What is polyploidy?
Polyploidy is the process of genome doubling that gives rise to
organisms with multiple sets of chromosomes. The term ploidy
(see glossary for this and other related terms) refers to the
number of complete genomes contained in a single cell. In general,
polyploid organisms contain a multiple or combination of the
chromosome sets found in the same or a closely related diploid
species. Polyploidy can arise from spontaneous somatic
chromosome duplication, or as a result of non-disjunction of the
homologous chromosomes during meiosis resulting in diploid
gametes (for review see Ramsey and Schemske, 2002). It can also
be artificially induced by treatment with drugs, such as
colchicine, which inhibits cell division. Polyploidy can occur in all or
most somatic cells of the organism or it can be restricted to a
specific tissue. In the latter case the preferred term is
endopolyploidy. Some examples of such specialized cells in animals
include the salivary gland cells in Drosophila or liver cells in
humans.
Historically, there has been much confusion over whether to
classify polyploids by mode of origin criteria or by cytological
criteria. Here we follow Ramsey and Schemske (2002) and adopt
mode of origin criteria: if the chromosomes of one genome within
an organism or species are simply duplicated, the resulting
polyploid is an autopolyploid. However, if genome duplication
occurs during a cross of two different species, the resulting
organism is referred to as an allopolyploid.
Why is polyploidy important?
Polyploidy has long been recognized as a prominent force shaping
the evolution of plants (Winge 1917; Karpchenko 1927; Stebbins,
1950; 1971), especially ferns (Wagner and Wagner, 1980; Werth
et al., 1985, Vogel et al., 1999) and flowering plants (Soltis and
Soltis, 2000; Wendel, 2000). Many important crop plants, such as
alfalfa, cotton, potato, and wheat, are obvious polyploids while
others, such as maize, soybean, and cabbage, retain the vestiges
of ancient polyploid events (paleopolyploids). Based on fossil
records, 70% of angiosperms were estimated to have had a
polyploidization event in their species’ history (Masterson 1994).
More recent evidence based on genome analyses suggest that
many more organisms have polyploid origins, including those with
small genomes such as Arabidopsis and yeast (AGI, 2000; Blanc et
al., 2003; Langkjaer et al., 2003).
An example of an
allopolyploid that
shows hybrid vigor
over its diploid
progenitors is
resynthesized
Brassica napus.
Although polyploidy is now widely recognized as a frequent event
in evolution, we don't fully understand why polyploids have been
so successful. Many polyploids are more vigorous than their
diploid progenitors and both auto- and allo-polyploids have built in
mechanisms for mantaining high levels of heterozygoisty. This
polyploids may exhibit a phenomenon similar to hybrid vigor, or
heterosis. Polyploids alos are known to exhibit new phenotype
variation that can arise with aor shortly after polyploid
formation. Our research group is studying the alteration in
genome structure and genome expression that could lead to these
new, potentially advantageous, phenotypes. Hybrid vigor, also
known as heterosis, is an agriculturally important phenomenon
describing the observation that the hybrid offspring of two
inbred genetically different varieties produces higher yields than
either one of the two parental lines.
How are polyploids formed?
Two main modes of origin of the polyploid condition are
recognized somatic doubling in mitosis, and nonreduction in
meiosis (Heilborn, 1934; Grant, 1971). The mechanism of somatic
doubling is exemplified by polyploid Primula kewensis, and
nonreduction was the mode of origin seen in polyploid
Rhaphobrassica. It used to be thought most that polyploids
formed by hybridization followed by chromosome doubling.
However, Harlan and deWet (1975) argued that unreduced
gametes played an important role. While agronomy researchers
took notice of this (e.g. Peloquin, 19XX), textbooks did not
change. Recently, a lot of theoretical modeling (Rodriguez, 1996;
Ramsey and Schemske, 1998, 2002) and fieldwork (Husband 1999,
2000) has contributed to the view that unreduced gametes and
triploid bridges are a major source of polyploid formation. This is
also a mechanism for how diploid and polyploid genomes can
interact (thus, the new polyploid species are not strictly sealed
off from its diploid progenitors).
During meiosis, homologous chromosomes pair and undergo
crossing over resulting in the exchange of parts of their
chromosomes. In diploid hybrids derived from crosses of two
species, chromosomes from the two species may differ or one of
the chromosomes may be absent. This can cause irregularities
during meiosis and may result in cell cycle arrest and subsequent
embryo abortion. However, if the chromosome number is doubled
in the hybrid, allotetraploids are formed, which have four sets of
chromosomes. This can occur by crossing autotetraploids of the
two species, or more likely in nature, by the fussion of unreduced
gametes. Allotetraploids generally will have pairing and crossing
over only within the two chromosomes of each original parent (the
homologous chromosomes AA) and only rarely between
chromosomes from the two original parents (the homeologous
chromosomes AA’). This meiotic behavior assures proper pairing
of the chromosomes and the correct assortment into gametes.
How do polyploids become established?
The frequency of polyploid events is exceedingly rare (estimated
to be 10-5 among offspring of diploids; Ramsey and Schemske,
1998). Although the formation of unreduced (2n) gametes is
considered to be rare in general (McCoy, 1982), 2n gamete
production is likely to play a major role in polyploid origins (Harlan
and deWet, 1975; Vorsa and Binghm, 1979). A number of factors
– genetic and environmental – have been shown to influence the
frequency of 2n gamete formation (Sax 1937; Thompson and
Lumaret 1991; Ramsey and Schemske 2002). Genetic factors also
control unreduced gamete formation (potato, Mok and Peloquin,
1975; Veilleux et al. 1982, Peloquin, in press; alfalfa, McCoy, 1982;
blueberry, Qu and Vorsa, 1999). Genes that control rates of
unreduced gamete production could become fixed in small
populations, and enable rare polyploids to become more frequent.
Environmental factors that affect 2n gamete formation include
sudden changes in temperature (heat or cold treatment),
dehydration, x-rays, uv light, infections, etc., and can induce
chromosome doubling (Sax, 1937). Otto and Whitton ?? Mable??
Other factors that can contribute to polyploid formation (aside
from unreduced gametes) include superior vegetative (clonal)
growth, perennial life history, niche separation, assortative
mating, and other fitness differences. Therefore, broad
generalizations may not apply to specific cases. As such,
different species need to be characterized and systematically
analysed to determine what mechansims are responsible for
bringing about the observed polyploid frequencies and subsequent
evolutionary patterns.
A critical first step in polyploid evolution is the establishment
and subsequent persistence of the neopolyploid (Fowler and Levin,
1984). A new and therefore rare polyploid in a diploid population
would be at a major fertility disadvantage, since most pollinations
of the polyploid will involve pollen from diploids. The
predominance of one cytotype excluding the rare cytotype from
reaching high frequences is known as the minority cytotype
exclusion principle (Husband, 1999; 2000). A number of models
have been developed to determine how polyploids may become
established in a diploid population (Fowler and Levin, 1984; Felber,
1991; Rodriguez, 1996; Husband, 2000). Parameters included in
these models include the production of unreduced (2n) gametes
by the diploid cytotype, the frequency of tetraploids formed with
each generation, multiple origins of polyploids over several
generations (given perenials versus annuals). Once 2n gamete
production exceeds a certain threshhold, the tetraploids are able
to replace diploids. The threshold varies by modifying
fertility/viability of the cytotypes. Frequency-dependent
processes can be overcome by reducing inter-cytotype matings,
so rare cytotypes could become established despite the minority
cytotype disadvantage.
How do polyploids acquire variation?
Polyploids can acquire variation both through mechanisms of
population genetics (gene flow with diploids and multiple origins of
polyploids), and through mechanisms that generate “de novo
variation” such as chromosomal rearrangements and epigenetic
phenomena.
Polyploidy has long been considered an important example of
instant or sympatric speciation, since polyploid species are mostly
reproductively isolated from their diploid progenitors (Stebbins
1950, 1971; Levin 1983). An interesting aspect related to
allopolyploidization or hybridization of different species is the
question of the “species barrier” when using a biological species
concept. Members of the same biological species are commonly
defined as related individuals of a population that can interbreed
and whose offspring are fertile. Thus, the horse and a donkey are
considered separate species because their hybrid offspring are
viable but infertile. In plants, hybridization of different species
is quite common and many of the well-known crop plants are
allopolyploids resulting from inter-species hybrids. Such
allopolyploids pose a challenge to phylogenetic species concepts,
which define species on strict monophyletic criteria. Over the
last decade this challenge has taken on additional relevance as
“polyploid species” have been found to form repeatedly in close
proximity to one another (Soltis and Soltis, 1993; 1999; 2000).
The polyphyly of “polyploid species” calls into question the very
definition of “species.” Allopolyploids – like other organisms with
reticulate evolutionary histories (e.g., eukaryotes, lichens) – give
biologists important examples when theorizing about evolutionary
entities. Aside from philosophical considerations about species
definitions, there are many implications for the multiplicity of
origins for polyploids. Multiple origins of polyploid species have
been reported for mosses, ferns, and many angiosperms
(reviewed in Vogel et al., 1999; Soltis and Soltis, 2000).
Allopolyploidy presents a paradox because it is both a diversifying
force and a genetic bottleneck (Stebbins, 1971). However, the
genetic bottleneck problem may be solved by the fact that
population-level genetic studies of polyploid plants and animals
indicate that polyploidy is not a rare event leading to unique and
uniform genotypes. Rather, the multiple independent formations
of polyploid species from heterozygous diploid progenitors may
provide a significant source of genetic variation (reviewed in
Soltis and Soltis, 1993; 1999; 2000).
Many new polyploids also are genetically unstable, and the next
section describes mechanisms that can lead to novel variation.
How do polyploids create novel variation?
Although polyploids initially attracted attention because of their
unique cytogenetics, it was soon apparent that polyploids can have
distinctive phenotypes and hybrid vigor useful for agriculture
(Randolph, 1941; Levin, 2002; Ramsey and Schemske, 2002).
Hybrid vigor, also known as heterosis, is an agriculturally
important phenomenon describing the observation that the hybrid
offspring of two inbred genetically different varieties produces
higher yields than either one of the two parental lines. Judging
from the success of many allopolyploid crop plants it may appear
as if a state of allopolyploidy generally allowed the plant greater
vigor. In contrast to hybrid vigor, some allopolyploids show
decreased vigor compared to their diploid progenitors for some
traits. An example of this is seed lethality for resynthesized
Arabidopsis suecica (Comai et al., 2000; Madlung et al., 2002).
Natural A. suecica does not show seed lethality, suggesting that
this trait changed over generation of natural selection. This and
other lines of evidence indicate that the genomes of new
allopolyploids can be unstable, perhaps due to the phenomena of
“genome shock” that may result from the union of different
genomes (McClintock, 1985). The changes in response to this
“genomic shock” may be the first steps in the diploidization
process, and they could involve changes in gene expression.
Over the last decade, it has become apparent that polyploid
genomes are not always a simple sum of their constituent
genomes, but products of dynamic genetic and epigenetic changes
that occur upon, or shortly after, polyploid formation. Epigenetic
changes, which involve alterations of gene expression without a
change in DNA sequence, are particularly intriguing because they
play essential roles in plant development and plant defense
against viruses and transposons. In nascent polyploids, observed
epigenetic phenomena include nucleolar dominance, changes in
DNA methylation and chromatin structure, triggering silencing or
activation of genes and (retro)transposons, and novel phenotypes
(reviewed in Matzke et al., 1999; Comai, 2000; Wendel, 2000; Liu
and Wendel, 2002, 2003; Osborn et al. 2003).
Since the immediate consequences of polyploidization can best be
studied in either synthetic or natural polyploids of recent
ancestry, research on polyploidy and epigenetics has taken place
primarily in experimental organisms. In addition, research in
polyploidy has undergone a renaissance because of the available
genomic and genetic resources in model organisms. Collectively,
these studies have documented that the degree of genetic and
epigenetic changes in recent natural and synthetic allopolyploids
varies across taxa. For example, Arabidopsis (Mittelsten Scheid
et al. 1996; Lee and Chen 2001; Madlung et al. 2002; Chen et al.
2003; Mittelsten Scheid et al. 2003), Brassica (Song et al. 1995;
Chen and Pikaard 1997; Pires et al. 2003), Triticum (Ozkan et al.
2001; Shaked et al. 2001; Kashkush et al. 2003), and Nicotiana
(Kenton et al. 1993; Lim et al. 2000; Mette et al. 2002)
demonstrate rapid genomic and epigenetic changes. In contrast,
synthetic Gossypium polyploids show few changes in overall
genome sequences, yet they display differential expression of
genes in different tissue types (Liu et al. 2001; Adams et al.
2003). These and other recent studies suggest that genetic and
epigenetic changes contribute to the potentially dynamic nature
of polyploids (Soltis and Soltis 1995). Studies of recent natural
polyploids are now revealing the link between these epigenetic
changes and the evolutionarily success of polyploid speciation.
Figure legend: Potential causes of novel variation in polyploids.
The merger of chromosomes from two diploid genomes (red and
blue) into a tetraploid genome can cause (1) increased variation of
dosage-regulated gene effects and expression (magnitudes of
allelic effects and expression shown by size of blocks for three
loci); (2) altered regulatory interactions (trans-acting regulatory
factors shown as dimeric proteins, with heterodimers not
functioning properly); (3) genetic changes affecting gene
expression (e.g., insertions, deletions, translocations and gene
conversions); and (4) epigenetic changes (repression or
derepression of gene expression caused by genome interaction of
chromatin modeling factors, which could also trigger movement of
transposable elements).