Eupolyploidy As a Mode in Plant Speciation

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ISSN 1022-7954, Russian Journal of Genetics, 2023, Vol. 59, No. 5, pp. 419–431. © Pleiades Publishing, Inc., 2023.
Russian Text © The Author(s), 2023, published in Genetika, 2023, Vol. 59, No. 5, pp. 493–506.
Eupolyploidy As a Mode in Plant Speciation
A. V. Rodionov*
Komarov Botanical Institute, Russian Academy of Sciences, St. Petersburg, 197376 Russia
*e-mail: avrodionov@mail.ru
Received July 17, 2022; revised September 1, 2022; accepted September 12, 2022
Abstract—When discussing phenomena of whole genome duplication, the terms “neopolyploid,” “meso-
polyploid,” and “paleopolyploid” are used in their modern “postgenomic” interpretation. In our opinion, in
long chain of gradual changes of polyploid genome during the transition from neopolyploids to paleopoly-
ploids, it makes sense to single out the eupolyploid stage—a state of a polyploid in which its polyploid nature
is beyond doubt, but the genome (karyotype) of the eupolyploid, unlike the neopolyploid, is already relatively
stable. Most so-called “polypoid species” are actually eupolyplids, the polyploid nature of their karyotype is
beyond doubt among researchers—geneticists, karyologists, and florists. Optionally, eupolyploids take part
in new rounds of interspecific hybridization either maintaining the level of ploidy of the parents or with the
emergence of an allopolyploid of a higher level of ploidy. Eupolyploidization of the genome is a mechanism
of radical and rapid plant speciation. In this way, tens of thousands of species of modern plants arose. Suc-
cessful combinations of alleles of eupolyploid subgenomes, large sizes characteristic of high polyploids, and
frequent transition to asexual reproduction can contribute to the successful development of new areas by
eupolyploids, adaptation to extreme conditions of existence at the edge of areas, but not to the acquisition of
new aromorphoses—this is speciation, but speciation on an already achieved level of evolutionary complexity,
a step that does not in itself lead to progressive evolution.
Keywords: polyploidy, evolution of genomes and karyotypes, plant cytogenetics
DOI: 10.1134/S1022795423050113
According to karyosystematists, about half of the
species of flowering plants are polyploids [1]. Only in
genera in which there are both diploids and polyploids
and therefore the definition of ploidy is beyond doubt,
there are at least 15% of polyploid species. Moreover,
in genera with low basic chromosome numbers x = 2–
7, the proportion of polyploids is significantly higher,
up to 50% [2]. The results of a comparative study of
linkage groups of representatives of all major phyloge-
netic branches of terrestrial plants showed that traces
of one or several acts of whole genome duplication
(WGD) are present in the genomes of all gymno-
sperms and angiosperms studied in this respect [3–5].
Therefore, it is not surprising that there are many
polyploids, but that there are many plants—about 50–
85%—in which the karyotype looks as diploid.
That one or more WGD events have taken place in
the evolution of the genomes of all gymnosperms and
angiosperms does not seem trivial. In representatives
of other phylogenetic branches, sister branches of seed
plants (Spermatophyta), WGD is not always detected.
There are no traces of WGD in the genomes of the
ancestors of multicellular land plants, charophytes [6].
Gene duplications—consequences of WGD—are not
found in the genomes of spike-moss Selaginella [7],
hornwort Anthoceros angustus [8], and common liver-
wort Marchantia polymorpha [9]. In contrast, the
ancestors of true mosses (Bryophyta), ferns, and
homospore lycopsids, as well as flowering plants,
experienced at least one WGD event in their history
[10]. It is noteworthy that about 70% of the registered
WGD events in the ancestors of modern plants imme-
diately preceded the period of ecological catastrophe
at the boundary of the Cretaceous, and there is reason
to believe that some features of the neopolyploid
genomes that appeared then helped their owners adapt
to new environmental conditions [3, 11].
WGD—AUTO- OR ALLOPOLYPLOIDIZATION?
A WGD event can occur in two different ways—a
species genome duplication can occur, such a poly-
ploidy with three or more identical genomes (AAA,
AAAA, …) being called an “autopolyploid,” while a
polyploid that arose after interspecific hybridization as
a result of doubling close, related, but not identical
genomes (AABB, AABBCC, etc.) is called an “allo-
polyploid.” It is not known how often auto- and allo-
polyplodes occur in nature. Estimates by different
authors, even when it comes to well-studied subjects,
vary significantly (cf. [12, 13]). It would seem that the
differences between autopolyploids and allopolyploids
are obvious—the multiplication of the genome of one
species in the first case and the multiplication of
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RODIONOV
genomes as a result of the combination of two or sev-
eral subgenomes derived from different species in the
second. There are two main methodological
approaches for differentiating auto- and allopoly-
ploids: taxonomic and karyological. A polyploid is
classified as an autopolyploid if an experienced taxon-
omist believes that the diploid ancestors of the poly-
ploid were plants of the same species, this being the
taxonomic method of differentiation. An equally solid
conclusion can be drawn from a karyological study: if
multivalents are formed in meiosis I during the pairing
of chromosomes, this is an autopolyploid; if the chro-
mosomes are paired and there are no multivalents, it is
an allopolyploid.
The problem is what should be considered different
species in the plant world. In the course of discussions
about the boundaries of species, it has been proposed
to distinguish between “biological” species that are
reproductively isolated from each other [1, 14, 15] and
“morphological” or “taxonomic” species, which are
natural populations with greater or lesser morphologi-
cal pecularities (morphological hiatus) and a charac-
teristic area within which that species can be found [1,
16–18]. Comparatively often, morphologically well-
distinguished plant species are capable of producing
viable, fully or partially fertile offspring when crossed.
It has been shown that the ability to produce viable
hybrids can be preserved in geographically separated
plant species for millions and tens of millions of years
[18]. When, due to climate change or human activities,
the ranges of “taxonomic” species are closed off, these
species can often quite successfully interbreed, yield-
ing fertile, often polyploid offspring. J.L. Stebbins
called this way in which polyploid species appear “the
secondary contact hypothesis” [19, 20]. “Taxonomic”
species have recently been most often distinguished on
the basis of a combination of their morphological fea-
tures and DNA barcode, implying that the presence of
a peculiar set of features and differences in DNA bar-
codes in itself is a basis for assuming the presence of
a reproductive barrier, additional evidence for the exis-
tence of which in this case are not required [21–23].
The question “what are we dealing with– an auto-
or allopolyploid?” a priori means that we may be deal-
ing with the result of interspecific crossing; hence, the
“parents” of the putative allopolyploid cannot be
assigned to “biological” species on the basis of the
indisputable criterion of a biological species—repro-
ductive isolation. It remains to be assumed that the
events of interspecific hybridization leading to the
appearance of allopolyploids occur with the participa-
tion of “taxonomic” or “morphological” species.
However, the boundaries of “taxonomic” species are
also controversial. The problem is that some taxonom-
ically significant plant traits are determined mono-
genically. For example, the species Avena clauda and
A. eriantha differ much in the morphology of the
flower and spikelet, but these differences are deter-
mined by the alleles of one gene. Both species can be
seen in mixed populations and it is known that hybrids
between them form easily and are fertile. This is an
example of two “good” morphological species; how-
ever, from a genetic point of view, their species status
is unjustified [15]. The opposite situation applies in
the case of the species A. damascena and A. prostrata—
it is difficult to distinguish them by morphology, but
they are reproductively isolated [15]. According to
L. Riesberg, et al. [24], only 70% of “taxonomic” spe-
cies are reproductively isolated. The frequency of
occurrence of reproductively isolated, but morpholog-
ically indistinguishable, cryptic plant species cannot
currently be calculated [25, 26].
The unresolved issues related to the taxonomic cri-
terion of auto- or allopolyplody include the problem of
the taxonomic status of cytotypes (chromosomal
races)—plants that are close to each other in morphol-
ogy, but have different levels of ploidy. Are they one
species or several different species? As a rule, cyto-
types of autopolyploid origin do not have significant
morphological differences, except perhaps for the size
of the cells and the size of the plant itself. They are
referred to different species only in rare cases, when
the ranges of cytotypes differ [26, 27]. On the contrary,
cytotypes of allopolyploid origin are often assigned to
different species and even genera, even when morpho-
logical differences between natural populations with
different genome/karyotype compositions are not
obvious [25–28].
The karyological criterion of the hybrid origin of a
polyploid is independent of the expert assessment by
taxonomist–morphologists of the species rank of its
ancestors. According to it, a species is considered an
allopolyploid if it does not have allosynthesis (chro-
mosome pairing in meiosis I with the formation of
multivalents) and disomic inheritance of alleles. On
the contrary, autopolyploids are characterized by mul-
tivalents in meiosis I and polysomic inheritance of
alleles [13, 29]. However, the production and cultiva-
tion of interspecific hybrids in the experimental field
and the study of their chromosomes in meiosis are
labor-intensive and take a long time, fitting poorly
into the modern practice of planning and financing
scientific projects. It is extremely rare that such a study
will concern objects outside the narrow circle of model
objects of plant genetics. Among representatives of
47 plant families, Z. Li et al. [30] identified only 208
polyploid species in which the behavior of chromo-
somes in meiosis was studied at least once. Among
them, taking into account the integrated phylogenetic,
cytological, and genetic data, 118 species were classi-
fied by the authors as allopolyploids and 90 as auto-
polyploids [12, 30]. However, in this sample, only 92
species had strictly bivalent pairing of chromosomes in
meiosis I, while multivalents (at least one multivalent
were observed in the meiotic prophase of 116 species.
What is important is that, of the polyploids that were
considered by the authors of the study as allopoly-
ploids, 48% of the species showed strictly bivalent

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EUPOLYPLOIDY AS A MODE IN PLANT SPECIATION 421
pairing and 52% of the species had one or more mul-
tivalents. Among autopolyploids, the corresponding
frequencies were 39 and 61% [30]. As expected, the
frequency of strictly bivalent pairing is higher in allo-
polyploids than in autopolyploids, but the differences
between the compared types of polyploids are insignif-
icant. The high frequency of occurrence of multiva-
lents in species that were considered allopolyploid and
the frequency of strictly bivalent pairing in autopoly-
ploids force one either to abandon the criterion
“strictly bivalent pairing ” as an indicator of the allo-
polyploid nature of the polyploid or to recognize that
the integrated “phylogenetic, cytological, and genetic
data” used by the authors to differentiate auto- and
allopolyploids [12, 30] do not allow one to correctly
distinguish between allo- and autopolyploids.
As a result, the role of autopolyploidy in the pro-
cesses of speciation in plants remains unclear or not
fully substantiated to date [26, 27, 29–31]. As a rule,
an autopolyploid differs from its diploid ancestors in
morphology [26, 27], transcriptome [32, 33], and pro-
teome [34] to a much lesser extent than an allopoly-
ploid. On the contrary, there is reason to believe that
active speciation, the appearance of taxonomically
significant innovations in the morphology and physi-
ology of the ancestors of modern wild plants and the
emergence and/or purposeful creation of numerous
agricultural crops were associated with allopolyploids,
i.e., polyploidization of genomes that accompanied
distant hybridization [3, 11–13, 29, 35, 36].
NEOPOLYPLOIDS, MESOPOLYPLOIDS,
EUPOLYPLOIDS, PALEOPOLYPLOIDS
When describing the phenomena associated with
the emergence of a new polyploid and its subsequent
transformations, the terms “neopolyploid,” “meso-
polyploid,” and “paleopolyploid” proposed by
C. Favarger [37] are used in their modern “postge-
nomic” interpretation [38]. At the same time, recently
emerged polyploids with a karyotype (genome) are
called “neopolyploids” that have a number of chro-
mosomes that is the result of a combination of com-
plete sets of chromosomes (subgenomes) of ancestral
diploid species. The term “paleopolyploid” is used to
describe a genome (karyotype) in which the chromo-
somal morphology and chromosome behavior in mei-
osis is diploid, and the polyploid past of the paleopoly-
ploid becomes apparent only after analysis of the
nuclear genome sequences. Mesopolyploid species
demonstrate diploid-like meiosis and a disomic inher-
itance of alleles and have a reduced, compared to the
neopolyploid, and often very low “quasi-diploid”
number of chromosomes; however, parental subge-
nomes in the mesopolyploid genome can still be dis-
tinguished cytogenetically or molecular phylogeneti-
cally [38]. In our opinion, in this chain of gradual
changes of the genome during transition from neo-
polyploids to paleopolyploids, it makes sense to distin-
guish the eupolyploid stage (“eu” from Greek ε,
“good; real, authentic, true”) as the state of a poly-
ploid in which its polyploid nature is beyond any
doubt (the karyotype is a combination of the karyo-
types of the parents), but the genome (karyotype) of
the eupolyploid, in contrast to the neopolyploid, is
already relatively stable [39, 40].
EU POLY PL OI DS : S ALTAT IO N S PEC IF IC AT IO N
BY MORPHOLOGICAL DESPECIALIZATION
AND PARTIAL REPRODUCTIVE ISOLATION
Most of the genomes/karyotypes of numerous
polyploid plant species are in the eupolyploid state,
the polyploid nature of the karyotype of which is not
in doubt among flora researchers. Among f lowering
plants, polyploid genomes more often appeared in the
family Poaceae; they were also common, but three
times rarer, than in grasses, in the Montiaceae and
Brassicaceae families. Very rarely, polyploidization
events took place in the order Arecales [41]. Typical
eupolyploids include numerous allotetraploid species
with an ordered, diploid type of chromosome segrega-
tion during meiosis. Such polyploids are called
“amphidiploids” (this term having been coined by
M.S. Navashin [42, p. 136]).
Problems with chromosome divergence in meiosis
and mitosis in neopolyploids are associated with an
important feature of eukaryotic centromeres—a prop-
erly functioning kinetochore is formed as a multicom-
ponent nucleic-protein complex, which is based on
the interaction of centromeric DNA rapidly changing
during taxon divergence and those domains of centro-
meric proteins CenH3 and CENP-C that interact with
centromeric DNA and also rapidly change in evolu-
tion [43, 44]. The ability to bind to the centromeric
DNA of another species in centromeric proteins can
be maintained for a long time. It was shown, for exam-
ple, that CenH3 of Lepidium and Zea can interact with
centromeric DNA of Arabidopsis, forming working
centromeres that separate chromosomes of Arabidop-
sis into daughter cells, but under competitive condi-
tions, when both CenH3 of Lepidium and CenH3 of
Arabidopsis are present in the genome, chromosomes
with “heterogeneous” kinetochores diverge worse,
often entering micronuclei and being eliminated [45].
Stabilization of chromosome segregation in a eupoly-
ploid can be achieved by the loss of centromeric DNA
from one of the parents, as is seen in the allotetraploid
Zingeria trichopoda [46], and/or homogenization of
the CenH3 genes towards one of the parents [47].
Losses of chromosomes during meiosis of neo- and
mesopolyploids are associated not only with the
imperfection of “bastard” centromeres, but also with
aberrant pairing of chromosomes in meiosis. Multiva-
lents in autopolyploids and allopolyploids increase the
probability of unequal segregation of chromosomes in
meiosis I, the appearance of zygotes and endosperm
with unbalanced chromosome sets [29]. Selection to

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RODIONOV
increase the fertility of a polyploid should go in the
direction of chromosome sets in which homologous
and homologous chromosomes would predominantly
or exclusively conjugate to form bivalents [12, 48, 49].
Several different mechanisms work to achieve this
result. First of all, the preconditions of meiosis con-
tribute to the preferential pairing of homologs rather
than homologs. In the interphase in somatic cells [46,
50, 51] and in the premeiotic interphase in polyploids
[52], subgenomes of different origin are more or less
spatially separated.
The preferential pairing of homologs over homo-
logs is also facilitated by the fact that during the diver-
gence of ancestral allopolyploid species, microinver-
sions have accumulated in the chromosomes of each
species, such as those found in the genome Triticum
[53] and Oryza [54]. No less important is the fact that,
during the divergence of the ancestors of allopoly-
ploids, their genomes experienced explosive amplifi-
cation of transposons of some families (new or previ-
ously small) and the disappearance of all or most of
the sequences from the transposon families of the
common ancestor. Such a scenario of changes in the
pattern of moderate repeats in the genome is called the
“birth-and-death” model [55]. For example, out of
the 33 families of retrotransposons in the genome of
the species Oryza punctata, six families occupying
25 million bp (6.3% of the genome) were not found in
the genomes of other rice species [54]. Tracing the fate
of 75 orthologous loci of LTR-containing retrotrans-
posons in eight of the most closely related species from
the related group O. sativa showed that these
sequences are lost from the genome at an average rate
of 3620 bp/Mya per transposon. Extrapolating these
data to the entire genome, we can predict that, if there
is no subsequent explosion of transpositions, then the
genome of O. sativa ssp. japonica will decrease by a
quarter of its size over the next 3–4 Ma [54].
The processes of predominant pairing of homolo-
gous chromosomes during meiosis of allopolyploids
are under genetic control [49, 56]. Alleles that sup-
press the pairing of homologous chromosomes have
been found in the diploid ancestors of polyploids in
different plant subfamilies, which is not surprising
since we know that they all went through several WGD
events. Apparently, a neopolyploid in most cases
receives them from its diploid (paleopolyploid) ances-
tors, but there are cases when bivalent pairing of chro-
mosomes was explained by new mutations [56–58].
Sometimes the transition from multivalent to bivalent
mating in neopolyploids occurs so quickly that it sug-
gests epigenetic regulation of the process [56].
The second stage, at which homolog pairing errors
are corrected, refers to the time of formation of the
synaptonemal complex (SC), when the formation of
SC between homologs proceeds efficiently and local
regions of SC that appeared between homologs are
sorted out [49, 59, 60].
In addition to problems with chromosome segrega-
tion, neopolyploids and mesopolyploids in somatic
cells have an increased frequency of chromosome
fragments and intergenomic translocations [61, 62].
There is a point of view that intergenomic transloca-
tions are one of the mechanisms for overcoming the
nuclear-cytoplasmic incompatibility of neopolyploids
[63, 64]. The possibility of intergenomic transloca-
tions is hampered by the fact that subgenomes of dif-
ferent origin in the interphase nucleus of allopoly-
ploids are located in different compartments [46, 50,
51]. It can be assumed that the same circumstance to
some extent limits the intergenomic migration of
transposons and other scattered repeats. We are con-
vinced of the existence of such a limitation by the phe-
nomenon of GISH hybridization, in which the
genome-wide DNA of one putative “ancestor”
hybridizes with the chromosomes of only one subge-
nome, but not with others (see, for example, 46, 65].
How long the differences in the sets of interspersed
repeats between subgenomes in allopolyploid in dif-
ferent families persist is unknown. For example, in
tetra- and hexaploid oats that formed 8–10 Mya [66],
the difference between A- and C-subgenomes in scat-
tered repeats revealed by GISH was retained [67],
while in Nicotiana nesophila, originated about 4.5 Mya,
the ancestors of which are believed to be N. sylvestris
And N. obtusifolia, GISH no longer detects differences
between subgenomes [68].
Optionally, eupolyploids can enter new rounds of
interspecific hybridization with the hybrid retaining
the ploidy level or with the appearance of an allopoly-
ploid of a higher ploidy level [69, 70]. It has been
shown that, in high-order polyploids, postzygotic iso-
lation of cytotypes is often less pronounced than in
hybridization of diploids and tetraploids [71]. Among
high-order polyploids, various variants of aneuploidy
are often found, which do not correlate with morpho-
logical hiatuses and are interpreted as a manifestation
of the intraspecific diversity of cytotypes . Incomplete
postzygotic isolation results in a continuous flow of
alleles between cytotypes among high-order poly-
ploids, which slows down the divergence of morpho-
types in multichromosomal polyploids [71]. In this
way, whole complexes of facultatively cross pollinating
natural cytotypes arise, partly apomictic or self-polli-
nating “microspecies,” which cannot be divided into
any “large” (“morphological”) species [17, 72]. This
situation occurs in many genera of grasses, for exam-
ple, in Poa, Elymus, Leymus, and Thinopyrum [73].
The emergence of eupolyploids with different lev-
els of polyploidy as a result of interspecific hybridiza-
tion is a radical and rapid method of speciation. In this
way, tens of thousands of species of modern plants
arose [41, 74]. So, as a result of hybridization between
the tetraploid North American species (2n = 4x = 32)
Symphyotrichum boreale (Asteraceae) and hexaploid
(2n = 6x = 48) S. novi-belgii, a rare endemic species
appeared—the decaploid (2n = 10x = 80) S. anti-

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EUPOLYPLOIDY AS A MODE IN PLANT SPECIATION 423
costense [75]. The highest known levels of polyploid-
ization among flowering plants are 16× in Artemisia
(Asteraceae) [76] and Primula (Primulaceae) [77],
24× Tradescantia (Commelinaceae), and 28× in Eleo-
charis and 32× in Cyperus (both Cyperaceae) [78].
High polyploids are relatively common in grasses: 18×
in Avenula adsurgens [79], Arundo donax [80] and
Anthoxanthum amarum [81], 20× in Helictochloa
lusitanica [69], 36× Andropogon barbinodis [82], and
38× in Poa litorosa [83].
Analysis of the chromosome numbers in the karyo-
types of about 30 thousand species of flowering plants
belonging to 147 families of 46 orders showed that
recently emerged polyploids (eupolyploids) are pres-
ent in all orders and in 139 out of 147 families1 [41].
A typical example of a eupolyploid is the karyotype
and genome of a hexaploid species that formed about
9000 years ago, Triticum aestivum (2n = 42, x = 7,
BBAADD), which arose as a result of the union of the
genomes of the tetraploid spelt (emmer) T. t urgi d u m
(2n = 28, BBAA) and the genome of a diploid (paleo-
polyploid) species Aegilops tauschii (2n = 14, DD).
That was only the last of the rounds of polyploidiza-
tion that led to the appearance of the species T. a e s -
tivum. Approximately 500–800 thousand years ago, it
was preceded by the appearance of the emmer tetra-
ploid genome as a result of hybridization of two diploid
(paleopolyploid) species: as for the pollinator plant,
the donor of subgene A, it was a species similar to
T. urartu , but diverged from T. urart u ~1.3 million
years earlier, and the mother plant donor of subge-
nome B, a species related to Ae. speltoides, but diverged
from a common ancestor with Ae. speltoides ~4.5 Ma
earlier [84–87]. We emphasize that the genome and
karyotype of modern lines and varieties of T. a es t i v u m
look stable, but the karyotype of resynthesized allo-
polyploids with the BBAADD genomic constitution
in the first generations is to some extent (depending on
the lineage of the parent species) unstable—at this
time, some of the duplicated sequences of protein-
coding genes is lost, and repeats (repeatome) have
been reorganized to some extent. However, as a rule,
the genome stabilizes after a few generations, and pair-
ing of chromosomes during meiosis proceeds without
multivalents [85, 86].
The similarity of linkage groups of three subge-
nomes of modern T. aestiv u m between themselves and
with the linkage groups of diploid ancestors (mac-
rosynthenia) is high; however, on average, every
75 million bp in the common wheat genome, microin-
versions with an average length of 10.5 million bp are
found, mainly lying in gene-poor regions [53]. In
terms of the number of genes, subgenomes A, B, and
D are approximately equal (35345, 35 643, and 34 212
genes, respectively). The subgenomes do not differ
1Alstroemeriaceae, Fagaceae, Grossulariaceae, Nepenthaceae,
Nothofagaceae, Schisandraceae, Smilacaceae, and Tamarica-
ceae.
significantly in the number of copies of transposons of
different classes. After polyploidization transposon
expansion did not occur in the genome of T. a estivu m
[53]. However, in the wheat genome, the processes of
gradual genomic diploidization (“genome fraction-
ation ” [3 8, 4 8]) have been on goi ng, but in an ev en wa y,
without discrimination of one of the subgenomes—in
the polyploid genome of T. aestivu m , each of the
subgenomes has already lost approximately 10% of
ancestral genes [53]. Perhaps this is precisely the indi-
cator of the quasi-stable state of the eupolyploid
genome. A somewhat different situation holds for the
allopolyploid genome of Avena sativa (karyotype
AACCDD)—the oats have 12% fewer genes in subge-
nome C than in subgenomes A and D; however, these
genes are not lost, but are translocated from a gene-
rich region of the C subgenome with a length of at least
226 million bp into chromosomes A and subgenomes
D—i.e., the hexaploid oat genome is also in a quasi-
stable state [87].
Á. Löve [88, 89] and D.R. Dewey [90], who stud-
ied Triticeae in detail, came to the conclusion that new
genera and species in Triticeae are formed by interspe-
cific hybridization and polyploidization through the
appearance of more and more new combinations of
subgenomes. Á. Löve [88, 89] suggested that a group
of closely related species that have either a specific
diploid genome or a specific combination of subge-
nomes characteristic of this genus only be considered
a genus. At the same time, autopolyploid multiplica-
tion of the genome or subgenome was not considered
sufficient to assign autopolyploid combinations to dif-
ferent genera (for example, karyotypes JJHH,
JJJJHH, and JJJJHHHH—karyotypes of species of
the same genus). The idea is attractive from a genetic
point of view, as well as close to that of L.N. Delaunay
[91], of distinguishing between minor, microevolu-
tionary changes in the size and morphology of chro-
mosomes that occur within the genus, and macroevo-
lutionary ones, significant reorganizations of chromo-
some sets. “Delaunay karyotype” is a taxonomic unit,
a group of species that differs in the morphology of its
chromosome set from another group of species,
another “Delaunay karyotype” [91].
Á. Löve [89] identified 24 variants of diploid
genomes in Triticeae, designated by Latin letters from
A to Z, and 15 variants of polyploid genomes, in the
formation of which 13 out of 24 possible primary dip-
loid genomes took part. In the system proposed by
Á. Löve, the number of genera in the Triticeae
increased, while, guided by the genomic criterion of
the genus, it was necessary to split up some well-
known traditional genera, such as Triticum:
T. mono co ccu s and T. ura r t u with the AA karyotype
entered the genus Crithodium, T. d u r um (AABB) was
assigned to the genus Gigachilon, and T. aest i v u m
(BBAADD) to the genus Triticum. The genome off
Hordeum vulgare and H. bulbosum was designated as I;
the genome of the remaining members of the genus

424
RUSSIAN JOURNAL OF GENETICS Vol. 59 No. 5 2023
RODIONOV
Hordeum, both diploids and polyploids, was desig-
nated as H [89, 92]. Over time, the letters of the
English alphabet to designate variants of genomes
began to be lacking; in particular, it turned out that, in
the species H. murinum, there was another primary
(diploid) genome, which was designated as Xu, while
the genome of the species H. gussoneanum and
H. marinum was called the Xa genome [92, 93]. Some
other modifications of the designation of genomes can
be found in [92].
As an example, we can cite three instances of spe-
ciation/genus formation in Triticeae [90] (Fig. 1).
When discussing the features of speciation in
plants, one should pay attention to the fact that the
same combinations of subgenomes (of the same
genus) can occur repeatedly at different times and at
different points of the ranges (Fig. 2). Thus, the dis-
junction of the ranges of eupolyploid species in some
cases may be a consequence of the independent origin
of polyploid natural races with a similar combination
of subgenomes in different territories, on different
continents.
The consistent application of the genomic concept
of the genus in taxonomy often did not coincide with
the discreteness of morphological characters that were
considered taxonomically significant in the systemat-
ics of grasses and was not supported or was supported,
but with reservations and exceptions, by experienced
plant taxonomists [28, 94–97]. However, it is not by
chance that N.I. Vavilov’s law of homologous series
[98, 99] was discovered, first of all, in the work with
Triticeae—an in-depth analysis of morphological vari-
ations in each cereal species can reveal almost the
entire complex of characters observed in other species
of this tribe. Only some of the characters are species-
specific, and only they can be considered as taxonom-
ically significant radicals [98, 99]. This is especially
noticeable when the morphological features of poly-
ploids are analyzed, as a rule, they are distinguished by
an amazing morphological diversity [28, 100].
R.V. Kamelin [96, p. 98, 100] rightly noted that the
establishment of the genomic composition of species
by pairwise crossing and laborious analysis of the
behavior of chromosomes in meiosis 1 [90, 97, 101] is
difficult, and hardly possible for many natural species.
Therefore, in the first decade of the 21st century, the
idea of delimitation of the genera of Triticeae (and not
only Triticeae) proposed by Loewe according to the
genomic criterion of genera did not seem convincing
to R.V. Kamelin and other systematic botanists, since
the genomes of polyploid grasses are complex in com-
position, and in 2005 there was no certainty that the
primary genomes of diploids and subgenomes of poly-
ploids had been identified unambiguously correctly
and that the evolution of modern diploids and poly-
ploids known to us went from diploids to polyploids,
and not vice versa. Not knowing the results of whole
genome sequencing, R.V. Kamelin [96] quite reason-
ably assumed what now has comparative genomic evi-
dence: genomes that appear to us as primary diploids
may in fact be recent derivatives of polyploid genomes.
However, on the other hand, the outstanding
agrostologist N.N. Tsvelev [28] wrote about the possi-
bilities of practical application of the genomic crite-
rion 30 years ago: “Currently, they [opportunities], of
course, are very limited, since genomic analysis [by
the Kihara and Dewey methods] requires very labor-
intensive studies. However, what is impossible now
may eventually become possible. It is likely that a new
technique will be developed that greatly facilitates
genetic analysis, which is undoubtedly very promising.
It is possible that in the future it will be possible to use
the redundant information contained in the genomes,
which will open up wide opportunities for creating
new taxa, and perhaps for recreating already extinct
taxa, the genomes of which are preserved in the chro-
mosome sets of living species, but are not used by them
in ontogeny. N.N. Tsvelev believed [28, 100] that the
genomic criterion of genera deserves attention, if only
because at the present time no unambiguous synapo-
morphies for constructing the Triticeae genera system
on the basis of taxonomically convincing morpholog-
ical hiatuses or reproductive isolation have been
found, and so it seems quite possible that new and
future methods for studying genomes may well to
make the genomic criterion of genera a tool in the
hands of a taxonomist–practitioner [28].
An important circumstance that largely determines
the morphological features of diploid and polyploid
Fig. 1. Example of taxonomy formation in the Triticeae tribe (from [90], modified).
Pseudoroegneria (2n = 14, SS)
Elymus lanceolatus (2n = 28, SSHH)
Pascophylum smithii
(2n = 56, SSHHJJNN)
Leymus triticoides (2n = 48, JJNN)
Psatyrostachys (2n = 14, NN)
Thinopyrum (2n = 14, JJ)
Critesion (2n = 14, HH)

RUSSIAN JOURNAL OF GENETICS Vol. 59 No. 5 2023
EUPOLYPLOIDY AS A MODE IN PLANT SPECIATION 425
grasses was pointed out by N.N. Tsvelev [100, 102].
One of the basic principles of the theory of evolution
states that, within a particular phylogenetic branch,
the characteristics of any common ancestor are more
primitive and unspecialized than the characteristics of
descendants on different branches of its tree, which
are always more or less specialized in proportion to the
time of their appearance [103]. The traditional view of
speciation and the evolution of morphological traits in
plants assumed that nonspecialized forms have evolu-
tionary potencies, that multidirectional processes of
specialization take place in each of the phylogenetic
branches, and specialized forms are not capable of
diversification [100, 102]. However, in grasses, species
with diploid karyotypes tend to be highly specialized
forms; often, these are species with narrow or broken
ranges, while their eupolyploid descendants resulting
from allopolyploidization with their complex combi-
na tion o f su bgen ome s lo ok d esp eciali zed. Th is is m an-
ifested in the fact that they have features that are more
ancient and, therefore, more primitive in the evolu-
tionary-morphological sense, as is observed, for
example, in polyploid Elymus compared to their dip-
loid ancestors from the genera Hordeum and Pseudo-
roegneria [73, 97]. Numerous polyploid Calamagrostis
sensu lato are less specialized than their probable dip-
loid ancestors from the genera Agrostis, Trisetum [73,
102, 104]. PacBio-sequencing of four long (about 1 kb)
low-copy regions of the nuclear genome of ferns from
the genus Botrychium (fam. Ophioglossaceae) showed
that numerous polyploids in this genus arose recently,
no more than 5 million years ago, as a result of recent
rapid “nonadaptive radiation,” when a relatively small
number of diploid species (12 out of 20 studied) as a
result of independent instances of interspecific
hybridization gave 19 tetraploid species and one hexa-
ploid species; moreover, the genomes of three diploid
species participated in the formation of tetraploid
subgenomes only once and the subgenome obtained
from B. pallidum was found in the genomes of seven
tetraploids and one hexaploid [105]. Thus, we see that,
with saltational speciation through allopolyploidiza-
tion and introgression, evolution seems to go back-
wards: highly specialized evolutionarily static diploid
Fig. 2. The same eupoliploid species/genus may occur more than once at different times and in different points of its range.
A' B'
BB B
BA
ABA'B 'AA'AAA'B

426
RUSSIAN JOURNAL OF GENETICS Vol. 59 No. 5 2023
RODIONOV
(actually paleopolyploid!) “ancestors,” as a result of
hybridization, gave rise to several or many eupolyploid
genera, which, in terms of the totality of characters,
look unspecialized.
The transition of a neopolyploid to a eupolyploid,
quasi-stable state often occurs in combination with the
transition to a perennial life form, self-pollination,
apomixis, and vegetative reproduction, which is
important when there are limited opportunities to find
a sexual partner [74, 106–109]. The polyploid state of
the genome itself does not increase resistance to low
temperatures [19, 20]; however, low temperatures,
salinity, and other environmental factors unfavorable
for this species that plants have to face at the boundar-
ies of their natural ranges, on disturbed lands, and in
newly developed ecological niches increase the proba-
bility of the appearance of gametes with an unreduced
number of chromosomes in plants with obligate or fac-
ultative sexual reproduction [110–112]. This is proba-
bly why there are many eupolyploids among invasive
species [113] and among endemic species of island
flora [108]. In the tundra of the Northern Hemi-
sphere, 51% of the species are polyploids; in the taiga
located to the south, 47% are [74]. In western Canada,
Greenland, and the European Arctic, 87% of endem-
ics are polyploids; in Beringia, these endemics are
69% [114, 115]; in Alaska, 55% [20].
Under extreme conditions of existence, the proba-
bility of interspecific hybridization and the appear-
ance of allopolyploids increases. An interesting and
instructive fact is given by N.N. Tsvelev [102]: species
of two species-rich sections of the genus Poa—Poa and
Stenopoa—often grow together without interbreeding
in a warm-temperate zone. Hybrids between them and
hybridogenic species descended from them are found
only in the Arctic and in the highlands.
Influencing the frequency of appearance of unre-
duced gametes, extreme climatic conditions contrib-
ute to the relative abundance of polyploids in the Arc-
tic, but there are not a large species diversity and
numerous populations here. The eupolyploid stable
state of the genome, combined with asexual reproduc-
tion, fixed heterozygosity, protection from inbreeding,
and unpredictable results of genetic drift, allows Arctic
polyploids to coexist and compete successfully with
previously adapted, and also a few diploid (paleopoly-
ploid), relatives for a long time [74, 114].
The Achilles heel of these polyploids, which are
perfectly adapted to environmental conditions, often
clonally reproducing and therefore stably transmitting
to their offspring the entire complex of adaptive traits
of extremals that have passed the selection, is a low
level of intraspecific variability. However, there is no
certainty that the next generations of this species will
not face new radical challenges from competing spe-
cies or habitats. In this case, nature has created a
mechanism of multiple variability and genetic drift
based on meiotic instability and dysploidy. A vivid
example of phenomena of this kind is given by Jens
Clausen [116]: a large and numerous bluegrass Poa
ampla (now, Poa juncifolia) grows in the prairies of the
northwestern United States. In his karyotype 2n = 63
chromosomes. Between 90 and 95% of viable seeds are
produced by the species apomictically, resulting in all
plants in the offspring having 63 chromosomes, phe-
notypically reproducing the parents. However, a small
part of the offspring, from 5 to 10%, is born as a result
of fertilization. As a rule, these are small, weak plants
differing in number of chromosomes. They had 2n =
56, 60–63, 66, 70, 82–84, 90–93, 98–102, 126, up to
2n = 147 chromosomes. Obviously, we have a kind of
reserve before us, the purposeful production of more
and more new variants of allele combinations, some of
which may turn out to be more successful than the
parental generation, in the event of an unpredictable
future, a new combination of environmental factors,
but, alas, an inevitable environmental crisis.
Successful combinations of alleles of eupolyploid
subgenomes that have passed through selection, large
sizes characteristic of high polyploids, and a transition
to asexual reproduction are all factors that contribute
to the successful development of new areas by eupoly-
ploids, adaptation to extreme conditions of existence
on the edge of areas. However, at the same time,
mutations in the genomes of polyploids are buffered,
and experimentally obtained polyploids, as a rule, do
not differ in anything fundamentally new from their
diploid ancestors [19, 20, 35, 117]. One gets the
impression that, by easily forming numerous new, to
some extent reproductively isolated, polyploid species,
the species and generic independence of which is
determined by the original combination of subge-
nomes, the event of WGD itself does not create any-
thing fundamentally new, that most of the numerous
polyploid species are “dead-end” branches on the
phylogenetic tree of flowering plants [19, 20, 48, 118].
Transition from a neopolyploid to a eupolyploid state
is a mechanism by which a new species is created, but
this is speciation at an already achieved level of evolu-
tionary complexity, a step that does not in itself lead to
progressive evolution.
Comparative genomics shows that in the long term,
a million or two years after WGD, carriers of paleop-
olyploid genomes have a chance to enter into a state of
“explosive” speciation (diversification) and give rise
to new large supraspecific taxa [3, 48, 119, 120]. This,
apparently, should be preceded by radical rearrange-
ments of the polyploid genome: diploidization of the
genome, its “fractionation,” and a decrease in the
number of chromosomes in the genome due to a series
of translocations (dysploidy) should occur [48, 119,
120]. In other words, speciation by creating new com-
binations of subgenomes and stabilization of the
genome in euploids, discussed in our article, and the
creation of new forms that give rise to new aromor-
phoses are two different directions of plant evolution.

RUSSIAN JOURNAL OF GENETICS Vol. 59 No. 5 2023
EUPOLYPLOIDY AS A MODE IN PLANT SPECIATION 427
FUNDING
This work was carried out within the framework of Rus-
sia n S cien c e Foun d atio n p roj ect n o. 2 2 -24 - 0 1117.
COMPLIANCE WITH ETHICAL STANDARDS
The author declares that he has no conflicts of interest.
This article does not contain the results of any studies
using animal or human subjects.
REFERENCES
1. Grant, V., Plant Speciation, New York: Columbia
Univ. Press, 1971.
2. Wood, T.E., Takebayashi, N., Barker, M.S., et al., The
frequency of polyploid speciation in vascular plants,
Proc. Natl Acad. Sci. U.S.A., 2009, vol. 106,
pp. 13875—13879.
https://doi.org/10.1073/pnas.0811575106
3. Van de Peer, Y., Mizrachi, E., and Marchal, K., The
evolutionary significance of polyploidy, Nat. Rev. Genet.,
2017, vol. 18, pp. 411—424.
https://doi.org/10.1038/nrg.2017.26
4. Liu, H., Wang, X., Wang, G., et al., The nearly com-
plete genome of Ginkgo biloba illuminates gymno-
sperm evolution, Nat. Plants, 2021, vol. 7, pp. 748—
756.
https://doi.org/10.1038/s41477-021-00933-x
5. Liu, Y., Wang, S., Li, L., et al., The Cycas genome and
the early evolution of seed plants, Nat. Plants, 2022,
vol. 8, pp. 389—401.
https://doi.org/10.1038/s41477-022-01129-7
6. Nishiyama, T., Sakayama, H., De Vries, J., et al., The
Chara genome: secondary complexity and implica-
tions for plant terrestrialization, Cell, 2018, vol. 174,
pp. 448—464.
https://doi.org/10.1016/j.cell.2018.06.033
7. Banks, J.A., Nishiyama, T., Hasebe, M., et al., The
Selaginella genome identifies genetic changes associat-
ed with the evolution of vascular plants, Science, 2011,
vol. 332, pp. 960—963.
https://doi.org/10.1126/science.1203810
8. Zhang, J., Fu, X.X., Li, R.Q., et al., The hornwort ge-
nome and early land plant evolution, Nat. Plants,
2020, vol. 6, pp. 107—118.
https://doi.org/10.1038/s41477-019-0588-4
9. Bowman, J.L., Kohchi, T., Yamato, K.T., et al., In-
sights into land plant evolution garnered from the
Marchantia polymorpha genome, Cell, 2 017, vol . 171,
pp. 287—304.
https://doi.org/10.1016/j.cell.2017.09.030
10. Szövényi, P., Gunadi, A., and Li, F.W., Charting the
genomic landscape of seed-free plants, Nat. Plants,
2021, vol. 7, pp. 554—565.
https://doi.org/10.1038/s41477-021-00888-z
11. Benton, M.J., Wilf, P., and Sauquet, H., The Angio-
sperm terrestrial revolution and the origins of modern
biodiversity, New Phytol., 2022, vol. 233, pp. 2017—
2035.
http s :// d oi . o r g/ 10 .1111/n p h.17 8 2 2
12. Barker, M.S., Arrigo, N., Baniaga, A.E., et al., On the
relative abundance of autopolyploids and allopoly-
ploids, New Phytol., 2016, vol. 210, pp. 391—398.
13. Doyle, J.J. and Sherman-Broyles, S., Double trouble:
taxonomy and definitions of polyploidy, New Phytol.,
2017, vol. 213, pp. 487—493.
http s :// d oi . o r g/ 10 .1111/n p h.14 2 7 6
14. Mayr, E., The biological species concept, Species Con-
cepts and Phylogenetic Theor y: A Debate, Wheeler, Q.D.
and Meier, R., Eds., New York: Columbia Univ. Press,
2000, pp. 17—29.
15. Ladizinsky, G., Studies in Oat Evolution: a Man’s Life
with Avena, Berlin: Springer-Verlag, 2012.
16. Komarov, V.L., Uchenie o vide u rastenii (stranitsa iz is-
torii biologii) (The Doctrine of the Species in Plants (a
Page from the History of Biology)), Moscow: Akad.
Nauk SSSR, 1940.
17. Tsvelev, N.N., The species as one of the taxa, Byull.
Mosk. O-va. Ispyt. Prir., Otd. Biol., 1995, vol. 100,
no. 5, pp. 62—68.
18. Levin, D.A., The long wait for hybrid sterility in flow-
ering plants, New Phytol., 2012, vol. 196, pp. 666—670.
19. Stebbins, G.L., Polyploidy and the distribution of the
arctic-alpine flora: new evidence and a new approach,
Bot. Helv., 1984, vol. 94, pp. 1—13.
20. Stebbins, G.L., The origin and success of polyploids in
the boreal circumpolar flora: a new analysis, Trans.
Bot. Sci. Edinburgh, 1986, vol. 45, pp. 17—31.
21. Liu, J., Moeller, M., Gao, L.-M., et al., DNA barcod-
ing for the discrimination of Eurasian yews (Tax us L,
Taxaceae) and the discovery of cryptic species, Mol.
Ecol. Resour., 2011, vol. 11, pp. 89—100.
h tt p s :/ / d oi . or g / 10 .1111 /j .17 5 5- 0 9 9 8. 2 01 0. 0 29 0 7. x
22. Bell, D., Long, D.G., Forrest, A.D., et al., DNA bar-
coding of European Herbertus (Marchantiopsida, Her-
bertaceae) and the discovery and description of a new
species, Mol. Ecol. Resour., 2012, vol. 12, pp. 36—47.
h tt p s :/ / d oi . or g / 10 .1111 /j .17 5 5- 0 9 9 8. 2 011. 0 3 05 3 .x
23. Gill, F.B., Species taxonomy of birds: which null hy-
pothesis? Auk, 2014, vol. 131, pp. 150—161.
https://do i.or g/10.16 42/AUK-13-206.1
24. Riesberg, L.H., Wood, T.E., and Baack, E.J., The na-
ture of plant species, Nature, 2006, vol. 440, pp. 524—
527.
https://doi.org/10.1038/nature04402
25. Shneyer, V.S. and Kotseruba, V.V., Cryptic species in
plants and their detection by genetic differentiation be-
tween populations, Ekol. Genet., 2014, vol. 12, no. 3,
pp. 12—26.
26. Soltis, D.E., Soltis, P.S., Schemske, D.W., et al., Au-
topolyploidy in angiosperms: have we grossly underes-
timated the number of species? Taxon, 2007, vol. 56,
pp. 13—30.
https://doi.org/10.2307/25065732
27. Shneyer, V.S., Punina, E.O., and Rodionov, A.V., In-
traspecif ic differences in ploidy and their taxonomic
interpretation, Bot. Zh., 2018, vol. 103, no. 5, pp. 555—
585.
https://doi.org/10.1134/S0006813618050010
28. Tsvelev, N.N., Genomic criteria for genera in higher
plants, Bot. Zh., 1991, vol. 76, no. 5, pp. 669—676.

428
RUSSIAN JOURNAL OF GENETICS Vol. 59 No. 5 2023
RODIONOV
29. Ramsey, J. and Schemske, D.W., Neopolyploidy in
flowering plants, Annu. Rev. Ecol. Syst., 2002, vol. 33,
pp. 589—639.
30. Li, Z., McKibben, M.T., Finch, G.S., et al., Patterns
and processes of diploidization in land plants, Annu.
Rev. Plant Biol., 2021, vol. 72, pp. 387—410.
https://doi.org/10.1146/annurev-arplant-050718-100344
31. Levin, D.A., Plant speciation in the age of climate
change, Ann. Bot., 2019, vol. 124, pp. 769—775.
https://doi.org/10.1093/aob/mcz108
32. Yu, Z., Haberer, G., Matthes, M., et al., Impact of
natural genetic variation on the transcriptome of auto-
tetraploid Arabidopsis thaliana, Proc. Natl Acad. Sci.
U. S. A., 2010, vol. 107, pp. 17809—17814.
https://doi.org/10.1073/pnas.1000852107
33. Liu, B. and Sun, G., Transcriptome and miRNAs
analyses enhance our understanding of the evolution-
ary advantages of polyploidy, Crit. Rev. Biotechnol.,
2019, vol. 39, pp. 173—180.
https://doi.org/10.1080/07388551.2018.1524824
34. Soltis, D.E., Misra, B.B., Shan, S., et al., Polyploidy
and the proteome, Biochim. Biophys. Acta, Proteins
Proteomics, 2016, vol. 1864, pp. 896—907.
https://doi.org/10.1016/j.bbapap.2016.03.010
35. Soltis, D.E., Visger, C.J., Marchant, D.B., and Soltis, P.S.,
Polyploidy: pitfalls and paths to a paradigm, Am. J.
Bot., 2016, vol. 103, pp. 1146—1166.
https://doi.org/10.3732/ajb.1500501
36. Rodionov, A.V., Shneyer, V.S., Gnutikov, A.A., et al.,
The dialectic of species: from initial uniformity,
through the greatest possible diversity to final unifor-
mity, Bot. Zh., 2020, vol. 105, no. 9, pp. 835—853.
https://doi.org/10.31857/S0006813620070091
37. Favarger, C., Sur l’emploi des nombres chromo-
somiques en géographie botanique historique, Ber.
Geobot. Inst. Rübel, 1961, vol. 32, pp. 119—146.
38. Mandáková, T., Joly, S., Krzywinski, M., et al., Fast
diploidization in close mesopolyploid relatives of Ara-
bidopsis, Plant Cell, 2010, vol. 22, pp. 2277—2290.
39. 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.
https://doi.org/10.1134/S1022795410120021
40. Rodionov, A.V., Amosova, A.V., Belyakov, E.A.,
et al., Genetic consequences of interspecific hybrid-
ization, its role in speciation and phenotypic diversity
of plants, Russ. J. Genet., 2019, vol. 55, no. 3, pp. 278—
294.
https://doi.org/10.1134/S1022795419030141
41. Zhan, S.H., Otto, S.P., and Barker, M.S., Broad vari-
ation in rates of polyploidy and dysploidy across flow-
ering plants is correlated with lineage diversification,
bioRxiv, 2021.
https://doi.org/10.1101/2021.03.30.436382
42. Navashin, M.S., Change in the number and morpho-
logical characteristics of chromosomes in interspecific
hybrids, Tr. Prikl. Bot., Genet. Sel., 1927, vol. 17, no. 3,
pp. 121—150.
43. Talbert, P.B., Bryson, T.D., and Henikoff, S., Adap-
tive evolution of centromere proteins in plants and an-
imals, J. Biol., 2004, vol. 3, no. 4, pp. 1—17.
https://doi.org/10.1186/jbiol11
44. Melters, D.P., Bradnam, K.R., Young, H.A., et al.,
Comparative analysis of tandem repeats from hun-
dreds of species reveals unique insights into cen-
tromere evolution, Genome Biol., 2013, vol. 14, no. 1,
pp. 1—20.
https://doi.org/10.1186/gb-2013-14-1-r10
45. Maheshwari, S., Tan, E.H., West, A., et al., Naturally
occurring differences in CENH3 affect chromosome
segregation in zygotic mitosis of hybrids, PLoS Genet.,
2015, vol. 11, no. 1, article number e1004970.
https://doi.org/10.1371/journal.pgen.1004970
46. Kotseruba, V., Gernand, D., Meister, A., and Hou-
ben, A., Uniparental loss of ribosomal DNA in the al-
lotetraploid grass Zingeria trichopoda (2n = 8), Ge-
nome, 2003, vol. 46, pp. 156—163.
https://doi.org/10.1139/g02-104
47. Marimuthu, M.P., Maruthachalam, R., Bondada, R.,
et al., Epigenetically mismatched parental cen-
tromeres trigger genome elimination in hybrids, Sci.
Adv., 2021, vol. 7, no. 47. eabk1151.
https://d oi.org/10.1126 /sciadv.abk1151
48. Mandáková, T. and Lysak, M.A., Post-polyploid dip-
loidization and diversification through dysploid
changes, Curr. Opinion Plant Biol., 2018, vol. 42,
pp. 55—65.
https://doi.org/10.1016/j.pbi.2018.03.001
49. Soares, N.R., Mollinari, M., Oliveira, G.K., et al.,
Meiosis in polyploids and implications for genetic
mapping: a review, Genes, 2021, vol. 12, p. 1517.
https://doi.org/10.339 0/genes12101517
50. Wang, M., Wang, P., Lin, M., et al., Evolutionary dy-
namics of 3D genome architecture following poly-
ploidization in cotton, Nat. Plants, 2018, vol. 4,
pp. 90—97.
https://doi.org/10.1038/s41477-017-0096-3
51. Concia, L., Veluchamy, A., Ramirez-Prado, J.S.,
et al., Wheat chromatin architecture is organized in
genome territories and transcription factories, Genome
Biol., 2020, vol. 21, no. 1.
https://doi.org/10.1186/s13059-020-01998-1
52. Barea, L., Redondo-Río, Á., Lucena-Marín, R.,
et al., Homologous chromosome associations in do-
mains before meiosis could facilitate chromosome rec-
ognition and pairing in wheat, Sci. Rep., 2022, vol. 12,
no. 1, pp. 1—11.
https://doi.org/10.1038/s41598-022-14843-1
53. International Wheat Genome Sequencing Consor-
tium, Shifting the limits in wheat research and breed-
ing using a fully annotated reference genome, Science,
2018, vol. 361, article number eaar7191.
54. Stein, J.C., Yu, Y., Copetti, D., et al., Genomes of 13
domesticated and wild rice relatives highlight genetic
conservation, turnover and innovation across the genus
Oryza, Nat. Genet., 2018, vol. 50, no. 2, pp. 285—296.
https://doi.org/10.1038/s41588-018-0040-0
55. Nei, M. and Rooney, A.P., Concerted and birth–
and–death evolution of multigene families, Annu. Rev.
Genet., 2005, vol. 39, pp. 121—152.
https://doi.org/0.1146/annurev.genet.39.073003.112240
56. Gonzalo, A., All ways lead to Rome—meiotic stabili-
zation can take many routes in nascent polyploid

RUSSIAN JOURNAL OF GENETICS Vol. 59 No. 5 2023
EUPOLYPLOIDY AS A MODE IN PLANT SPECIATION 429
plants, Genes, 2022, vol. 13, no. 1, p. 147.
https://doi.org/10.339 0/genes13010147
57. Viegas, W.S., Mello-Sampayo, T., Feldman, M., and
Avivi, L., Reduction of chromosome pairing by a
spontaneous mutation on chromosomal arm 5DL of
Triticum aestivum, Can. J. Genet. Cytol., 1980, vol. 22,
pp. 569—575.
https://doi.org/10.1139/g80-062
58. Svačina, R., Sourdille, P., Kopecký, D., and Bartoš, J.,
Chromosome pairing in polyploid grasses, Front. Plant
Sci., 2020, vol. 11, p. 1056.
https://doi.org/10.3389/fpls.2020.01056
59. Jenczewski, E. and Alix, K., From diploids to allopoly-
ploids: the emergence of efficient pairing control genes
in plants, Crit. Rev. Plant Sci., 2004, vol. 23, pp. 21—
45.
https://doi.org/10.1080/07352680490273239
60. Cuñado, N., Blazquez, S., Melchor, L., et al., Under-
standing the cytological diploidization mechanism of
polyploid wild wheats, Cytogenet. Genome Res., 2005,
vol. 109, pp. 205—209.
https://doi.org/10.1159/000082401
61. Tang, Z.X., Fu, S.L., Yan, B.J., et al., Unequal chro-
mosome division and inter-genomic translocation oc-
curred in somatic cells of wheat—rye allopolyploid, J.
Plant. Res., 2012, vol. 125, pp. 283—290. .
https://doi.org/10.1007/s10265-011-0432-z
62. Luo, J., Zhao, L., Zheng, J., et al., Karyotype mosa-
icism in early generation synthetic hexaploid wheats,
Genome, 2020, vol. 63, pp. 329—336.
https://doi.org/10.1139/gen-2019-0148
63. Gill, B.S. and Chen, P.D., Role of cytoplasm-specific
introgression in the evolution of the polyploid wheats,
Proc. Natl. Acad. Sci. U. S. A., 1987, vol. 84, no. 19,
pp. 6800—6804.
https://doi.org/10.1073/pnas.84.19.6800
64. Badaeva, E.D., Shelukhina, O.Y., Dedkova, O.S.,
et al., Comparative cytogenetic analysis of hexaploid
Avena L. species, Russ. J. Genet., 2011, vol. 47, no. 6,
pp. 783—795.
https://doi.org/10.1134/S1022795411060068
65. Amosova, A.V., Badaeva, E.D., Muravenko, O.V., and
Zelenin, A.V., An improved method of genomic in situ
hybridization (GISH) for distinguishing closely related
genomes of tetraploid and hexaploid wheat species,
Russ. J. Dev. Biol., 2009, vol. 40, no. 2, pp. 90—94.
https://doi.org/10.1134/S1062360409020040
66. Liu, Q., Lin, L., Zhou, X., et al., Unraveling the evo-
lutionary dynamics of ancient and recent polyploid-
ization events in Avena (Poaceae), Sci. Rep., 2017,
vol. 7, no. 1, pp. 1—13.
https://doi.org/10.1038/srep41944
67. Jellen, E.N., Gill, B.S., and Cox, T.S., Genomic in
situ hybridization differentiates between A/D- and C-
genome chromatin and detects intergenomic translo-
cations in polyploid oat species (genus Avena), Ge-
nome, 1994, vol. 37, pp. 613—618.
68. Lim, K.Y., Kovarik, A., Matyasek, R., et al., Sequence
of events leading to near-complete genome turnover in
allopolyploid Nicotiana within five million years, New
Phytol., 2007, vol. 175, pp. 756—763.
http s :// d oi . o r g/ 10 .1111/j .14 69 - 8137. 200 7.02121. x
69. Winterfeld, G., Schneider, J., Perner, K., and Röser, M.
Polyploidy and hybridization as main factors of specia-
tion: complex reticulate evolution within the grass ge-
nus Helictochloa, Cytogen. Genome Res., 2014, vol. 142,
pp. 204—225.
https://doi.org/10.1159/000361002
70. Suissa, J.S., Kinosian, S.P., Schafran, P.W., et al., Ho-
moploid hybrids, allopolyploids, and high ploidy levels
characterize the evolutionary history of a western
North American quillwort (Isoëtes) complex, Mol.
Phylogen. Evol., 2022, vol. 166, article number 107332.
https://doi.org/10.1016/j.ympev.2021
71. Sutherland, B.L. and Galloway, L.F., Postzygotic iso-
lation varies by ploidy level within a polyploid com-
plex, New Phytol., 2017, vol. 213, pp. 404—412.
72. Kamelin, R.V., Speciation in flowering plants, Tr.
Zool. Inst. Russ. Akad. Nauk, 2009, suppl. 1, pp. 141—
149.
73. Tsvelev, N.N. and Probatova, N.S., Zlaki Rosii (Grass-
es of Russia), Moscow: KMK, 2019.
74. Rice, A., Šmarda, P., Novosolov, M., et al., The global
biogeography of polyploid plants, Nat. Ecol. Evol.,
2019, vol. 3, pp. 265—273.
https://doi.org/10.1038/s41559-018-0787-9
75. Vaezi, J. and Brouillet, L., Origin of Symphyotrichum
anticostense (Asteraceae: Astereae), an endemic, high
polyploid species of the Gulf of St. Lawrence region,
based on morphological and nrDNA evidence, Bota-
ny, 2022.
https://doi.org/10.1139/cjb-2021-0145
76. Pellicer, J., Garcia, S., Garnatje, T., et al., Chromo-
some counts in Asian Artemisia L. (Asteraceae) spe-
cies: from diploids to the first report of the highest
polyploid in the genus, Bot. J. Linn. Soc., 2007,
vol. 153, pp. 301—310.
h tt p s :/ / d oi . or g / 10 .1111 / j. 10 9 5- 8 3 39 . 20 0 7. 0 0 611. x
77. Guggisberg, A., Mansion, G., Kelso, S., and Conti, E.,
Evolution of biogeographic patterns, ploidy levels, and
breeding systems in a diploid–polyploid species com-
plex of Primula, New Phytol., 2006, vol. 171, pp. 617—
632.
h tt p s :/ / d oi . or g / 10 .1111 /j .1 4 69 - 813 7. 20 0 6 . 017 22 . x
78. Kaur, H., Mubarik, N., Kumari, S., and Gupta, R.C.,
Chromosome numbers and basic chromosome num-
bers in monocotyledonous genera of the Western Hi-
malayas (India), Acta Biol. Cracov., Ser. Bot., 2014,
vol. 56, no. 2, pp. 9—19.
https://doi.org/10.2478/abcsb-2014-0016
79. Winterfeld, G., Schneider, J., Perner, K., and Röser, M.,
Origin of highly polyploid species: different pathways
of auto- and allopolyploidy in 12–18x species of Ave-
nula (Poaceae), Int. J. Plant Sci., 2012, vol. 173,
pp. 399—411.
https://doi.org/10.1086/664710
80. Hardion, L., Verlaque, R., Rosato, M., et al., Impact
of polyploidy on fertility variation of Mediterranean
Arundo L. (Poaceae), C. R. Biol., 2015, vol. 338,
pp. 298—306.
https://doi.org/10.1016/j.crvi.2015.03.013
81. Chumová, Z., Krejčíková, J., Mandáková, T., et al.,
Evolutionary and taxonomic implications of variation
in nuclear genome size: lesson from the grass genus

430
RUSSIAN JOURNAL OF GENETICS Vol. 59 No. 5 2023
RODIONOV
Anthoxanthum (Poaceae), PLoS One, 2015, vol. 10,
no. 7. p. e0133748.
https://doi.org/10.1371/journal.pone.0133748
82. Gould, F.W., Pollen size as related to polyploidy and
speciation in the Andropogon saccharoides—A. barbin-
odis complex, Brittonia, 1957, vol. 9, no. 2, pp. 71—75.
83. Hair, J.B. and Beuzenberg, E.J., High polyploidy in a
New Zealand Poa, Nature, 1961, vol. 189, pp. 160—
160.
84. Li, L.F., Zhang, Z.B., Wang, Z.H., et al., Genome se-
quences of the five Sitopsis species of Aegilops and the
origin of polyploid wheat B subgenome, Mol. Plant,
2022, vol. 15, pp. 488—503.
https://doi.org/10.1016/j.molp.2021.12.019
85. Levy, A.A. and Feldman, M., Evolution and origin of
bread wheat, Plant Cell, 2022, article number koac130.
https://doi.org/10.1093/plcell/koac130
86. Eilam, T., Anikster, Y., Millet, E., et al., Nuclear DNA
amount and genome downsizing in natural and syn-
thetic allopolyploids of the genera Aegilops and Triti-
cum, Genome, 2008, vol. 51, pp. 616—627.
https://doi.org/10.1139/G08-043
87. Kamal, N., Tsardakas Renhuldt, N., Bentzer, J., et al.,
The mosaic oat genome gives insights into a uniquely
healthy cereal crop, Nature, 2022, vol. 606, pp. 113—
119 .
https://doi.org/0.1038/s41586-022-04732-y
88. Löve, Á., Generic evolution of the wheat grasses, Biol.
Zentralbl., 1982, vol. 101, pp. 199—212.
89. Löve, Á., Conspectus of the Triticeae, Feddes Repert.,
1984, vol. 95, pp. 425—521.
90. Dewey, D.R., The genomic system of classification as
a guide to intergeneric hybridization with the perennial
Triticeae, in Gene Manipulation in Plant Improvement,
Boston, MA: Springer-Verlag, 1984, pp. 209—279.
91. Delaunay, L.N., Comparative karyological study of
Muscari Mill. and Bellevalia Lapeyr. species, Vestn. Ti-
fliss. Bot. Sada, 1922, vol. 2, no. 1, pp. 1—32.
92. Wang, R.R.-C., von Bothmer, R., Dvorak, J., et al.,
Genome symbols in the Triticeae (Poaceae), in Her-
barium Publications, Logan, Uta: Uta State Publ.,
1994, paper 20. https://digitalcommons.usu.edu/her-
barium_pubs/20.
93. Blattner, F.R., Taxonomy of the genus Hordeum and
barley (Hordeum vulgare), in The Barley Genome,
Cham: Springer-Verlag, 2018, pp. 11—23.
94. Baum, B.R., Estes, J.R., and Gupta, P.K., Assessment
of the genomic system of classification in the Triticeae,
Am. J. Bot., 1987, vol. 74, pp. 1388—1395.
95. Barkworth, M.E., Taxonomy of the Triticeae: a histor-
ical perspective, Hereditas, 1992, vol. 116, pp. 1—14.
96. Kamelin, R.V., Lektsii po sistematike rastenii: glavy te-
oreticheskoi sistematiki rastenii (Lectures on Plant Sys-
tematics: Chapters in Theoretical Plant Systematics),
Barnaul: Azbuka, 2004.
97. Yen, C., Yang, J.-L., Yen, Y., and Kihara, H., Áskell
Löve and the modern genetic concept of the genera in
the tribe Triticeae (Poaceae), J. Syst. Evol., 2005,
vol. 43, pp. 82—93.
98. Vavilov, N.I., The law of homologous series in varia-
tion, J. Genet., 1922, vol. 12, pp. 47—89.
99. Vavilov, N.I., Zakon gomologicheskikh ryadov v nasled-
stvennoi izmenchivosti (The Law of Homological Series
in Hereditary Variation), Moscow: Selkhozgiz, 1935.
100. Tsvelev, N.N., On the possibility of despecialization
by hybridogenesis on the example of the evolution of
the tribe Triticeae of the grass family (Poaceae), Zh.
Obshch. Biol., 1975, vol. 36, no. 1, pp. 90—99.
101. Kihara, H., Genom Analyse bei Triticum und Aegilops,
Cytologia, 1930, vol. 1, no. 3, pp. 263—284.
102. Tsvelev, N.N., Hybridization as one of the factors for
increasing biological diversity and a genomic criterion
for genera in higher plants, in Biologicheskoe raznoo-
brazie: podkhody k izucheniyu i sokhraneniyu (Biodi-
versity: Approaches to Study and Conservation), St.
Petersburg, 1992, pp. 193—201.
103. Simpson, G.G., Tempo and Mode in Evolution, New
York: Columbia Univ. Press, 1944.
104. Saarela, J.M., Bull, R.D., Paradis, M.J., et al., Molec-
ular phylogenetics of cool-season grasses in the sub-
tribes Agrostidinae, Anthoxanthinae, Aveninae,
Brizinae, Calothecinae, Koeleriinae and Phalaridinae
(Poaceae, Pooideae, Poeae, Poeae chloroplast group 1),
PhytoKeys, 2017, vol. 87, pp. 1—139.
https://doi.org/10.3897/ phytokeys.87.12774
105. Dauphin, B., Grant, J.R., Farrar, D.R., and Roth-
fels, C.J., Rapid allopolyploid radiation of moonwort
ferns (Botrychium; Ophioglossaceae) revealed by Pac-
Bio sequencing of homologous and homeologous nu-
clear regions, Mol. Phylogenet. Evol., 2018, vol. 120,
pp. 342—353.
https://doi.org/10.1016/j.ympev.2017.11.025
106. Schinkel, C.C., Kirchheimer, B., Dellinger, A.S.,
et al., Correlations of polyploidy and apomixis with el-
evation and associated environmental gradients in an
alpine plant, AoB Plants, 2016, vol. 8, pp. 1—16.
https://doi.org/10.1093/aobpla/plw064
107. Herben, T., Suda, J., and Klimešová, J., Polyploid
species rely on vegetative reproduction more than dip-
loids: a re-examination of the old hypothesis, Ann.
Bot., 2017, vol. 120, pp. 341—349.
https://doi.org/10.1093/aob/mcx009
108. Meudt, H.M., Albach, D.C., Tanentzap, A.J., et al.,
Polyploidy on islands: its emergence and importance
for diversification, Front. Plant Sci., 2021, vol. 12,
p. 637214.
https://doi.org/10.3389/fpls.2021.637214
109. Villa, S., Montagna, M., and Pierce, S., Endemism in
recently diverged angiosperms is associated with poly-
ploidy, Plant Ecol., 2022, vol. 223, pp. 479—492.
https://doi.org/10.1007/s11258-022-01223-y
110. Pécrix, Y., Rallo, G., Folzer, H., et al., Polyploidiza-
tion mechanisms: temperature environment can in-
duce diploid gamete formation in Rosa sp., J. Exp.
Bot., 2011, vol. 62, pp. 3587—3597.
https://doi.org/10.1093/jxb/err052
111. Klatt, S., Schinkel, C.C., Kirchheimer, B., et al., Ef-
fects of cold treatments on fitness and mode of repro-
duction in the diploid and polyploid alpine plant Ra-
nunculus kuepferi (Ranunculaceae), Ann. Bot., 2018,
vol. 121 , pp. 1287—1298.
112. Fox, D.T., Soltis, D.E., Soltis, P.S., et al., Polyploidy:
a biological force from cells to ecosystems, Trends Cell

RUSSIAN JOURNAL OF GENETICS Vol. 59 No. 5 2023
EUPOLYPLOIDY AS A MODE IN PLANT SPECIATION 431
Biol., 2020, vol. 30, pp. 688—694.
https://doi.org/10.1016/j.tcb.2020.0 6.006
113. Prentis, P.J., Wilson, J.R., Dormontt, E.E., et al.,
Adaptive evolution in invasive species, Trends Plant
Sci., 2008, vol. 13, pp. 288—294.
114. Brochmann, C., Brysting, A.K., Alsos, I.G., et al.,
Polyploidy in arctic plants, Biol. J. Linn. Soc., 2004,
vol. 82, pp. 521—536.
h tt p s :/ / d oi . or g / 10 .1111 /j .1 0 9 5- 8 312 . 2 00 4 . 0 03 37 .x
115. 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.
116. Clausen, J., Introgression facilitated by apomixis in
polyploid Poa, Euphytica, 1961, vol. 10, pp. 87—94.
https://doi.org/10.1007/BF00037208
117. Soltis, D.E., Visger, C.J., and Soltis, P.S., The poly-
ploidy revolution then… and now: Stebbins revisited,
Am. J. Bot., 2014, vol. 101, pp. 1057—1078.
https://doi.org/10.3732/ajb.1400178
118. Mayrose, I., Zhan, S.H., Rothfels, C.J., et al., Recent-
ly formed polyploid plants diversify at lower rates, Sci-
ence, 2011, vol. 333, p. 1257.
https://doi.org/10.1126/science.1207205
119. Schranz, M.E., Mohammadin, S., and Edger, P.P.,
Ancient whole genome duplications, novelty and di-
versification: the WGD Radiation Lag-Time Model,
Curr. Opin. Plant Biol., 2012, vol. 15, pp. 147—153.
https://doi.org/10.1016/j.pbi.2012.03.011
120. Wang, X., Morton, J.A., Pellicer, J., et al., Genome
downsizing after polyploidy: mechanisms, rates and
selection pressures, Plant J., 2021, vol. 107, pp. 1003—
1015.
http s :// d oi . o r g/ 10 .1111/t p j.153 6 3