NEWS AND COMMENTARY
Allopolyploid genomes...............................................................
The complex nature of allopolyploid
plant genomes
MJ Hegarty and SJ Hiscock
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Heredity advance online publication, 3 June 2009; doi:10.1038/hdy.2009.61
P
olyploidy is a major creative force
in plant evolution, from ferns to
flowering plants. Estimates suggest
that B70% of flowering plants have
undergone at least one whole-genome
duplication event during their evolutionary
history (Levin, 2002), and that
2­4% of all speciation events involve
polyploidisation (Otto and Whitton,
2000). The majority of polyploid plants
arise through the combined effects of
interspecific hybridisation and polyploidy
(allopolyploidy), and much attention
has focused on understanding what
happens when divergent genomes are
brought together by these processes.
A recent study by Buggs et al. (2009)
has shown that at a genomic level the
possible outcomes of allopolyploidy are
not always as predictable as we might
expect. As it is known that many
polyploid genomes eventually return
to a diploid-like state through loss or
divergence of duplicated genes, Buggs
et al. (2009) set out to determine the
timing of these events in the allotetraploid
hybrid Tragopogon miscellus. This
hybrid is an excellent system to examine
the timing of genomic changes associated
with allopolyploidy, as it is
known to have arisen within the last
80 years, unlike many other natural
hybrids that have formed many thousands
or even millions of years ago,
such as wheat (Peterson et al., 2006) or
cotton (Adams et al., 2003). By assaying
the detectability of cleaved amplified
polymorphic sequence markers on both
genomic DNA and cDNA, Buggs et al.
(2009) were able to determine whether
parental gene copies for 10 loci were
being lost or silenced in 57 hybrids from
five natural populations. They were
also able to compare these hybrids to
a resynthesised allotetraploid created
under glasshouse conditions. They
found that, across 10 homoeologous
gene pairs in the 57 natural hybrids,
3.2% of loci had been rendered undetectable
in the genomic DNA, suggesting
loss of one parental gene copy. In
addition, analysis of seven of these
homoeologue pairs using cDNA as a
template showed that expression of one
parental gene copy had been lost in
6.8% of loci. In none of these cases,
silencing or allele loss was detected in
the resynthesised allopolyploid.
These findings demonstrate that silencing
and/or elimination of parental
gene copies in Tragopogon allopolyploids
is not an immediate consequence of
interspecific hybridisation or genome
duplication, but rather an ongoing
process that varies in frequency among
different hybrid populations. As the
authors note, this is in stark contrast to
the evidence from some other allopolyploid
systems, for example, allohexaploid
bread wheat (Triticum aestivum),
where some gene loss occurs immediately
upon interspecific hybridisation
and again after polyploidisation (Ozkan
et al., 2001; Shaked et al., 2001). Nevertheless,
other allopolyploids are also
known to be subjected to an ongoing
process of recombination between
homoeologous chromosomes (Figure 1),
for example Brassica, which shows
gradual loss of certain parental DNA
fragments (Song et al., 1995; Gaeta et al.,
2007). The timing of parental gene
silencing in the Tragopogon hybrids also
differs from that observed in other
systems. Immediate changes to gene
expression occur upon interspecific hybridisation
in cotton (Flagel et al., 2008)
in a manner that can be both temporally
or spatially dependent, even within a
single cell (Adams et al., 2003; Hovav
et al., 2008). Immediate changes to
gene expression have also been observed
in other hybrids, notably Arabidopsis
suecica allotetraploids (Wang et al.,
2006), and in Senecio allopolyploids
(Hegarty et al., 2005) where distinct
changes to gene expression are associated
with both interspecific hybridisation
and genome duplication (Hegarty
et al., 2006). Such changes in gene
expression are not simply the `additive'
product of the progenitor species because
B24% of the affected genes display
non-additive expression in both
cotton (Flagel et al., 2008) and Senecio
(Hegarty et al., 2008), with the percentage
of microarray features displaying
non-additive expression in Senecio being
similar to that seen in A. suecica at 3 and
5%, respectively (Wang et al., 2006;
Hegarty et al., 2008). In Senecio, 42% of
genes showing non-additive changes in
expression also showed `trangressive'
patterns of gene expression--that is,
expression change significantly higher
or lower than that observed in either
parent (Hegarty et al., 2008). Buggs et al.
(2009) suggest that the contrast between
findings in Tragopogon and the other
systems may be due to their methodology,
which detects only the presence or
absence of gene expression, and is not
capable of distinguishing changes to
expression level in cases where complete
silencing does not occur. Nonetheless,
they raise the important point
that allopolyploidy may vary in its
effects between species. This is certainly
true at the level of chromosomal organisation
in the case of allotetraploid
cotton, which shows none of the largescale
genetic rearrangements typically
observed in plant hybrids (Liu et al.,
Figure 1 Loss of parental DNA due to recombination between homoeologous chromosomes.
This figure shows a simplified representation of recombination between homoeologues in an
allopolyploid, leading to loss of DNA from one parent. A reciprocal exchange between
homoeologues is followed by segregation of the recombinants such that certain gametes
(boxed) may not possess either the original parental chromatid type or both recombinants,
resulting in loss of one homoeologous fragment in offspring derived from these gametes
(Figure adapted from Nicolas et al., 2008).
Heredity (2009), 1­2
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2001), nor does it seem to undergo any
widespread changes in the pattern of
DNA methylation seen in systems such
as Spartina (Liu et al., 2001; Salmon et al.,
2005). As Buggs et al. (2009) note, the
level of divergence between the progenitors
of a given hybrid is likely to be
a factor in differences between hybrid
systems, and, therefore, must be taken
into account when making predictions
as to the likely genetic and epigenetic
consequences of genome mergers and
duplication events.
The processes by which two genomes
adapt to coexistence within the same
nucleus are complex and can differ
markedly between species. Ongoing
studies of natural hybrid systems, such
as Tragopogon and Senecio--where hybridisation
and polyploidy have arisen
relatively recently from an evolutionary
perspective--are therefore crucial to
identifying these processes and the
factors that drive them. Given the recent
resurgence of interest in recreating
allopolyploid crop species to improve
genetic diversity, the more data we can
gather on the consequences of allopolyploidisation,
the better.
Dr MJ Hegarty is at the Institute of Biological,
Environmental and Rural Sciences, Aberystwyth
University, Edward Llwyd Building, Penglais,
Aberystwyth, Ceredigion SY23 3DA, UK and
Professor SJ Hiscock is at the School of Biological
Sciences, University of Bristol, Woodland Road,
Bristol BS8 1UG, UK
e-mail: ayh@aber.ac.uk
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Editor's suggested reading:
Kalisz S, Kramer EM (2008). Variation and
constraint in plant evolution and development.
Heredity 100: 171­177.
Sjo¨din P, Hedman H, Shavorskaya O, Finet C,
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degeneration of an old duplicated flowering
time gene in Brassica nigra. Heredity 98:
375­384.
Wu CA, Lowry DB, Cooley AM, Wright KM,
Lee YW, Willis JH (2008). Mimulus is an
emerging model system for the integration of
ecological and genomic studies. Heredity 100:
220­230.
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