Polyploidy

By: Margaret Woodhouse, Ph.D., Diana Burkart-Waco & Luca Comai, Ph.D. (Plant Biology
and Genome Center, UC Davis) © 2009 Nature Education

Citation: Woodhouse, M., Burkart-Waco, D. & Comai, L. (2009) Polyploidy. Nature

Education 2(1)

Polyploids are common among plants, as well as among certain groups of fish and amphibians.
How does this interesting condition crop up, and what advantages and disadvantages does it
impart?

Introduction

Polyploidy is the heritable condition of possessing more than two complete sets of
chromosomes. Polyploids are common among plants, as well as among certain groups of fish
and amphibians. For instance, some salamanders, frogs, and leeches are polyploids. Many
of these polyploid organisms are fit and well-adapted to their environments. In fact, recent
findings in genome research indicate that many species that are currently diploid, including
humans, were derived from polyploid ancestors (Van de Peer & Meyer, 2005). These species
that have experienced ancient genome duplications and then genome reduction are referred to
as paleopolyploids. This article discusses the mechanisms underlying polyploidy, and both the
advantages and disadvantages of having multiple sets of chromosomes.

Mechanisms of Polyploidy

Figure 1
How does an organism become polyploid? Polyploids arise when a rare mitotic or meiotic
catastrophe, such asnondisjunction, causes the formation of gametes that have a complete
set of duplicate chromosomes. Diploid gametes are frequently formed in this way. When
a diploid gamete fuses with a haploid gamete, a triploid zygote forms, although these
triploids are generally unstable and can often be sterile. If a diploid gamete fuses with
another diploid gamete, however, this gives rise to a tetraploid zygote, which is potentially
stable. Many types of polyploids are found in nature, including tetraploids (four sets of
chromosomes), hexaploids (six sets of chromosomes), and other chromosome-pair
multiples (Figure 1).

Figure 2

Researchers usually make a distinction between polyploids that arise within a species
and those that arise due to thehybridization of two distinct species. The former are known
as autopolyploids, while the latter are referred to as allopolyploids. Autopolyploids are
essentially homozygous at every locus in the genome. However, allopolyploids may have
varying degrees of heterozygosity depending on the divergence of the parental genomes.
Heterozygosity is apparent in the gametes that polyploids produce. Allopolyploids can
generally be distinguished from autopolyploids because they produce a more diverse set of
gametes (Figure 2).

Different species exhibit different levels of tolerance for polyploidy. For example, polyploids
form at relatively highfrequency in flowering plants (1 per 100,000 individuals), suggesting
that plants have a remarkably high tolerance forpolyploidy. This is also the case for some
species of fish and frogs. However, higher vertebrates do not appear to tolerate polyploidy
very well; in fact, it is believed that 10% of spontaneous abortions in humans are due to the
formation of polyploid zygotes.
Advantages of Polyploidy

Figure 3: Polyploid formation and ensuing meiotic and mitotic irregularities.

The figure illustrates the chromosomal composition and behavior of diploids and derived
polyploids at different developmental times in meiosis (a, b) and mitosis (c).

Copyright 2005 Nature Publishing Group. Comai, L., The advantages and
disadvantages of being polyploid, Nature Reviews Genetics 6, 836-846

Due to the high incidence of polyploidy in some taxa, such as plants, fish, and frogs, there
clearly must be some advantages to being polyploid. A common example in plants is the
observation of hybrid vigor, or heterosis, whereby thepolyploid offspring of two diploid
progenitors is more vigorous and healthy than either of the two diploid parents. There
are several possible explanations for this observation. One is that the enforced pairing
of homologouschromosomes within an allotetraploid prevents recombination between
the genomes of the original progenitors, effectively maintaining heterozygositythroughout
generations (Figure 3). This heterozygosity prevents the accumulation of recessive
mutations in the genomes of later generations, thereby maintaining hybrid vigor. Another
important factor is generedundancy. Because the polyploid offspring now have twice as
many copies of any particular gene, the offspring are shielded from the deleterious effects
of recessive mutations. This is particularly important during the gametophytelife stage. One
might envision that, during the haploid stage of the life cycle, any allele that is recessive
for a deleterious mutation will not be masked by the presence of a dominant, normally
functioning allele, allowing the mutation to cause developmental failure in the pollen or
the egg sac. Conversely, a diploidgamete permits the masking of this deleterious allele
by the presence of thedominant normal allele, thus protecting the pollen or egg sac from
developmental dysfunction. This protective effect of polyploidy might be important when
small, isolated populations are forced to inbreed.

Another advantage conferred by gene redundancy is the ability to diversifygene function

over time. In other words, extra copies of genes that are not required for normal organism
function might end up being used in new and entirely different ways, leading to new
opportunities in evolutionary selection(Adams & Wendel, 2005).

Interestingly, polyploidy can affect sexuality in ways that provide selective advantages. One
way is by disrupting certain self-incompatibility systems, thereby allowing self-fertilization.
This might be the result of the interactions between parental genomes in allopolyploids
(Comai et al., 2000). Another way is by favoring the onset of asexual reproduction, which is
associated withpolyploidy in both plants and animals. This switch in reproductive strategies
may improve fitness in static environments.

Disadvantages of Polyploidy

For all the advantages that polyploidy can confer to an organism, there are also a great
number of disadvantages, both observed and hypothesized. One of these disadvantages
relates to the relative changes between the size of the genome and the volume of the
cell. Cell volume is proportional to the amount of DNA in the cell nucleus. For example,
doubling a cell's genome is expected to double the volume of space occupied by the
chromosomes in thenucleus, but it causes only a 1.6-fold increase in the surface area
of the nuclear envelope (Melaragno et al., 1993). This can disrupt the balance of factors
that normally mediate interactions between the chromosomes and nuclear components,
including envelope-bound proteins. The peripheral positioning of telomeric and centromeric
heterochromatin may be disturbed as well, because there is less relative surface space on
the nuclear envelopeto accommodate this positioning (Fransz et al., 2002).

Polyploidy can also be problematic for the normal completion of mitosis and meiosis.
For one, polyploidy increases the occurrence of spindle irregularities, which can lead
to the chaotic segregation of chromatids and to the production of aneuploid cells in
animals and yeast. Aneuploid cells, which have abnormal numbers of chromosomes,
are more readily produced in meioses involving three or more sets of chromosomes
than in diploid cells. Autopolyploids have the potential to form multiple arrangements of
homologous chromosomes at meiotic metaphase I (Figure 2), which can result in abnormal
segregation patterns, such as 3:1 or 2:1 plus one laggard. (Laggard chromosomes do not
attach properly to the spindle apparatus and thus randomly segregate to daughter cells.)
These abnormal segregation patterns cannot be resolved into balanced products, and
random segregation of multiple chromosome types produces mostly aneuploid gametes
(Figure 3). Chromosome pairing at meiosis I is more constrained in allopolyploids than in
autopolyploids, but the stable maintenance of the two parental chromosomal complements
also requires the formation of balanced gametes.

Another disadvantage of polyploidy includes potential changes in gene expression. It is

generally assumed that an increase in the copy number of all chromosomes would affect
all genes equally and should result in a uniform increase in gene expression. Possible
exceptions would include genes that respond to regulating factors that do not change
proportionally with ploidy. We now have experimental evidence for such exceptions in
several systems. In one interesting example, investigators compared the mRNA levels
per genome for 18 genes in 1X, 2X, 3X, and 4X maize. While expression of most genes
increased with ploidy, some genes demonstrated unexpected deviations from expected
expression levels. For example, sucrose synthaseshowed the expected proportional
expression in 2X and 4X tissues, but its expression was three and six times higher,
respectively, in 1X and 3X tissues. Two other genes showed similar, if less extreme, trends.
Altogether, about 10% of these genes demonstrated sensitivity to odd-numberedploidy
(Guo et al., 1996).

Epigenetic instability can pose yet another challenge for polyploids. Epigenetics refers
to changes in phenotype and gene expression that are not caused by changes in DNA
sequence. According to the genomic shock hypothesis, disturbances in the genome, such
as polyploidization, may lead to widespread changes in epigenetic regulation. Although
there are few instances of documented epigenetic instability in autopolyploids, there are a
couple of intriguing examples worth mentioning. In one case, transgene silencing occurred
more frequently in Arabidopsis thaliana tetraploids than in A. thalianadiploids, suggesting
an effect of ploidy on chromosome remodeling (Mittelsten Scheid et al., 1996). However,
several factors cannot be ruled out in the observation of this phenomenon, including
duplication of the strong 35S promoter from cauliflower mosaic virus in the transgene. In
another case, the activation of a DNA transposon of the Spm/CACTA family was observed
in autopolyploids. Unfortunately, the generality of this change could not be determined
because multiple independent autopolyploids were not examined.

Conversely, extensive evidence for epigenetic remodeling is available in allopolyploids.

Structural genomic changes, such as DNA methylation, and expression changes are
reported to accompany the transition to alloploidy in several plant systems, including
Arabidopsis and wheat (Shaked et al., 2001). The most detailed information is available
for the model system Arabidopsis. For instance, in a cross of A. thaliana and A. arenosa,
epigenetically regulated genes were identified by comparing transcripts from the
autotetraploid parents to transcripts from the neoallopolyploid progeny. A. thalianagenes
affected by epigenetic regulation were defined as those that responded to the transition
from autopolyploidy to allopolyploidy. Altogether, between 2% and 2.5% of A. thaliana
genes were estimated to have undergone regulatory changes during the transition to
allopolyploidy. A more detailedmicroarray study that examined the regulation of 26,000
genes in Arabidopsis neoallopolyploids detected a transcriptome divergence between the
progenitors of more than 15%, due to genes that were highly expressed in A. thaliana and
not in A. arenosa or vice versa. Significantly, expression of approximately 5% of the genes
diverged from the mid-parent value in two independently derived allotetraploids, consistent
with nonadditive generegulation after hybridization (Wang et al., 2006). Taken together,
these results suggest that the instability syndrome of neoallopolyploids may be attributed
primarily to regulatory divergence between the parental species, leading to genomic
incompatibilities in the allopolyploid offspring.

Aneuploidy might also be a factor in epigenetic remodeling in neoallopolyploids, either by

altering the dosage of factors that are encoded by chromosomes that have greater or fewer
than the expected number of copies leading to changes in imprinted loci, or by exposing
unpaired chromatinregions to epigenetic remodeling mechanisms. In the latter case, this
susceptibility of meiotically unpaired DNA to silencing was first reported for the fungus
Neurospora crassa, but it appears to be a general phenomenon. Therefore, some of the
epigenetic instability that is observed in allopolyploids might result from aneuploidy.

Evolutionary Potential of Polyploid Organisms

At first sight, the epigenetic changes observed in polyploids would seem to be deleterious
because of their disruptive effects on regulatory patterns established by selection. However,
these epigenetic changes might instead increase diversity and plasticity by allowing for
rapid adaptation in polyploids. One example may be the widespread dispersal of the
invasive allopolyploid Spartina angelica. However, it is not clear whether the success of
thisspecies can be attributed to fixed heterosis or to the increased variability that results
from epigenetic remodeling. Polyploidy is also believed to play a role in the rapid adaptation
of some allopolyploid arctic flora, probably because their genomes confer hybrid vigor and
buffer against the effects ofinbreeding. However, fertility barriers between species often
need to be overcome in order to form successful allopolyploids, and these barriers may
have an epigenetic basis.

Summary
Recent studies have provided interesting insights into the regulatory and genomic
consequences of polyploidy. Together with the emerging evidence of ancestral duplication
through polyploidization in model plant, fungus, and animal species, knowledge of these
consequences has stimulated thinking about the relationship between early polyploidization
events, the success of the polyploidy, and the long-term fate of new species.