Download The causes and molecular consequences of polyploidy in

1
The causes and molecular consequences of polyploidy in flowering plants
2
3
Short title: Plant polyploidy
4
5
Authors: Gaurav D. Moghe1,2, Shin-Han Shiu1,2,3,*
6
7
Affiliations:
8
1,2
9
State University, East Lansing, MI 48824, USA
10
Programs in Genetics and Quantitative Biology, 3 Department of Plant Biology, Michigan
* Corresponding author ([email protected])
11
12
Correspondence address:
13
2265 Molecular Plant Sciences Building., Dept. of Plant Biology, Michigan State University,
14
East Lansing, MI, 48824
15
Phone #: 517-353-7196
16
17
Keywords:
18
Whole genome duplication, plants, adaptation, expression divergence, fractionation, molecular
19
consequences of polyploidy
20
21
22
1
1
Abstract
2
Polyploidy is an important force shaping plant genomes. All flowering plants are descendants of
3
an ancestral polyploid species, and up to 70% of extant vascular plant species are believed to be
4
recent polyploids. Over the past century, a significant body of knowledge has accumulated
5
regarding the prevalence and ecology of polyploid plants. In this review, we summarize our
6
current understanding of the causes and molecular consequences of polyploidization in
7
angiosperms. We also provide a discussion on the relationships between polyploidy and
8
adaptation and suggest areas where further research may provide a better understanding of
9
polyploidy.
10
2
1
Introduction
2
Polyploidization results in multiplication of the genome and an increase in gene content
3
that frequently leads to morphological and physiological differences between polyploids and
4
their diploid progenitors1. Polyploidy is widespread among flowering plants2,3 and has been
5
postulated as an answer to "Darwin's abominable mystery" regarding the causes behind the rapid
6
acceleration in the diversification of angiosperms in earth's evolutionary history4,5. It is also a
7
major route for origination of new genes via gene duplication and subsequent diversification6,7.
8
Although we have a fairly good idea about the extent of polyploidy in eukaryotes 8–10 and the
9
modes of diversification of duplicate genes derived from polyploidy11, there is still a
10
considerable debate about whether polyploidy indeed confers an evolutionary advantage to the
11
organism and if yes, does it contribute to speciation? In addition, although the primary pathways
12
of polyploid generation have been known for some time12, only recently have we begun to
13
identify the molecular consequences of polyploidization.
14
In this review, we first focus on the genetic and environmental factors that influence the
15
rates of polyploidization. Second, we discuss the impact of polyploidization at the molecular
16
level. Third, we summarize recent studies on the impact of polyploidy on morphology,
17
physiology, and stress biology. Finally, we discuss current evidence on how polyploidy
18
contributes to adaptation and speciation. Our goal in this review is to present a brief overview of
19
our current state of understanding regarding a few different aspects of polyploidy. For additional
20
information, we refer the reader to several excellent resources2,3,13–17 that have covered these
21
topics in greater detail.
22
Causes of polyploidization in flowering plants
23
Cytological pathways leading to polyploidization
24
Diploids mostly propagate by producing haploid gametes, which combine to produce
25
diploid progeny (Figure 1A). In rare cases, polyploids can arise via the somatic doubling of
26
chromosomes in the zygote (Figure 1B) or through the production of unreduced gametes (Figure
27
1C-E). The primary mechanism for polyploid generation is thought to be via the latter12,18.
28
Theoretical models considering unreduced gamete formation and fertilities of plants with
29
different ploidy levels have been used to predict equilibrium ploidy frequencies19–21. Notably, to
30
fit the existing data on ploidy frequency observed in multiple autopolyploid species, the
3
1
unreduced gamete frequency was estimated to be 0.89%21. This high rate of unreduced gamete
2
production is consistent with its involvement in angiosperm polyploidy.
3
Unreduced gametes can be formed in three different ways: 1) pre-meiotic genome
4
doubling due to endoreplication mechanisms including endocycling (alternating periods of S
5
phase, where DNA is replicated, and gap phase, without cell division), endomitosis (mitosis
6
without the final cell division)22, or nuclear fusion, 2) via impairments in meiosis, which can
7
affect either the first or the second meiotic divisions and 3) via post-meiotic genome doubling12.
8
The unreduced gametes from diploids (2X, with X being the base chromosome number of the
9
species) can lead to a tetraploid (4X) in one step by hybridization between unreduced male and
10
female gametes (Type I pathway, Figure 1C,D) or through the creation of an intermediate
11
triploid (Type II pathway, Figure 1E)19. Given that unreduced gametes can be produced at an
12
appreciable frequency21, it is conceivable that unreduced gametes generated in two individuals,
13
or from the same individual (if selfing is feasible), may hybridize and generate polyploids
14
through the Type I pathway.
15
In the Type II pathway, an unreduced gamete hybridizes with a normal gamete to
16
produce triploid plants (3X). The triploid produces mostly aneuploid gametes, which are
17
generally not viable, and a small percentage of viable X, 2X or 3X gametes. These gametes can
18
then hybridize with other X, 2X or 3X gametes to generate plants of higher ploidy levels (Figure
19
1E). Hence, triploid plants are regarded as a "bridge" towards polyploidy (triploid bridge), rather
20
than a dead end (triploid block)12. Currently, it remains unclear which pathway is more
21
prevalent13. Although the production of 3X gametes required in the Type II pathway would be
22
rare in nature, unreduced gametes in artificially generated hybrids of multiple Brassica species
23
are produced at a much higher frequency than in their parents. These gametes have a size
24
distribution corresponding to >2X genome complement, and they are more viable than reduced
25
gametes in the Brassica hybrids. These results support the hypothesis that the triploid bridge
26
scenario may be more prevalent for polyploids generated from inter-specific hybridridization12.
27
Genetic components contributing to polyploidization
28
Several A. thaliana genes that can influence the frequency of unreduced gamete
29
formation have been identified23,24. For example, ~60% of the seeds produced from a mutated
30
version of the SWI1/DYAD protein are triploid25. SWI1/DYAD is required for a proper meiosis
31
I in both male and female germ cells. In the swi1/dyad mutant, cells skip the reduction division
4
1
in meiosis I and directly advance to the equatorial division in meiosis II, producing
2
predominantly unreduced gametes26,27. Mutations in several other genes lead to the production of
3
unreduced gametes by affecting different meiotic and mitotic steps. For example, mutations in
4
the GLUCAN SYNTHASE LIKE 8 protein, which lays down the glucan chains at cell plates
5
during cell division, lead to a flower containing both diploid and polyploid somatic cells. The
6
polyploid cells then go on to produce unreduced gametes28.
7
As discussed earlier, one important step in the pathway to polyploidy is the formation of
8
triploid intermediates. The major challenge upon forming this intermediate is the “triploid
9
block”, originally described as the difficulty in generating viable triploids through diploid-
10
tetraploid crosses29, which can lead to reproductive isolation of the newly formed polyploid due
11
to minority cytotype exclusion30. A recent study demonstrated that one genetic component of the
12
triploid block in A. thaliana is a paternally expressed gene ADMETOS31. The authors of this
13
study carried out a mutant screen in a jason mutant background, which produces unreduced
14
gametes at a high frequency but 30% of the triploid seeds produced are aborted. The admetos-1
15
jason double mutant, on the other hand, has only 2% aborted triploid seeds. The admetos-1
16
mutant is a gain-of-function mutant with elevated expression of the ADMETOS gene31. These
17
results suggest that there is genetic control over triploid formation. While such genetic control
18
may exist to create a post-zygotic reproductive barrier for gene flow between species, naturally
19
occurring variation in such control mechanisms may provide an opportunity for polyploids to be
20
generated.
21
Together with the finding that unreduced gamete formation is a trait with high heritability
22
(e.g. 0.40 to 0.60 in alfalfa and clover32,33), at least in domesticated crops experiencing artificial
23
selection, polyploid formation through unreduced gamete and triploid bridge formation is
24
expected to have a significant genetic component. Although these genetic studies are highly
25
informative, it remains unclear whether these newly identified genes are involved in increasing
26
or decreasing the rate of polyploid formation in nature. If these genes are the targets of selection
27
for polyploidization frequency, they may display substantial variation between plant species
28
and/or populations that have variable relative abundances of individuals with different ploidy
29
levels.
5
1
Relationship between environment and polyploidy
2
Nearly 80 years ago, it was demonstrated that a correlation exists between polyploidy and
3
latitudinal cline34, suggesting potential habitat differentiation between plants with different
4
ploidy levels due to the differences in latitudinal environment. Additionally, it was shown in
5
1920 that hot water treated Pisum root tips have increased frequency of tetraploidy in somatic
6
cells35. In 1932, Randolf demonstrated that high temperature (47-48°C) results in an increased
7
frequency of tetraploid embryos in maize36. Subsequently, a number of studies have established
8
that environmental stress, including temperature stress, herbivory, pathogen attack, nutritional
9
stress and water stress, lead to an elevated rate of unreduced gamete production12.
10
In addition to observations linking environmental stress, polyploidy and unreduced
11
gamete production, a large number of studies have focused on how environment influences
12
chromosome behavior and unreduced gamete production18. Although unreduced gametes can be
13
produced due to pre-meiotic, meiotic, or post-meiotic aberrations, recent studies have shown that
14
environmentally induced production of unreduced pollen is mainly due to meiotic irregularities,
15
particularly during telophase II. In Rosa species, the proportion of unreduced pollen produced
16
due to elevated temperature (36°C) differs greatly at different microspore stages37. The elevated
17
temperature led to formation of normal rose pollen tetrads as well as abnormal dyads, triads, and
18
polyads as a result of mis-orientation of meiotic spindles.
19
Although similarly affected during telophase II, the formation of A. thaliana unreduced
20
pollen due to cold shock (4-5°C) is not due to defects in spindle fibers attached to the
21
chromosomes but mainly due to abnormalities in equatorial cell plate formation as a result of
22
misplaced microtubules28. Because the aberration in cell plate formation occurs during telophase
23
II, the cell plate separating homologous chromosomes is in place but the one separating sister
24
chromatids is defective. Therefore, instead of forming pollen tetrads (1X), 2X dyads are formed,
25
each containing two sets of exactly identical chromosomes. It is not clear if the differences in
26
the mechanistic details (spindles vs. cell plate formation) are due to the differences in the type of
27
stress applied or due to differences between species.
28
In this section, we reviewed studies focused on finding the genetic and environmental
29
causes of polyploidization, most of which act by affecting mitosis or meiosis thus producing
30
unreduced gametes. A polyploid, once created, has to establish itself, and the process of
31
neopolyploid establishment continues in the backdrop of molecular and physiological changes
6
1
occurring due to genome duplication (and merging two different genomes in allopolyploids) that
2
a neopolyploid has to go through1. In the remainder of the review, we focus on the impact of
3
polyploidy on genome content, on gene expression, on morphology and finally on adaptation.
4
Impact of polyploidy on genome content
5
Changes in genome organization
6
Polyploids have a tendency to return to a diploidized state over time, experiencing
7
changes in chromosomes organization, gene order, expression, epigenetic modification, and
8
biological network topology (Figures 2-4), a phenomenon known as diploidization38.
9
Diploidization may begin with large scale changes in the genome of neopolyploid plants such as
10
abnormal chromosome segregation, rearrangement, and breakage39,40 and may occur in a
11
haphazard manner in the initial few decades after polyploidization41 (Figure 2A,B). For example,
12
in synthetic allotetraploids between double haploid Brassica oleracea (C genome) and B. rapa
13
(A genome), chromosomal segregation aberrations lead to extensive aneuploidy as early as the
14
first generation, when the aneuploidy rate is 24%. This rate rises to 95% in the 11th generation42.
15
Despite the high rate of aneuploidy, the number of homeologs for a particular chromosome is
16
frequently maintained at four copies; i.e. the loss of chromosome 1 from the A genome is usually
17
associated with gain of the same chromosome from the C genome and vice versa. This
18
compensating aneuploidy suggests a dosage balance requirement at least in the early generations.
19
Compensating aneuploidy also occurs in the naturally occurring allotetraploid Tragopogon
20
miscellus, wherein 85% of aneuploid plants were found to have the expected chromosome
21
number43. Chromosomal losses in early generations have also been reported for synthetic
22
allohexaploids (Triticum aestivum44, Brassica carinata x B. rapa44, A. thaliana x A. suecica45) as
23
well as in autopolyploid potato46, alfalfa and corn47. Recently, the cause of such chromosomal
24
losses, which occur due to meiotic instabilities, was tracked down to a single quantitative trait
25
locus called BOY NAMED SUE (BYS) in synthetic allopolyploids of A. thaliana x A. arenosa48.
26
The authors speculate that the BYS locus may play a role in A. suecica, which is a naturally
27
occurring allopolyploid of A. thaliana x A. arenosa, in ensuring that homeologous chromosomes
28
don't pair with each other, a process that may lead to chromosomal dosage irregularities in the
29
progeny48.
7
1
In addition to changes in chromosome numbers, newly generated polyploids display an
2
elevated rate of genome rearrangements leading to loss of chromosomal fragments (Figure 2A).
3
By tracking a limited number of markers, synthetic autotetraploids of Paspalum notatum49 and
4
Elymus elongatus50 were shown to lose ~10% of genome sequence in the first generation. In
5
Phlox drumondii, up to 25% reduction in parental DNA content was observed as early as the
6
third generation50. On the contrary, studies in synthetic A. thaliana autopolyploids reveal little to
7
no loss51. These observations suggest that genome rearrangement can be prominent in allo- and
8
some auto-polyploids.
9
Gene duplicate loss and retention
10
Polyploidization initially results in multiplication of gene content, however, the
11
predominant fate of gene duplicates is loss52. Studies of newly sequenced genomes shed light on
12
the extent of gene loss in species which underwent polyploidization events several million years
13
ago (MYA). In the A. thaliana genome, only 17% of duplicates were retained after a
14
paleopolyplodization (β) event took place ~50 MYA53. In the paleopolyploid Glycine max, two
15
rounds of whole genome duplications took place ~59 and ~13 MYA54. In the homologous genes
16
from the more recent duplication event, 56.6% of duplicates are no longer detectable, compared
17
to 74.1% genes lost after the older Glycine polyploidization. Thus the rates of gene loss are 4.4%
18
and 1.3% per million years for the younger and the older duplication event, respectively,
19
indicating that gene loss rate is high initially but slows down over time54. In Brassica rapa and
20
Raphanus raphanistrum, which experienced genome triplication ~25 MYA55–57, assuming the
21
ancestral gene number prior to triplication was similar to that in A. thaliana (~30,000), the
22
number of extant B. rapa genes (~41,000) and R. raphanistrum genes (~38,000) indicates that as
23
many as 55% of the genes derived from genome triplication were lost58,59.
24
The process of loss of polyploidy-derived genes is referred to as “fractionation”, a
25
collection of mutational mechanisms leading to the removal of duplicates derived from
26
polyploidization60,61 (Figure 2B). Studies of gene collinearity between duplicate regions in A.
27
thaliana62, Z. mays63 and B. rapa64 suggest a bias in the genes lost from certain parental
28
genomes. In B. rapa, one of the three subgenomes experienced significantly fewer gene losses
29
than the others58,65. This phenomenon is also reflected at the expression level, where genes
30
located on one subgenome tend to have higher expression than others, indicating genome
31
dominance66. The duplicated gene copy producing the most RNA molecules appears to be the
8
1
one retained63. It has recently been suggested that transposon silencing due to small RNAs may
2
contribute to the phenomenon of genome dominance, with the parental genome having the
3
lowest proportion of transposons being the more dominant66. Fractionation of genes also leads to
4
preferential gene retention, which has been reviewed recently61. Retained duplicates derived
5
from polyploidization have a number of distinguishing characteristics compared to genes that
6
remain single copy, including biased gene function67,68, higher gene complexity (number of
7
exons and protein domains)69,70, higher levels of gene expression71, significant parental genome
8
dominance63,72 and higher network connectivity62. Duplicate genes playing a role in stress
9
response, development, signaling and transcriptional regulation tend to be retained, a feature
10
consistent across multiple polyploidization events and time scales59,70.
11
Why are duplicates with these types of characteristics retained? Retained duplicates may
12
experience a brief period of complete functional redundancy, but eventually obtain new
13
functions6, and/or partition ancestral functions leading to subfunctionalization73. In addition to
14
these mechanisms, the retention of duplicate genes may be due to balanced gene drive/gene
15
balance74,75, functional buffering69, dosage selection76 and escape from adaptive conflict77
16
(reviewed by Innan and Kondrashov11 and Edger and Pires78). Among the mechanisms
17
explaining duplicate retention, some imply adaptive evolution (e.g. neofunctionalization, dosage
18
selection) while the others require the need for purifying selection to maintain the ancestral
19
functions (e.g. subfunctionalization, dosage balance). Examples of adaptive duplication are
20
accumulating but it remains unclear what fraction of gene duplicates was fixed due to adaptive
21
evolution79.
22
Mutation and transposable element activities
23
Because more than one gene copy is present, increased ploidy can mask the effect of
24
deleterious mutations80. Meanwhile, the newly formed polyploid species has a very small
25
effective population size, assuming postzygotic isolation from its parental diploids. In this
26
situation, genetic drift is expected to play a more dominant role in polyploid evolution. Therefore
27
the selective pressure against any mutation in polyploid genomes would be more relaxed; leading
28
to increased frequencies of otherwise deleterious alleles. Although it is not clear whether the
29
spontaneous mutation rate is higher in polyploids compared to diploids, there is generally a
30
higher mutation density in mutagenized polyploids compared to diploids81. Because this pattern
31
is similar between natural and synthetic polyploids, and because the mutations tend to exist in
9
1
heterozygous states, the elevated mutation density is likely a consequence of masking recessive
2
deleterious mutations81. In a comparison between wheat Triticum aestivum, which experienced
3
recent whole genome duplication, and three other non-duplicated grass species, there are more
4
non-synonymous substitutions, gene structural rearrangements, and alternative splice forms of
5
genes in wheat82, suggesting relaxed selection on deleterious alleles.
6
The elevated mutation rate in polyploids can also be due to elevated transposable element
7
activities83,84. The proliferation of transposons in polyploids is expected due to reduced
8
population size, masked deleterious transposon insertion, and/or conflict in transposition
9
repressors due to genome merger84 (Figure 2C). Despite this expectation, current studies present
10
conflicting results regarding whether proliferation of transposons is correlated with
11
polyploidy83,84. For example, the numbers of transposons in the Au short interspersed nuclear
12
element (SINE) family in natural polyploid wheat species are significantly higher than those in
13
diploids85, although it is difficult to ascertain whether the difference observed is due to
14
polyploidy, hybridization, and/or lineage divergence. Additionally, one of three synthetic
15
allopolyploids has higher number of Au SINEs by the fourth generation85. In this case, it remains
16
unclear whether genome doubling or hybridization contributes to the higher number of Au SINEs
17
observed.
18
Studies on the activities of transposons in autopolyploids are also contradictory. In A.
19
thaliana synthetic autotetraploids, activation of Sunfish, a DNA transposon, was observed39. On
20
the other hand, a study assaying naturally occurring autotetraploid A. arenosa accessions found
21
evidence for purifying selection against expansion of Ac-III transposon family86. In addition to
22
the possibility of transposon proliferation, transposons may be involved in recombination events
23
leading to sequence losses in polyploid genomes87–89. For example, illegitimate recombination
24
mediated by TE elements was shown to underlie the variation observed between diploid and
25
polyploid wheat species in the Hardness locus90. Such transposon-mediated recombination can
26
also contribute to differential expansion and contraction of subgenomes as shown in maize91.
27
10
1
Impact of polyploidy on gene expression and biological network
2
Expression divergence between homeologs
3
In addition to experiencing widespread changes at the DNA level, polyploids have
4
considerable differences in gene expression compared to diploids, and this has been reviewed
5
extensively92–96. Divergence in the expression states of duplicated genes may lead to the
6
following outcomes: they may gain new expression states (neo-functionalization6), partition their
7
ancestral functions (sub-functionalization73) or lose their expression state completely leading to
8
eventual pseudogenization52. In A. thaliana, 57% and 75% of the duplicates derived from the
9
more recent α and the older β polyploidization events were found to have diverged in
10
expression67. It was also found that whole genome duplicates tend to diverge in expression at a
11
slower rate than tandem duplicates, presumably because entire intergenic regions are duplicated
12
during polyploidization, but only a fraction might end up being duplicated during tandem
13
duplication due to the random nature of DNA breakage and recombination97.
14
In allopolyploids, the combination of gene sets in two species is expected to create a
15
“transcriptome shock”, defined as abrupt and rapid changes in patterns of parental gene
16
expression in the polyploid98. Through a number of intriguing studies in the past decade or so,
17
several basic features have emerged regarding homeolog expression in allopolyploids. The
18
transcriptome shock contributes to significant differences in expression levels between
19
homeologs in allopolyploids, albeit to varying extents94, and the corresponding genes in diploid
20
parents have been documented in Arabidopsis99, B. napus100, and cotton101. But a recent study
21
also shows that in wheat synthetic polyploids fewer than 1% of genes show non-additive
22
expression102. In addition, concerns on how non-additivity is defined in polyploids have been
23
raised103. Nonetheless, analysis of non-additive patterns of expression in allopolyploid
24
homeologs has lead to the discovery of two related phenomena, “homeolog expression bias" and
25
"expression level dominance"104 (Figure 3A).
26
Homeolog expression bias takes place when one homeolog tends to have significantly
27
reduced level of expression or is silenced altogether in the allopolyploid105. For example, in the
28
first RNA-sequencing study examining expression bias in cotton polyploids, 59-62% and 48% of
29
genes are differentially expressed when comparing diploids against the natural and synthetic
30
polyploids, respectively106. It was found that genes from a particular subgenome were expressed
11
1
in allopolyploids, and the nature of the subgenome differed in the natural alopolyploid vs.
2
synthetic allopolyploid106.
3
distinguishing homeolog origins, only 0.71-0.75% of genes have no detectable expression in
4
synthetic polyploids. Given that the cotton allopolyploidization event took place 1-2 MYA107,
5
there may have been insufficient time for gene loss and/or the expression of pseudogenized
6
copies are still detectable. Related to homeolog expression bias, expression level dominance
7
(originally called genomic dominance) describes a situation where the sum of expression levels
8
of a homeologous gene pair tends to be more similar to that in one parent, regardless of the
9
expression level of the gene in the parent in question104,108. These phenomena have been well-
10
documented in multiple natural and synthetic allopolyploids. The cause of expression biases may
11
be partially attributed to cis and trans regulatory differences between the hybridized genomes109
12
and epigenetic regulation, which is discussed in a later section.
13
Contribution of hybridization and genome doubling to transcriptome shock
Interestingly, among over 25,000 cotton genes containing SNPs
14
In addition to homeolog expression bias and expression level dominance, another focus is
15
on the relative contribution of genome doubling and hybridization to non-additive expression in
16
allopolyploids. Through comparisons of hybrid diploids, synthetic allopolyploids, and
17
neopolyploids (particularly Senecio and Tragopogon species, which formed in the past 100
18
years110,111), the effect of hybridization as well as genome doubling on gene expression changes
19
has been quantified, and these studies suggest that hybridization likely plays a more dominant
20
role. For example, only 88 genes are differentially expressed between A. thaliana diploid and
21
synthetic isogenic autotetraploids, compared to >1,700 genes with significantly different
22
expression levels between synthetic allotetraploid A. thaliana x A. arenosa and the average of
23
two parents112. In a study of diploid, autotetraploid, and autohexaploid Helianthus decapetalus,
24
ploidy level does not contribute significantly to expression differences113. Similarly in Senecio,
25
twice as many genes in S. x baxteri, a triploid hybrid between S. vulgaris (2n=4x) and S.
26
squalidus (2n=2x), are differentially expressed compared to the parental species than in a
27
synthetic allohexaploid derived from the triploid S. x baxteri98. Interestingly, genome doubling in
28
fact ameliorates the effect of hybridization in Senecio98, a finding that is also reported in
29
neopolyploid Spartina114. Thus the non-additive gene expression changes in these allopolyploids
30
is likely due to inter-specific hybridization and not simply genome doubling.
12
1
Although hybridization seems to play a dominant role, studies in cotton, Spartina, and
2
domesticated rice subspecies suggest the contribution of genome doubling may be important. In
3
the natural polyploid cotton, among assayed genes with expression bias toward one parental
4
diploid, only 25% are biased in the same direction as the diploid hybrid101, suggesting the
5
expression bias in the remaining 75% is due to genome doubling. However, allopolyploid cotton
6
was established ~1-2 MYA. Thus one cannot rule of the possibility that the expression bias is
7
due to regulatory variation that accumulated in the past 1-2 million years. In Spartina, the
8
allopolyploid tends to have a higher number of transgressively over-expressed genes compared
9
to species hybrid114, again suggesting a prominent role of genome doubling. Nonetheless, given
10
that the parental Spartina species are hexaploids, it remains unclear if the findings are applicable
11
to comparisons between lower ploidy levels. On the other extreme, genome doubling seems to
12
have a more prominent role in transcriptome shock than hybridization in a comparison between a
13
hybrid of Oryza sativa subsp. indica and japonica and synthetic tetraploid rice109. But given that
14
there has been repeated hybridization between japonica and indica115, it remains unclear how
15
hybridization may have impacted the findings.
16
Involvement of epigenetic modifications and small RNAs in transcriptome shock
17
Transcriptome shock results in non-additive gene expression and silencing of homeologs.
18
In allopolyploids, trans factors and cis regulatory components from two genetic backgrounds can
19
interact due to the hybridization between two genomes, contributing to changes in gene
20
expression between polyploids and their diploid progenitors116,117. In addition, epigenetic factors
21
including DNA methylation, histone modifications, and small RNA have been implicated in
22
modulating gene expression in allpolyploids66,116,118–122. Extensive DNA methylation changes
23
have been reported between allopolyploids and their parents in Brassica napus123, wheat124,
24
Spartina anglica88,125 and Arabidopsis126 (Figure 3B). Inconsistent with the above observations,
25
the synthetic allopolyploid Cucumis hystrix x sativus has approximately the same methylation
26
density compared to the parents or the F1 hybrids127.
27
The direct involvement of DNA methylation in expression changes between homeologs
28
has also been demonstrated. In the natural allotetraploid A. suecica, the transcription factor TCP3
29
was silenced when chemical inhibitors of DNA methyltransferases were applied105, suggesting
30
methylation is important for proper TCP3 expression. Another line of evidence comes from
31
methyltransferase 1 (MET1) RNA interference (RNAi) lines in the A. suecica background128.
13
1
Notably, only 200 genes were found to be differentially expressed between A. suecica wildtype
2
plants and MET1 RNAi lines and only 34 of these 200 genes overlap with the ~1400 genes with
3
expression changes in synthetic tetraploids between A. thaliana and A. arenosa (the presumed
4
diploid parents of A. suecica)112. In addition, 33 of the 200 differentially expressed genes in
5
MET1 RNAi lines are pseudogenes or transposons128. Thus, MET1 mediated DNA methylation
6
differences between diploids and polyploids appear to be more relevant to controlling
7
heterochromatic states than to contributing to transcriptome shock. Nonetheless, the DNA
8
methylation machinery is complex129 and more loss-of-function studies will be necessary for a
9
more complete picture of the influence of DNA methylation on transcriptome shock.
10
Similar to DNA methylation, there are indications that histone modifications likely play a
11
significant role in transcriptome shock. Using diploids derived from transgenic autotetraploid A.
12
thaliana containing epialleles that either silence or allow the expression of a resistance gene
13
marker130, a screen for mutants releasing the silencing effect of the epiallele resulted in
14
identification of loss-of-function alleles in DECREASE IN DNA METHYLATION1 (DDM1) and
15
HOMOLOGOUS GENE SILENCING1 (HOG1)131. Global changes in both DNA and histone
16
methylation in the mutant background likely contribute to silencing release. Although the
17
epiallele action appears to be tied to the ploidy level130, it remains to be determined whether the
18
mutations in DDM1 and/or HOG1 contribute to similar phenomenon in a polyploidy
19
background. In addition to histone methylation, histone acetylation is implicated in transcriptome
20
shock based on studies of a histone deacetylase (ATHD1/ATHDA19) mutant132. Genes
21
differentially regulated between wildtype and athd1/athda19 mutants overlap significantly with
22
genes differentially expressed between synthetic allopolyploid Arabidopsis and the diploid
23
parents.
24
In addition to DNA methylation and histone modifications, the expression profiles of
25
small RNAs including both micro RNA and small interfering (both repeat-associated and trans-
26
acting) RNAs are affected post-polyploidization (Figure 3C). Such changes have been
27
documented in resynthesized allotetraploids of A. thaliana x arenosa133 and Ae. tauschii x
28
Triticum turgidum134. As with DNA methylation and histone modification, mutants in genes
29
controlling small RNA biogenesis have been used to study the impact of small RNA on
30
transcription and other phenotypic changes associated with polyploidy. RNAi lines interfering
31
with the expression of DICER LIKE-1 and ARGONAUTE 1, both involved in small RNA
14
1
biogenesis, have been created135. Similar to the DNA methylation machinery, the complexity of
2
epigenetic regulatory machineries in plants is well appreciated136. Additional loss-of-function
3
studies in polyploids will be highly informative. In addition to their effect on transcription, as
4
discussed earlier, small RNAs may contribute to the phenomenon of genome dominance66. Aside
5
from transcriptional regulatory mechanisms, a recent study examining ribosome associated
6
transcripts in the recently formed (∼100,000 years ago) allotetraploid G. dolichocarpa indicated
7
that transcripts subject to translational regulation tend to be retained homeologs from an ancient
8
whole genome duplication event137. It will be interesting to perform similar experiments in the
9
diploid parents and F1s to assess the impact of genome doubling and genome merger on
10
translational regulation.
11
Perturbations of biological networks due to polyploidy
12
Preferential retention and loss of genes, coupled with extensive transcriptional and
13
genomic changes post-polyploidy, necessarily leads to alterations in the molecular networks
14
operating in the organism (Figure 4). The network level changes in turn are expected to affect the
15
phenotype of the organism. Such phenotypic impact has been reviewed recently using flowering
16
time as an example120. While most retention/loss events may be random, there is evidence for
17
preferential retention/loss of certain types of genes. According to the "gene balance hypothesis",
18
the random loss of genes can result in a perturbation of stoichiometric relationships between
19
gene products, leading to genomic imbalance in a newly created polyploid and loss of fitness138.
20
Hence, neopolyploid lineages which happen to retain certain types of genes may be able to better
21
establish themselves.
22
There is a growing body of literature discussing the functional evolution of gene
23
duplicates derived from whole genome duplication76,138,139. For example, studies in B. rapa show
24
that genes involved in circadian rhythm such as CIRCADIAN CLOCK ASSOCIATED 1 and
25
LATE ELONGATED HYPOCOTYL were preferentially retained post polyploidization, leading to
26
an altered flowering time pathway140. Such preferential retention was also found in A. thaliana
27
genes duplicated in the α polyploidization event 50-65 MYA related to specific metabolic
28
pathways141 as well as MADS-box genes involved in various aspects of plant development142. In
29
poplar, two duplicate
30
paleopolyploidization event are expressed at different times of the year and have distinct roles in
31
influencing
flowering
genes
time
FLOWERING
and
vegetative
LOCUS T1
growth143.
and
T2
derived from
Sub-functionalization
of
a
two
15
1
polyploidization derived phytochrome (PHY) genes in maize – PHY B1 and B2 - where the two
2
proteins have both overlapping and unique functions in seedlings and adult plants, is also
3
known144.
4
Most of our understanding of the impact of polyploidy on biological network evolution
5
comes from budding yeast, Saccharomyces cerevisiae, which underwent a polyploidization event
6
~100 MYA145. This polyploidization event was associated with a large scale rewiring of the
7
transcriptional network via changes in cis-regulatory motif usage, which led to the evolution of
8
facultatively anaerobic post-polyploidization species whereas several pre-polyploidization
9
species are aerobic146. It was also found that despite 100 million years of evolution, genetic
10
redundancy may still exist between several pairs of duplicated genes, although there is evidence
11
of significant partitioning of ancestral functions and gain of new functions between these
12
pairs147.
13
Impact of polyploidy on morphology and physiology
14
Morphological alterations
15
Some fundamental commonalities in morphology and physiology are found among
16
polyploid species, however, the specific outcomes of a particular polyploidization event can vary
17
widely between taxa (reviewed in Levin, 2002148). Anatomically, polyploids have larger cell
18
volumes, stomatal guard cells, pollen, and seeds compared to diploids. Polyploids also have
19
broader and thicker leaves with fewer stems per plant (reviewed in Otto and Whitton, 2000149).
20
Such changes may affect processes such as water relations, gas exchange, cold tolerance and
21
shade tolerance of polyploid plants1. Some phenotypic modifications may occur due to increased
22
DNA content in the nucleus and a need to maintain a particular nuclear-to-cytoplasmic volume
23
ratio, while other changes may be induced by genome restructuring and regulatory and network
24
level modifications. For example, in a synthetic autotetraploid line of A. thaliana, larger aerial
25
organs compared to the diploid are a result of faster expansion rates and a longer expansion
26
duration during cell division. Such behavior is due to up-regulation of cyclin dependent kinases
27
in tetraploids compared to diploids150.
28
Polyploidization is also expected to impact the morphology of the reproductive system by
29
affecting the size of the flower, relative sizes of petals, the spatial relationships between different
30
floral organs as well as flowering time of the plant151. These changes can influence pollinator
16
1
preferences. In addition to morphological changes in reproductive structure, polyploidy may lead
2
to the breakdown of self-incompatibility. In the Solanaceae family, polyploid species are
3
significantly more likely to be self-compatible than diploid species152. A broader study of 235
4
angiosperm species also found a significant association between polyploidy and selfing153.
5
However, a study on self-sterility data from 1266 angiosperm species contrasting self-
6
compatible, self-incompatible, and mix-mating groups found that polyploid species did not tend
7
to be more self-compatible compared to diploids154. If the results of the latter study are true,
8
there may be a short-term breakdown of self-incompatability in the neopolyploids enabling it to
9
establish its population154, after which self-compatibility gets established again. Alternatively,
10
other features associated with the mating system such as inflorescence size, floral display,
11
pollinator behaviour may minimize the effect of reproductive isolation due to polyploidization in
12
neopolyploids. Nonetheless, one issue with the 1266 species study is that phylogenetic
13
relationships are not considered154, although there is non-random association between phylogeny
14
and mating system. In addition, the selfing rate was binned into three broad categories. On the
15
other hand, the 235 species study considered species phylogeny and modeled selfing rate as a
16
continuous variable despite a smaller sample size153. Thus the lack of correlation between
17
polyploidy and selfing rate in the 1266 species study can be due to confounding factors of
18
phylogenetic relations and selfing rate binning.
19
Physiological changes and stress tolerance
20
Polyploidy significantly influences photosynthesis (reviewed in Warner and Edwards,
21
1993155), and this effect is particularly obvious under stress conditions. In greenhouse grown
22
Betula papyrifer, water stress treatment leads to a complete cessation of photosynthesis in
23
diploids but not in penta- and hexapolyploids. Such behavior can be partly attributed to earlier
24
stomata closure in diploids156. But it remains unclear if the photosynthetic activities under water
25
deficit in polyploid is advantageous because it would contribute to carbon fixation even under
26
stress or whether it is detrimental due to water loss. Under excess light, the capacity for photo-
27
protection and non-photosynthetic electron transport are higher in the natural allotetraploid G.
28
dolichocarpa than in its diploid progenitors157. This enhanced photo-protection appears
29
beneficial because the allotetraploid is reported to photobleach later than its diploid progenitors.
30
Because of the prevalence of polyploid plants and the perceived broader ecological
31
tolerance (reviewed in Otto and Whitton 2000149), one potential physiological consequence of
17
1
polyploidy is its increased tolerance to environmental stress. However, the degree of
2
environmental stress tolerance does not necessarily correlate with cytotypes (see Maherali et al,
3
2009158 and references therein). Taking drought tolerance as an example, in a comparison
4
between the fireweed Chamerion angustifolium diploid and tetraploids (both natural and
5
synthetic) in a controlled environment, the natural tetraploids took 20-30% longer to wilt
6
compared to both diploid and synthetic tetraploids158, consistent with the higher xylem hydraulic
7
conductivity observed in natural tetraploids. However, the vulnerability of stems to drought-
8
induced cavitation was similar among C. angustifolium cytotypes. In field grown tetraploid and
9
hexaploid Atriplex canescens159, the leaf-specific hydraulic conductivity as well as susceptibility
10
to cavitation was lower in plants with higher ploidy levels. The inconsistency between earlier
11
studies and the two recent ones highlighted above can be attributed to, for example, differences
12
in whether the studies were conducted in controlled or natural environments, how physiological
13
measurements were taken, and how and when the polyploids were established.
14
Polyploids are also hypothesized to be more resistant to pathogens160. Mathematical
15
models of interactions between pathogens and either diploids or neopolyploids have shown that
16
newly formed polyploid populations of hosts are expected to be more resistant161. However,
17
similar to studies of the relationships between polyploidy and abiotic stress tolerance, the few
18
empirical studies conducted so far have generated mixed results162,163. For plant-insect
19
interactions, the autotetrapolid gooseberry-leaf alumroot Heuchera grossulariifolia is more likely
20
to be attacked by the specialist moth herbivore Greya politella than diploids164. In another field
21
study of the resistance of H. grossulariifolia to three moth species G. politella, G. piperella, and
22
Eupithecia misturata was tested165. Interestingly, G. piperella tends to attack and lay eggs on
23
diploids, suggesting herbivore species may provide selective pressure differently due to
24
differences in ploidy levels. Nonetheless, it remains unclear whether there are additional genetic
25
differences independent from polyploidy that contribute to the difference.
26
27
Polyploidy and adaptation
28
Survival in adverse environments
29
The question of whether polyploidization contributes to the long-term evolutionary
30
success of plant species has been raised repeatedly since Stebbins166. There are already a number
18
1
of excellent reviews on this topic17,149,167,168, thus, in this section, we focus on providing a
2
summary of earlier findings and a discussion of some recent results.
3
Polyploids are more frequent at higher elevations, higher latitudes and may be more
4
tolerant to dry conditions38,158,169, suggesting a fitness advantage for polyploids under those
5
environments. The timing of multiple polyploidization events in angiosperms coincides with the
6
timing of the creation of the Cretaceous-Tertiary boundary170. This coincidence has led to the
7
hypothesis that species with genome doubling could adapt better to the changing environment
8
than their diploid relatives during the mass extinction event. However, considering the influence
9
of environmental factors on unreduced gamete formation, it is also possible that the intense
10
climatic changes during the mass extinction event may have increased the frequency of
11
unreduced gamete formation, creating polyploids at a faster rate than normal. In addition,
12
polyploids were found to be more successful in colonizing the Arctic after deglaciation than
13
diploids169. A study sampling 640 endangered and 81 invasive species worldwide has led to the
14
conclusion that endangered species tend to be diploids while invasive species tend to be
15
polyploids, suggesting that polyploidization may increase tolerance to diverse ecological
16
conditions171. It has also been shown that polyploid A. thaliana accessions are more tolerant to
17
and have better reproductive success under high salinity compared to diploid cytotypes172. It will
18
be particularly interesting to determine if such high salinity adaptation can also be observed
19
under field conditions.
20
Not all findings support the notion that polyploids tend to survive better in adverse
21
environments. A 1940 study of 100 polyploid and diploid plant species found no correlation
22
between polyploidy and winter hardiness173. More recently, in a study of two diploid and one
23
polyploid species from each of 144 North American plant genera, no association was found
24
between ploidy level and species range area, minimum/maximum temperature, precipitation, or
25
latitudes174. Furthermore, as discussed in the previous section, physiological changes associated
26
with polyploidy do not necessarily confer superior tolerance and/or resistance to abiotic and
27
biotic factors. These observations suggest that the relationship between polyploidy and
28
adaptation is quite complex and may depend on not only the species undergoing polyploidization
29
but also the environment.
19
1
Local adaptation
2
In addition to the meta-analyses discussed above, multiple studies provide specific
3
examples of adaptation that are potentially due to polyploidy. In H. grossulariifolia, pollinators
4
visit tetraploid individuals more often than diploid ones175. Similarly in the fireweed C.
5
angustifolium, where populations ranges of polyploid and diploid varieties overlap, tetraploids
6
have a disproportionately higher number of bee visits and a greater pollen siring advantage
7
compared to diploids176,177. The invasiveness of allotetraploid cordgrass Spartina anglica may
8
indicate a fitness increase due to polyploidy, however, this is more likely a consequence of
9
heterosis than genome doubling178.
10
In wild yarrow Achillea borealis, which has hexaploid and tetraploid populations
11
occupying nearby but different environments, there is clear evidence of local adaptation, and
12
polyploidization is likely the initial trigger for diversification and adaptation to a new habitat179.
13
Consistent with this notion, the evolvability of the neo-autotetraploid C. angustifolium is higher
14
than both diploid and established autotetraploids, suggesting that genome doubling, without
15
hybridization, may initially alter evolutionary rate and contribute to adaptive evolution180. In
16
addition, reciprocal transplant experiments demonstrated that C. angustifolium diploids and
17
tetraploids survived best at their native elevations181. Overall, these observations suggest that
18
polyploidization may have positive fitness consequences and can lead to adaptation to local or
19
regional environments.
20
Species richness
21
Polyploidy leads to instantaneous reproductive isolation of polyploid individuals through
22
the phenomenon of minority cytotype exclusion1,30, but such individuals also possess a greater
23
capacity for functional innovation. If polyploids in general have better fitness compared to
24
diploids, the speciation rate of polyploids may be higher than that of diploids. Multiple
25
observations suggest a positive association between species richness and percent polyploid
26
species in different plant clades7,149,182. Additionally, a large number of species in major plant
27
families such as Poaceae183, Asteraceae184, Brassicaceae57 and the subfamily Papilionoideae185
28
have descended from a polyploid ancestor, suggesting a possible increase in diversification rates
29
post-polyploidization. Overall, it has been estimated that a significant proportion - ~15% of
30
angiosperm and ~31% of fern speciation events - may have been accompanied by ploidy
31
increase186. On the contrary, some other studies provide conflicting results. One study arrived at
20
1
the conclusion that polyploids tend to have lower diversification rates than diploids and have a
2
greater chance of extinction187. It has also been estimated that only 2-4% of polyploidization
3
events in angiosperms have actually resulted in speciation149. In addition, analyses of genome
4
sequences of flowering plants suggests that the difference in the estimated timing between
5
successive detectable paleopolyploidization events is ~10-30 million years in flowering plant
6
lineages5. Thus, considering the abundance of polyploids among flowering plants, most of the
7
polyploidization events were not recorded in the genomes of extant species. The inference is that
8
most of these polyploids have gone extinct.
9
These observations suggest two possibilities - either a majority of the polyploid lineages
10
indeed go extinct, making them "evolutionary dead ends"166, or they hybridize with their parental
11
species, creating lineages of mixed ploidy. It seems that both of these scenarios might occur in
12
nature. Hybridization between polyploids and their diploid ancestors has been reported in natural
13
populations of multiple species such as C. angustifolium188, species of the genus Epidendrum189
14
and Jacobaea190 and several others191, in regions known as hybrid zones191. Mathematical
15
simulations on whether a triploid hybrid between an autotetraploid and a diploid can help a
16
tetraploid population to establish suggest that even partially fit triploids can assist in long-term
17
tetraploid fixation19. Thus, polyploidization may not necessarily be an "evolutionary dead end"
18
but may create interesting possibilities for further innovation in the lineage.
19
20
Conclusions
21
In this article, we highlight the findings that the formation of a polyploid is associated
22
with extensive changes at the genomic, epigenetic, transcriptional and network levels. These
23
genomic, transcriptomic, and other omic changes must have contributed to morphological,
24
physiological, and ecological “phenotype” differences between polyploids and their diploid
25
progenitors. However, the exact molecular changes responsible for the phenotypic differences
26
between cytotypes remain unclear in most cases. Also, we have a relatively better understanding
27
of the molecular and phenotypic consequences of allopolyploidy than autopolyploidy, and
28
studies comparing and contrasting mechanisms of molecular evolution in these two forms of
29
polyploidy are lacking. For example, it is not clear whether the rate of neo- and sub-
30
functionalization and pseudogenization differ between auto and allopolyploids, given the
31
homeologs in allopolyploids are already slightly divergent from each other. Also, given the
21
1
extent of functional redundancy is higher in autopolyploids, do mutations have a stronger
2
deleterious effects in allopolyploids than autopolyploids? Additional research would be needed
3
to address these questions.
4
In a review by Soltis et al13, a number of intriguing questions are raised regarding what
5
we still don’t know about polyploidy. To expand on the long list, one challenge lies in
6
establishing the genetic basis in cases where polyploids are shown to be successful. Among the
7
unknowns, one particularly challenging question is whether polyploids are more successful than
8
their diploid progenitors13. A related question is under what ecological situations is polyploidy
9
adaptive. Theoretical considerations as well as empirical evidence have provided contradictory
10
answers to these two questions so far17,149,166–168. Nevertheless, the second question is more
11
tractable as it does not require any generalizations and can be examined experimentally on a
12
species-by-species basis. Polyploidy is an extreme form of duplication and can be seen as a
13
mutation mechanism. Considering the nearly neutral theory of molecular evolution 192, the null
14
hypothesis is that the effect of polyploidy is neutral or nearly neutral. In this framework, we can
15
test under what situations, e.g. different abiotic/biotic environments, the null hypothesis can be
16
rejected.
17
Taking C. angustifolium as an example, diploid and tetraploid varieties show significant
18
differences in drought tolerance158. Given the understanding of drought tolerance in model
19
plants193,194, a targeted survey of candidate gene transcription in field conditions can potentially
20
be informative. The optimal timing for the assay is not trivial to determine and molecular
21
changes other than transcription can be more important. In addition, drought tolerance may not
22
be the main environmental factor, highlighting the need to assess potentially relevant
23
abiotic/biotic factors in controlled environments in addition to the field. Nonetheless, a candidate
24
gene approach is a reasonable starting point. In case the candidate gene approach does not bear
25
fruit, because sampling the "omes" – genomes, transcriptomes, proteomes, or metabolomes – of
26
“non-model” species is no longer a rate limiting step, a global study of molecular changes may
27
provide viable hypotheses for further testing. These considerations are not unique to C.
28
angustifolium but other polyploid study systems as well. We surmise that good experimental
29
designs incorporating both molecular and ecological considerations of polyploids have the
30
potential to make the most impact in the near future.
31
22
1
2
Competing interests
No competing interests exist
3
4
Acknowledgements
5
We would like to thank the two anonymous reviewers as well as the editor for providing us
6
critical feedback on the manuscript. SHS is supported by National Science Foundation grants
7
DEB-0919452 and IOS-1126998.
8
Figure and table legends
9
10
Figure 1: Pathways of tetraploid formation from diploid plants. The symbol X represents the
11
base chromosome number of the species, with 1X corresponding to haploid gametes. (A) The
12
normal pathway wherein a diploid is produced as F1 progeny of two diploid parents. (B) Somatic
13
doubling leading to tetraploid (4X) generation from diploid. (C) Fusion of unreduced gametes
14
can lead to tetraploid generation in one step. (D) A diploid produced in F1 may generate a certain
15
proportion of aneuploid gametes (AP, most of which are not viable) and unreduced gametes that
16
can lead to tetraploid generation in F2. The frequency of unreduced gamete formation can be
17
high if the parents belong to different species and F1 is a hybrid. (E) The triploid bridge scenario
18
where an intermediate triploid produces unreduced gametes leading to generation of tetraploids
19
and individuals of higher ploidy. These pathways of tetraploid formation have been adapted from
20
information presented in Ramsey and Schemske, 1998. For example polypoids formed via each
21
pathway, as well as pathways of formation of polyploids of higher ploidy levels, please refer to
22
the original publication.
23
24
Figure 2: Genomic consequences of polyploidy. (A) P1: Parent 1, P2: Parent 2. Some possible
25
scenarios with respect to genomic rearrangements such as chromosome loss, chromosomal
26
translocation and chromosome fragment loss have been depicted in a simplified manner using
27
only two chromosomes. (B) The process of gene loss in a parent-of-origin manner, termed
28
fractionation. In the depicted scenario, the chromosomal copy from P2 loses most of the genes.
29
(C) Proliferation of transposable elements over time. Such proliferation may lead to changes in
30
gene order, gene function and gene expression.
23
1
2
Figure 3: Effects of polyploidy on gene expression and epigenetic regulation (A) A
3
hypothetical scenario depicted expression divergence upon polyploidization. P1: Parent 1, P2:
4
Parent 2. In “Homeolog expression bias”, the homeologous genes are expressed in a parent-of-
5
origin manner. In “Expression level dominance”, the sum of the expression level of both the
6
genes is similar to that in one parent. (B) A gene which is silenced by DNA methylation in the
7
parent is demethylated upon polyploidization or hybridization, leading to its transcription by
8
RNA polymerase. (C) A gene with a repressor bound to its promoter region is not expressed in
9
the parent but upon polyploidization is expressed as the repressor is removed due to regulation
10
by small RNAs transcribed elsewhere in the genome.
11
12
Figure 4: Effect of polyploidy on gene networks P1: Parent 1, P2: Parent 2. An example of two
13
genes - Gene 1 and Gene 2 - in parents P1 and P2 is shown. Each square represents a genetic or
14
physical interaction of Gene 1 or Gene 2. After polyploidization, over the course of several
15
generations, the network topology begins to evolve. If both the homeologous copies do not
16
undergo gene loss via deletion or pseudogenization and are retained, divergence between them
17
will lead to eventual sub-functionalization or neo-functionalization between duplicates, changing
18
the network topology and possibly, network function.
24
1
References
2
3
4
1.
Ramsey J., Schemske D.W. 2002. Neopolyploidy in Flowering Plants. Annu. Rev. Ecol.
Syst. 33: 589–639.
5
6
2.
Tate J.A., Soltis P.S., Soltis D.E. 2005. Chapter 7 - Polyploidy in Plants. In T. Ryan
Gregory. ed; The Evolution of the Genome. Academic Press. p 371–426.
7
8
9
3.
Husband B.C., Baldwin S.J., Suda J. 2013. The Incidence of Polyploidy in Natural Plant
Populations: Major Patterns and Evolutionary Processes. In Leitch IJ,Greilhuber
J,Dolezel J,et al. ed; Plant Genome Diversity Volume 2. Springer Vienna. p 255–276.
10
11
4.
Friedman W.E. 2009. The meaning of Darwin’s “abominable mystery.”Am. J. Bot. 96: 5–
21.
12
13
5.
Jiao Y., Wickett N.J., Ayyampalayam S., Chanderbali A.S., et al. 2011. Ancestral
polyploidy in seed plants and angiosperms. Nature 473: 97–100.
14
6.
Ohno S. 1970. Evolution by gene duplication. New York: Springer-Verlag.
15
16
7.
Soltis D.E., Albert V.A., Leebens-Mack J., Bell C.D., et al. 2009. Polyploidy and
angiosperm diversification. Am. J. Bot. 96: 336–348.
17
18
8.
Gregory R., Mable B. 2005. Chapter 8 – Polyploidy in Animals. In The Evolution of the
Genome. Elsevier Academic Press.
19
20
9.
Albertin W., Marullo P. 2012. Polyploidy in fungi: evolution after whole-genome
duplication. Proc. R. Soc. B 279: 2497–2509.
21
22
10.
Soppa J. 2013. Evolutionary advantages of polyploidy in halophilic archaea. Biochem.
Soc. Trans. 41: 339–343.
23
24
11.
Innan H., Kondrashov F. 2010. The evolution of gene duplications: classifying and
distinguishing between models. Nat. Rev. Genet. 11: 97–108.
25
26
12.
Ramsey J., Schemske D.W. 1998. Pathways, mechanisms, and rates of polyploid
formation in flowering plants. Annu. Rev. Ecol. Syst. 29: 467–501.
27
28
13.
Soltis D.E., Buggs R.J.A., Doyle J.J., Soltis P.S. 2010. What we still don’t know about
polyploidy. Taxon 59: 1387–1403.
29
14.
Soltis D.E., Soltis P.S. 2012. Polyploidy and Genome Evolution. New York: Springer.
30
31
15.
Leitch I.J., Greilhuber J., Dolezel J., Wendel J. 2013. Plant Genome Diversity Volume 2 Physical Structure, Behaviour and Evolution of Plant Genomes. Vienna: Springer-Verlag.
25
1
2
3
16.
Stöck M., Lamatsch D.K. 2013. Trends in Polyploidy Research in Animals and Plants:
Reprint Of: Cytogenetic and Genome Research 2013, Vol. 140, Issues 2-4. Basel: S.
Karger.
4
5
17.
Madlung A. 2013. Polyploidy and its effect on evolutionary success: old questions
revisited with new tools. Heredity 110: 99–104.
6
7
8
18.
Bretagnolle F., Thompson J.D. 1995. Tansley Review No. 78. Gametes with the stomatic
chromosome number: Mechanisms of their formation and role in the evolution of
autopolypoid plants. New Phytol. 129: 1–22.
9
10
19.
Husband B.C. 2004. The role of triploid hybrids in the evolutionary dynamics of mixedploidy populations. Biol. J. Linn. Soc. 82: 537–546.
11
12
20.
Yamauchi A., Hosokawa A., Nagata H., Shimoda M. 2004. Triploid bridge and role of
parthenogenesis in the evolution of autopolyploidy. Am. Nat. 164: 101–112.
13
14
21.
Suda J., Herben T. 2013. Ploidy frequencies in plants with ploidy heterogeneity: fitting a
general gametic model to empirical population data. Proc. R. Soc. B 280: 20122387.
15
16
22.
Fox D.T., Duronio R.J. 2013. Endoreplication and polyploidy: insights into development
and disease. Development 140: 3–12.
17
18
23.
Brownfield L., Köhler C. 2011. Unreduced gamete formation in plants: mechanisms and
prospects. J. Exp. Bot. 62: 1659–1668.
19
20
24.
De Storme N., Geelen D. 2013. Sexual polyploidization in plants--cytological mechanisms
and molecular regulation. New Phytol. 198: 670–684.
21
22
25.
Ravi M., Marimuthu M.P.A., Siddiqi I. 2008. Gamete formation without meiosis in
Arabidopsis. Nature 451: 1121–1124.
23
24
26.
Siddiqi I., Ganesh G., Grossniklaus U., Subbiah V. 2000. The dyad gene is required for
progression through female meiosis in Arabidopsis. Development 127: 197–207.
25
26
27
27.
Mercier R., Vezon D., Bullier E., Motamayor J.C., et al. 2001. SWITCH1 (SWI1): a novel
protein required for the establishment of sister chromatid cohesion and for bivalent
formation at meiosis. Genes Dev. 15: 1859–1871.
28
29
30
28.
De Storme N., Copenhaver G.P., Geelen D. 2012. Production of diploid male gametes in
Arabidopsis by cold-induced destabilization of post-meiotic radial microtubule arrays.
Plant Physiol. 160: 1808–1826.
31
32
29.
Marks G.E. 1966. The origin and significance of intraspecific polyploidy: Experimental
evidence from Solanum chacoense. Evolution 20: 552–557.
33
34
30.
Levin D.A. 1975. Minority Cytotype Exclusion in Local Plant Populations. Taxon 24: 35–
43.
26
1
2
31.
Kradolfer D., Wolff P., Jiang H., Siretskiy A., et al. 2013. An imprinted gene underlies
postzygotic reproductive isolation in Arabidopsis thaliana. Dev. Cell 26: 525–535.
3
4
32.
Parrott W.A., Smith R.R. 1986. Recurrent selection for 2n pollen formation in red clover.
Crop Sci. 26: 1132–1135.
5
6
33.
Tavoletti S., Mariani A., Veronesi F. 1991. Phenotypic recurrent selection for 2n pollen
and 2n egg production in diploid alfalfa. Euphytica 57: 97–102.
7
8
34.
Tischler G. 1935. Die Bedeutung der Polyploidie für die Verbreitung der Angiospermen.
Bot. Jahrbucher 76: 1–36.
9
10
11
35.
Sakamura T. 1920. Experimentelle studien über die Zell und Kerntcilung, mit besonderer
Rücksicht auf Form, Grösse und Zahl dei Chromosomen. J Coll Sci Imp Univ Tokyo 39:
221.
12
13
36.
Randolph L.F. 1932. Some Effects of High Temperature on Polyploidy and Other
Variations in Maize. Proc. Natl. Acad. Sci. U. S. A. 18: 222–229.
14
15
16
37.
Pécrix Y., Rallo G., Folzer H., Cigna M., et al. 2011. Polyploidization mechanisms:
temperature environment can induce diploid gamete formation in Rosa sp. J. Exp. Bot. 62:
3587–3597.
17
38.
Grant V. 1981. Plant Speciation. Columbia University Press.
18
19
39.
Madlung A., Tyagi A.P., Watson B., Jiang H., et al. 2005. Genomic changes in synthetic
Arabidopsis polyploids. Plant J. 41: 221–230.
20
21
22
40.
Gaeta R.T., Pires J.C., Iniguez-Luy F., Leon E., et al. 2007. Genomic changes in
resynthesized Brassica napus and their effect on gene expression and phenotype. Plant
Cell 19: 3403–3417.
23
24
25
41.
Buggs R.J.A., Doust A.N., Tate J.A., Koh J., et al. 2009. Gene loss and silencing in
Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids.
Heredity 103: 73–81.
26
27
28
42.
Xiong Z., Gaeta R.T., Pires J.C. 2011. Homoeologous shuffling and chromosome
compensation maintain genome balance in resynthesized allopolyploid Brassica napus.
Proc. Natl. Acad. Sci. U. S. A. 108: 7908–7913.
29
30
31
43.
Chester M., Gallagher J.P., Symonds V.V., Cruz da Silva A.V., et al. 2012. Extensive
chromosomal variation in a recently formed natural allopolyploid species, Tragopogon
miscellus (Asteraceae). Proc. Natl. Acad. Sci. U. S. A. 109: 1176–1181.
32
33
34
44.
Mestiri I., Chagué V., Tanguy A.-M., Huneau C., et al. 2010. Newly synthesized wheat
allohexaploids display progenitor-dependent meiotic stability and aneuploidy but
structural genomic additivity. New Phytol. 186: 86–101.
27
1
2
3
45.
Matsushita S.C., Tyagi A.P., Thornton G.M., Pires J.C., et al. 2012. Allopolyploidization
lays the foundation for evolution of distinct populations: evidence from analysis of
synthetic Arabidopsis allohexaploids. Genetics 191: 535–547.
4
46.
Lamm R. 1945. Cytogenetic studies in Solanum, sect. Tuberarium. Hereditas 31: 1–129.
5
6
47.
Shaver D.L. 1962. A study of aneuploidy in autotetraploid maize. Can. J. Genet. Cytol. 4:
226–233.
7
8
9
48.
Henry I.M., Dilkes B.P., Tyagi A., Gao J., et al. 2014. The BOY NAMED SUE
quantitative trait locus confers increased meiotic stability to an adapted natural
allopolyploid of Arabidopsis. Plant Cell 26: 181–194.
10
11
49.
Martelotto L.G., Ortiz J.P.A., Stein J., Espinoza F., et al. 2007. Genome rearrangements
derived from autopolyploidization in Paspalum sp. Plant Sci. 172: 970–977.
12
13
14
50.
Eilam T., Anikster Y., Millet E., Manisterski J., et al. 2009. Genome size in natural and
synthetic autopolyploids and in a natural segmental allopolyploid of several Triticeae
species. Genome 52: 275–285.
15
16
51.
Ozkan H., Tuna M., Galbraith D.W. 2006. No DNA loss in autotetraploids of Arabidopsis
thaliana. Plant Breed. 125: 288–291.
17
18
52.
Li W.H., Gojobori T., Nei M. 1981. Pseudogenes as a paradigm of neutral evolution.
Nature 292: 237–239.
19
20
53.
Blanc G., Hokamp K., Wolfe K.H. 2003. A recent polyploidy superimposed on older
large-scale duplications in the Arabidopsis genome. Genome Res. 13: 137–144.
21
22
54.
Schmutz J., Cannon S.B., Schlueter J., Ma J., et al. 2010. Genome sequence of the
palaeopolyploid soybean. Nature 463: 178–183.
23
24
25
55.
Yang Y.W., Lai K.N., Tai P.Y., Li W.H. 1999. Rates of nucleotide substitution in
angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and
other angiosperm lineages. J. Mol. Evol. 48: 597–604.
26
27
28
56.
Town C.D., Cheung F., Maiti R., Crabtree J., et al. 2006. Comparative genomics of
Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal
after polyploidy. Plant Cell 18: 1348–1359.
29
30
31
57.
Beilstein M.A., Nagalingum N.S., Clements M.D., Manchester S.R., et al. 2010. Dated
molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc. Natl.
Acad. Sci. U. S. A. 107: 18724–18728.
32
33
58.
Wang X., Wang H., Wang J., Sun R., et al. 2011. The genome of the mesopolyploid crop
species Brassica rapa. Nat. Genet. 43: 1035–1039.
28
1
2
3
59.
Moghe G.D., Hufnagel D.E., Tang H., Xiao Y., et al.Consequences of whole genome
triplication as revealed by comparative genomic analyses of the wild radish Raphanus
raphanistrum and three other Brassicaceae species. Plant Cell in press
4
5
60.
Langham R.J., Walsh J., Dunn M., Ko C., et al. 2004. Genomic duplication, fractionation
and the origin of regulatory novelty. Genetics 166: 935–945.
6
7
8
61.
Freeling M. 2009. Bias in plant gene content following different sorts of duplication:
tandem, whole-genome, segmental, or by transposition. Annu. Rev. Plant Biol. 60: 433–
453.
9
10
11
62.
Thomas B.C., Pedersen B., Freeling M. 2006. Following tetraploidy in an Arabidopsis
ancestor, genes were removed preferentially from one homeolog leaving clusters enriched
in dose-sensitive genes. Genome Res. 16: 934–946.
12
13
14
63.
Schnable J.C., Springer N.M., Freeling M. 2011. Differentiation of the maize subgenomes
by genome dominance and both ancient and ongoing gene loss. Proc. Natl. Acad. Sci. U.
S. A. 108: 4069–4074.
15
16
64.
Cheng F., Wu J., Fang L., Sun S., et al. 2012. Biased gene fractionation and dominant
gene expression among the subgenomes of Brassica rapa. PLoS ONE 7: e36442.
17
18
19
65.
Tang H., Woodhouse M.R., Cheng F., Schnable J.C., et al. 2012. Altered patterns of
fractionation and exon deletions in Brassica rapa support a two-step model of
paleohexaploidy. Genetics 190: 1563–1574.
20
21
22
66.
Woodhouse M.R., Cheng F., Pires J.C., Lisch D., et al. 2014. Origin, inheritance, and gene
regulatory consequences of genome dominance in polyploids. Proc. Natl. Acad. Sci. U. S.
A. 111: 5283–5288.
23
24
67.
Blanc G., Wolfe K.H. 2004. Functional divergence of duplicated genes formed by
polyploidy during Arabidopsis evolution. Plant Cell 16: 1679–1691.
25
26
27
68.
Hanada K., Zou C., Lehti-Shiu M.D., Shinozaki K., et al. 2008. Importance of lineagespecific expansion of plant tandem duplicates in the adaptive response to environmental
stimuli. Plant Physiol. 148: 993–1003.
28
29
30
69.
Chapman B.A., Bowers J.E., Feltus F.A., Paterson A.H. 2006. Buffering of crucial
functions by paleologous duplicated genes may contribute cyclicality to angiosperm
genome duplication. Proc. Natl. Acad. Sci. U. S. A. 103: 2730–2735.
31
32
33
70.
Jiang W.K., Liu Y.L., Xia E.H., Gao L.Z. 2013. Prevalent role of gene features in
determining evolutionary fates of whole-genome duplication duplicated genes in
flowering plants. Plant Physiol. 161: 1844–1861.
34
35
71.
Pál C., Papp B., Hurst L.D. 2001. Highly expressed genes in yeast evolve slowly. Genetics
158: 927–931.
29
1
2
3
72.
Chang P.L., Dilkes B.P., McMahon M., Comai L., et al. 2010. Homoeolog-specific
retention and use in allotetraploid Arabidopsis suecica depends on parent of origin and
network partners. Genome Biol. 11: R125.
4
5
73.
Force A., Lynch M., Pickett F.B., Amores A., et al. 1999. Preservation of duplicate genes
by complementary, degenerative mutations. Genetics 151: 1531–1545.
6
7
74.
Freeling M., Thomas B.C. 2006. Gene-balanced duplications, like tetraploidy, provide
predictable drive to increase morphological complexity. Genome Res. 16: 805–814.
8
9
75.
Birchler J.A., Veitia R.A. 2007. The Gene Balance Hypothesis: From classical genetics to
modern genomics. Plant Cell 19: 395–402.
10
11
76.
Conant G.C., Wolfe K.H. 2008. Turning a hobby into a job: how duplicated genes find
new functions. Nat. Rev. Genet. 9: 938–950.
12
13
77.
Des Marais D.L., Rausher M.D. 2008. Escape from adaptive conflict after duplication in
an anthocyanin pathway gene. Nature 454: 762–765.
14
15
78.
Edger P.P., Pires J.C. 2009. Gene and genome duplications: the impact of dosagesensitivity on the fate of nuclear genes. Chromosome Res. 17: 699–717.
16
17
79.
Kondrashov F.A. 2012. Gene duplication as a mechanism of genomic adaptation to a
changing environment. Proc R Soc B 279: 5048–5057.
18
80.
Haldane J.B.S. 1932. The Causes of Evolution. Princeton University Press.
19
20
81.
Tsai H., Missirian V., Ngo K.J., Tran R.K., et al. 2013. Production of a high-efficiency
TILLING population through polyploidization. Plant Physiol. 161: 1604–1614.
21
22
23
82.
Akhunov E.D., Sehgal S., Liang H., Wang S., et al. 2013. Comparative analysis of
syntenic genes in grass genomes reveals accelerated rates of gene structure and coding
sequence evolution in polyploid wheat. Plant Physiol. 161: 252–265.
24
25
83.
Parisod C., Alix K., Just J., Petit M., et al. 2010. Impact of transposable elements on the
organization and function of allopolyploid genomes. New Phytol. 186: 37–45.
26
27
28
84.
Parisod C., Senerchia N. 2012. Responses of Transposable Elements to Polyploidy. In
Grandbastien MA,Casacuberta JM. ed; Plant Transposable Elements. Springer Berlin
Heidelberg. p 147–168.
29
30
31
85.
Ben-David S., Yaakov B., Kashkush K. 2013. Genome-wide analysis of short interspersed
nuclear elements SINES revealed high sequence conservation, gene association and
retrotranspositional activity in wheat. Plant J. 76: 201–210.
32
33
34
86.
Hazzouri K.M., Mohajer A., Dejak S.I., Otto S.P., et al. 2008. Contrasting patterns of
transposable-element insertion polymorphism and nucleotide diversity in autotetraploid
and allotetraploid Arabidopsis species. Genetics 179: 581–592.
30
1
2
3
87.
Beaulieu J., Jean M., Belzile F. 2009. The allotetraploid Arabidopsis thaliana-Arabidopsis
lyrata subsp. petraea as an alternative model system for the study of polyploidy in plants.
Mol. Genet. Genomics 281: 421–435.
4
5
6
88.
Parisod C., Salmon A., Zerjal T., Tenaillon M., et al. 2009. Rapid structural and epigenetic
reorganization near transposable elements in hybrid and allopolyploid genomes in
Spartina. New Phytol. 184: 1003–1015.
7
8
89.
Petit M., Guidat C., Daniel J., Denis E., et al. 2010. Mobilization of retrotransposons in
synthetic allotetraploid tobacco. New Phytol. 186: 135–147.
9
10
11
90.
Chantret N., Salse J., Sabot F., Rahman S., et al. 2005. Molecular basis of evolutionary
events that shaped the hardness locus in diploid and polyploid wheat species (Triticum and
Aegilops). Plant Cell 17: 1033–1045.
12
13
91.
Bruggmann R., Bharti A.K., Gundlach H., Lai J., et al. 2006. Uneven chromosome
contraction and expansion in the maize genome. Genome Res. 16: 1241–1251.
14
15
92.
Adams K.L., Wendel J.F. 2005. Novel patterns of gene expression in polyploid plants.
Trends Genet. 21: 539–543.
16
17
93.
Adams K.L. 2007. Evolution of duplicate gene expression in polyploid and hybrid plants.
J. Hered. 98: 136–141.
18
19
94.
Jackson S., Chen Z.J. 2010. Genomic and expression plasticity of polyploidy. Curr. Opin.
Plant Biol. 13: 153–159.
20
21
22
95.
Birchler J.A. 2012. Insights from paleogenomic and population studies into the
consequences of dosage sensitive gene expression in plants. Curr. Opin. Plant Biol. 15:
544–548.
23
24
96.
Hegarty M., Coate J., Sherman-Broyles S., Abbott R., et al. 2013. Lessons from natural
and artificial polyploids in higher plants. Cytogenet. Genome Res. 140: 204–225.
25
26
97.
Zou C., Lehti-Shiu M.D., Thomashow M., Shiu S.-H. 2009. Evolution of stress-regulated
gene expression in duplicate genes of Arabidopsis thaliana. PLoS Genet. 5: e1000581.
27
28
29
98.
Hegarty M.J., Barker G.L., Wilson I.D., Abbott R.J., et al. 2006. Transcriptome shock
after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr.
Biol. CB 16: 1652–1659.
30
31
99.
Wang J., Tian L., Lee H.S., Wei N.E., et al. 2006. Genome-wide non-additive gene
regulation in Arabidopsis allotetraploids. Genetics 172: 507–517.
32
33
34
100. Xu Y., Zhong L., Wu X., Fang X., et al. 2009. Rapid alterations of gene expression and
cytosine methylation in newly synthesized Brassica napus allopolyploids. Planta 229:
471–483.
31
1
2
3
101. Flagel L., Udall J., Nettleton D., Wendel J. 2008. Duplicate gene expression in
allopolyploid Gossypium reveals two temporally distinct phases of expression evolution.
BMC Biol. 6: 16.
4
5
102. Chelaifa H., Chagué V., Chalabi S., Mestiri I., et al. 2013. Prevalence of gene expression
additivity in genetically stable wheat allohexaploids. New Phytol. 197: 730–736.
6
7
103. Gianinetti A. 2013. A criticism of the value of midparent in polyploidization. J. Exp. Bot.
64: 4119–4129.
8
9
10
104. Grover C.E., Gallagher J.P., Szadkowski E.P., Yoo M.J., et al. 2012. Homoeolog
expression bias and expression level dominance in allopolyploids. New Phytol. 196: 966–
971.
11
12
105. Lee H.S., Chen Z.J. 2001. Protein-coding genes are epigenetically regulated in
Arabidopsis polyploids. Proc. Natl. Acad. Sci. U. S. A. 98: 6753–6758.
13
14
106. Yoo M.-J., Szadkowski E., Wendel J.F. 2013. Homoeolog expression bias and expression
level dominance in allopolyploid cotton. Heredity 110: 171–180.
15
16
107. Wendel J.F., Cronn R.C. 2003. Polyploidy and the evolutionary history of cotton. In
Advances in Agronomy. Academic Press. p 139–186.
17
18
108. Rapp R.A., Udall J.A., Wendel J.F. 2009. Genomic expression dominance in
allopolyploids. BMC Biol. 7: 18.
19
20
109. Xu C., Bai Y., Lin X., Zhao N., et al. 2014. Genome-Wide Disruption of Gene Expression
in Allopolyploids but Not Hybrids of Rice Subspecies. Mol. Biol. Evol. : msu085.
21
22
110. Ownbey M. 1950. Natural hybridization and amphiploidy in the genus Tragopogon. Am. J.
Bot. 37: 487–499.
23
24
111. Lowe A., Abbott R.J. 2003. A new British species Senecio eboracensis (Asteraceae)
another hybrid derivative of S. vulgaris L. and S. squalidus L. Watsonia 24: 375–388.
25
26
112. Wang J., Tian L., Lee H.-S., Wei N.E., et al. 2006. Genomewide nonadditive gene
regulation in Arabidopsis allotetraploids. Genetics 172: 507–517.
27
28
113. Church S.A., Spaulding E.J. 2009. Gene expression in a wild autopolyploid sunflower
series. J. Hered. 100: 491–495.
29
30
31
114. Chelaifa H., Monnier A., Ainouche M. 2010. Transcriptomic changes following recent
natural hybridization and allopolyploidy in the salt marsh species Spartina x townsendii
and Spartina anglica (Poaceae). New Phytol. 186: 161–174.
32
33
115. Yang C., Kawahara Y., Mizuno H., Wu J., et al. 2012. Independent domestication of
Asian rice followed by gene flow from japonica to indica. Mol. Biol. Evol. 29: 1471–1479.
32
1
2
116. Chen Z.J. 2007. Genetic and epigenetic mechanisms for gene expression and phenotypic
variation in plant polyploids. Annu. Rev. Plant Biol. 58: 377–406.
3
4
117. Comai L. 2000. Genetic and epigenetic interactions in allopolyploid plants. Plant Mol.
Biol. 43: 387–399.
5
6
118. Doyle J.J., Flagel L.E., Paterson A.H., Rapp R.A., et al. 2008. Evolutionary genetics of
genome merger and doubling in plants. Annu. Rev. Genet. 42: 443–461.
7
8
119. Chen Z.J. 2010. Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci.
15: 57.
9
10
120. Mayfield D., Chen Z.J., Pires J.C. 2011. Epigenetic regulation of flowering time in
polyploids. Curr. Opin. Plant Biol. 14: 174–178.
11
12
121. Ng D.W., Lu J., Chen Z.J. 2012. Big roles for small RNAs in polyploidy, hybrid vigor,
and hybrid incompatibility. Curr. Opin. Plant Biol. 15: 154–161.
13
14
122. Madlung A., Wendel J.F. 2013. Genetic and epigenetic aspects of polyploid evolution in
plants. Cytogenet. Genome Res. 140: 270–285.
15
16
17
123. Lukens L.N., Pires J.C., Leon E., Vogelzang R., et al. 2006. Patterns of sequence loss and
cytosine methylation within a population of newly resynthesized Brassica napus
allopolyploids. Plant Physiol. 140: 336–348.
18
19
20
124. Shaked H., Kashkush K., Ozkan H., Feldman M., et al. 2001. Sequence elimination and
cytosine methylation are rapid and reproducible responses of the genome to wide
hybridization and allopolyploidy in wheat. Plant Cell 13: 1749–1760.
21
22
125. Salmon A., Ainouche M.L., Wendel J.F. 2005. Genetic and epigenetic consequences of
recent hybridization and polyploidy in Spartina (Poaceae). Mol. Ecol. 14: 1163–1175.
23
24
25
126. Madlung A., Masuelli R.W., Watson B., Reynolds S.H., et al. 2002. Remodeling of DNA
methylation and phenotypic and transcriptional changes in synthetic Arabidopsis
allotetraploids. Plant Physiol. 129: 733–746.
26
27
127. Chen L., Chen J. 2008. Changes of cytosine methylation induced by wide hybridization
and allopolyploidy in Cucumis. Genome 51: 789–799.
28
29
30
128. Chen M., Ha M., Lackey E., Wang J., et al. 2008. RNAi of met1 reduces DNA
methylation and induces genome-specific changes in gene expression and centromeric
small RNA accumulation in Arabidopsis allopolyploids. Genetics 178: 1845–1858.
31
32
129. Law J.A., Jacobsen S.E. 2010. Establishing, maintaining and modifying DNA methylation
patterns in plants and animals. Nat. Rev. Genet. 11: 204–220.
33
1
2
3
130. Mittelsten Scheid O., Afsar K., Paszkowski J. 2003. Formation of stable epialleles and
their paramutation-like interaction in tetraploid Arabidopsis thaliana. Nat. Genet. 34: 450–
454.
4
5
6
131. Baubec T., Dinh H.Q., Pecinka A., Rakic B., et al. 2010. Cooperation of multiple
chromatin modifications can generate unanticipated stability of epigenetic States in
Arabidopsis. Plant Cell 22: 34–47.
7
8
9
132. Ha M., Ng D.W.-K., Li W.-H., Chen Z.J. 2011. Coordinated histone modifications are
associated with gene expression variation within and between species. Genome Res. 21:
590–598.
10
11
12
133. Ha M., Lu J., Tian L., Ramachandran V., et al. 2009. Small RNAs serve as a genetic
buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids.
Proc. Natl. Acad. Sci. U. S. A. 106: 17835–17840.
13
14
134. Kenan-Eichler M., Leshkowitz D., Tal L., Noor E., et al. 2011. Wheat hybridization and
polyploidization results in deregulation of small RNAs. Genetics 188: 263–272.
15
16
17
135. Lackey E., Ng D.W.-K., Chen Z.J. 2010. RNAi-mediated down-regulation of DCL1 and
AGO1 induces developmental changes in resynthesized Arabidopsis allotetraploids. New
Phytol. 186: 207–215.
18
19
136. Pikaard C.S., Mittelsten-Scheid O. 2014. Epigenetic Regulation in Plants.
D,Jenuwein T,Reinberg D. ed; Epigenetics. CSHL Press.
20
21
137. Coate J.E., Bar H., Doyle J.J. 2014. Extensive translational regulation of gene expression
in an allopolyploid (Glycine dolichocarpa). Plant Cell 26: 136–150.
22
23
138. Birchler J.A., Veitia R.A. 2012. Gene balance hypothesis: connecting issues of dosage
sensitivity across biological disciplines. Proc. Natl. Acad. Sci. U. S. A. 109: 14746–14753.
24
25
139. De Smet R., Van de Peer Y. 2012. Redundancy and rewiring of genetic networks
following genome-wide duplication events. Curr. Opin. Plant Biol. 15: 168–176.
26
27
28
140. Lou P., Wu J., Cheng F., Cressman L.G., et al. 2012. Preferential retention of circadian
clock genes during diploidization following whole genome triplication in Brassica rapa.
Plant Cell 24: 2415–2426.
29
30
31
141. Bekaert M., Edger P.P., Pires J.C., Conant G.C. 2011. Two-phase resolution of polyploidy
in the Arabidopsis metabolic network gives rise to relative and absolute dosage
constraints. Plant Cell 23: 1719–1728.
32
33
34
142. Veron A.S., Kaufmann K., Bornberg-Bauer E. 2007. Evidence of interaction network
evolution by whole-genome duplications: a case study in MADS-box proteins. Mol. Biol.
Evol. 24: 670–678.
In Allis
34
1
2
3
143. Hsu C.Y., Adams J.P., Kim H., No K., et al. 2011. FLOWERING LOCUS T duplication
coordinates reproductive and vegetative growth in perennial poplar. Proc. Natl. Acad. Sci.
U. S. A. 108: 10756–10761.
4
5
6
144. Sheehan M.J., Kennedy L.M., Costich D.E., Brutnell T.P. 2007. Subfunctionalization of
PhyB1 and PhyB2 in the control of seedling and mature plant traits in maize. Plant J. 49:
338–353.
7
8
145. Wolfe K.H., Shields D.C. 1997. Molecular evidence for an ancient duplication of the
entire yeast genome. Nature 387: 708–713.
9
10
146. Ihmels J., Bergmann S., Gerami-Nejad M., Yanai I., et al. 2005. Rewiring of the yeast
transcriptional network through the evolution of motif usage. Science 309: 938–940.
11
12
147. Conant G.C., Wolfe K.H. 2006. Functional partitioning of yeast co-expression networks
after genome duplication. PLoS Biol. 4: e109.
13
14
148. Levin D. 2002. Phenotypic consequences of chromosome doubling. In The role of
chromosomal change in plant evolution. Oxford University Press. p 134–149.
15
16
149. Otto S.P., Whitton J. 2000. Polyploid incidence and evolution. Annu. Rev. Genet. 34: 401–
437.
17
18
150. Li X., Yu E., Fan C., Zhang C., et al. 2012. Developmental, cytological and transcriptional
analysis of autotetraploid Arabidopsis. Planta 236: 579–596.
19
20
151. Te Beest M., Le Roux J.J., Richardson D.M., Brysting A.K., et al. 2012. The more the
better? The role of polyploidy in facilitating plant invasions. Ann. Bot. 109: 19–45.
21
22
152. Robertson K., Goldberg E.E., Igić B. 2011. Comparative evidence for the correlated
evolution of polyploidy and self-compatibility in Solanaceae. Evolution 65: 139–155.
23
24
153. Barringer B.C. 2007. Polyploidy and self-fertilization in flowering plants. Am. J. Bot. 94:
1527–1533.
25
26
154. Mable B.K. 2004. Polyploidy and self-compatibility: Is there an association? New Phytol.
162: 803–811.
27
28
155. Warner D.A., Edwards G.E. 1993. Effects of polyploidy on photosynthesis. Photosynth.
Res. 35: 135–147.
29
30
31
156. Li W.L., Berlyn G.P., Ashton P.M.S. 1996. Polyploids and their structural and
physiological characteristics relative to water deficit in Betula papyrifera (Betulaceae).
Am. J. Bot. USA
32
33
34
157. Coate J.E., Powell A.F., Owens T.G., Doyle J.J. 2013. Transgressive physiological and
transcriptomic responses to light stress in allopolyploid Glycine dolichocarpa
(Leguminosae). Heredity 110: 160–170.
35
1
2
158. Maherali H., Walden A.E., Husband B.C. 2009. Genome duplication and the evolution of
physiological responses to water stress. New Phytol. 184: 721–731.
3
4
5
159. Hao G.-Y., Lucero M.E., Sanderson S.C., Zacharias E.H., et al. 2013. Polyploidy enhances
the occupation of heterogeneous environments through hydraulic related trade-offs in
Atriplex canescens (Chenopodiaceae). New Phytol. 197: 970–978.
6
160. Levin D.A. 1983. Polyploidy and Novelty in Flowering Plants. Am. Nat. 122: 1–25.
7
8
161. Oswald B.P., Nuismer S.L. 2007. Neopolyploidy and pathogen resistance. Proc. R. Soc. B
274: 2393–2397.
9
10
11
162. Schoen D.J., Burdon J.J., Brown A.H. 1992. Resistance of Glycine tomentella to soybean
leaf rust Phakopsora pachyrhizi in relation to ploidy level and geographic distribution.
Theor. Appl. Genet. 83: 827–832.
12
13
163. Busey P., Giblin-Davis R.M., Center B.J. 1993. Resistance in Stenotaphrum to the sting
nematode. Crop Sci. USA
14
15
164. Thompson J.N., Cunningham B.M., Segraves K.A., Althoff D.M., et al. 1997. Plant
polyploidy and insect/plant interactions. Am. Nat. 150: 730–743.
16
17
165. Nuismer S.L., Thompson J.N. 2001. Plant polyploidy and non-uniform effects on insect
herbivores. Proc R Soc B 268: 1937–1940.
18
166. Stebbins C.L. 1950. Variation and evolution in plants. London: Oxford University Press.
19
167. Otto S.P. 2007. The evolutionary consequences of polyploidy. Cell 131: 452–462.
20
21
168. Fawcett J.A., Peer Y.V. de. 2010. Angiosperm polyploids and their road to evolutionary
success. Trends Evol. Biol. 2: e3.
22
23
169. Brochmann C., Brysting A.K., Alsos I.G., Borgen L., et al. 2004. Polyploidy in arctic
plants. Biol. J. Linn. Soc. 82: 521–536.
24
25
26
170. Fawcett J.A., Maere S., Van de Peer Y. 2009. Plants with double genomes might have had
a better chance to survive the Cretaceous-Tertiary extinction event. Proc. Natl. Acad. Sci.
U. S. A. 106: 5737–5742.
27
28
171. Pandit M.K., Pocock M.J.O., Kunin W.E. 2011. Ploidy influences rarity and invasiveness
in plants. J. Ecol. 99: 1108–1115.
29
30
172. Chao D.-Y., Dilkes B., Luo H., Douglas A., et al. 2013. Polyploids exhibit higher
potassium uptake and salinity tolerance in Arabidopsis. Science 341: 658–659.
31
32
173. Bowden W.M. 1940. Diploidy, polyploidy, and winter hardiness relationships in the
flowering plants. Am. J. Bot. 27: 357–371.
36
1
2
174. Martin S.L., Husband B.C. 2009. Influence of phylogeny and ploidy on species ranges of
North American angiosperms. J. Ecol. 97: 913–922.
3
4
175. Segraves K.A., Thompson J.N. 1999. Plant polyploidy and pollination: floral traits and
insect visits to diploid and tetraploid Heuchera grossulariifolia. Evolution 53: 1114–1127.
5
6
7
176. Kennedy B.F., Sabara H.A., Haydon D., Husband B.C. 2006. Pollinator-mediated
assortative mating in mixed ploidy populations of Chamerion angustifolium (Onagraceae).
Oecologia 150: 398–408.
8
9
177. Baldwin S.J., Husband B.C. 2011. Genome duplication and the evolution of conspecific
pollen precedence. Proc. R. Soc. B 278: 2011–2017.
10
11
178. Ainouche M.L., Fortune P.M., Salmon A., Parisod C., et al. 2009. Hybridization,
polyploidy and invasion: lessons from Spartina (Poaceae). Biol. Invasions 11: 1159–1173.
12
13
179. Ramsey J. 2011. Polyploidy and ecological adaptation in wild yarrow. Proc. Natl. Acad.
Sci. U. S. A. 108: 7096–7101.
14
15
180. Martin S.L., Husband B.C. 2012. Whole genome duplication affects evolvability of
flowering time in an autotetraploid plant. PLoS ONE 7: e44784.
16
17
181. Martin S.L., Husband B.C. 2013. Adaptation of diploid and tetraploid chamerion
angustifolium to elevation but not local environment. Evolution 67: 1780–1791.
18
19
182. Vamosi J.C., Dickinson T.A. 2006. Polyploidy and diversification: A phylogenetic
investigation in Rosaceae. Int. J. Plant Sci. 167: 349–358.
20
21
22
183. Paterson A.H., Bowers J.E., Chapman B.A. 2004. Ancient polyploidization predating
divergence of the cereals, and its consequences for comparative genomics. Proc. Natl.
Acad. Sci. U. S. A. 101: 9903–9908.
23
24
25
184. Barker M.S., Kane N.C., Matvienko M., Kozik A., et al. 2008. Multiple
paleopolyploidizations during the evolution of the Compositae reveal parallel patterns of
duplicate gene retention after millions of years. Mol. Biol. Evol. 25: 2445–2455.
26
27
185. Cannon S.B., Ilut D., Farmer A.D., Maki S.L., et al. 2010. Polyploidy did not predate the
evolution of nodulation in all legumes. PloS One 5: e11630.
28
29
186. Wood T.E., Takebayashi N., Barker M.S., Mayrose I., et al. 2009. The frequency of
polyploid speciation in vascular plants. Proc. Natl. Acad. Sci. U. S. A. 106: 13875–13879.
30
31
187. Mayrose I., Zhan S.H., Rothfels C.J., Magnuson-Ford K., et al. 2011. Recently formed
polyploid plants diversify at lower rates. Science 333: 1257.
32
33
34
188. Sabara H.A., Kron P., Husband B.C. 2013. Cytotype coexistence leads to triploid hybrid
production in a diploid-tetraploid contact zone of Chamerion angustifolium (Onagraceae).
Am. J. Bot. 100: 962–970.
37
1
2
3
189. Marques I., Draper D., Riofrío L., Naranjo C. 2014. Multiple hybridization events,
polyploidy and low postmating isolation entangle the evolution of neotropical species of
Epidendrum (Orchidaceae). BMC Evol. Biol. 14: 20.
4
5
6
190. Sonnleitner M., Weis B., Flatscher R., Garcia P.E., et al. 2013. Parental ploidy strongly
affects offspring fitness in heteroploid crosses among three cytotypes of autopolyploid
Jacobaea carniolica (Asteraceae). PLoS ONE 8: e78959.
7
8
191. Petit, Bretagnolle, Felber. 1999. Evolutionary consequences of diploid-polyploid hybrid
zones in wild species. Trends Ecol. Evol. 14: 306–311.
9
10
192. Ohta T. 1992. The nearly neutral theory of molecular evolution. Annu. Rev. Ecol. Syst. 23:
263–286.
11
12
13
193. Umezawa T., Fujita M., Fujita Y., Yamaguchi-Shinozaki K., et al. 2006. Engineering
drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr.
Opin. Biotechnol. 17: 113–122.
14
15
194. Hu H., Xiong L. 2013. Genetic engineering and breeding of drought-resistant crops. Annu.
Rev. Plant Biol. 65: 83–108.
16
38
Figure 4
Interacting
partners
Genetic/physical
interaction or
co-expression
Homeologous
genes
Gene 1
P1
Gene 2
P2
Homeologous
genes
Polyploidization
Divergence
Sub-functionalization
Neo-functionalization
Gene loss
Figure 4: Effect of polyploidy on gene networks P1: Parent 1, P2: Parent 2. An example of two genes Gene 1 and Gene 2 - in parents P1 and P2 is shown. Each square represents a genetic or physical interaction of Gene 1 or Gene 2. After polyploidization, over the course of several generations, the network topology begins to evolve. If both the homeologous copies do not undergo gene loss via deletion or pseudogenization and are retained, divergence between them will lead to eventual sub-functionalization or neofunctionalization between duplicates, changing the network topology and possibly, network function.
Figure 2: Molecular consequences of polyploidy. The myriad effects of polyploidy at the molecular level are
explained in this schematic.
Figure 1
A.
Parents
2X
2X
Gametes
X
X
B.
2X
F1
2X
2X
X
X
2X
4X
D.
Parents
2X
2X
Gametes
X
X
2X
2X
2X
E.
AP
X
2X
2X
2X
X
3X
2X
AP
X
2X
3X
Gamete 1
X 2X
X 2X 3X
X 2X 3X
X 2X 3X 4X
2X 3X 4X
Gamete 2
Gamete 2
Unreduced
gamete
formation
4X
Zygote
somatic
doubling
Gamete 1
F2
2X
2X
F1
F1
gametes
C.
2X 3X 4X 5X
3X 4X 5X 6X
Figure 1: Pathways of tetraploid formation from diploid plants. The symbol X represents the base chromosome number of the species, with 1X corresponding to haploid gametes. (A) The normal pathway wherein a diploid
is produced as F1 progeny of two diploid parents. (B) Somatic doubling leading to tetraploid (4X) generation from
diploid. (C) Fusion of unreduced gametes can lead to tetraploid generation in one step. (D) A diploid produced in
F1 may generate a certain proportion of aneuploid gametes (AP, most of which are not viable) and unreduced
gametes that can lead to tetraploid generation in F2. The frequency of unreduced gamete formation can be high if
the parents belong to different species and F1 is a hybrid. (E) The triploid bridge scenario where an intermediate
triploid produces unreduced gametes leading to generation of tetraploids and individuals of higher ploidy. These
pathways of tetraploid formation have been adapted from information presented in Ramsey and Schemske, 1998.
For example polypoids formed via each pathway, as well as pathways of formation of polyploids of higher ploidy
levels, please refer to the original publication.
Figure 2
A.
P1
Chromosome loss
P2
Chr A
Translocation
t
Chr B
Chromosomal fragment loss
B.
P1
P2
t
Homeologous
genes
Gene losses
C.
Transposable element
P1
P2
Homeologous
genes
Transcriptional
activation or
repression
t
Proliferation
Insertion into gene
Figure 2: Genomic consequences of polyploidy. (A) P1: Parent 1, P2: Parent 2. Some possible scenarios with
respect to genomic rearrangements such as chromosome loss, chromosomal translocation and chromosome
fragment loss have been depicted in a simplified manner using only two chromosomes. (B) The process of gene
loss in a parent-of-origin manner, termed fractionation. In the depicted scenario, the chromosomal copy from P2
loses most of the genes. (C) Proliferation of transposable elements over time. Such proliferation may lead to
changes in gene order, gene function and gene expression.
Figure 2: Molecular consequences of polyploidy. The myriad effects of polyploidy at the molecular level are
explained in this schematic.
Figure 3
Expression level
A.
Homeologous
genes
P1
2
1
2
3
4
2
2
3
4
1
1
0
P2
1
0
Genes
Genes
Polyploidization
Divergence
Expression
level dominance
Homeolog
expression bias
Expression level
2
1
0
1
2
3
4
1
2
3
4
2
1
0
Genes
DNA
methylation
B.
Gene
Polyploidization
Demethylation
RNA
polymerase
Gene
Transcribed
mRNA
C.
Repressor
Gene
RNA
polymerase
Polyploidization
small RNA transcription
Gene
small RNAs
Transcribed
mRNA
Figure 3: Effects of polyploidy on gene expression and epigenetic regulation (A) A hypothetical
scenario showing expression divergence upon polyploidization. P1: Parent 1, P2: Parent 2. In “Homeolog
expression bias”, the homeologous genes are expressed in a parent-of-origin manner. In “Expression level
dominance”, the sum of the expression level of both the genes is similar to that in one parent. (B) A gene
which is silenced by DNA methylation in the parent is demethylated upon polyploidization or hybridization,
leading to its transcription by RNA polymerase. (C) A gene with a repressor bound to its promoter region is
not expressed in the parent but upon polyploidization is expressed as the repressor is removed due to
regulation by small RNAs transcribed elsewhere in the genome.