosomes 5AL, 5DL, 5AS,
3DS, 3AS, 3AL, 3BL, and 3DL were identified, but
they are less well studied and their absence does not
compensate for the loss of the Ph1 locus [86, 88].
The frequency of gametes with unbalanced chro-
mosome sets can be reduced by increasing the inter-
ference. In this case, in one multivalent one crossin-
gover will occur [83]. A decrease in the recombination
frequency in polyploids in comparison with their dip-
loid ancestors is often observed [83, 85].
Not only karyotypes but also neopolyploid
genomes are extremely unstable. Neopolyploids and
“old” allopolyploids gradually lose part of the dupli-
cated genes. For example, the banana (Musa acumi-
nate) genome (2n = 22) 75–100 million years ago
passed through three rounds of allopolyploidization
and now consists of 36542 protein-coding genes. Most
of these genes (65.4%) occur as one single copy in the
genome, and only 10% of the genes retain all four cop-
ies of ancestral genomes [68]. The allopolyploid
2019
284 RODIONOV et al.
genome of wheat (T. aestivum) lost 10000–16000
genes that were previously present in the genomes of
its diploid ancestors [69]. Comparison of allopoly-
ploid genomes of monocots, Rosidae, and Asteridae
showed that, in all phylogenetic branches of plants,
the routes to local genome diploidization were the
same. In other words, genes involved in the regulation
processes (“response to stimulus”) tend to persist in a
large number of copies, and genes whose products
participate in metabolic and catalytic processes
quickly lose paralogs and are diploidized [68, 69, 89,
90]. Genes coding proteins which act as homodimers
(homopolymers) are diploidized first. Genes whose
products act as part of heteropolymers are more often
retained as paralogs [89, 90].
As allopolyploid persists, the genes transcribed by
RNA polymerase I and III, including 18S–5.8S–26S
rRNA and 5S rRNA genes [15, 16, 55, 70, 71, 91–94]
and probably snoRNA genes, are also diploidized [91].
Zingeria pisidica, an allopolyploid resulting from the
hybridization of Z. biebersteiniana and Colpodium sp.,
lost the 35S rRNA genes of Z. biebersteiniana, and
only small number of 5S rRNA genes of this species
remained [55]. For all polyploid Avena species, both
hexaploids and tetraploids with the genomic constitu-
tion ABC and AC, only 1.4–2% of the C subgenome
genes were retained, all of which carry multiple muta-
tions, both substitutions and deletions, and appar-
ently, they no longer are active in the allopolyploid
genome [92, 93]. In the genome of the allotetraploid
species Iris versicolor, all 18–26S rRNA genes origi-
nated from I. virginica; the loci of the second ancestor,
I. setosa, were not detected. At the same time, the allo-
polyploid retained both 5S rRNA loci of I. virginica,
but only one of the two 5S rRNA loci of I. setosa [94].
Note that the rapid loss of rRNA genes of one of
the allopolyploid genome ancestors does not always
occur. It is absent or it goes slowly, for example, in
allopolyploid peonies [95, 96].
The mechanisms of gene loss by polyploids are
clear only in very general terms [97]. It can be sug-
gested that gene losses occur owing to meiotic recom-
bination at the direct repeats in the gene flanking
regions. It is possible that gene excision takes place
with active participation of DNA transposons that
possess the necessary tools for such activity [98].
Unequal crossingover can be considered as the gene
loss mechanism only in combination with the hypoth-
esis that the product of an unequal crossingover, a
chromosome that has lost a gene, has better chances to
participate in fertilization than its homolog, which
increased in size after an unequal exchange.
The proposal that the polyploid genome “deparal-
ogization” occurs due to the mechanisms similar to
those in the nematode genome, where the somatic cell
differentiation is accompanied by regular excision of
1000 to 2000 protein-coding genes [99], seems more
attractive. It could be a CRISP-like system [100],
RUSSIAN JOURNAL OF GENETICS
based on noncoding RNAs such as miRNA, siRNA,
or piRNA, a system aimed at marking and excision of
inactive copies of protein-coding genes and, in some
cases, at excision of transposons. A low transcription
level of one of the paralogs and its complete or partial
heterochromatinization would be signs that served as
signals for the paralog excision by the CRISP-like sys-
tem. It was earlier demonstrated that the allopolyploid
genome most often lost the genes of the subgenome
that was less actively transcribed [94, 101, 102].
In addition to excision, during step-by-step poly-
ploid genome diploidization, genes can initially be lost
in the functional sense, first terminating transcription
owing to epigenetic changes or mutations [97] and
only then being excised and removed.
In some cases, in the genomes of first-generation
hybrids, transposon expansion is observed, which in
Nicotiana and Helianthus hybrids seems to be accom-
panied by mutations in protein-coding genes and
transpositions [103, 104]. However, this is not always
the case. For instance, in the resynthesized T. aestivum
[105] and Brassica napus [106] and in the neopoly-
ploid Spartina anglica [107], transposon expansion
was absent. In other cases, only some transposons
were activated in the hybrid, for example, the gypsy
transposon in Aegilops, while transposons of other
families remain immobilized [108].
In stabilized genomes, there are defense mecha-
nisms against transposon expansion. In somatic cells,
inactivation of their own “domesticated” transposons
takes place by methylation of transposon DNA and
suppression of its transcription with the participation
of ARGONAUTE4 protein and RNA polymerase V,
as well as 24-nucleotide siRNA molecules transcribed
from transposons, a process called RNA-directed
DNA methylation (RdDM) [109, 110]. siRNA from
the somatic cells of mother plant then enters the
embryo and the endosperm, ensuring their normal
development [111]. The mechanism of H3K27
trimethylation by means of POLYCOMB REPRES-
SIVE COMPLEX 2 (PRC2) [112] is also involved in
the transposon inactivation. The paternal plant is also
involved in the transposon inactivation. In this case,
transcription of “domesticated” transposons is first
activated in the pollen vegetative cell nucleus, and
then their transcripts degrade to form 21-nucleotide
siRNA, which enters the sperm cell and then the
embryo and endosperm, inactivating transposons
there and ensuring normal development [110, 113,
114]. Apparently, the transposon expansion in hybrids
is associated with the problems of alien transposon
identification as a material that must be inactivated
and destroyed. In other words, before the RNA copy
of alien transposon is cleaved, it must be recognized
and targeted with special miRNAs, which is not always
possible.
The combination of two heterologous genomes in
one nucleus, as a rule, but not always, leads to nonad-
Vol. 55 No. 3 2019
 GENETIC CONSEQUENCES OF INTERSPECIFIC HYBRIDIZATION
ditive change in the transcription of the parental
genomes [115]. A classic example of suppressing the
gene transcription of one of the parents and retaining
the gene transcription of another ancestor is the phe-
nomenon of nucleolar dominance in hybrids discov-
ered by M.S. Navashin [116]. This phenomenon, as we
now know, is only sometimes associated with the
rRNA inactivation [117], while more often the loss of
rRNA of one of the parents occurs [55, 93, 118].
In allopolyploid hybrids of Arabidopsis, about 5%
of the genes (about 1300 genes) change the expression
level, and in most cases, this change is associated with
the repression of the genes of one of the parents. The
genes obtained by a hybrid from A. thaliana, a species
the morphological characters of which are suppressed
in a hybrid, are repressed more frequently [119]. The
reasons for nonadditive subgenome transcription in
allopolyploids are unclear. Most likely, it is a matter of
different affinity of subgenomes with cis- and trans-
factors that regulate transcription, activators, and
transcription silencers [120]. It is supposed that one of
the factors determining which genes will be tran-
scribed in the hybrid, and which will not, may be the
saturation of the subgenome by transposons. Trans-
posons are usually methylated, their transcription
and, to some extent, the transcription of neighboring
genes are suppressed. Perhaps, this is the reason for
unequal and nonadditive transcription of subgenomes
in polyploids [120, 121].
The transcriptome diversity in neopolyploid
increases in comparison with the parents due to alter-
native splicing [122, 123]. For instance, in the resyn-
thesized Brassica napus, in comparison with the
parental genes, splicing of 26–30% of genes changed
after hybridization and polyploidization [123].
Indeed, because of alternative splicing, two initially
identical genes can produce mature translatable RNA
with different exon combinations. At the extreme,
these can be two completely different mRNA mole-
cules, with a mutually exclusive set of exons. New pos-
sibilities for the emergence of genes with new func-
tions are created by the retention of some previously
untranslated introns in one of the transcript variants.
Finally, different functions may simply be associated
with different polyadenylation sites. Fixing two differ-
ent splicing patterns in duplicated gene copies in two
polyploid homeologs is a way to separate the functions
of these genes in the near future.
In interspecific hybrids, the transcriptome changes
do not necessarily correlate with proteome changes.
The study of the allopolyploid proteomes of Arabidop-
sis, Triticum, Gossypium, and Tragopogon showed that
proteomes were generally more stable than transcrip-
tomes; their characteristics mainly reflected the pro-
teomes of the parental species (review [124]). How-
ever, some interesting and, perhaps, important differ-
ences in the representation of individual proteins in
the hybrid proteomes were demonstrated. For
RUSSIAN JOURNAL OF GENETICS Vol. 55 No. 3
285
instance, the genome of cotton (Gossypium hyrsutum)
consists of the A and D subgenomes, but they are
expressed with different efficiency. In the allopoly-
ploid proteome, proteins of the D subgenome domi-
nate, while proteins of the A subgenome are repre-
sented to a lesser extent [125]. In some cases, the allo-
polyploid produces proteins that are absent from the
proteomes of its diploid ancestors [126, 127]. The
mechanisms of this phenomenon are probably associ-
ated with new variants of post-transcriptional protein
modifications in hybrids [127]. Combining in a single
cell of homeologous nonadditively transcribed
genomes or nonadditively translated transcriptomes
can create new regulatory networks on the basis of
hybridogenic proteomes that are adequate to the new
state of the organism and its environment [125, 128].
Comparison of the proteomes of allopolyploids and
autopolyploids gives the expected result; i.e., the pro-
teomes of autopolyploids are always less different from
the proteomes of their diploid ancestors [127, 128].
It is clear from general considerations that the
changes in the proteome and different representation
of subgenomes in the proteome of allopolyploids can
affect the metabolome of the hybridogenous species.
Research in this direction is important primarily
because the metabolome profiles of polyploids and of
their diploid ancestors can serve as indicators of the
resistance of natural races and cultivated plants to
biotic and abiotic stresses [129, 130], as well as a tool
in searching for producers of biologically active sub-
stances [131]. Indeed, it was demonstrated that, for
example, the allotetraploid plants of Artemisia annua
produced more terpenoids and saponins per unit
weight than the diploid representatives of the genus
[132]. Centaurinum pannonicum, the allopolyploid
hybrid of the two tetraploid species, C. erythraea and
C. littorale, has obvious nonadditive quantitative
changes in the metabolome profile in comparison
with the parental species [133]. Comparative analysis
of the metabolome profiles in the species complex of
Brachypodium distachyon, B. stacei, and B. hybridum,
where the first two species are diploid ancestors of the
third species, revealed a species-specific pattern of
metabolome profiles; in particular, the content of
citrulline, which plays an important role in nitrogen
transport and is an important biochemical indicator of
plant resistance to salinity and drought, was signifi-
cantly higher in the allopolyploid [134].
Autoploidy to a lesser extent can also affect the
metabolite profile of polyploid. For instance, tetara-
ploid autopolyploid Catharanthus roseus produces
more vinblastine than its diploid ancestors [135].
Mishra et al. [136] reported that autopolyploid plants
of opium poppy Papaver somniferum were character-
ized by considerably higher morphine content com-
pared to diploid plants.
2019
286 RODIONOV et al.

Genome polyploidization events in the family Brassicaceae (330 genera, 3700 species)
70–65 20 13–17 5–9 3–4 <0.1

Brassica oleracea
Time scale (MYR) B. napus
D Brassica rapa
B. juncea
E Brassica nigra
Arabidopsis thaliana
Genome
J
Cleome polyploidization
in the ancestor
Carica papaya of modern
Brassicaceae
Vitis vinifera

Fig. 2. Genome polyploidization events in Brassicaceae (according to Jenczewski et al. [162], modified).

STABILIZED EUPOLYPLOID Gradual diploidization of the eupolyploid genome

GENOME AND GRADUAL
KARYOTYPE DIPLOIDIZATION
The first step to the polyploid genome diploidiza-
tion is realized through the pairing control genes.
Generation after generation, suppression of homeolo-
gous pairing in meiosis along with gradual loss of part
of the genes and part of the chromosomes of one of the
neopolyploid subgenomes stabilizes the hybrid
genome. At this stage, the allopolyploid karyotype
looks like the karyotype of a typical polyploid, in
which homologous and homeologous chromosomes
can be more or less reliably identified. We call such
karyotypes eupolyploids [40, 137, 138].
Eupolyploids have different fates. Some of them
may participate in the following distant crosses,
accompanied by whole-genome duplication of the
second and following orders, as happened, for exam-
ple, during the formation of the T. aestivum genome
(2n = 42, x = 7) or occurred and occurs with the
genomes of the Brassica genus (Figs. 2, 3).
through translocations converts it into a karyotype,
which from the karyological (cytological) point of
view is indistinguishable from a diploid one, with
some relatively low basic chromosome number char-
acteristic of the genus. Paying attention to such karyo-
type, for example, to the karyotype of Avena longiglu-
mis, typical of cereals, with 2n = 14, x = 7 [87] or to
karyotypes of Zingeria biebersteiniana and Colpodium
versicolor with 2n = 4, x = 2 [55, 56, 141], it is difficult
to believe that the genomes of all these species passed
through 4–5 whole-genome duplication events. The
Black mustard
Brassica nigra
2n = 16
BB
Abyssinian
cabbage Brown mustard
Brassica carinata Brassica juncea

However, in eupolyploids, another fate is possible.

Over time, some eupolyploid chromosomes become 2n = 16 + 18 2n = 20 + 16
involved in chromosomal rearrangements. Gradually, BBCC AABB
or saltationally, due to translocations, deletions, or
inversions, the karyotype is rearranged, and the num-
ber of chromosomes is reduced. Moreover, in the
genome, hot spots of chromosomal rearrangements in
centromeric and subtelomeric regions, as well as the
regions where linkage groups (genomic blocks) are rel- 2n = 18 2n = 20 + 18 2n = 20
atively constant, can be distinguished. Translocations CC AACC AA
are not necessarily reciprocal. For instance, in poly-
ploid Avena species, the C-subgenome fragments are Brassica oleracea Brassica napus Brassica rapa
translocated to chromosomes of the A and D subge- Cabbage Rape Turnip
nomes, but not vice versa [87]. Often, the whole chro-
mosome arm is translocated, and whole chromosomes Fig. 3. Interspecific hybridization accompanied by poly-
are inserted into centromeric regions of other chromo- ploidization and the appearance of new species in the
somes [139, 140]. genus Brassica.

RUSSIAN JOURNAL OF GENETICS Vol. 55 No. 3 2019

 GENETIC CONSEQUENCES OF INTERSPECIFIC HYBRIDIZATION
polyploid nature of such karyotypes can be revealed
only in comparative genomic studies. Such genomes
and such karyotypes are called paleopolyploid.
Reaching the level of eupolyploid or paleopolyploid,
kinship groups again enter into hybridization and the
cycle repeats again: interspecific hybridization, fol-
lowed by genomic shock, gradual genome and karyo-
type stabilization, secondary diploidization, and
interspecific hybridization [12, 138].
It seems likely that the burst of variability in the
period of genomic shock is the stage at which new
genome and karyotype states may arise. The rear-
rangements that have taken place determine whether
the carriers of these particular genomes in the evolving
environmental conditions will experience the fate of
the evolutionary-stasis phylogenetic branch, or their
descendants will pass through active processes of
adaptive radiation and taxon formation. It can be sup-
posed, at least in some cases, that cytological second-
ary diploidization of the genome and karyotype is the
trigger of speciation [142], which with some probabil-
ity is associated with the achievement of a fundamen-
tally new state of the phenotype (a specific complex of
morphological and physiological traits characteristic,
for example, of families). In another case, chromo-
somal races, more or less high polyploids, will give rise
to new forms that deserve the status of new species,
subspecies, or varieties , but for tens of millions of
years retain phenotypes without obvious signs of evo-
lution, called progressive, with obedience carrying not
always the fair name of evolutionary dead ends [45].
GENOME ALLOPOLYPLOIDIZATION
AND PHENOTYPIC
AND GENETIC CULTIVAR DIVERSITY
In fields and arable lands, in gardens, and on dis-
turbed lands around the settlements of agricultural
workers, as a result of their livelihood, plants of differ-
ent species, previously geographically isolated from
each other, grew, which formed the conditions for
spontaneous and, in other cases, purposeful hybrid-
ization. Due to the above-described phenomena
accompanying the genomic shock state, episodes of
intraspecific and interspecific, more or less distant
hybridization provided extensive material for subse-
quent targeted or unintentional selection [143, 144].
The fields of pioneers of agriculture that were infested
with accompanying species formed the conditions for
the process of pre-domestication [144], the uninten-
tional selection in primary weeds for the traits and
properties (such as the loss of spike fragility in field
weed rye), which made them economically valuable
plants. Special attention to this issue was paid by
N.I. Vavilov [145].
The tendency to create botanical gardens, which
started in Europe in the 14th century and expanded in
the 16th century, first for practical purposes, like
apothecary gardens, and then for collection purposes,
RUSSIAN JOURNAL OF GENETICS Vol. 55 No. 3
287
as places where living curiosities from all over Europe
were combined with those from the newly discovered
lands of Southeast Asia, the New World, and Australia
[146], should be noted. This provided the background
for the emergence of new forms of distant hybrids.
Spontaneous plant hybridization in botanical gardens
is a relatively frequent phenomenon, which is one of
the urgent problems of the ex situ conservation of spe-
cies diversity [147].
Interspecific and intraspecific crosses, both in pur-
poseful attempts to create new varieties and in sponta-
neous hybridization of invasive species, were accom-
panied by genomic shock, i.e., unpredictable changes
in the genome, epigenome, transcriptome, proteome,
metabolome, and cultivar phenotype, and in compar-
ison with wild ancestors, carriers of individual ele-
ments of the complex of characters, which is com-
monly called the domestication syndrome [148], were
isolated. Among these characters, high fertility, mor-
phological polymorphism, adaptive plasticity, and
often, especially in garden crops, allometric growth in
comparison with wild ancestors can be distinguished.
As is shown above, one of the signs of the genomic
shock syndrome characteristic of the first-generation
hybrids is the expansion of transposons. Comparison
of cultivated plants and their wild relatives clearly
shows that the history of many cultivars included the
stage of transposon expansion [149, 150]. Insertions of
some of the transposons influenced the phenotype.
Analysis of mutations that led to crop domestication
[151] showed that of 60 analyzed genes associated with
the domestication syndrome, 35 carried single nucle-
otide substitutions in comparison with wild ancestors,
23 genes had indels, and in 9 genes the mutations were
caused by transposon insertions. Since at least part of
the indels could also have been the consequence of
transposon excision and insertion, in more than 15%
of cases, the signs of domestication were the conse-
quence of the transposon expansion. A striking exam-
ple of such a case is the insertion of the Hopscotch
transposon into the regulatory region of the teosinte
branched1 (tb1) gene, which occurred in the ancestors
of maize [152].
A MITE transposon insertion into the 3'-end of the
CrabApple Fruit Size (CAFS) gene of the apple
genome, the product of which is miRNA172p micro-
RNA, inhibits translation of the APETALA2 (AP2)
gene family, which results in the increase in the apple
size. The transposon insertion into the genome was
recorded in the Tien Shan Mountains, somewhere on
the border of modern Kazakhstan and China. An
increase in the fruit size made the apple tree an attrac-
tive agricultural crop that began to spread in Eurasia
4000–6000 years ago over the Great Silk Road [153].
In some cases, seedless cultivars have commercial
value. A dem1 LTR retrotransposon insertion into
fourth intron of the MdPI gene (encodes the MADS
box transcription factor) inactivates this gene, which is
2019
288 RODIONOV et al.
observed in the Rae Ime seedless apple cultivar. The
insertion of the same transposon into sixth intron of
the same gene was detected in the Spencer and Wel-
lington Bloomless seedless apple cultivars [154].
The Rider LTR transposon was inserted into the
sun locus of the Solanum lycopersicum chromosome 7,
which controls auxin transport, and brought with it
several genes of chromosome 10, which resulted in the
appearance of the tomato line with elongated fruits
[155].
Thousands of grape cultivars are divided into two
groups: the grapes are red and white. The berry color
is determined by the presence or absence of anthocy-
anin in the berry skin. It was demonstrated that all
studied white grape cultivars, but not red cultivars,
have a Gret1 (gypsy) LTR retrotransposon insertion
upstream of the ATG start codon (position –181) of
the VvMYBA1 gene, which blocks the transcription of
this gene [156, 157]. In the Flame Muscat (colored
form of the Muscat of Alexandria cultivar) and Ruby
Oruyama (colored form of the Italia cultivar) cultivars,
the unstable colored forms of the Muscat Brown and
Black Frontignac, grown in Languedoc, again lost the
transposon, of which only one LTR remained, which
resulted in partial coloration reversion [157, 158].
A similar event, but with the opposite result, occurred
in the genome of the Brassica oleracea var. botrytis
cauliflower. In this case, a Harbinger DNA trans-
poson insertion into the regulatory region of the
BoMyb2 gene results in the purple plant color [159].
Salman-Minkov et al. [160] showed that polyploids
were considerably more frequent among domesticated
plant species than among wild representatives of the
same taxa. Very many polyploids are found among the
tuber and root crops, among those crops that are
grown for fiber, and among cereals. It seems likely that
karyotype polyploidization in domesticated plants was
important and was supported by artificial selection for
several reasons, including larger sizes of polyploids in
comparison with their diploid ancestors, and also that
polyploid species are usually reproductively isolated
from diploid relatives [161].
Summarizing this section of the review, it should
be pointed out once again that many of the domestica-
tion syndrome characteristics of cultivated plants,
considerably distinguishing them from their wild pre-
decessors, probably appeared in the phenotype as the
direct or distant result of interspecific hybridization
and only later were picked up by conscious or uncon-
scious selection.
In conclusion, it should be noted that a complex of
diverse genetic and epigenetic events accompanying
interspecific hybridization may be the main cause of
noticeable morphological and genetic diversity of cul-
tivated plants. The selection of economically import-
ant species, at all stages of its development, is insepa-
rable from interline, intercultivar, and interspecific
hybridization. Such interspecific and intraspecific
RUSSIAN JOURNAL OF GENETICS
crossings should be accompanied by genomic shock,
i.e., unpredictable changes in the genome, epigenome,
transcriptome, proteome, metabolome, and pheno-
type of cultivars and adventive species in comparison
with their wild ancestors. From this complex of diverse
features, which are commonly called the domestica-
tion syndrome, the carriers of individual attractive ele-
ments were gradually selected.
ACKNOWLEDGMENTS
We thank I.N. Golubovskaya for valuable com-
ments 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 Founda-
tion for Basic Research (grant nos. 17-00-00340
KOMFI (17-00-00336, 17-00-00337, 17-00-00340),
18-04-01040, 18-34-00257).
COMPLIANCE WITH ETHICAL STANDARDS
The authors declare that they have no conflict of
interest. This article does not contain any studies
involving animals or human participants performed by
any of the authors.
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.
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.
3. Lotsy, J.P., Evolution by Means of Hybridization, The
Hague: Martinus Nijhoff, 1916.
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.
5. Popov, M.G., Osnovy florogenetiki (Basics of Floroge-
netics), Moscow: Akad. Nauk SSSR, 1963.
6. Anderson, E., Introgressive Hybridization, New York:
Hafner, 1969.
7. Winge, Ø., The chromosomes: their numbers and gen-
eral importance, C. R. Trav. Lab. Carlsberg, 1917,
vol. 13, pp. 131—275.
8. Rosenberg, O., Cytologische und morphologische
Studien an Drosera longifolia × rotundifolia Kungliga,
Sven. Vetensk.-Akad. Skr. Naturskyddsarenden Handl.,
1909, vol. 43, pp. 1—64.
Vol. 55 No. 3 2019
 GENETIC CONSEQUENCES OF INTERSPECIFIC HYBRIDIZATION
9. Federley, H., Das Verhalten der Chromosomen bei der
Spermatogenese der Schmetterlinge Pygaera anacho-
reta, curtula und pigra sowie einiger ihrer Bastarde, Z.
Indukt. Abstamm.- Vererbungsl., 1913, vol. 9, pp. 1—110.
10. Karpechenko, G.D., Hybrids of Raphanus sativus L. ×
Brassica oleracea L., J. Genet., 1924, vol. 14, pp. 375—
396.
11. De Vries, H., Species and Varieties, Their Origin by
Mutation, Chicago: The Open Court, 1905.
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. doi
10.3732/ajb.1500501
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.
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. doi 10.1186/s12862-017-1105-x
16. Oxelman, B., Brysting, A.K., Jones, G.R., et al., Phy-
logenetics of allopolyploids, Ann. Rev. Ecol. Evol. Syst.,
2017, vol. 48, pp. 543—557.
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.
18. Punina, E.O., Mordak, E.V., Timukhin, I.N., and Lit-
vinskaya, 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.
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. doi 10.3732/ajb.14002
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 bor-
der of its range in the European part of Russia, in Bio-
logicheskie resursy: izuchenie, ispol’zovanie, okhrana
(Biological Resources: Study, Use, Conservation),
Vologda: Vologda Gos. Univ., 2016, pp. 85—88.
22. Orlova, L.V. and Egorov, A.A., Systematics and geo-
graphical distribution of Finnish spruce (Picea fennica
(Regel) Kom., Pinaceae), Nov. Sist. Vysshikh Rast.,
2011, vol. 42, pp. 5—23.
23. Tamayo-Ordóñez, M.C., Espinosa-Barrera, L.A.,
Tamayo-Ordóñez, Y.J., et al., Advances and perspec-
tives in the generation of polyploid plant species,
Euphytica, 2016, vol. 209, pp. 1—22.
24. De Storme, N. and Mason, A., Plant speciation
through chromosome instability and ploidy change:
cellular mechanisms, molecular factors and evolution-
RUSSIAN JOURNAL OF GENETICS Vol. 55 No. 3
289
ary relevance, Curr. Plant Biol., 2014, vol. 1, pp. 10—
33. doi.org/10.1016/j.cpb.2014.09.002
25. Simanovskii, S.A. and Bogdanov, Yu.F., Genetic con-
trol of meiosis in plants, Russ. J. Genet., 2018, vol. 54,
no. 4, pp. 384—402.
26. Satina, S. and Blakeslee, A.F., Cytological effects of a
gene in Datura which causes dyad formation in sporo-
genesis, Bot. Gaz., 1935, vol. 96, pp. 521—532.
doi.org/10.1086/334498
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. doi 10.1242/jcs.03054
28. Chelysheva, L., Diallo, S., Vezon, D., et al., AtREC8
and AtSCC3 are essential to the monopolar orienta-
tion of the kinetochores during meiosis, J. Cell Sci.,
2005, vol. 118, pp. 4621—4632.
29. d’Erfurth, I., Cromer, L., Jolivet, S., et al., The
CYCLIN-A CYCA1;2/TAM is required for the meio-
sis I to meiosis II transition and cooperates with OSD1
for the prophase to first meiotic division transition,
PLoS Genet., 2010, vol. 6. e1000989
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 ini-
tiation of meiosis, Proc. Natl. Acad. Sci. U.S.A., 2009,
vol. 106, pp. 3603—3608. doi 10.1073/pnas.0810115106
31. Andreuzza, S. and Siddiqi, I., Spindle positioning,
meiotic nonreduction, and polyploidy in plants, PLoS
Genet., 2008, vol. 4. e1000272. doi 10.1371/jour-
nal.pgen.1000272
32. Ramsey, J. and Schemske, D.W., Neopolyploidy in
flowering plants, Annu. Rev. Ecol. Syst., 2002, vol. 33,
pp. 589—639.
33. Kreiner, J.M., Kron, P., and Husband, B.C., Fre-
quency and maintenance of unreduced gametes in nat-
ural plant populations: associations with reproductive
mode, life history and genome size, New Phytol., 2017,
vol. 214, pp. 879—889. doi 10.1111/nph.14423
34. Müntzing, A., The evolutionary significance of auto-
polyploidy, Hereditas, 1936, vol. 21, pp. 263—378.
35. Darlington, C.D., Recent Advances in Cytology, Phila-
delphia: Blakiston, 1937.
36. Grant, V., The Origins of Adaptations, New York:
Columbia Univ. Press, 1963.
37. Goldblatt, P., Polyploidy in angiosperms: monocoty-
ledons, in Polyploidy: Biological Relevance, Lewis,
W.H., Ed., New York: Plenum, 1980, pp. 219—239.
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. doi 10.1073/pnas.0811575106
39. Probatova, N.S., Annotated list of chromosome num-
bers in species of the Poaceae family from the Russian
Far East, in Komarovskie chteniya (Komarov Read-
ings), 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
2019
290 RODIONOV et al.
interpretation, Bot. Zh., 2018, vol. 103, no. 5, pp. 555—
585.
41. Segraves, K.A. and Anneberg, T.J., Species interac-
tions and plant polyploidy, Am. J. Bot., 2016, vol. 103,
pp. 1326—1335. doi 10.3732/ajb.1500529
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.
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. doi 10.1007/s13353-
014-0231-z
44. Flagel, L.E. and Wendel, J.F., Gene duplication and
evolutionary novelty in plants, New Phytol., 2009,
vol. 183, pp. 557—564. doi 10.1111/j.1469-
8137.2009.02923.x
45. Arrigo, N. and Barker, M.S., Rarely successful poly-
ploids and their legacy in plant genomes, Curr. Opin.
Plant Biol., 2012, vol. 15, pp. 140—146. doi
10.1016/j.pbi.2012.03.010
46. Kostoff, D., Studies on polyploid plants, J. Genet.,
1938, vol. 37, pp. 129—209.
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.
doi.org/10.1111/jse.12253
48. Van de Peer, Y., Mizrachi, E., and Marchal, K., The
evolutionary significance of polyploidy, Nat. Rev.
Genet., 2017, vol. 18, pp. 411—424. doi
10.1038/nrg.2017.26
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. doi
10.1016/j.pbi.2012.03.011
50. Tank, D.C., Eastman, J.M., Pennell, M.W., et al.,
Nested radiations and the pulse of angiosperm diversi-
fication: increased diversification rates often follow
whole genome duplications, New Phytol., 2015,
vol. 207, pp. 454—467. doi 10.1111/nph.13491
51. Clark, J.W. and Donoghue, P.C., Constraining the
timing of whole genome duplication in plant evolu-
tionary history, Proc. Biol. Sci., 2017, vol. 284,
p. 20170912. doi 10.1098/rspb.2017.0912
52. Clarkson, J.J., Dodsworth, S., and Chase, M.W.,
Time-calibrated phylogenetic trees establish a lag
between polyploidisation and diversification in Nicoti-
ana (Solanaceae), Plant Syst. Evol., 2017, vol. 303,
pp. 1001—1012. doi.org/10.1007/s00606-017-1416-9
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.
54. Schwarzacher, T., Heslop-Harrison, J.S., and Ana-
mthawat-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.
RUSSIAN JOURNAL OF GENETICS
55. Kotseruba, V., Gernand, D., Meister, A., and Hou-
ben, A., Uniparental loss of ribosomal DNA in the
allotetraploid grass Zingeria trichopoda (2n = 8),
Genome, 2003, vol. 46, pp. 156—163.
56. Rodionov, A.V., Kotseruba, V.V., Kim, E.S., et al.,
Grass genome and chromosome sets evolution, Tsi-
tologiya, 2013, vol. 55, no. 4, pp. 225—229.
57. Tu, Y., Sun, J., Liu, Y., et al., Production and charac-
terization 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. doi 10.1007/s00299-008-0513-1
58. Ding, L., Zhao, Z.G., Ge, X.H., and Li, Z.Y., Differ-
ent timing and spatial separation of parental chromo-
somes in intergeneric somatic hybrids between Bras-
sica napus and Orychophragmus violaceus, Genet. Mol.
Res., 2014, vol. 13, pp. 2611—2618. doi 10.4238/2014
59. Gernand, D., Rutten, T., Varshney, A., et al., Unipa-
rental chromosome elimination at mitosis and inter-
phase in wheat and pearl millet crosses involves micro-
nucleus formation, progressive heterochromatiniza-
tion, and DNA fragmentation, Plant Cell, 2005,
vol. 17, pp. 2431—2438.
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. doi
10.1016/j.molp.2017.12.009
61. Clausen, R.E. and Mann, M.C., Inheritance in Nico-
tiana tabacum: 5. The occurrence of haploid plants in
interspecific progenies, Proc. Natl. Acad. Sci. U.S.A.,
1924, vol. 10, pp. 121—124.
62. Kasha, K.J. and Kao, K.N., High frequency haploid
production in barley (Hordeum vulgare L.), Nature,
1970, vol. 225, pp. 874—876.
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.
65. Cheng, B.F., Séguin-Swartz, G., and Somers, D.J.,
Cytogenetic and molecular characterization of inter-
generic hybrids between Brassica napus and Orycho-
phragmus violaceus, Genome, 2002, vol. 45, pp. 110—
115.
66. Finch, R.A., Tissue-specific elimination of alternative
whole parental genomes in one barley hybrid, Chromo-
soma, 1983, vol. 88, pp. 386—393.
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.
doi 10.1038/hdy.2009.81
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. doi 10.1038/nature11241
Vol. 55 No. 3 2019
 GENETIC CONSEQUENCES OF INTERSPECIFIC HYBRIDIZATION
69. Brenchley, R., Spannagl, M., Pfeifer, M., et al., Anal-
ysis of the bread wheat genome using whole-genome
shotgun sequencing, Nature, 2012, vol. 491, pp. 705—
710. doi 10.1038/nature11650
70. Xiong, Z., Gaeta, R.T., and Pires, J.C., Homoeolo-
gous shuffling and chromosome compensation main-
tain genome balance in resynthesized allopolyploid
Brassica napus, Proc. Natl. Acad. Sci. U.S.A., 2011, vol.
108, pp. 7908—7913. doi 10.1073/pnas.1014138108
71. Lipman, M.J., Chester, M., Soltis, P.S., and Soltis, D.E.,
Natural hybrids between Tragopogon mirus and T. mis-
cellus (Asteraceae): a new perspective on karyotypic
changes following hybridization at the polyploid level,
Am. J. Bot., 2013, vol. 100, pp. 2016—2022. doi
10.3732/ajb.1300036
72. Pagliarini, M.S., Meiotic behavior of economically
important plant species: the relationship between fer-
tility and male sterility, Genet. Mol. Biol., 2000, vol. 23,
pp. 997—1002.
73. Clausen, J., Introgression facilitated by apomixis in
polyploid Poas, Euphitica, 1961, vol. 10, pp. 87—94.
74. Shevchenko, S.V. and Zubkova, N.V., Some aspects of
reproductive biology of Clematis L. (family Ranuncu-
laceae Juss.), Tr. Nikitsk. Bot. Sada, 2008, vol. 129,
pp. 6—21.
75. Talbert, P.B., Bryson, T.D., and Henikoff, S., Adap-
tive evolution of centromere proteins in plants and ani-
mals, J. Biol., 2004, vol. 3, p. 18.
76. Ishii, T., Karimi-Ashtiyani, R., and Houben, A., Hap-
loidization via chromosome elimination: means and
mechanisms, Annu. Rev. Plant Biol., 2016, vol. 67,
pp. 421—438. doi 10.1146/annurev-arplant-043014-
114714
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. doi
10.1073/pnas.1103190108
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. doi
10.1101/gad.255554.114
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.
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. doi
10.1073/pnas.1300153110
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. doi
10.1105/tpc.113.120626
RUSSIAN JOURNAL OF GENETICS Vol. 55 No. 3
291
82. Hollister, J.D., Polyploidy: adaptation to the genomic
environment, New Phytol., 2015, vol. 205, pp. 1034—
1039.
83. Lloyd, A. and Bomblies, K., Meiosis in autopolyploid
and allopolyploid Arabidopsis, Curr. Opin. Plant Biol.,
2016, vol. 30, pp. 116—122. doi
10.1016/j.pbi.2016.02.004
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.
85. Griffiths, S., Sharp, R., Foote, T.N., et al., Molecular
characterization of Ph1 as a major chromosome pair-
ing locus in polyploid wheat, Nature, 2006, vol. 439,
pp. 749—752.
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. doi 10.1016/j.ympev.2017.05.025
87. Nikoloudakis, N. and Katsiotis, A., Comparative
molecular and cytogenetic methods can clarify meiotic
incongruities in Avena allopolyploid hybrids, Caryolo-
gia, 2015, vol. 68, pp. 84—91.
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. doi 10.1111/j.1469-8137.2009.03084.x
89. Chen, E.C., Najar, C.F.B.A., Zheng, C., et al., The
dynamics of functional classes of plant genes in redip-
loidized ancient polyploids, BMC Bioinf., 2013, vol. 14,
suppl. 15, p. S19. doi 10.1186/1471-2105-14-S15-S19
90. Veitia, R.A., Gene duplicates: agents of robustness or
fragility?, Trends Genet., 2017, vol. 33, pp. 377—379.
doi 10.1016/j.tig.2017.03.006
91. Scannell, D.R., Byrne, K.P., Gordon, J.L., et al.,
Multiple rounds of speciation associated with recipro-
cal gene loss in polyploid yeasts, Nature, 2006,
vol. 440, pp. 341—345.
92. Tyupa, N.B., Kim, E.S., Loskutov, I.G., and Rodi-
onov, 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.
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 allopoly-
ploid Iris versicolor, Ann. Bot., 2007, vol. 100, pp. 219—
224. doi 10.1093/aob/mcm116
95. Sang, T., Crawford, D.J., and Stuessy, T.F., Docu-
mentation 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.
96. Punina, E.O., Machs, E.M., Krapivskaya, E.E., et al.,
Interspecific hybridization in the genus Paeonia (Paeoni-
aceae): polymorphic sites in transcribed spacers of the 45S
2019
292 RODIONOV et al.
rRNA genes as indicators of natural and artificial peony
hybrids, Russ. J. Genet., 2012, vol. 48, no. 7, pp. 684—697.
https://doi.org/10.1134/S1022795412070113.
97. Albalat, R. and Cañestro, C., Evolution by gene loss,
Nat. Rev. Genet., 2016, vol. 17, pp. 379—391. doi
10.1038/nrg.2016.39
98. Muñoz-López, M. and García-Pérez, J.L., DNA
transposons: nature and applications in genomics,
Curr. Genomics, 2010, vol. 11, pp. 115—128. doi
10.2174/138920210790886871
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. doi 10.1101/gr.225730.117
100. Qiu, G.H., Genome defense against exogenous
nucleic acids in eukaryotes by non-coding DNA
occurs through CRISPR-like mechanisms in the cyto-
sol and the bodyguard protection in the nucleus,
Mutat. Res. Rev. Mutat. Res., 2016, vol. 767, pp. 31—41.
doi 10.1016/j.mrrev.2016.01.001
101. Flagel, L.E. and Wendel, J.F., Evolutionary rate varia-
tion, genomic dominance and duplicate gene expres-
sion evolution during allotetraploid Cotton speciation,
New Phytol., 2010, vol. 186, pp. 184—193. doi
10.1111/j.1469-8137.2009.03107.x
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. doi 10.1073/pnas.1101368108
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.
104. Petit, M., Guidat, C., Daniel, J., et al., Mobilization of
retrotransposons in synthetic allotetraploid tobacco,
New Phytol., 2010, vol. 186, pp. 135—147. doi
10.1111/j.1469-8137.2009.03140.x
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. doi
10.1111/tpj.12285
106. Sarilar, V., Palacios, P.M., Rousselet, A., et al., Allo-
polyploidy 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. doi
10.1111/nph.12156
107. Parisod, C., Salmon, A., Zerjal, T., et al., Rapid struc-
tural and epigenetic reorganization near transposable
elements in hybrid and allopolyploid genomes in Spar-
tina, New Phytol., 2009, vol. 184, pp. 1003—1015. doi
10.1111/j.1469-8137.2009.03029.x
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. doi 10.1111/mec.13515
RUSSIAN JOURNAL OF GENETICS
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. doi 10.1038/nrg3683
110. Fultz, D., Choudury, S.G., and Slotkin, R.K., Silenc-
ing of active transposable elements in plants, Curr.
Opin. Plant Biol., 2015, vol. 27, pp. 67—76. doi
10.1016/j.pbi.2015.05.027
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. doi 10.1111/tpj.13910
112. Gehring, M., Genomic imprinting: insights from
plants, Annu. Rev. Genet., 2013, vol. 47, pp. 187—208.
doi 10.1146/annurev-genet-110711-155527
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. doi 10.1038/nplants.2016.30
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. doi 10.1038/s41588-017-
0032-5
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. doi 10.1146/annurev-genet-
120213-092159
116. Navashin, M., Chromosome alterations caused by
hybridisation and their bearing upon certain general
genetic problems, Cytologia, 1934, vol. 5, pp. 169—
203.
117. Pikaard, C.S., Genomic change and gene silencing in
polyploids, Trends Genet., 2001, vol. 17, pp. 675—677.
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/10.1134/S2079086417020062.
119. Wang, J., Tian, L., Lee, H.S., et al., Genome wide
nonadditive gene regulation in Arabidopsis allotetra-
ploids, Genetics, 2006, vol. 172, pp. 507—517.
https://doi.org/10.1534/genetics.105.047894
120. Bottani, S., Zabet, N.R., Wendel, J.F., and Veitia, R.A.,
Gene expression dominance in allopolyploids: hypothe-
ses and models, Trends Plant Sci., 2018, Feb. 9, p. S1360-
1385(18)30014-1. doi 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. doi 10.1101/gr.091678.109
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. doi
10.4137/BBI.S33716
123. Zhou, R., Moshgabadi, N., and Adams, K.L., Exten-
sive changes to alternative splicing patterns following
allopolyploidy in natural and resynthesized poly-
Vol. 55 No. 3 2019
 GENETIC CONSEQUENCES OF INTERSPECIFIC HYBRIDIZATION
ploids, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108,
pp. 16122—16127. doi 10.1073/pnas.1109551108
124. Soltis, D.E., Misra, B.B., Shan, S., et al., Polyploidy and
the proteome, Biochim. Biophys. Acta, 2016, vol. 1864,
pp. 896—890. doi 10.1016/j.bbapap.2016.03.010
125. Hu, G., Houston, N.L., Pathak, D., et al., Genomi-
cally biased accumulation of seed storage proteins in
allopolyploid cotton, Genetics, 2011, vol. 189,
pp. 1103—1115. doi 10.1534/genetics.111.132407
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.
127. Koh, J., Chen, S., Zhu, N., et al., Comparative pro-
teomics 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
128. Ng, D.W., Zhang, C., Miller, M., et al., Proteomic
divergence in Arabidopsis autopolyploids and allopoly-
ploids and their progenitors, Heredity, 2012, vol. 108,
pp. 419—430. doi 10.1038/hdy.2011.92
129. Onda, Y., Hashimoto, K., Yoshida, T., et al., Determi-
nation of growth stages and metabolic profiles in
Brachypodium distachyon for comparison of develop-
mental context with Triticeae crops, Proc. Biol. Sci.,
2015, vol. 282(1811). pii: 20150964. doi
10.1098/rspb.2015.0964
130. Pasquet, J.-C., Chaouch, S., Macadre, C., et al., Dif-
ferential 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. doi
10.1186/1471-2164-15-629
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. doi
10.1111/tpj.13485
132. Banyai, W., Sangthong, R., Karaket, N., et al., Over-
production of artemisinin in tetraploid Artemisia
annua L., Plant Biotechnol., 2010, vol. 27, pp. 427—
433. doi.org/10.5511/plantbiotechnology.10.0726a
133. Banjanac, T., Dragićević, M., Šiler, B., et al., Chemo-
diversity of two closely related tetraploid Centaurium
species and their hexaploid hybrid: metabolomic
search for high-resolution taxonomic classifiers, Phy-
tochemistry, 2017, vol. 140, pp. 27—44. doi
10.1016/j.phytochem.2017.04.005
134. López-Álvarez, D., Zubair, H., Beckmann, M., et al.,
Diversity and association of phenotypic and metabo-
lomic traits in the close model grasses Brachypodium
distachyon, B. stacei and B. hybridum, Ann. Bot., 2016,
vol. 119, pp. 545—561. doi 10.1093/aob/mcw239
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. Biotech-
nol., 2011:793198. doi 10.1155/2011/793198
136. Mishra, B.K., Pathak, S., Sharma, A., et al., Modulated
gene expression in newly synthesized autotetraploid of
RUSSIAN JOURNAL OF GENETICS Vol. 55 No. 3
293
Papaver somniferum L., S. Afr. J. Bot., 2010, vol. 76,
pp. 447—452. http://dx.doi.org/10.1016/j.sajb.2010.02.090.
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.
138. Rodionov, A.V., Interspecific hybridization and poly-
ploidy 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 Brachypo-
dium distachyon, Nature, 2010, vol. 463, pp. 763—768.
doi 10.1038/nature08747
140. Salse, J., Deciphering the evolutionary interplay
between subgenomes following polyploidy: a paleog-
enomics approach in grasses, Am. J. Bot., 2016,
vol. 103, pp. 1167—1174. doi 10.3732/ajb.1500459
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.
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
143. Ellstrand, N.C. and Schierenbeck, K.A., Hybridiza-
tion as a stimulus for the evolution of invasiveness in
plants?, Proc. Natl. Acad. Sci. U.S.A., 2000, vol. 97,
pp. 7043—7050.
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.
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 Cul-
ham, A., Hybridization in ex situ plant collections:
conservation concerns, liabilities, and opportunities,
in Ex situ Plant Conservation: Supporting Species Sur-
vival in the Wild, Guerrant E.O.J., Havens K., and
Maunder, M., Eds., Washington: Island Press, 2004,
pp. 19—438.
148. Hammer, K., Das Domestikationssyndrom, in Kul-
turpflanze, 1984, vol. 32, pp. 11—34.
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. doi
10.3389/fpls.2016.01448
150. Oliver, K.R., McComb, J.A., and Greene, W.K.,
Transposable elements: powerful contributors to
angiosperm evolution and diversity, Genome Biol.
2019
294 RODIONOV et al.
Evol., 2013, vol. 5, pp. 1886—1901. doi
10.1093/gbe/evt141
151. Meyer, R.S. and Purugganan, M.D., Evolution of
crop species: genetics of domestication and diversifi-
cation, Nat. Rev. Genet., 2013, vol. 14, pp. 840—852.
doi 10.1038/nrg3605
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. doi 10.1038/ng.942
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. doi 10.1111/tpj.13021
154. Yao, J.-L., Dong, Y., and Morris, B.A., Parthenocar-
pic 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. doi 10.1073/pnas.983.1306
155. Xiao, H., Jiang, N., Schaffner, E., et al., A retrotrans-
poson-mediated gene duplication underlies morpho-
logical variation of tomato fruit, Science, 2008,
vol. 319, pp. 1527—1530. doi 10.1126/science.1153040
156. Kobayashi, S., Goto-Yamamoto, N., and Hirochika, H.,
Retrotransposon-induced mutations in grape skin
color, Science, 2004, vol. 304, p. 982.
RUSSIAN JOURNAL OF GENETICS
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.
158. Kobayashi, S., Goto-Yamamoto, N., and Hirochika, H.,
Association of VvmybA1 gene expression with antho-
cyanin production in grape (Vitis vinifera) skin-color
mutants, J. Jpn. Soc. Hort. Sci., 2005, vol. 74, pp. 196—
203.
159. Chiu, L.W., Zhou, X., Burke, S., et al., The purple
cauliflower arises from activation of a MYB transcrip-
tion factor, Plant Physiol., 2010, vol. 154, pp. 1470—
1480. doi 10.1104/pp.110.164160
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.
doi 10.1038/nplants.2016.115
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. doi 10.1016/j.tig.2009.12.006
162. Jenczewski, E., Chevre, A.M., and Alix, K., Chromo-
somal 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.
Translated by N. Maleeva
Vol. 55 No. 3 2019