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Homoeologous recombination in
allopolyploids: the polyploid ratchet
Author for correspondence:
J. Chris Pires
Tel: +1 573 8820619
Email: [email protected]
Robert T. Gaeta and J. Chris Pires
Division of Biological Sciences, University of Missouri, Columbia, MO 65211-7310, USA
Received: 12 August 2009
Accepted: 24 September 2009
Summary
New Phytologist (2010) 186: 18–28
doi: 10.1111/j.1469-8137.2009.03089.x
Key words: allopolyploidy, Brassica,
chromosome rearrangement, gene
conversion, homoeologous recombination,
Muller’s ratchet, polyploidy, recombination.
Polyploidization and recombination are two important processes driving evolution
through the building and reshaping of genomes. Allopolyploids arise from hybridization and chromosome doubling among distinct, yet related species. Polyploids
may display novel variation relative to their progenitors, and the sources of this
variation lie not only in the acquisition of extra gene dosages, but also in the genomic changes that occur after divergent genomes unite. Genomic changes (deletions, duplications, and translocations) have been detected in both recently formed
natural polyploids and resynthesized polyploids. In resynthesized Brassica napus allopolyploids, there is evidence that many genetic changes are the consequence of
homoeologous recombination. Homoeologous recombination can generate novel
gene combinations and phenotypes, but may also destabilize the karyotype and
lead to aberrant meiotic behavior and reduced fertility. Thus, natural selection
plays a role in the establishment and maintenance of fertile natural allopolyploids
that have stabilized chromosome inheritance and a few advantageous chromosomal rearrangements. We discuss the evidence for genome rearrangements that
result from homoeologous recombination in resynthesized B. napus and how these
observations may inform phenomena such as chromosome replacement, aneuploidy, non-reciprocal translocations and gene conversion seen in other polyploids.
Introduction
Cytogenetic studies provided the earliest observations for
genomic shock and meiotic instabilities inherent to newly
formed hybrids and polyploids (Navashin, 1934; Stebbins,
1971; Grant, 1975; Sybenga, 1975; McClintock, 1984;
Levin, 2002). In the last decade, molecular data from resynthesized and natural allopolyploids indicate that genetic and
epigenetic changes are common consequences of polyploidization across a wide range of species (Wendel, 2000; Osborn et al., 2003b; Chen, 2007; Doyle et al., 2008;
Hegarty & Hiscock, 2008; Leitch & Leitch, 2008; Soltis &
Soltis, 2009). We understand little of the mechanisms that
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lead to these changes and know even less about their directed or random nature. However, data from some species
suggest that genetic changes may result from homoeologous
recombination. Recombination involves some of the most
important mechanisms contributing to genetic variation
and genome structural diversity in plants (Gaut et al.,
2007). It is a process that generates novel combinations of
genetic material, eliminates deleterious mutations and plays
a role in DNA repair. During meiosis in plants, recombination predominantly occurs among allelic sequences on
homologous chromosomes; however, in allopolyploids
which lack diploid pairing fidelity recombination may occur
ectopically among paralogous or homoeologous sequences.
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Homoeologous recombination may lead to reciprocal
exchange and gene conversion, explaining many of the small
and large genetic changes detected in newly formed allopolyploids.
Our goal in this paper is to give an overview of mechanisms of recombination in plants, chromosome pairing,
recombination and segregation in allopolyploids, and how
these mechanisms might contribute to genetic changes in
natural and resynthesized polyploids. We review the evidence for homoeologous recombination and chromosome
rearrangements in Brassica napus polyploids. We introduce
the idea of a ‘polyploid ratchet’ (inspired by ‘Muller’s
ratchet’, Muller, 1964; Felsenstein, 1974) to account for the
high frequency of genetic changes in early generations of resynthesized B. napus when compared with natural, domesticated B. napus. Finally, we suggest that B. napus offers a
window into allopolyploid genome evolution involving
deletions, chromosome rearrangements, chromosome
replacement and aneuploidy – all phenomena now being
reported in natural allopolyploids such as Tragopogon (Lim
et al., 2008; Z. Xiong & J. C. Pires, unpublished). We
hypothesize that homoeologous recombination, multivalent
pairing, and segregation of translocation heterozygotes are
plausible mechanisms for dynamic structural changes in
allopolyploids, included gene loss and conversion.
Mechanisms of recombination in plants
Meiosis and the genes responsible for carrying out recombination are highly conserved (Zickler & Kleckner, 1999;
Bhatt et al., 2001; Anderson and Stack, 2002). Many plant
homologs for genes involved in meiotic recombination have
been identified (for review see Schwarzacher, 2003; Schuermann et al., 2005). During meiosis, homologous chromosomes undergo reciprocal exchange (crossing over; CO) and
gene conversion (noncrossover; NCO), events leading to
novel haplotypes. Recombination is initiated by doublestrand DNA breaks (DSBs) (Fig. 1). Homologous recombination is the major route for DSB repair during meiosis,
which involves homology search, DNA synthesis and DNA
repair. Two models have been used to explain CO and
NCO: the double-strand break-repair (DSBR) model,
which suggests a mechanism for reciprocal exchange and
gene conversion during meiotic recombination (Szostak
et al., 1983; Fig. 1a–e), and the synthesis-dependent strand
annealing (SDSA) model, which can explain gene conversions (Nassif et al., 1994; Rubin & Levy, 1997; Puchta,
2005; Cromie & Smith, 2007; Fig. 1f–g). Evidence from
several model organisms suggests that while the DSBR
model provides a likely explanation for many COs, it cannot explain all NCOs (Cromie & Smith, 2007). Most
DSBs are repaired in a nonreciprocal manner, and few
involve COs (Mezard et al., 2007). While reciprocal
exchanges can be quite large, the size of gene conversion
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varies (generally a few hundred to a few thousand base
pairs) (Hilliker et al., 1994; Xu et al., 1995; Haubold et al.,
2002). For example, conversion tracts in maize may range
from 1 to 3 kb (Dooner & Martinez-Ferez, 1997).
The main factor driving recombination between any two
sequences is homology (for a review see Naranjo & Corredor, 2008). During meiosis in plants, DSBs are induced by
Spo11 homologs (a topoisomerase-related enzyme) during
leptotene (Keeney et al., 1997; Keeney, 2001). These breaks
lead to exposed single-stranded DNAs which act as targets
for homology search, a process involving homologs of
Rad51 and DMC1 (Franklin & Cande, 1999; Paques &
Haber, 1999; Pawlowski et al., 2003). In maize, RAD51
foci have been observed along synapsed chromosomes,
which are believed to be the locations where homologous
strand invasion has led to the formation of recombination
joints (Franklin et al., 1999). Telomere and centromere
clustering may also play a role in chromosome association,
however, in plants, homology is essential to homologous
chromosome pairing (Dernburg et al., 1995; Dawe, 1998;
Stewart & Dawson, 2008).
Meiotic recombination predominantly occurs among
homologous chromosomes (for a review see Naranjo &
Corredor, 2008) but it does not occur randomly along
chromosomes and hotspots vary among species (Anderson
et al., 2001; Anderson & Stack, 2002; Jensen-Seaman
et al., 2004). Hotspots have been found within genes in
maize (Civardi et al., 1994; Xu et al., 1995) and in intergenic regions in Arabidopsis thaliana (Kim et al., 2007).
While many plants display a propensity for recombination
at the distal ends of chromosomes near the telomeric or
subtelomeric regions and lack recombination near the centromere (Drouaud et al., 2006), the reverse is true in some
species of Allium (Khrustaleva et al., 2005). Meiotic recombination predominantly occurs among allelic regions of
homologous chromosomes (for a reviewed see Naranjo &
Corredor, 2008). Recombination can also occur among
repeats within the same chromosome (intrachromosomal
exchange; Lysak et al., 2006), unequally among repeats on
homologous chromosomes (see Jelesko et al., 2004) or promiscuously among nonhomologous chromosomes that
share some degree of homology (for a review see Gaut et al.,
2007; Mezard et al., 2007). The consequence of these
events includes genetic change (Fig. 2).
DNA repair may also cause mutations. During DNA
synthesis, DSBs can initiate breakage-induced replication
during which stalled replication forks undergo strand breakage and single-strand invasion of sister or non-sister chromatids, which are used as templates for DNA repair
(reviewed by Sung & Klein, 2006). The transfer of genetic
material is nonreciprocal, and can result in gene conversion.
Double strand breaks in somatic cells can also be repaired
by nonhomologous end joining (NHEJ), which has no
requirement for homology (Puchta, 1999; reviewed by Puc-
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(a)
(f)
(b)
(c)
(d)
(e)
(g)
Reciprocal exchange
Gene conversion
Gene conversion
Fig. 1 Meiotic recombination may lead to crossover and ⁄ or gene conversion. The double strand break-repair (DSBR; b–e) and the synthesisdependent strand annealing (SDSA; f–g) models for recombination are shown. Homologous chromosomes (grey and black) are shown with
both chromatids, each of which is shown with both strands. (a) Under the DSBR and SDSA models, recombination is initiated by a doublestrand break (DSB) in one chromatid. Double-stranded DNAs are resected (degraded by nucleases) at 5¢ ends, exposing 3¢ single strands, which
invade homologous chromatids (b,f). (b) Under the DSBR model, the displaced strand forms a D-loop that invades the broken chromatid and
hybridizes with the other free 3¢ single-stranded DNA, forming recombination joints. (c) 5¢ to 3¢ synthesis (arrow heads) extends invading
DNA, and branch migration leads to heteroduplexes (checkered) near the point of exchange. Heteroduplexes are stretches of DNA composed
of hybridized homologous single-stranded DNAs that have mismatches, which are recognized by mismatch-repair machinery. Two Holliday
junctions are formed. (d) If one Holliday junction is cut in the strands involved in exchange, and the other is cut in the strands not involved in
exchange (arrows), reciprocal recombination of flanking regions will occur. Heteroduplexes will be repaired, and if an invading strand is used
as the repair template, gene conversion will also occur (not shown). (e) If both Holliday junctions are cut in the strands involved in exchange
(arrows) or both are cut in the strands not involved in exchange, no crossover will occur; however, if the heteroduplexes are repaired using the
invading strand as a template, gene conversion results. (f) Under the SDSA model, a single-strand DNA invades a homologous sequence and
copies the invaded sequence via DNA synthesis. (g) The reaction concludes with strand ‘pull out’, and mismatch repair of heteroduplexes,
which can lead to gene conversion.
hta, 2005). Errors during NHEJ can result in insertions and
deletions at the site of ligation, and the ligation of unlinked
DNA may generate translocation (Pipiras et al., 1998; Puchta, 2005). For example, in Arabidopsis unlinked DSBs can
act as substrates for reciprocal exchange by both homologous recombination and non-homologous end joining
(Pacher et al., 2007).
In summary, recombination during meiosis and DNA
repair can cause chromosomal rearrangements (deletions,
duplications, gene conversions and translocations) in
somatic or meiotic cells. While genetic variation may arise
in the genomes of somatic cells of a multicellular organism
during development, most will not contribute to gametophytic tissues or be transmitted to the next generation.
Meanwhile, genetic changes that arise during meiosis as a
consequence of recombination have a better chance of contributing novel variation to the next generation. In the fol-
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lowing sections we explore the consequences of homoeologous recombination in allopolyploids.
Chromosome pairing, recombination, and
segregation in allopolyploids
In this review, we distinguish allopolyploidy from autopolyploidy by parentage (Ramsey & Schemske, 1998, 2002)
and not chromosome pairing behavior. Allopolyploids may
arise from the fusion of unreduced gametes or by hybridization followed by genome doubling (for a review see Ramsey
& Schemske, 1998; Comai, 2005). The consequence is that
two or more divergent genomes (subgenomes) reside within
one nucleus, each of which contains complete sets of
homologous chromosomes. Sets of homologous chromosomes in a polyploid are considered homoeologous to one
or more sets from the other subgenomes if the chromo-
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(a)
Deletion
(b)
Deletion
Duplication
X
(c)
X
Homoeologous reciprocal
exchange
Homoeologous
translocation
Fig. 2 Recombination and chromosome rearrangement. (a) Deletion by intrachromatid recombination among duplicated sequences in
diploids and polyploids. (b) Deletions and duplications caused by unequal pairing and crossover (CO) among repeat sequences on homologous
chromosomes in diploids and polyploids. (c) Intergenomic deletions and duplications can result from homoeologous recombination in an
allotetraploid.
somes share a common ancestral type (and thus genomic
synteny). As a result, a somewhat challenging scenario is
posed during meiosis in allopolyploids compared with diploids. Homologous chromosomes must pair faithfully and
nonhomologous associations avoided, lest the genome be
subject to a breakdown in disomic inheritance, the consequences of which may include chromosome rearrangements
and aneuploidy (Figs 2c, 3).
Strict homologous chromosome pairing is displayed by
both diploids and diploidized allopolyploids (Sybenga,
1975). Disomic inheritance requires paired centromeres
that are aligned for equal segregation of homologs in Meiosis I and equational segregation of chromatids during Meiosis II. At the other extreme, inheritance in an allopolyploid
may resemble that of an autopolyploid, in which there is no
discrimination between the multiple sets of homologous
chromosomes (see Cifuentes et al. (2010) in this volume). Most allopolyploids fall somewhere between these
two extremes, and in some cases some chromosomes may
behave in a disomic manner, while others may pair as multivalents. Stebbins (1971) refers to this situation as ‘segmental allopolyploidy.’ Multivalents can result in the interlocking of homoeologous and homologous chromosomes,
and during metaphase pairing configurations may include
cross-structures, rings and chains of chromosomes
(Sybenga, 1975; Grant, 1975: Fig. 3). The segregation of
chromosomes from these structures often leads to duplication and deficiency gametes, and aneuploidy, all of which
lead to reduced fertility (Gillies, 1989). Segregation for any
given gene is a consequence of centromere proximity and
the frequency and distribution of crossovers among paired
chromosomes.
There is significant evidence that homologous (and thus
homoeologous) pairing is under genetic control. In the
well-studied allohexaploid bread wheat, three distinct, yet
related genomes coordinate meiotic pairing such that all
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three sets of chromosomes (A, B and D genomes) pair
faithfully with their homologs and segregate disomically.
Genetic control of chromosome pairing is mediated by the
PH1 locus (Okamoto, 1957; Riley & Chapman, 1958;
Sears, 1977; Griffiths et al., 2006). Mutations at this locus
lead to homoeologous recombination and gross chromosomal rearrangement (Qi et al., 2007). The PH1 locus
includes 70 Mb region of chromosome 5B; however,
although it is 50 yr since its first discovery, we are only
starting to understand the mechanism through which it
acts. Similarly, in B. napus polyploids the PrBn locus regulates chromosome pairing, although its effect is only
observed strongly at the allohaploid and allotriploid levels
(Jenczewski et al., 2003; Nicolas et al., 2009).
While mispairing may involve homoeologous associations, it may also include paralogous associations, both of
which lead to complicated modes of inheritance, chromosomal rearrangement, and aneuploidy. For example, the
genome of B. napus contains approximately six copies of
many loci because the progenitors species each contain
approximately three loci resulting from ancient duplications
(defined as paralogs). In B. napus allohaploids, most bivalents observed during meiosis show allosyndesis (involving pairing of homoeologous chromosomes), while up to
30% show autosyndesis (involving chromosomes within the
same parental genome that presumably contain duplicated
regions) (Nicolas et al., 2009). If pairing and recombination occur among homoeologous or paralogous sequences,
disomic inheritance is disrupted and genome rearrangements may result; however, there is limited data on the rate
of genetic changes resulting from paralogous associations in
allotetraploids. Since pairing control and fertility are often
related, it is assumed that fertile allopolyploids must have
either had some level of pre-existing control over pairing, or
in some way acquired genetic control for this during their
evolution. It is also possible that structural changes that
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(a)
CA
A′
CA
A′′
(b)
Alt
all
A′′
Adj2
Adj1
all
CA
A
CA
(c)
Other
M1 chromosome
segregations
+
and
Chromosome
loss and
replacement
+0
3:1
4:0
Aneuploidy
Fig. 3 Meiosis I in an allopolyploid carrying a homoeologous translocation. In this example, homoeologous chromosomes A (black
bars) and C (grey bars) are shown. (a) The C-homoeologs carry a
terminal translocation from the distal end of the A chromosome (CA)
resulting from homoeologous recombination in a previous generation. Lines carrying such translocations pair in a cross-like configuration. (b) In this example, if we assume no new recombination,
chromosome segregation that is alternate (Alt) or adjacent 1 (Adj1)
will generate daughter cells of the parental type. However, if
adjacent 2 (Adj2) segregation occurs, daughter cells will be produced that lack one homoeolog or the other. In this way, homoeologous chromosome loss and replacement can occur, as well as the
loss of homoeologous centromeres. (c) Depending on the location
and number of crossovers, meiosis I chromosome segregation could
also lead to nondisjunction (3 : 1 or 4 : 0 chromosome segregations)
and aneuploidy.
occur in newly formed polyploids (e.g. expansion or contraction of repeat elements or other genomic rearrangements) contribute to divergence among homoeologous
chromosomes and facilitate proper homolog pairing.
Genetic changes in natural and resynthesized
polyploids: from pattern to mechanism
Evidence for genetic changes in polyploids has been found
in resynthesized polyploids (e.g. Arabidopsis suecica,
B. napus, Triticum aestivum, Gossypium hirsutum, Nicotiana
tabacum and Triticale) and natural polyploid species (e.g.
Tragopogon, Senecio, Spartina and Glycine). Studies have
reported on sequence deletion (Ozkan et al., 2001; Shaked
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et al., 2001; Ma & Gustafson, 2006, 2008; Tate et al.,
2006, 2009), gene conversion (Wendel et al., 1995; Kovarik et al., 2004, 2005, 2008; Salmon et al., 2010), rDNA
loci changes (Lim et al., 2000, 2008; Joly et al., 2004; Pontes et al., 2004), transposon activation (Kashkush et al.,
2002, 2003; Madlung et al., 2005; Parisod et al., 2010),
chromosomal rearrangements (Kenton et al., 1993; Parkin
et al., 1995; Lim et al., 2004, 2006; Pires et al., 2004;
Udall et al., 2005; Gaeta et al., 2007), and aneuploidy
(Lim et al., 2008). However, despite the renaissance in
observations of genetic changes, we have made less progress
on identifying the underlying mechanisms of these changes.
Genetic changes in polyploids are frequently observed
using molecular markers; however, the problem with marker analysis in polyploids is that genetic changes are often
detected after the initial event has occurred, leaving the
details of their origins a mystery. Indeed, many studies
resort to ‘bandology’, counting missing parental markers as
gene losses. In some cases parental bands share the same
molecular weight, making it difficult identify some deletions unless stringent methods for resolution are used (e.g.
single-strand conformation analysis). In addition, markers
that are not sensitive to duplications cannot distinguish
gene losses or gene conversion from loss ⁄ duplication events
as discussed below. This limitation is further exacerbated by
a general difficulty in distinguishing between homologous
and homoeologous markers. It is useful to have mapped
molecular markers to distinguish linked events, as a single
deletion or rearrangement could account for the loss of
many genes. Strong evidence for the mechanisms of genetic
change comes from the use of genome-wide mapped molecular markers, combined with physical analysis of chromosomes by fluorescent in situ hybridization (FISH). Recently,
there has been renewed interest in using cytogenetic analysis
with FISH in polyploids (Lim et al., 2007, 2008; Pires &
Hertweck, 2008; Z. Xiong & J. C. Pires, unpublished).
Studies in B. napus have provided strong evidence that homoeologous recombination contributes to genetic changes
(Jenczewski et al., 2003; Pires et al., 2004; Udall et al., 2005;
Leflon et al., 2006; Liu et al., 2006; Osborn et al., 2003a;
Gaeta et al., 2007; Nicolas et al., 2007, 2008, 2009; Cifuentes et al., 2010; Szadkowski et al., 2010). In B. napus
mapping populations and resynthesized polyploids, restriction fragment length polymorphism markers have revealed
both the loss and the duplication of homoeologous loci
(Parkin et al., 1995; Sharpe et al., 1995; Osborn et al.,
2003a; Pires et al., 2004; Udall et al., 2005; Gaeta et al.,
2007). These changes have been described as homoeologous
nonreciprocal transpositions (HNRTs) because they are
detectable when the loss of one homoeologous marker occurs
together with a duplication of the other (loss ⁄ duplications).
However, as rightly pointed out by Nicolas et al. (2008); the
term ‘nonreciprocal’ is a bit misleading because the initial
event is probably an intergenomic crossover (CO), and may
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therefore have been reciprocal. Reciprocal exchanges are difficult to detect because individuals carrying them will demonstrate marker additivity. However, reciprocal exchanges
segregate during self-pollinations and their products are
detectable when they are homozygous, thus appearing nonreciprocal (Figs 2c, 4). When loss–duplication dosage
changes are observed among linked homoeologous markers,
HNRTs are visible as cytological translocations (Z. Xiong &
J. C. Pires, unpublished).
In recently formed Tragopogon allopolyploids, the loss of
genetic markers has also been found to correlate with karyotype changes observable by FISH, possibly caused by homoeologous recombination in some instances (Tate et al.,
2006, 2009; Lim et al., 2008). Research with Nicotiana and
Arabidopsis allopolyploids has found that rDNA loci may be
lost (or homogenized) or translocated after polyploidization,
and in some cases unit amplification has been observed (Lim
et al., 2000; Pontes et al., 2004; Kovarik et al., 2008). In
these species rDNA loss and homogenization may have
resulted from homoeologous recombination and gene conversion, and random segregation, or from chromosome
breakage and NHEJ. Pontes et al. (2004) suggested that
transposon-mediated breakage and recombination might
also play an important role in rDNA restructuring in A. suecica; this is corroborated by the observation that transposons
are found in high densities near the nucleolus organizer
region that is most unstable in the allopolyploid. Unit
amplification reported in Nicotiana may have resulted from
unequal crossing over (see Fig. 2b; Kovarik et al., 2008). In
some resynthesized species, deletions have been reported to
occur specifically in the paternal genome (Song et al., 1995;
Skalicka et al., 2005). These events could also be caused by
intrachromatid exchanges (see Fig. 2a) or transposon excision; however, the reason for their paternally directed nature
remains unknown. In resynthesized wheat, low-copy, coding
and non-coding sequences are lost from specific chromosomes and subgenomes (Feldman et al., 1997; Ozkan et al.,
2001; Shaked et al., 2001; Kashkush et al., 2002). Because
homoeologous pairing is strongly suppressed in wheat by the
PH1 locus, some of these deletions could be caused by intrachromosomal recombination (Fig. 2a) or DNA transposon
excision. In contrast to most resynthesized allopolyploids,
few genetic changes have been detected in resynthesized
Gossypium and mapping studies suggest that intergenomic
translocations are rare in natural allopolyploids, suggesting
that homoeologous pairing and recombination are rare
events in this species (Rong et al., 2004; Liu et al., 2001).
Homoeologous recombination and chromosome
rearrangements in B. napus allotetraploids; the
case of the polyploid ratchet
Lukens et al. (2006) and Gaeta et al. (2007) studied a population of 50 independently resynthesized B. napus allopo-
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lyploids in the S0 : 1 (S0) and S5 : 6 (S5) generations.
These self-pollinated allopolyploids were created using doubled-haploid parents, allowing for unambiguous identification of mapped homoeologous molecular markers.
Homoeologous translocations were detected at a very low
frequency in the S0 generation of these resynthesized allopolyploid lines when bulked DNA samples of 8–12 individuals per line were analysed. In the S5 generation nearly 5%
of markers analysed were deleted, most of which resulted
from HNRTs. Rearrangements were not randomly distributed across the genome and occurred frequently among
highly similar homoeologous linkage groups A1–C1, A2–
C2 and A3–C3. Reciprocal forms of most rearrangements
were found segregating in independent lineages. Some of
the markers that detected rearrangement in this population
of resynthesized allopolyploids had previously detected
preexisting and de novo homoeologous rearrangements in
synthetic · natural mapping populations (Udall et al.,
2005). Similarly, these same chromosomes underwent
frequent homoeologous pairing and recombination in
other studies of resynthesized B. napus allohaploids and
allotetraploids (Jenczewski et al., 2003; Szadkowski et al.,
2010).
Three markers at the end of A1–C1 homoeologous linkage groups were used for genotyping several lines across
generations, as well as individual plants (segregants) within
generations (Gaeta et al., 2007; supplemental data). As stated above, when S1 segregants within each line were bulked
for analysis of the S0 generation polyploids, genetic changes
were extremely rare; however, when individual S1 plants
derived from eight independent S0 lines were genotyped,
rearrangements were segregating from the first meiosis at a
low frequency (3 ⁄ 118 S1 segregants carried a HNRT), indicating that some HNRTs were missed in the bulk analysis.
A reciprocal exchange among a pair of homoeologs during
meiosis would generate reciprocal forms at a frequency of
c. 1 ⁄ 16 segregants following self-pollination under disomic
inheritance (Fig. 4). The three HNRTs detected among segregants occurred in three different lines at frequencies of
1 ⁄ 14, 1 ⁄ 15, and 1 ⁄ 16, respectively (see Gaeta et al., 2007;
supplemental data). This frequency is very similar to the
expected frequency (1 ⁄ 16); however, owing to limited sample size, further analysis is warranted. Within a self-pollinated lineage, a single homoeologous exchange would lead
to an array of progeny genotypes carrying various dosages
and arrangements of homoeoalleles (Fig. 4).
Genetic marker analysis on bulked DNA across generations revealed that some HNRTs progressed across generations (Fig. 5; see Gaeta et al., 2007; supplemental data). In
one example, an interstitial rearrangement was extended
toward the telomere in a later generation (Fig. 5a). In
another case, we detected a terminal rearrangement that
preceded the detection of a linked, interstitial rearrangement in a later generation (Fig. 5b). In this second example,
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(a)
x
(b)
Fig. 4 Simplified model of segregating homoeologous exchange in
self-pollinated resynthesized allotetraploid Brassica napus. Grey
chromosomes represent A1 from the Brassica rapa subgenome and
black chromosomes represent C1 from Brassica oleracea subgenome. (a) Recombination among homoeologous chromatids
occurs, and segregation of exchange products assuming a disomic
chromosome model of inheritance (homologs move to opposite
poles and recombined homoeologs move to opposite poles). Each
form of the reciprocal exchange (or in the case of gene conversion,
the nonreciprocal change) would segregate 3 : 1 in the gametes. (b)
Self-pollination would fix opposite forms of HNRTs in c. 1 ⁄ 16 progenies, parental types in c. 4 ⁄ 16 progenies, rearranged but balanced
(reciprocal translocations) individuals in c. 2 ⁄ 16 progenies, and most
progenies (c. 8 ⁄ 16) would be heterozygous for one form of the rearrangement or its reciprocal and contain a 3 : 1 dosage of parental
homoeoalleles. The two lines fixed for homoeologous rearrangements (upper left and lower right corners) are detectable by molecular marker analysis. A 1 ⁄ 16 frequency is similar to what has been
observed in segregants derived from the first round of meiosis in
resynthesized allopolyploids (Gaeta et al., 2007, supplementary
data). This model is an oversimplification, and when pairing occurs
among homoeologs the resulting chromosome segregation patters
would be dependent on the location, size, and frequency of chiasmata, and segregation may fall between disomic and tetrasomic
models.
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the linked, interstitial transposition detected in the later
generations was nonreciprocal for the other parental fragment. Several rounds of homoeologous pairing and genetic
exchange could explain these results. Initial exchanges may
have destabilized subsequent pairing events, leading to more
extensive chromosome rearrangements in subsequent meioses. In each case, individual segregants were genotyped
from the generation before the detection of a HNRT in the
bulk analysis, and almost invariably the HNRTs were segregating 3 : 1 (see Fig. 5). Rearrangements of variable length
(determined by the number of linked markers involved)
were observed in some segregating individuals, and in one
case reciprocal rearrangements were detected (1 ⁄ 16 carried
one form and 1 ⁄ 16 carried the reciprocal form). Together,
these data suggest that homoeologous translocations in
resynthesized B. napus allopolyploids originated from intergenomic recombination events that segregated in a somewhat disomic pattern and fixed during the process of
selfing. As intergenomic homogenization occurred through
the fixation of translocations, sequence similarity increased
between homoeologs and may have increased homoeologous pairing and exchange. Over many generations translocation heterozygotes would increase, leading to distorted
segregation, aneuploidy, chromosome loss-and replacement
and centromere homogenization (see Fig. 3). The consequence is somewhat ratchet-like (polyploid ratchet), leading
to increased instability in the absence of acquired pairing
control. These types of chromosome anomalies have
recently been reported in recently formed natural Tragopogon allopolyploids and may arise as a consequence of homoeologous recombination (Lim et al., 2008).
Mapping studies in natural B. napus have detected preexisting and de novo homoeologous rearrangements (Parkin
et al., 1995; Sharpe et al., 1995; Udall et al., 2005), but
they occur at a much lower frequency than that which been
observed in resynthesized lines (Song et al., 1995; Gaeta
et al., 2007). Similarly, comparative genome analyses
among extant Brassica oleracea, Brassica rapa, and B. napus
have found little evidence for extensive rearrangement in
genome microstructure (Rana et al., 2004). As genetic variation in homoeologous pairing exists in B. napus (Jenczewski et al., 2003; Liu et al., 2006), the higher rate of change
in resynthesized lines could be attributed to the genetic
background of the parental lines used for synthesis.
Perhaps a better explanation for fewer observed homoeologous recombination events seen in domesticated vs resynthesized B. napus is that it is a consequence of natural
selection. Domesticated B. napus likely underwent natural
selection during its early evolution and currently undergoes
selection for fertility and other agronomic traits. Thus,
extensive genome rearrangements may have been selected
against. By contrast, resynthesized genotypes have been
selected for extreme flowering time (Pires et al., 2004)
or self-pollinated without selection by single-seed descent,
The Authors (2009)
Journal compilation New Phytologist Trust (2009)
New
Phytologist
Research review
(a)
S0 - S3
S4
S0 - S1
S2 - S4
S5
Review
nificant variation to gene expression and phenotypes (Pires
et al., 2004; Gaeta et al., 2007), and this may help a new
polyploid become established or exploit new niches. Resynthesized lines with extensive rearrangements generally show
low fertility (Gaeta et al., 2007), and in nature such lines
would probably not contribute to future generations. Any
rearrangements that beget further mispairing and rearrangement lead to a ‘polyploid-ratchet’ effect, and will likely be
selected against. Future studies can test these hypotheses in
resynthesized B. napus lines by allowing selection in
field-type analyses in natural environments or selection for
fertility.
(b)
S5
Fig. 5 The case of the polyploid ratchet. After an initial exchange
among homoeologs, further pairing and exchange in future meioses
can lead to additional translocation. The consequence is ‘ratchetlike’, leading to increased instability. Gaeta et al. (2007) analysed
several self-pollinated B. napus allopolyploids from generations S0
to S5. Examples from two resynthesized polyploid lines (A and B) are
shown. Grey chromosomes represent A1 from the Brassica rapa
subgenome and black chromosomes represent C1 from the Brassica
oleracea subgenome. Three markers at the end of A1–C1 homoeologous groups were used to screen bulked tissue across generations,
and individual plants (segregants) within generations (see Gaeta
et al., 2007, supplemental data). (a) In line A, an interstitial
nonreciprocal transposition was detected in the S4 generation (loss
of B. rapa markers, duplication of B. oleracea markers). A terminalized translocation was detected in the S5 generation and was
segregating in exactly 25% of 16 S4 plants when individually
genotyped. Because the terminalized translocation was not yet fixed
it went undetected in the bulk analysis of the S4 generation. Thus,
the rearrangement detected in the S5 generation had arisen as a
consequence of several rounds of meiosis and genetic exchange
during self-pollination. (b) In line B, a distal ⁄ terminal nonreciprocal
translocation was detected in the S2 generation by the two most
terminal markers screened. Again, exactly 25% of 16 S1 plants were
segregating for this rearrangement. In the S5, the most proximal
marker detected a linked, interstitial rearrangement; however, it was
nonreciprocal for the other parent relative to the distal rearrangement. This proximal rearrangement was segregating in three of 16
individual S4 plants. These observations are consistent with several
rounds of genetic exchange, which resulted in larger, more complex
rearrangements.
despite extensive rearrangements and deleterious phenotypes (Gaeta et al., 2007). Homoeologous rearrangements
in the early generations after formation can contribute sig-
The Authors (2009)
Journal compilation New Phytologist Trust (2009)
Conclusions
Molecular analysis in polyploids has provided evidence
that the genomic events that follow polyploidization
include genetic and epigenetic changes, changes in gene
expression and changes in phenotypic variation. However,
the mechanisms of, and consequences for, these changes
are still largely unknown. Studies in B. napus polyploids
have pointed to homoeologous pairing and recombination
as a key mechanism for genome restructuring; however,
there is still much to be learned regarding the consequences of homoeologous rearrangement on aneuploidy
and chromosome dosage changes, and whether it contributes to deletion and gene conversion reported in other
polyploids. Recent studies in Tragopogon that included
FISH analysis provided evidence that deletions and rDNA
changes detected in recent allopolyploids might also be the
consequences of homoeologous rearrangements (Lim et al.,
2008). While studies of newly resynthesized allopolyploids
continue to provide a window on the early events following hybridization and polyploidization, future studies
should include large numbers of independently resynthesized or recently formed natural polyploids, ideally with
multiple parental genotypes and reciprocal crosses. This
would allow for statistically relevant comparisons of the
relative propensities of different mutations (e.g. structural
vs epigenetic; nonreciprocal vs reciprocal) across genotypes
within a species and among different species or higher
taxa. In addition, analyses must go beyond simple ‘bandology’ and combine mapped dosage-sensitive markers with
cytogenetics to reveal not only patterns of genetic changes
but also mechanisms of change. Future studies might
address how environmental variations contribute to genome structure through analysis of newly formed allopolyploids over several generations under field-like conditions,
or by selection for specific phenotypes (Pires et al., 2004).
Resynthesized polyploids provide a unique model for
studying the role of recombination on genetic changes,
and how novel mutations may lead to new phenotypes
and heterosis that may be important for niche exploitation
and speciation under natural selection.
New Phytologist (2010) 186: 18–28
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25
26
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Research review
Acknowledgements
The term ‘polyploid ratchet’ was coined by Luca Comai in
2006. We thank two anonymous reviewers for their helpful
comments. J.C.P. is supported by the USA National
Science Foundation (DBI 0501712 and DBI 0638536).
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