Copyright  1998 by the Genetics Society of America
Comparative Mapping Between Arabidopsis thaliana and Brassica nigra Indicates
That Brassica Genomes Have Evolved Through Extensive Genome Replication
Accompanied by Chromosome Fusions and Frequent Rearrangements
Ulf Lagercrantz
Department of Plant Biology, Swedish University of Agricultural Sciences, S-750 07 Uppsala, Sweden
Manuscript received March 27, 1998
Accepted for publication July 24, 1998
ABSTRACT
Chromosome organization and evolution in the Brassicaceae family was studied using comparative
linkage mapping. A total of 160 mapped Arabidopsis thaliana DNA fragments identified 284 homologous
loci covering 751 cM in Brassica nigra. The data support that modern diploid Brassica species are descended
from a hexaploid ancestor, and that the A. thaliana genome is similar in structure and complexity to those
of each of the hypothetical diploid progenitors of the proposed hexaploid. Thus, the Brassica lineage
probably went through a triplication after the divergence of the lineages leading to A. thaliana and B. nigra.
These duplications were also accompanied by an exceptionally high rate of chromosomal rearrangements.
The average length of conserved segments between A. thaliana and B. nigra was estimated at 8 cM. This
estimate corresponds to 90 rearrangements since the divergence of the two species. The estimated rate of
chromosomal rearrangements is higher than any previously reported data based on comparative mapping.
Despite the large number of rearrangements, fine-scale comparative mapping between model plant A. thal-
iana and Brassica crops is likely to result in the identification of a large number of genes that affect
important traits in Brassica crops.
ONE important aspect of genome evolution is polyploid (Masterson 1994). Furthermore, recent ge-
changes in organization of the DNA caused by netic mapping has revealed cryptic polyploids indicating
duplications and chromosomal rearrangements. Com- that the level of polyploidy has been underestimated in
parative linkage mapping has indicated that many ani- several species (Helentjaris et al. 1988; Reinisch et al.
mal and plant genomes have remained surprisingly con- 1994; Moore et al. 1995; Lagercrantz and Lydiate
served during evolution (O'Brien et al. 1988; Whitkus 1996). Recent studies have also suggested that poly-
et al. 1992; Ahn and Tanksley 1993; Morizot 1994; ploidization may be accompanied by rapid genomic
Moore et al. 1995). However, a variation between differ- change (Song et al. 1995; Kenton et al. 1993; Chen and
ent evolutionary lineages in the rate of chromosomal Armstrong 1994; Jellen et al. 1994; Lagercrantz
evolution is evident, both from cytogenetic work (Wil- and Lydiate 1996; Shoemaker et al. 1996; Leitch and
son et al. 1974, 1977; Bush et al. 1977; Eldridge and Bennet 1997).
Close 1993) and comparative mapping (Nadeau and The family Brassicaceae (Cruciferae) is widely distrib-
Taylor 1984; Barendse et al. 1994; Johansson et al. uted and comprises more than 3000 species in approxi-
1995; Graves 1996; Ehrlich et al. 1997). This pattern mately 350 genera. The family includes important crops
has led O'Brien et al. (1988) to suggest that karyotypes such as Brassica oleracea, B. napus, and B. rapa, as well as
are generally conservative but occasionally undergo ra- the extensively studied model plant Arabidopsis thaliana.
diation or "shuffles." The cause of these sporadic shuf- The family's major centers of diversity are southwestern
fles is still under debate. In plants, conservation of and central Asia and the Mediterranean region. Second-
surprisingly large chromosomal segments has been ob- ary centers of diversity are in the arctic, western North
served in the Graminae family (Moore et al. 1995), while America, and the mountains of South America (Price
tomato and chili pepper, in the Solanaceae family, often et al. 1994).
have been cited as a pair of species that differ by a Species within the family exhibit a continuous range of
relatively large number of rearrangements (Tanksley haploid chromosome numbers from 5 to 15, excluding a
et al. 1988; Prince et al. 1993). large number of known polyploid species with higher
Polyploidy is particularly common among plants. It chromosome numbers. Previous comparative mapping
has been estimated that up to 80% of angiosperms are has indicated that present-day diploid species in the
Brassica genus are derived from a hexaploid ancestor
(Lagercrantz and Lydiate 1996). Furthermore, pre-
Address for correspondence: Department of Plant Biology, Swedish
liminary comparisons between Brassica species andUniversity of Agricultural Sciences, Box 7080, S-750 07 Uppsala,
Sweden. E-mail: ulf.lagercrantz@vbiol.slu.se A. thaliana have indicated that the A. thaliana genome
Genetics 150: 1217­1228 (November 1998)
1218 U. Lagercrantz
cross population of 88 individuals in which it was possible tohas a complexity corresponding to one of the three
score segregation of markers from both the F1 and (highlysubgenomes of modern diploid Brassica species (Lager-
heterozygous) recurrent parents. Linkage maps from meioses
crantz et al. 1996; Scheffler et al. 1996; Cavell et al. in the F1 and recurrent parents were initially developed sepa-
1998). Comparative mapping data have also indicated rately using MAPMAKER 3.0 (Lander et al. 1987; Lincoln et
al. 1992) and then integrated using JoinMap (Stam 1993).a relatively high rate of chromosomal rearrangements
The integration of two linkage maps can introduce orderingin the Brassicaceae family (Kowalski et al. 1994;
errors, particularly if few markers are common to both maps.Lagercrantz and Lydiate 1996; Osborn et al. 1997).
This potential source of inaccuracy caused few problems in
With one exception, previous comparisons between the the current analysis as a majority of the loci positioned on the
Brassica and Arabidopsis genomes have been limited map from the recurrent parent were also positioned on the F1
map (Lagercrantz and Lydiate 1996). All loci were detectedto small genomic regions (Lagercrantz et al. 1996;
using Southern hybridization analysis as described by Lager-Scheffler et al. 1996; Cavell et al. 1998). The only
crantz and Lydiate (1995), except that washing was carriedacross-genome comparison published so far (Kowalski
out at a lower stringency (2 SSC, 0.1% SDS at 65 ). Hybridiza-
et al. 1994) was based on a low marker density (the 75 tion probes were prepared by PCR or gel isolation of inserts
previously positioned B. oleracea loci had an average and labeled with [32
P]dCTP.
A set of 160 DNA fragments from the A. thaliana genomespacing of one locus per 13 cM; Slocum et al. 1990).
were used as RFLP probes. The probes were derived from theBecause of the limitations of incomplete polymorphism
following sources (prefix, reference, and source in parenthe-in the B. oleracea population, the degree of genome
ses): 69 genomic PstI clones (mi, Liu et al. 1996, Ohio Stock
replication in B. oleracea was also underestimated in that Center); 21 anonymous cDNAs (ve, D. Bouchez, personal
study. Consequently, to elucidate the relationship be- communication, Ohio Stock Center); 18 genomic clones from
the ARMS set (m, Fabri and Schaeffner 1994, Ohio Stocktween the uniquely small genome of A. thaliana and the
Center); 20 anonymous cDNAs (um, McGrath et al. 1993,highly replicated Brassica genomes, there is a need for
Ohio Stock Center); 8 anonymous cDNAs (y and tai224, un-additional comparative mapping data. The apparently
published data, Ohio Stock Center); and six YAC end probes
high rate of chromosomal rearrangements in the Brassi- and 3 anonymous cDNAs (L, R, and c, Lagercrantz et al.
caceae family also requires an exceptionally high density 1996, Dr. G. Coupland). In addition, the following character-
of markers. ized A. thaliana genes were used: Phytochrome A, B, and C
(phy, Sharrock and Quail 1989, Dr. P. Quail); Athb3, Athb7,The complete genome sequence of A. thaliana will
Athb13 (Athb, So¨derman 1996, Dr. P. Engstro¨m); Chalconebe available within a few years (Ecker 1998), and the
synthase (chs, Feinbaum and Ausubel 1988, Dr. G. Coup-
function of many of the identified genes will become land); Ara (Matsui et al. 1989, Dr. H. G. Nam); Rps2 (rps2,
elucidated. An understanding of the complex relation- Mindrinos et al. 1994, Dr. F. Ausubel); Gpa1 (gpa1, Ma et al.
ship between the small genome of A. thaliana and its 1990, Dr. H. Ma); GapC (gapC, Shih et al. 1991, Dr. M-C.
Shih); Rns1 (rns1, Bariola et al. 1994, Dr. P. Green); Ag (ag,highly replicated close relatives in the Brassica genus
Yanofsky et al. 1990); Ga1 (ga1, Sun and Kamiya 1994);could have a great impact on the understanding of the
and Pg11 (pg11, Gallant and Goodman, unpublished data).
biology and the improvement of the important Brassica
Probes for these were derived from cDNA clones, except for
crops. Chs2 (genomic clone) and Ag, Ga1, and Pg11 (PCR amplified
To obtain a more comprehensive picture of the rela- from genomic A. thaliana DNA; Konieczny and Ausubel
1993).tionships between A. thaliana and the members of the
Most probes (88%) were mapped in A. thaliana using theBrassica genus, I applied a large number of previously
recombinant inbred (RI) population of Lister and Deanmapped A. thaliana probes to a highly polymorphic map-
(1993). The positions of the loci detected by a few of these
ping population of B. nigra. This strategy yielded a high probes were inferred from physical mapping data. Thirteen
marker density (an average spacing of one locus per A. thaliana expressed sequence tags (ESTs) (ve29, ve30, ve45,
3 cM), and a high proportion of replicated loci mapped. ve50, ve53, ve57, y22, y29, y33, y34, y35, y36, and y37) were
assigned to YAC clones (ve clones, D. Bouchez, personal com-Compared to earlier studies, these data allowed a much
munication; y clones, http://genome-www.stanford.edu/more detailed comparison comprising the entire A. thal-
Arabidopsis/ EST2YAC.html/), and the genetic map position
iana genome. The data support that diploid Brassica was inferred from the position on the RI map of genetically
genomes contain three copies of a basic genome similar mapped fragments from the same YAC clone. The genetic
in size to the A. thaliana genome, and that chromosome map positions of all loci on the RI map were extracted from
the map published electronically (http://nasc.nott.ac.uk/evolution in Brassicaceae seems to involve an exception-
new ri map.html/).ally high rate of chromosomal rearrangements. The
Nineteen probes were mapped in separate A. thaliana
comparative data also have implications for the possibili-
crosses (Ara and PhyB, Hauge et al. 1993; 17 of the um probes,
ties of transferring genetic resources and information McGrath et al. 1993). Loci segregating in two crosses were
between A. thaliana and Brassica species. used to infer the relative order of loci mapped in one cross
only. Several of the um probes also detect multiple loci in
A. thaliana. This complicates the identification of the true
orthologous/homeologous loci in B. nigra. In this study, umMATERIALS AND METHODS
loci in A. thaliana and B. nigra were considered homeologous
if they were positioned next to another homeologous locusThe B. nigra genetic map was developed using a previously
pair detected with a non-um probe. Consequently, occasionaldescribed mapping population (Lagercrantz and Lydiate
1995). The population was a highly polymorphic, first back- erroneous classifications of true homeologous locus pairs
1219Rapid Chromosomal Evolution in Brassicaceae
would result in an underestimate of the number of re- in many cases. However, a few large chromosomal seg-
arrangements that have occurred since the divergence of the ments have remained largely intact since the divergence
lineages leading to A. thaliana and B. nigra. Data from the
of Arabidopsis and Brassica, and for these segments,um probes were excluded in calculations of the degree of
which occur as single copy in A. thaliana, there areduplication in B. nigra.
Polymorphic loci detected using the A. thaliana probes were strong indications that they occur in three homeologous
positioned on the B. nigra genetic map relative to 288 loci copies in B. nigra (Figure 2). At least 40 cM of the
previously mapped using Brassica RFLP probes (Lager- top of A. thaliana chromosome 5 is present in three
crantz and Lydiate 1995).
homeologous copies on linkage groups G2, G5, and G8
in B. nigra. Two of the B. nigra segments appear collinear
with the A. thaliana segment, while the third segment
RESULTS
on G5 contains a large inversion compared to that of
A total of 160 mapped DNA fragments from the A. A. thaliana.
thaliana genome revealed 284 polymorphic loci that Furthermore, large portions of A. thaliana chromo-
were incorporated into the existing B. nigra linkage map some 2 seem to correspond to three homeologous seg-
(Figure 1). With one exception, each B. nigra linkage ments in B. nigra (Figure 2). The bottom 40 cM of A. thal-
group contained loci detected with probes from all five iana chromosome 2 corresponds to a contiguous 50-cM
A. thaliana chromosomes (Figure 1, Table 1). This pat- tract on B. nigra G6, while the homeologous segments
tern indicates that substantial chromosomal rearrange- on B. nigra G1 and G8 are interrupted by segments from
ments have occurred since the divergence of the ances- other A. thaliana chromosomes (Figures 1 and 2). Loci
tors to A. thaliana and B. nigra. homologous to those from the top half of A. thaliana
To be able to elucidate the true degree of collinearity chromosome 2 are scattered mainly on the three linkage
between the genomes of A. thaliana and B. nigra, the groups in B. nigra: G3­G5.
highly duplicated nature of the B. nigra genome has to In addition, a 40-cM segment of A. thaliana chromo-
be fully appreciated. A majority of A. thaliana probes some 3 corresponds to three homeologous tracts in
detect a single locus in A. thaliana (Cavell et al. 1998; B. nigra (Figure 2). The three B. nigra tracts are all
Chang et al. 1988). In contrast, in B. nigra, the A. thali- associated with tracts homeologous to A. thaliana chro-
ana probes detected on average 1.8 polymorphic loci mosome 1 segments (depicted in gray in Figure 2). In
per probe, which is close to the 1.9 loci per probe de- two of the B. nigra tracts, the A. thaliana chromosome
tected in the same population using Brassica RFLP 3 homeologous segments are interrupted by the tract
probes (Lagercrantz and Lydiate 1996). Both those homeologous to chromosome 1, and for the third tract,
estimates are clearly underestimates of the true level of an inversion seems to have placed the chromosome 1
duplication caused by residual monomorphism (Lager- homeologous tract at the end of the linkage group.
crantz and Lydiate 1996). Even if the degree of poly- Triplicated homeologous copies are also discernible for
morphism is as high as 70% (as estimated in the present more limited regions of the A. thaliana genome (data
study), the probability that all loci in a triplicate set not shown), but as the homeologous regions get smaller,
are polymorphic is 34%. Thus, in a hexaploid where it becomes progressively more difficult to detect tripli-
virtually every probe should identify three homeologous cated copies, if they exist, because of lack of polymor-
loci, about one-third of these triplicate loci would be phic loci.
mapped, even in this extremely polymorphic popula- Although it is not possible to identify triplicated struc-
tion. tures in B. nigra corresponding to the entire A. thaliana
Previous mapping using Brassica RFLP probes has genome, probes from the different A. thaliana chromo-
suggested that the entire B. nigra genome appears to somes detected a similar level of duplication, ranging
consist of large, duplicated segments, with the majority from 1.4 to 1.9 loci per probe (Table 1; F4137 1.8, P
of RFLP loci detecting three dispersed, homeologous loci 0.1), indicating that none of the A. thaliana chromo-
(Lagercrantz and Lydiate 1995, 1996). The present somes are significantly over- or underrepresented in
study supports these findings. The mapping population duplicate homeologous copies in B. nigra. To get a more
used by Lagercrantz and Lydiate (1995, 1996) was complete description of replicated regions correspond-
also used in the present study, and the additional 284 ing to different A. thaliana segments, an even higher
loci based on A. thaliana probes corroborated the pre- density of markers is needed.
viously identified triplicated segments comprising virtu- The scattered distribution of markers from different
ally the whole B. nigra genome (data not shown). These A. thaliana chromosomes on all B. nigra linkage groups
data support the hypothesis that B. nigra is descended suggests that a very large number of chromosomal re-
from a hexaploid ancestor. arrangements have occurred since the divergence from
How does this triplicated nature of the B. nigra ge- a common ancestor. Simply counting the number of
nome correspond to the structure of the A. thaliana breakpoints that are needed to account for markers
genome? Because of the high frequency of rearrange- from different A. thaliana chromosomes that are adja-
cent on B. nigra linkage groups yields 79 breakpointsments (see below), collinear segments are quite short
1220 U. Lagercrantz
Figure 1.--Comparative map of A. thaliana and B. nigra. The eight linkage groups of B. nigra (G1­G8) are represented by
vertical lines. Loci on the right of each linkage group were detected using probes previously mapped in A. thaliana. The
chromosomal locations of A. thaliana loci detected using these probes are shown with different colors as indicated. Loci on the
left of each linkage group were previously located using Brassica RFLP probes (Lagercrantz and Lydiate 1995). Recombination
distances are given in Kosambi centimorgans.
1221Rapid Chromosomal Evolution in Brassicaceae
TABLE 1
Number of polymorphic loci detected with RFLP probes from different A. thaliana chromosomes
B. nigra linkage group
A. thaliana No. of Total Loci/
chromosome probes 1 2 3 4 5 6 7 8 no. loci probe
1 33 5 7 10 12 7 9 5 0 55 1.7
2 18 7 1 6 3 2 5 2 6 32 1.8
3 22 9 2 1 3 5 5 11 6 42 1.9
4 27 2 4 7 2 9 2 2 10 38 1.4
5 39 1 22 1 6 13 5 5 8 61 1.6
1-5 140 24 36 25 26 36 26 25 30 228 1.6
All probes 160 26 44 40 30 42 36 29 37 284 1.8
Probes known to detect more than one locus in A. thaliana are excluded except in the last row (all probes).
(Figure 1). This calculation does not account for the cases, inversions either in the Arabidopsis or the Brassica
lineage are needed to account for the different orderfact that several blocks of loci syntenic with particular
A. thaliana chromosomes are not collinear. For exam- of homeologous loci.
To obtain a more detailed picture of the number andple, on B. nigra G2, neither the block on top homeologus
to A. thaliana chromosome 1 nor the large, contiguous types of rearrangements that have occurred during the
evolution of Arabidopsis and Brassica from a commonblock homeologous to A. thaliana chromosome 5 are
collinear with their A. thaliana counterparts. In both ancestor, an attempt was made to reconstruct ancestral
Figure 2.--Large A. thaliana chromosomal segments correspond to triplicated homeologous segments in B. nigra. Detailed
comparative linkage maps of selected segments of the A. thaliana genome. A 40-centimorgan segment of A. thaliana chromosome
5 corresponds to three homeologous tracts on G2, G5, and G8 in B. nigra. The bottom half of A. thaliana chromosome 2 is
homeologous to segments on B. nigra G1, G6, and G8. Forty centimorgans of the top of A. thaliana chromosome 3 corresponds
to triplicated segments, one on B. nigra G1 and two on G7. The numbers connected with lines to loci on A. thaliana chromosome
2 indicate linkage group location of homologous loci in B. nigra. Those B. nigra loci are not adjacent on their respective linkage
groups and, thus, are not connected by vertical lines (representing synthenic segments) in the figure.
1222 U. Lagercrantz
Figure 3.--Tentative mod-
els for the evolution of B. nigra
G1 and G8 (see text for de-
tails). The present-day B. nigra
linkage groups are shown on
the left. , inversions; , ad-
ditional chromosome breaks
(fissions of translocations) that
are necessary to explain the dif-
ferences between A. thaliana
and B. nigra linkage groups; T,
loci where the A. thaliana ho-
mologue is located close to a
telomere; C, positions that in
A. thaliana correspond to posi-
tions close to a centromere.
The color of the different loci
indicate the chromosomal lo-
cation of the A. thaliana locus
detected with the correspond-
ing probe, as in Figure 1.
chromosomal segments by invoking a minimal number sions, as illustrated for linkage groups G1 and G8 in
Figure 3. Invoking six inversions on B. nigra G8 resultsof rearrangements resulting in segments collinear with
tracts in the A. thaliana genome. The B. nigra linkage in four syntenic blocks, two of which are apparently
contiguous and collinear with A. thaliana.groups show a typical pattern of relatively large blocks
of markers from particular A. thaliana chromosomes The other two blocks (homeologous to segments
from A. thaliana chromosomes 3 and 4) are also collin-interrupted by a few markers from one or more other
A. thaliana chromosomes. This distribution can, to a ear, but they probably lack an internal piece of the
segment, as indicated by an additional breakpoint inlarge extent, be explained by a limited number of inver-
1223Rapid Chromosomal Evolution in Brassicaceae
TABLE 2 two or more markers. An estimate of the number of
chromosomal rearrangements based on these data re-Estimated number of inversion and translocations/
quires the number of chromosomes in the last commonfusions since the divergence of A. thaliana and B. nigra
ancestor of A. thaliana and B. nigra. This number is not
known, but it will only affect the estimate marginally.Linkage Translocations/
group Inversions fusions Total Assuming tentatively that the ancestor to B. nigra has 15
chromosomes (three copies of the A. thaliana genome)1 5 4 9
results in an estimate of 87 rearrangements. Assuming2 9 7 16
conservatively that the ancestor to B. nigra has 8 chromo-3 11 8 19
4 13 7 20 somes results in a marginally higher estimate of 94 re-
5 8 6 14 arrangements. In comparisons of the number of re-
6 3 5 8 arrangements with other species (see discussion), an
7 7 8 15
estimate of 90 rearrangements was used.
8 6 5 11
Several loci that map close to the telomeres onTotal 62 50 112
A. thaliana chromosomes have homologous loci map-
ping internally on B. nigra linkage groups. The positions
of some of those loci in B. nigra suggest that direct
Figure 3. This conclusion is based on the fact that the telomere-telomere fusion might have been important
A. thaliana homologues to loci flanking the breakpoints in the restructuring of Brassica genomes. In the hypoth-
are separated by a large segment, and that within this esized scenario for G8 (Figure 3), there are at least
A. thaliana segment there are at least subsegments that three positions where adjacent blocks corresponding to
correspond to three homeologues on other B. nigra two different A. thaliana chromosomes are joined by
linkage groups. loci that have homologues close to the telomeres in
It should be pointed out that there are other possible A. thaliana.
scenarios for the chromosomal evolution than those The positions of centromeres on the genetic map of
presented in Figure 3, but the fact that a single inversion A. thaliana have been reported recently (Round et al.
often places scattered makers, not only in a syntenic 1997). In Figure 3, homologous positions to some of
block, but also in a collinear position, makes the pro- the A. thaliana centromeres have been inferred through
posed scenario attractive. The estimates of the number the positions of B. nigra homologues to centromere-
of rearrangements are shown in Table 2. The estimates linked loci in A. thaliana. The proposed locations of the
range from 8 to 20 rearrangements per B. nigra linkage regions that are homologous to A. thaliana centromeres
group, resulting in a total of 112 rearrangements. These are close to the breakpoints of chromosomal re-
estimates should be regarded as maximum estimates arrangements in all cases (Figure 3). In at least two
based on the present data as all interruptions of synteny cases, however, the positions of flanking loci indicate
are not necessarily the result of chromosomal re- that the breakpoint has not been in the centromere
arrangements. There are a number of segments in Fig- itself. On G1, mi19b and mi291c map in a cluster of
ure 1 that are defined by a single locus. An alternative loci from different A. thaliana chromosomes. The cen-
explanation to the occurrence of such single loci dis- tromere is located between mi19 and mi291 in A. thali-
rupting an otherwise syntenic segment could be the ana, suggesting that the chromosome break resulting
transposition of a duplicated small segment or even in the different structures in A. thaliana and B. nigra
partial transcripts. took place outside these flanking markers. Similarly, on
To reduce the potential bias caused by single deviant B. nigra G8, the homologous segment to A. thaliana
loci, the number of rearrangements and the length of chromosome 4 includes y29b and mi306a mapping
conserved segments were also estimated from map dis- closely together. Assuming that the mapping data in
tances between the outmost markers of conserved seg- A. thaliana are correct, the homologues to these two
ments (Nadeau and Taylor 1984). Using this method, loci flank the centromere.
a single deviant locus will only affect the estimate if it
disrupts an otherwise collinear segment. In the present
DISCUSSION
data, however, the single deviant loci are always located
at the breakpoint between different segments (Figure Replication in Brassica genomes: The A. thaliana ge-
1). Even when a single deviant locus is flanked by loci nome is one of the smallest among higher plants, with
homologous to the same A. thaliana chromosome (e.g., an estimate of 145 million bp (Mbp, Arumuganathan
as for ve23b about two-thirds down on G2; Figure 1), and Earle 1991) distributed on five chromosomes in
this locus does not interrupt collinearity as it is located at the haploid complement. In the Brassicaceae family,
an inversion breakpoint. The estimate of the conserved chromosome numbers and DNA content show a large
length using mapping data from B. nigra is 8 cM. This variation, from a low in A. thaliana to 19 chromosome
pairs and 1235 million bp per haploid complement inestimate is based on 41 conserved segments, including
1224 U. Lagercrantz
B. napus. It has been suggested that the small genome A. thaliana are located close to a telomere often map
size of A. thaliana results from an exceptionally low internally on B. nigra linkage groups (Figure 3). B. nigra
amount of repetitive DNA and high gene density (Mey- G8 comprises six such homologous loci, indicating six
erowitz 1992; Bevan et al. 1998). The present study interstitial telomeric sites. Preliminary data (J. Fahle-
and other comparative mapping data now suggest that son, T. Axelsson and U. Lagercrantz, unpublished
these attributes might be typical for most Brassicaceae results) indicate that at least some of these sites actually
species, and that the differences in genome content, to contain sequences hybridizing to the telomeric repeat
a large extent, are caused by different degrees of whole- from A. thaliana (Richards and Ausubel 1988). Fur-
genome replication. Comparative mapping among the thermore, comparative mapping of B. oleracea (n 9),
three diploid species--B. nigra, B. oleracea, and B. rapa-- B. nigra (n 8), and B. rapa (n 10) support that
supports the hypothesis that these genomes were de- changes in chromosome numbers caused by chromo-
scended from a hexaploid ancestor with three copies some fusion or fission are frequent and also have oc-
of a rearranged unit genome still discernible (Lager- curred recently in the Brassicaceae family (Lager-
crantz and Lydiate 1996). There is also good evidence crantz and Lydiate 1996).
that B. napus is an amphidiploid arisen from the hybrid- Rapid chromosomal evolution in Brassica genomes:
ization of the two diploid species B. oleracea and B. rapa A number of comparative analyses of genomes within
or close relatives (U 1935; Parkin et al. 1995). the animal and plant kingdoms have suggested that the
In the present study, the few large segments that have rate of chromosomal rearrangements is surprisingly low
remained largely intact since the divergence of the an- in most cases (Nadeau and Taylor 1984; O'Brien et
cestors of Brassica and Arabidopsis are present in three al. 1988; Moore et al. 1995). However, the present study
homeologous copies in B. nigra, but in a single copy in indicates that the evolution of genomes in the Brassica-
A. thaliana. In addition, there are a number of smaller ceae family involves an unusually high rate of chromo-
segments of the A. thaliana genome that have three somal rearrangements. Different methods for estimat-
homeologous copies in B. nigra. Although it was not ing the amount of rearrangements since the divergence
possible to detect three homeologous copies of every of Arabidopsis and Brassica lineages resulted in figures
single segment of the A. thaliana genome, the present
ranging from 79 to 112. To compare the A. thaliana-
data support that the A. thaliana genome is similar in
B. nigra data with previously published data, I used the
complexity to the triplicated unit genome of the diploid
estimate of 90 rearrangements obtained using the
Brassica species. Furthermore, the B. nigra genome
method of Nadeau and Taylor (1984). The number
(0.97 pg/diploid nucleus; Arumuganathan and Earle
of rearrangements in other species was also recalculated
1991) is approximately three times larger than that of
from published data using the same method (Table 3,
A. thaliana (0.3 pg/diploid nucleus; Arumuganathan
Figure 4). This method has shown to be remarkably
and Earle 1991). Parallel comparisons of limited por-
good, even with small sample sizes; modest genetic maps
tions of the A. thaliana and B. napus genomes (Schef-
and possible mapping errors do not seem to influence
fler et al. 1996; Osborn et al. 1997; Cavell et al. 1998)
results dramatically (Ehrlich et al. 1997).
are congruent with the present data, showing an average
Estimates of the divergence times between different
of six homeologous copies of A. thaliana segments in
species and genera in the Brassicaceae family varythe amphidiploid B. napus. Kowalski et al. (1994) also
widely. Divergence time ranging from 10 million years,found evidence for triplication of some homeologous
based on paleopalynological data (Muller 1981), to 35copies of A. thaliana segments in the B. oleracea genome,
million years, based on DNA sequence data from thebut a genome-wide triplication was not suggested. The
rbcL gene (R. Price, personal communication), havelower marker density and limited polymorphism in this
been suggested for the lineages leading to Arabidopsisearlier study probably led to a systematic underestima-
and Brassica. Even if we conservatively assume a diver-tion of genome replication in Brassica.
gence time of 35 million years, the A. thaliana-B. nigraAssuming that the lineage leading to the present-
comparison reveals an exceptionally high rate of chro-day diploid Brassica species has indeed gone through
mosomal rearrangements (Table 3, Figure 4). Amonga triplication of the genome, these replications must
previous comparisons, humans and mice are amonghave been accompanied by a number of chromosome
those that have diverged most rapidly (Ehrlich et al.fusion events to reduce the chromosome number. It is
1997). The estimate of the length of conserved segmentsnot likely that the common ancestor of Arabidopsis and
from Copeland et al. (1993) of 8.8 cM results in anBrassica had a considerably lower number than A. thali-
estimate of 144 rearrangements between man andana. If the common ancestor also had 5 chromosomes
mouse (Ehrlich et al. 1997). Assuming a divergenceand this genome was triplicated, the chromosome num-
time of rodents and primates of 114 million years (Jankeber had to be reduced from 15 to 8 in the lineage
et al. 1994) yields an estimate of 0.63 rearrangementsleading to B. nigra.
per million years. Even in comparison to the divergenceThe present comparative mapping data support such
of mouse and man, A. thaliana-B. nigra, with approxi-a reduction in chromosome numbers through chromo-
some fusions. In B. nigra, homologues to loci that in mately 3 rearrangements per million years, stands out
1225Rapid Chromosomal Evolution in Brassicaceae
TABLE 3
Estimated number of chromosomal rearrangements and
approximate divergence times for various taxa
Divergence Number of
Species/genera time (million yr) rearrangements a
B. rapa-B. oleracea 1 b
5 h
B. nigra-B. rapa 20 b
10 h
B. nigra-B. oleracea 20 b
12 h
A. thaliana-B. nigra 35 b
90 i
Lycopersicon-Solanum 10 c
5 j
Lycopersicon-Capsicum 40 c
14 k
Oryza-Zea 66 d
35 l
Sorghum-Zea 24 e
15 m
Gossypium spp. 10 f
9 n
Homo-Sus 93 g
35 o
Sus-Mus 114 g
77 o
Figure 4.--Estimated number of chromosomal rearrange-
Homo-Mus 114 g
144 p
ments differentiating various animal species pairs and plant
species pairs vs. approximate divergence times. All estimatesa
Estimates based on the method presented by Nadeau and
are based on comparative linkage mapping. , comparisonsTaylor (1984), except Lycopersicon-Solanum and Gossyp-
between species in the Brassicaceae family; , comparisonsium A/D genome comparisons, which were direct counts from
including Mus; , all other comparisons. The straight line ispublished data (Tanksley et al. 1992; Reinisch et al. 1994).
estimated from linear regression excluding data from Brassica-Recalculations from original publications were performed on
ceae ( ) and Mus ( ).some data (Whitkus et al. 1992; Ahn et al. 1993; Prince et al.
1993; Lagercrantz and Lydiate 1996).
b
R. Price (personal communication).
sica, it is not possible to conclude if the high rate ofc
Paterson et al. (1996).
d
E. Kellogg, (personal communication). chromosomal divergence is typical of Brassicaceae spe-
e
Gaut and Doebley (1997). cies that have diverged more recently than A. thalianaf
Wendel (1989).
and B. nigra. Sequence data from the large subunit ofg
Janke et al. (1994).
rubisco suggest that B. nigra diverged from B. rapa/h
Lagercrantz and Lydiate (1996).
oleracea 20 mya and B. rapa diverged from B. oleraceai
This study.
j
Tanksley et al. (1992). 1 mya (R. Price, personal communication). If these
k
Prince et al. (1993). data are reasonably correct, the rate of chromosomall
Ahn et al. (1993).
rearrangements in these lineages does not seem to bem
Whitkus et al. (1992).
higher that in most other plant and animal species (Ta-n
Reinisch et al. (1994).
ble 3, Figure 4).o
Johansson et al. (1995).
p
Copeland et al. (1993). Why has the rate of chromosomal repatterning been
so high between A. thaliana and B. nigra? Population
structure and recent polyploidization are probably im-
as having experienced an extreme rate of chromosomal portant factors contributing to the rapid rearrange-
repatterning. ments of Brassicaceae chromosomes. The present study
Kowalski et al. (1994) obtained an estimate of at and other data (Lagercrantz and Lydiate 1996) sug-
least 26 rearrangements since the divergence of A. thali- gest that modern diploid species of Brassica and related
ana and B. oleracea. This estimate is considerably lower genera have descended from a common hexaploid an-
than that obtained in the present study. A considerable cestor and are, thus, degenerate hexaploids. It seems
part of this difference most likely results from a lower likely that the replications have occurred through am-
marker density in the previous study. Comparative map- phidiploidization the same way as novel amphidiploids
ping data between limited chromosomal regions of such as B. napus, B. juncea, and B. carinata are derived
A. thaliana and B. napus support an extremely high from hybridization between different diploids (U 1935;
rate of rearrangements for some chromosomal regions Parkin et al. 1995; Axelsson et al. 1998). Allopolyploidi-
(Osborn et al. 1997). A 14-cM tract on the B. napus zation is likely to result in an increase in aberrant mei-
linkage group N2 corresponds to segments from four otic pairing and translocations among homeologous
different A. thaliana chromosomes. If such highly re- chromosomes. Studies of resynthesized B. napus plants
arranged regions are common, as also indicated in the show that intergenomic translocations are surprisingly
present study, a marker density of 15 cM [as for frequent between chromosomes from B. oleracea and
B. oleracea markers on the A. thaliana map of Kowalski B. rapa (Lydiate et al. 1993; U. Lagercrantz and
et al. (1994)] is likely to underestimate the true level of D. Lydiate, unpublished results).
rearrangements. Chromosome fusions after duplication also might
have resulted indirectly in an increase of the frequencyBecause of the poor data on divergence times in Bras-
1226 U. Lagercrantz
of rearrangements. As discussed above, polyploidization sica species, and were rearrangements mainly confined
to a short period after polyploidization? Have re-in the Brassica lineage has probably been followed by an
extensive reduction in chromosome number through arrangement frequencies been higher in species where
chromosome numbers have been reduced as a result ofchromosome fusion events. These fusions have appar-
ently resulted in interstitially located telomere repeats chromosomal fusions, or is the frequency of rear-
rangements mainly an effect of population structure?[ITRs (TTTAGGG)n]. There are several independent
data suggesting that such ITRs may be particularly prone Practical implications: Obviously, the highly repli-
cated nature of Brassica genomes must be acknowl-to recombination, breakage, and fragility (Hastie and
Allshire 1989; Meyne et al. 1990; Barnett et al. 1993; edged. It is likely that many important traits in Brassica
species are controlled by duplicated genes originatingBertoni et al. 1994; Slijepcevic et al. 1996). The posi-
tion of ITRs in the B. nigra genome (J. Fahleson, from previous whole-genome replications. Identifica-
tion of such duplicate genes would facilitate the under-T. Axelsson and U. Lagercrantz, unpublished re-
sults) supports their involvement in chromosomal rear- standing of the genetics and the improvement of various
agronomic traits.rangements. The ITRs that have been positioned are
almost exclusively located at the breakpoints between There are also good prospects for utilization of the
rich source of biological information and genetic re-conserved blocks in the B. nigra genome.
Assuming no selective advantage of chromosomal re- sources emanating from A. thaliana research. Even
though the rearrangements have been frequent sincearrangements (Lande 1979), the rate of chromosomal
rearrangements depends on mutation rate and random the divergence of Arabidopsis and Brassica, the average
length of conserved segments between A. thaliana andfixation rate. The effect of replication provides an expla-
nation as to the generation of a relatively high number B. nigra was estimated at 8 cM. Thus, mapping a Brassica
gene to an interval of 10 cM is often likely to allowof new rearrangements in Brassicaceae genomes. How-
ever, a key step in karyotype evolution is the fixation of the identification of the homeologous collinear region
in A. thaliana. It should be kept in mind that somenewly arisen chromosomal rearrangements. Transloca-
tions and inversions are generally deleterious when het- regions of the genome are considerably more rear-
ranged, which will require much more detailed map-erozygous, but have normal fitnesses when homozygous
(White 1973). The fixation of such rearrangements ping. There is also a lack of data on the amount of
fine-scale rearrangements that are not detected usingrequires small, isolated populations and is aided greatly
by self-fertilization (Lande 1979). Many wild Brassica- comparative linkage mapping data. Such local re-
arrangements could obviously complicate the identifi-ceae species occupy marginal fragmentated habitats,
such as maritime cliffs (Snogerup et al. 1990; Mithen cation of homologous genes in A. thaliana and Brassica
solely on the basis of their map position.et al. 1995). This distribution is likely to result in small
deme sizes and high turnover rates of local populations. Still, with the prospect that a large proportion of the
genes in A. thaliana will soon be identified, further fine-The exposed habitat is likely to lead to relatively fre-
quent local extinction and recolonization. Local fixa- scale comparative mapping in the Brassicaceae family
is likely to result in the identification of a large numbertion is favored by small, reproductively isolated demes
and selfing. Once established in a deme, a negatively of genes that affect important traits in different Brassica
crops.heterotic gene arrangement can spread in homozygous
form through a subdivided population by random local I thank L. Andersson, T. Axelsson, and two anonymous reviewers
extinction and recolonization. Although the population for valuable comments. I am also grateful to the Arabidopsis Biological
Resource Center and the people listed in materials and methodsstructure of Brassicaceae species in the past is largely
for kindly sending DNA clones. This work was supported by grantsunknown, the present-day population structure of many
from the Swedish Natural Science Research Council and the Carl
species suggests an explanation as to the high rate of
Trygger Foundation.
chromosomal rearrangements evident in some lineages
of Brassicaceae. A combination of an enhanced level of
chromosomal mutations caused by genome replication
LITERATURE CITED
and a population structure characterized by small deme
size may have contributed to the exceptionally high rate Ahn, S., and S. Tanksley, 1993 Comparative linkage maps of the rice
and maize genomes. Proc. Natl. Acad. Sci. USA 90: 7980­7984.of rearrangements observed between A. thaliana and
Ahn, S., J. Anderson, M. Sorrells and S. Tanksley, 1993 Homeol-
B. nigra. ogous relationships of rice, wheat and maize chromosomes. Mol.
Gen. Genet. 241: 483­490.Additional comparative mapping studies within the
Arumuganathan, K., and E. D. Earle, 1991 Nuclear DNA contentBrassicaceae, also including species closely related to
of some important plant species. Plant Mol. Biol. Rep. 9: 208­218.
A. thaliana, and more precise estimates of divergence Axelsson, T., C. Bowman, D. Lydiate and U. Lagercrantz, 1998
RFLP mapping indicates conserved A and B genome linkagetimes between species within Brassicaceae will shed
groups in Brassica juncea. Proceedings, Plant Genome VI, p. 133.more light on the rapid chromosomal evolution ob-
Barendse, W., S. Armitage, L. Kossarek, A. Shalom, B. Kirkpatrick
served in the present study. Has rapid chromosome et al., 1994 A genetic linkage map of the bovine genome. Nat.
Genet. 6: 227­235.evolution been restricted mainly to the polyploid Bras-
1227Rapid Chromosomal Evolution in Brassicaceae
Bariola, P., C. Howard, C. Taylor, M. Verburg, V. Jaglan et somes reveals islands of conserved organization. Genetics 138:
499­510.al., 1994 The Arabidopsis ribonuclease gene RNS1 is tightly
Lagercrantz, U., and D. Lydiate, 1995 RFLP mapping in Brassicacontrolled in response to phosphate limitation. Plant J. 6: 673­
nigra indicates differing recombination rates in male and female685.
meiosis. Genome 38: 255­264.Barnett, M., V. Buckle, E. Evans, A. Porter, D. Rout et al., 1993
Lagercrantz, U., and D. Lydiate, 1996 Comparative genome map-Telomere directed fragmentation of mammalian chromosomes.
ping in Brassica. Genetics 144: 1903­1910.Nucleic Acids Res. 21: 27­36.
Lagercrantz, U., J. Putterill, G. Coupland and D. Lydiate, 1996Bertoni, L., C. Attolini, L. Tessera, E. Mucciolo and E. Giulotto,
Comparative mapping in Arabidopsis and Brassica, fine scale1994 Telomeric and nontelomeric (TTAGGG)n sequences in
genome collinearity and congruence of genes controlling flow-gene amplification and chromosome stability. Genomics 24:
ering time. Plant J. 9: 13­20.53­62.
Lande, R., 1979 Effective deme size during long-term evolutionBevan, M., I. Bancroft, E. Bent, K. Love, H. Goodman et al., 1998
estimated from rates of chromosomal rearrangements. EvolutionAnalysis of 1.9 Mb of contiguous sequence from chromosome 4
33: 234­251.of Arabidopsis thaliana. Nature 391: 485­488.
Lander, E., P. Green, J. Abrahamson, A. Barlow, M. Daly et al.,Bush, G., S. Case, A. Wilson and J. Patton, 1977 Rapid speciation
1987 MAPMAKER: an interactive computer package for con-and chromosomal evolution in mammals. Proc. Natl. Acad. Sci.
structing primary genetic linkage maps of experimental and natu-USA 74: 3942­3946.
ral populations. Genomics 1: 174­181.Cavell, A., D. Lydiate, I. Parkin, C. Dean and M. Trick, 1998 A
Leitch, I., and M. Bennett, 1997 Polyploidy in angiosperms.30 centimorgan segment of Arabidopsis thaliana chromosome 4
Trends Plant Sci. 2: 470­476.has six collinear homologues within the Brassica napus genome.
Lincoln, S., M. Daly and E. Lander, 1992 Mapping Genes ControllingGenome 41: 62­69.
Quantitative Traits with MAPMAKER/QTL 1.1, Ed. 2. WhiteheadChang, C., J. L. Bowman, A. W. De John, E. S. Lander and E. M.
Institute Technical Report, Cambridge, MA.Meyerowitz, 1988 Restriction fragment length polymorphism
Lister, C., and C. Dean, 1993 Recombinant inbred lines for map-linkage map for Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA
ping RFLP and phenotypic markers in Arabidopsis thaliana. Plant85: 6856­6860.
J. 4: 745­750.Chen, Q., and K. Armstrong, 1994 Genomic in situ hybridization
Liu, Y., N. Mitsukawa, C. Lister, C. Dean and R. Whittier, 1996in Avena sativa. Genome 37: 607­612.
Isolation and mapping of a new set of 129 RFLP markers inCopeland, N., N. Jenkins, D. Gilbert, J. Eppig, L. Maltais et al.,
Arabidopsis thaliana using recombinant inbred lines. Plant J. 10:1993 A linkage map of the mouse: current applications and
733­736.future prospects. Science 262: 57­66.
Lydiate, D., A. Sharpe, U. Lagercrantz and I. Parkin, 1993 Map-Ecker, J., 1998 Genes blossom from a weed. Nature 391: 438­439.
ping the Brassica genome. Outlook Agric. 22: 85­92.Ehrlich, J., D. Sankoff and J. Nadeau, 1997 Synteny conservation
Ma, H., M. Yanofsky and E. Meyerowitz, 1990 Molecular cloningand chromosome rearrangements during mammalian evolution.
and characterization of GPA1, a G protein alpha subunit geneGenetics 147: 289­296.
from Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 87: 3821­Eldridge, M., and R. Close, 1993 Radiation of chromosome shuf-
3825.fles. Curr. Opin. Genet. Dev. 3: 915­922.
Masterson, J., 1994 Stomatal size in fossil plants: evidence for poly-Fabri, C., and A. Schaeffner, 1994 An Arabidopsis thaliana RFLP
ploidy in majority of angiosperms. Science 264: 421­424.mapping set to localize mutations to chromosomal regions. Plant
Matsui, M., S. Sasamoto, T. Kunieda, N. Nomura and R. Ishizaki,J. 5: 149­156.
1989 Cloning of Ara, a putative Arabidopsis thaliana gene homol-Feinbaum, R., and F. Ausubel, 1988 Transcription regulation of
ogous to the Ras-related gene family. Gene 76: 313­320.the Arabidopsis thaliana chalcone synthase gene. Mol. Cell. Biol.
McGrath, J. M., M. M. Jansco and E. Pichersky, 1993 Duplicate
8: 1985­1992.
sequences with a similarity to expressed genes in the genome of
Gaut, B., and J. Doebley, 1997 DNA sequence evidence for the
Arabidopsis thaliana. Theor. Appl. Genet. 86: 880­888.
segmental allotetraploid origin of maize. Proc. Natl. Acad. Sci.
Meyerowitz, E., 1992 Introduction to the Arabidopsis genome, pp.
USA 94: 6809­6814.
102­118 in Methods in Arabidopsis Research, edited by C. Koncz,
Graves, J., 1996 Mammalians that break the rules: genetics of marsu-
N. Chua and J. Schell. World Scientific, Singapore.
pials and monotremes. Annu. Rev. Genet. 30: 233­260.
Meyne, J., R. Baker, H. Hobart, T. Hsu, O. Ryder et al., 1990 Distri-
Hastie, N., and R. Allshire, 1989 Human telomeres: fusion and
bution of non-telomeric sites of the (TTAGGG)n telomeric se-
interstitial sites. Trends Genet. 5: 326­331.
quence in vertebrate chromosomes. Chromosoma 99: 3­10.
Hauge, B., S. Hanley, S. Cartinhour, J. Cherry and H. Goodman,
Mindrinos, M., F. Katagiri, G. Yu and F. Ausubel, 1994 The
1993 An integrated genetic/RFLP map of the Arabidopsis thali-
A. thaliana disease resistance gene RPS2 encodes a protein con-
ana genome. Plant J. 3: 745­754. taining a nucleotide-binding site and leucine-rich repeats. Cell
Helentjaris, T., D. Weber and S. Wright, 1988 Identification of 78: 1089­1099.
the genomic locations of duplicate nucleotide sequences in maize Mithen, R., A. F. Raybold and A. Giamoustaris, 1995 Divergent
by analysis of restriction fragment length polymorphims. Genetics selection for secondary metabolites between wild populations of
118: 353­363. Brassica oleracea and its implications for plant-herbivore interac-
Janke, A., G. Feldmaier-Fuchs, W. Kelley Tomas, A. von Haeseler tions. Heredity 75: 472­484.
and S. Pa¨a¨bo, 1994 The marsupial mitochondrial genome and Moore, G., K. Devos, Z. Wang and M. Gale, 1995 Grasses line up
the evolution of the placental mammals. Genetics 137: 243­256. and form a circle. Curr. Biol. 5: 737­739.
Jellen, E., B. Gill and T. Cox, 1994 Genomic in situ hybridization Morizot, D., 1994 Reconstructing the gene map of the vertebrate
differentiates between A/D- and C-genome chromatin and de- ancestor. Anim. Biotech. 5: 113­122.
tects intergenomic translocations in polyploid oat species (genus Muller, J., 1981 Fossil pollen records of extant angiosperms. Bot.
Avena). Genome 37: 613­618. Rev. 47: 1­142.
Johansson, M., H. Ellegren and L. Andersson, 1995 Comparative Nadeau, J., and B. Taylor, 1984 Lengths of chromosomal segments
mapping reveals extensive linkage conservation--but with gene conserved since divergence of man and mouse. Proc. Natl. Acad.
order rearrangements--between the pig and the human ge- Sci. USA 81: 814­818.
nomes. Genomics 25: 682­690. O'Brien, S., H. Seuánez and J. Womack, 1988 Mammalian genome
Kenton, A., A. S. Parokonny, Y. Y. Gleba and M. D. Bennett, 1993 organization: an evolutionary view. Annu. Rev. Genet. 22: 323­
Characterization of the Nicotiana tabacum L. genome by molecular 351.
cytogenetics. Mol. Gen. Genet. 240: 159­169. Osborn, T. C., C. Kole, I. A. P. Parkin, A. G. Sharpe, M. Kuiper et
Konieczny, A., and F. Ausubel, 1993 A procedure for mapping al., 1997 Comparison of flowering time genes in Brassica rapa,
Arabidopsis mutations using co-dominant ecotype-specific PCR- B. napus and Arabidopsis thaliana. Genetics 146: 1123­1129.
based markers. Plant J. 4: 403­410. Parkin, I., A. Sharpe, D. Keith and D. Lydiate, 1995 Identification
Kowalski, S., T. Lan, K. Feldmann and A. Paterson, 1994 Compar- of the A and C genomes of amphidiploid Brassica napus (oilseed
rape). Genome 38: 1122­1131.ative mapping of Arabidopsis thaliana and Brassica oleracea chromo-
1228 U. Lagercrantz
Paterson, A., T. Lan, K. Reischmann, C. Chang, Y. Lin et al., 1996 Snogerup, S., M. Gustafsson and R. von Bothmer, 1990 Brassica
sect. Brassica (Brassicaceae). I. Taxonomy and variation. Willeno-Toward a unified genetic map of higher plants, transcending the
monocot-dicot divergence. Nat. Genet. 14: 380­382. wia 19: 271­365.
So¨derman, E. 1996 Genes encoding homeodomain-leucine zipperPrice, R., J. Palmer and I. Al-Shehbaz, 1994 Systematic relation-
ships of Arabidopsis: a molecular and morphological perspective, proteins in Arabidopsis thaliana. Ph.D. thesis, Uppsala University,
Uppsala Sweden.pp. 7­19 in Arabidopsis, edited by E. Meyerowitz and C. Somer-
ville. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, Song, K., P. Lu, K. Tang and T. Osborn, 1995 Rapid genome
change in synthetic polyploids of Brassica and its implications forNY.
polyploid evolution. Proc. Natl. Acad. Sci. USA 92: 7719­7723.Prince, J., E. Pochard and S. Tanksley, 1993 Construction of a
Stam, P., 1993 Construction of integrated genetic linkage maps bymolecular linkage map of pepper and a comparison of synteny
means of a new computer package: JoinMap. Plant J. 3: 739­744.with tomato. Genome 36: 404­417.
Sun, T., and Y. Kamiya, 1994 The Arabidopsis GA1 locus encodesReinisch, A., J. Dong, C. Brubaker, D. Stelly, J. Wendel et al., 1994
the cyclase ent-kaurene synthetase A of gibberellin biosynthesis.A detailed RFLP map of cotton, Gossypium hirsutum Gossypium
Plant Cell 6: 1509­1518.barbadense: chromosome organization and evolution in a disomic
Tanksley, S., M. Ganal, J. Prince, M. de Vicente, M. Bonierbalepolyploid genome. Genetics 138: 829­847.
et al., 1992 High density molecular maps of the tomato andRichards, E., and F. Ausubel, 1988 Isolation of a higher eukaryotic
potato genomes. Genetics 132: 1141­1160.telomere from Arabidopsis thaliana. Cell 53: 127­136.
Tanksley, S., R. Bernatzky, N. Lapitan and J. Prince, 1988 Con-Round, E., S. Flowers and E. Richards, 1997 Arabidopsis thaliana
servation of gene repertoire but not gene order in pepper andcentromere regions: genetic map positions and repetitive DNA
tomato. Proc. Natl. Acad. Sci. USA 85: 6419­6423.structure. Genome Res. 7: 1045­1053.
U, N., 1935 Genomic analysis in Brassica with special reference toScheffler, J., A. Sharpe, H. Schmidt, P. Sperling, I. Parkin et
the experimental formation of B. napus and peculiar mode ofal., 1996 Desaturase multigene families of Brassica napus arose
fertilization. Jpn. J. Bot. 7: 389­452.through genome duplication. Theor. Appl. Genet. 94: 583­591.
Wendel, J., 1989 New world cottons contain old world cytoplasm.Sharrock, R., and P. Quail, 1989 Novel phytochrome sequences
Proc. Natl. Acad. Sci. USA 86: 4132­4136.in Arabidopsis thaliana: structure, evolution, and differential ex-
White, M., 1973 Animal Cytology and Evolution. William Clowes andpression of a plant regulatory photoreceptor family. Genes Dev.
Sons, London.3: 1745­1757.
Whitkus, R., J. Doebley and M. Lee, 1992 Comparative genome
Shih, M., P. Heinrich and H. Goodman, 1991 Cloning and chromo-
mapping of sorghum and maize. Genetics 132: 1119­1130.
somal mapping of nuclear genes encoding chloroplast and cyto-
Wilson, A., V. Sarich and L. Maxon, 1974 The importance of gene
solic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis
rearrangements in evolution: evidence from studies of rates of
thaliana. Gene 104: 133­138.
chromosomal, protein, and anatomical evolution. Proc. Natl.
Shoemaker, R., T. Olson and V. Kanazin, 1996 Soybean genome Acad. Sci. USA 71: 3028­3030.
organization: evolution of a legume genome, pp. 139­150 in Wilson, A., T. White, S. Carlson and L. Cherry, 1977 Molecular
Genomes of Plants and Animals: 21st Stadler Genetics Symposium, ed- evolution and cytogenetic evolution, pp. 375­393 in Molecular
ited by J. P. Gustafson and R. Flavell. Plenum Press, New York. Human Cytogenetics, ICN-UCLA Symposia on Molecular and Cellular
Slijepcevic, P., Y. Xiao, I. Dominguez and A. Natarajan, Biology, Vol. VII, edited by E. A. Sparkes. Academic Press, San
1996 Spontaneous and radiation-induced chromosomal break- Francisco.
age at interstitial telomeric sites. Chromosoma 104: 596­604. Yanofsky, M., H. Ma, J. Bowman, G. Drews, K. Feldmann et al.,
Slocum, M. K., S. S. Figdore, W. C. Kennard, J. Y. Suzuki and T. C. 1990 The protein encoded by the Arabidopsis homeotic gene
Osborn, 1990 Linkage arrangements of restriction fragment agamous resembles transcription factors. Nature 346: 35­39.
length polymorphism loci in Brassica oleracca. Theor. Appl. Genet.
80: 57­64. Communicating editor: J. A. Birchler