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9 TRENDS"
I Plant Science
Building blocks
of crucifer genomes
NO signal at the crossroads
Bio-hydrogen production
Photoperiodic control of flowering
Novel traits through RNA interference
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MLSĽV1ĽR
The ABC's of comparative genomics in
the Brassicaceae: building blocks of
crucifer genomes y
M. Eric Schranz1
, Martin A. Lysak2,3
and Thomas Mitchell-Olds1
1
Department of Biology, Duke University, Durham, NC 27708, USA
2
Department of Functional Genomics and Proteomics, Masaryk University, Brno 62500, Czech Republic
3
Jodrell Laboratory, Royal Botanic Gardens, Kew, TW9 3AB, UK
f |
In this review we summarize recent advances in our
understanding of phylogenetics, polyploidization and
comparative genomics in the family Brassicaceae. These
findings pave the way for a unified comparative genomic
framework. We integrate several of these findings into a
simple system of 24 conserved chromosomal blocks
(labeled A-X). The naming, order, orientation and
color-coding of these blocks are based on their positions
in a proposed ancestral karyotype (n = 8), rather than by
their position in the reduced genome of Arabidopsis
thaliana [n = 5). We show how these crucifer building
blocks can be rearranged to model the genome structures
of A thaliana, Arabidopsis lyrata, Capsella rubella
and Brassica rapa. A framework for comparison
between species is timely because several crucifer genome-sequencing
projects are underway.
A unified comparative genomic framework for the
Brassicaceae
The angiosperm family Brassicaceae (the mustard family)
contains several important research and agricultural species,
the foremost being the model species Arabidopsis
thaliana (Arabidopsis) and the Brassica crops. In addition,
several related species are the focus of active research
communities, including Arabidopsis lyrata, Capsella
rubella, and other genera such as Boechera, Lepidium,
Thellungiella (also known as Eutrema) and Thlaspi. Comparative
genomics in the Brassicaceae has largely focused
on direct comparisons between A. thaliana and the species
of interest. However, several of the factors that made
Arabidopsis ideal for genome sequencing, particularly its
reduced genome size and chromosome number (157 Mb,
n - 5) [1], reduce its utility as a standard in comparative
genomics. Arabidopsis shows extensive genome and chromosome
reshuffling compared with other Brassicaceae
species. Several recent studies have tackled these obstacles,
providing useful insights into the history and organization
of crucifer genomes.
Our goal is to discuss these recent findings, focusing on
advances in our understanding of phylogenetics, polyploidization
and comparative genomics, which pave the way
for a unified comparative genomic framework across the
Corresponding author: Schranz, M.E. (eric.schranz@duke.edu).
Available online 6 October 2006.
Brassicaceae. We integrate several of these findings into a
simple system of structural sub-divisions representing
chromosome blocks that are conserved in the species of
Brassicaceae characterized to date. These crucifer building
blocks can be rearranged to model the genome structures of
A. thaliana, A. lyrata, C. rubella and Brassica rapa. This
block system can be used to visualize comparative genome
structure of other crucifer species as additional genetic
mapping, cytogenetic and genomic data accumulate. A
framework for comparison between species is particularly
timely because genome-sequencing projects are currently
underway for A. lyrata, C. rubella, Thellungiella halophila
and B. rapa.
Comparative genomics in plants: the Crop Circle
'and beyond
The seminal comparative genetic mapping done in the
grass family (Poaceae), which includes many important
domesticated cereal and forage crops, resulted in the
synthesis of the 'Crop Circle' [2-6]. This approach placed
the small-genome of rice at the center of the circle and then
aligned the maps of larger genome grass crops (including
corn, sorghum, wheat, oat, fox millet and sugar cane). A
large degree of colinearity was found among genomes
(however, see Ref. [7]). The rice genome (~400Mb,
n - 12) can be subdivided into ~30 blocks that can be
shuffled to represent the other grass genomes, such as
Glossary
Acrocentric chromosomes: chromosome arms of significantly unequal length
with the centromere near to one chromosome end.
Comparative Chromosome Painting (CCP}: in plant cytogenetics CCP is
fluorescence in situ hybridization (FISH) of chromosome-specific large-insert
DNA clones, microdissected or flow-sorted DNA probes of a reference species
to chromosomes of another species.
Metacentric chromosomes: both arms are of roughly equal length with the
centromere in the middle. Submetacentric chromosomes have one arm
slightly shorter than another. In crucifer cytogenetics, short and long
chromosome arms are usually described as top and bottom arms, respectively.
Pericentric inversion: a chromosome rearrangement in which two breakpoints
occur in a chromosome (one on each arm), the centerpiece including the
centromere is inverted and rejoined with the rest of the chromosome.
Chromosome symmetry can be altered as a result of the changed position of
the centromere (metacentric chromosome converted into an acrocentric
chromosome).
Reciprocal translocations: a chromosome rearrangement involving the
exchange of chromosome segments between two chromosomes.
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536 Review TRENDS in Plant Science Vol.11 No.11
Box 1. Chromosome number reduction via pericentric inversion-reciprocal translocation events
The relative placement of centromeres and telomeres is crucial to
understanding the evolution of crucifer genomes and the definition
of conserved genomic blocks. Most observations of karyotype
evolution and chromosome number reduction can be explained by
rearrangements via pericentric inversion followed by reciprocal
translocation [33]. The basic steps involved in this cycle are as
follows (Figure I):
(1) A pericentric inversion occurs that moves the centromere of a
(sub)metacentric chromosome towards the end of the chromosome,
creating an acrocentric chromosome.
(2) A reciprocal translocation occurs between the centric end of this
acrocentric chromosome and a subtelomeric region of another
chromosome.
(3) There are two products of the translocation event: a large 'fusion'
chromosome and a small mini-chromosome made up mostly of
the centromere of the acrocentric chromosome and of the
subtelomeric segment of the other. It is hypothesized that the
mini-chromosomes are free of essential genes and meiotically
unstable and, hence, are eliminated. If the subtelomeric region of
the second chromosome involved in the reciprocal translocation
comprises a nucleolar organizing region (NOR), the NOR is lost
together with the mini-chromosome.
Although this mechanism explains how centromeres can be lost and
chromosome number reduced, evolutionary pathways leading to the
chromosome number increase are less clear. Chromosome number
can be increased by a polyploid event and the subsequent loss of
several chromosome types, or as a result of a meiotic non-disjunction.
Whether chromosome fission and neocentromere formation can play a
role in karyotype evolution towards increased chromosome numbers
needs to be investigated.
NOR
.
CEN

Pericentric
inversion
]
I
Figure I
Reciprocal
translocation
Mini-chromosome
eliminated
TRENDS in Plant Science
bread wheat (~17 000 Mb, n = 21). In recent years there
has been a push to integrate genetic maps and genomics
across other families, particularly those with several
domesticated crops, such as the Fabaceae [8,9], Rosaceae
[10], Solanaceae [11], Asteraceae (The Compositae Genome
Project: http://compgenomics.ucdavis.edu) and Brassicaceae
[12-14].
Brassicaceae: phytogeny and genome duplications
An accurate phylogeny is essential for comparative studies
within the Brassicaceae. Knowledge of natural phylogenetic
relationships allows estimates of: (i) derived versus
ancestral states for numerous characters (morphological,
cytological, biochemical), (ii) evolutionary distances and
divergence times between groups and (iii) the positioning
of evolutionary events to particular nodes or clades on the
phylogenetic tree. Recent studies have classified the 338
genera and ~3700 species of Brassicaceae into 25 tribes
[15] based on nuclear- [16] and chloroplast-encoded [15]
markers. Sixteen of the 25 tribes can be further grouped
into one of three lineages (referred to as Lineages I--III)
[15]. Although the system is incomplete with some genera
having a provisional position and some that are not analyzed
yet, this taxonomie classification [15] provides the
most up-to-date reference point for comparative studies in
this family.
The discernment and appreciation of whole-genome
duplication (polyploidy) within lineages is also crucial
for comparative studies within the Brassicaceae [17].
Based on the 'traditionaľ definition of polyploids, it has
been estimated that ~37% of Brassicaceae species are of
polyploid origin (defined as n > 14) [18]. However, in recent
years it has become apparent that ancient polyploidy, or
paleopolyploidy, events have also played a major role in
crucifer evolution. Analysis of the A. thalicma genome has
revealed extensive intra- and inter-chromosomal segmental
duplications that were interpreted as relics of a wholegenome
duplication event [19-22]. Additional analyses
indicate that Arabidopsis ancestors underwent three
rounds (1-3R, or y, ß and a, respectively) of whole-genome
duplications [23-25]. The most recent (3R or a) polyploidy
event appears to be unique to the Brassicaceae, having
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TRENDS in Plant Science
occurred ~40 million years ago (mya), after divergence
from its sister family Cleomaceae [26,27].
In addition to the 3R polyploidy event occurring across
the family, there is also evidence for an additional ancient
triplication event that is unique to the tribe Brassiceae.
Several comparative maps between A. thaliana and Brassica
suggested that numerous regions homeologous to the
Arabidopsis genome are triplicated within Brassica genomes
because of an ancestral hexaploidy event [28].
Recently, additional evidence for the genome triplication
in Brassica was found by sequencing [29,30], genetic [31],
and cytogenetic [32,33] methods. These studies support the
hypothesis of a common hexaploid ancestor in the ancestry
of Brassica and the tribe Brassiceae. However, there is
some controversy regarding the ancient hexaploid hypothesis
because some genomic regions are present in less or
more than three copies in Brassica genomes. Other phenomena
(such as ancient tetraploidy and/or segmental
duplication) could also explain the current genomic structure
of Brassica [34,35].
Comparative mapping and genomics in the
Brassicaceae
The genome sequencing of A. thaliana was a major landmark
in plant biology and transformed a rather unassuming
weed into the reference point for most comparative
studies [20]. The reduced genome size and low chromosome
number (n = 5) made Arabidopsis ideal for genome sequencing,
but complicates its use in comparative studies. It is
tempting to place Arabidopsis at the center of a Brassicaceae
genomics circle in the same way rice was placed at the
center of the Crop Circle [2-6]. However, most of the other
species in its tribe, the Camelineae, have the base chromosome
number n = 8, in common with at least 37% of Brassicaceae
species [18]. Thus, when comparisons are made
between an n = 8 taxon and the A. thaliana genome, chromosome
rearrangements that are unique to A. thaliana
must be (re)accounted for. Recent studies suggest that
comparison with an 'ancestral karyotype' of n = 8 would
considerably expedite genomic comparisons [33,36]. Introduction
of the ancestral n = 8 karyotype would also facilitate
comparisons between more distantly related groups
within the family.
Comparative genetic maps have recently been constructed
for two n = 8 Camelineae species, C. rubella
[37] and A. lyrata [38,39], by examining the positions of
Arabidopsis genetic markers in their genomes. This mapping
has shown that both n = 8 genomes are largely
colinear with the reduced n = 5 genome of A. thaliana,
and that all three taxa share large conserved genomic
blocks [37-39]. Furthermore, A. lyrata and C. rubella
possess almost identical genome structure, presumably
resembling an ancestral n = 8 karyotype of A. thaliana
[36].
Comparative chromosome painting (CCP) (see Glossary)
has been used within a phylogenetic framework to
examine the chromosome number reduction that occurred
in A. thaliana [33]. One of the most important conceptual
shifts of this paper was the use of the n = 8 ancestral
karyotype (AK), based on A. lyrata and C. rubella maps,
as the reference point. The CCP analysis used
ˇ1.11 No.11 537
chromosome-specific BAC contig probes of A. thaliana
arranged and colored according to the colinear segments
found in genetic maps of A. lyrata and C. rubella [37-39].
The CCP study also provided information about the positions
of centromeres in the ancestral karyotype [33], which
has been corroborated by genetic mapping in A. lyrata
[40,41].
In addition to examining the chromosome reduction of
A. thaliana, Martin Lysak et al. [33] also examined other
karyotypes with reduced chromosome number (n = 6 and 7)
of two taxa from the tribe Camelineae (Neslia, Turritis)
and one taxon from Descurainieae (Hornungia). The
results revealed that all species analyzed share conserved
chromosome segments that can be related to the ancestral
karyotype [33]. Furthermore, the results suggested a common
mechanism for chromosome number reduction via a
pericentric inversion followed by reciprocal translocation
(Box 1).
Besides Arabidopsis and its closest relatives, comparative
analyses are concentrated on economically important
brassicas and some other species from the tribe Brassiceae.
Comparing the Arabidopsis genome with those of Brassica
species has a long and somewhat controversial history. The
difficulty in establishing syntenic relationships between
Brassica and A. thaliana is caused by the aforementioned
derived nature of the A. thaliana genome, relatively large
phylogenetic distance between the two genera [42], the
paleopolyploid nature of Brassiceae genomes [28,31,43],
and the low marker densities of some Brassica genetic
maps.
Despite these difficulties, a superb recent study [31] has
[made a comprehensive comparison that places almost 90%
of the Brassica napus mapped length into conserved syntenic
blocks relative to A. thaliana. Isobel Parkin et al. [31]
placed 1327 genetic loci on the 19 linkage groups of
Ancestral karyotype (AK)
Arabidopsis lyrata and Capsella rubella
AK1 AK2 AK3 AK4 AK5 AK6 AK7 AK8
A
D
í * °l S
|
V
:
>
E
F
1 T
' W
j
M Q X
U s, ˇ
U
.
N
R
CC
TRENDS ir Plant Science
Figure 1. Genome blocks in the 'ancestral karyotype' {n= 8) based on cytology and
genetic maps of Arabidopsis lyrata and Capsella rubella. Genome blocks are
labeled A-X. The order, orientation, and color-coding of each block is based on
their positions in the ancestral karyotype of Lysak ef al. [33]. Each block is one of
eight colors, with each color corresponding to one of the chromosomes, beginning
with block A o n the top of AK1 and ending with block X at the bottom of AK8. Each
block is considered to be in the upright orientation in the ancestral karyotype. The
colored circles indicate centromeric positions. Because only the Arabidopsis
thaliana genome is currently sequenced, the boundaries of the blocks are defined
by their At locus names (shown in Figure 2). Block boundaries are based mostly on
the homology of probes used in a genetic mapping study in Brassica napus
to A thaliana [31]. However, we refined and defined some blocks based on the
A lyrata genetic mapping and cytogenetic results [33,38,39]. Specifically, we have
added block K and divided two Brassica blocks into two (N and O, and G and H).
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538 Review TRENDS in Plant Science Vol.11 No.11
AT1
rAt1g01560
AT2
F
At2g01250
At2g03750
At2g05170
At2g07733
At2g15670
, At1g19330
'At1g19850 H
Arabidopsis thaliana
AT3 AT4
- At3g01040 m-- At4g00030
O
* At4g04955
AT5
I
At2g21140
At2g21160
H
At1g36240
At1g43590
10
At2g31040
. At3g25520 T
At3g25855
At3g29772
M
I
At4g08690
At4g 12070
A14g 12750
* AHg 16143 n
At4g 16250
At5g01240
5
At2g47730
.At1gE6145
ˇAt1gE6520
At1g63770
At1g65040
-At1g80420
At3g43740
. At3g49970
* At3g50950
* At3g62790
* A14g38770
I 
w
. At5g22030
* At5g22800
- AI5g28897
-At5g32621
At5g41900
- A15g42970
* Ai5g48520
* At5g49430
. At5g60390
' At5g60550
- At5g67385
TRENDS in Plant Science
Figure 2. Genome blocks and block boundaries mapped onto the reduced karyotype (n = 5) of Arabidopsis thaliana. The genome blocks defined by their position in the
ancestral karyotype (n = 8) (Figure 1) are reorganized to show the evolution of the reduced karyotype of A thaliana{n = 5). The boundaries of the blocks are defined by their
At locus names. Most of the chromosome fusions occurred via pericentric inversion-reciprocal translocation events involving (peri)centromeric and (sub)telomeric regions
(see Box 1). Blocks that have been inverted relative to the ancestral karyotype are represented by black downward-pointing arrows on the left of the block and by the block
letter being upside-down (blocks D, P and V). Blocks that are in the opposite orientation, but not inverted, relative to the ancestral karyotype are represented by a gray
downward-pointing arrow on the right of the block and by the block letter being upside-down (blocks R, Q and S). Fusion of blocks from different ancestral chromosomes is
shown by adjacent blocksof different colors. Of the eight ancestral karyotype centromeres, only three appear to have maintained the same flanking pericentromeric regions
at both borders in A thaliana (AK1 =CEN1 between blocks B and C, AK3 = CEN2 between blocks G and H, and AK5 = CEN3 between blocks L and M). The other five
centromeres have been lost or rearranged by pericentric inversion-reciprocal translocation events. Three centromeres present in the ancestral karyotype species have been
lost: the centromeres of AK2 (between blocks D and E), AK4 (between blocks I and J) and AK8 (between blocks V and W) are no longer present in A thaliana. There is only
one major non-centromere-associated translocation, namely the reciprocal translocation of blocks K and F between AK3 and AK5 during the evolution of AT2 and AT3.
allopolyploid B. napus. These 19 linkage groups, which are
labeled Nl-19, correspond to the ten chromosomes of
B. rapa (Nl-10) and the nine chromosomes of B. oleracea
(Nll-19). This analysis identified 21 syntenic blocks
shared by B. napus and A. thaliana genomes that could
be duplicated and rearranged to represent 90% of the
B. napus genome. These conserved blocks (with an average
size of ~4.8 Mb in A. thaliana) represent colinear regions
that have been maintained since the divergence of the
Arabidopsis and Brassica lineages ~20 mya [31,44]. The
identification of such conserved blocks, along with recent
comparative mapping in A. lyrata and C. rubella [37-39],
and the definition ofthe ancestral karyotype [33] has paved
the way for genomic comparisons across the Brassicaceae.
ABC's: the conserve! blocks of crucifer genomes
An important step toward a unified comparative genomics
system across the Brassicaceae can be accomplished by
integrating the colinear regions identified between
B. napus and A. thaliana [31] with the concept of the
n - 8 ancestral karyotype shared byA. lyrata and Capsella
[33]. We propose a set of 24 genomic blocks (A-X) within
the ancestral karyotype that represent an extension to the
set of 21 blocks proposed for Brassica by Parkin et dl. [31].
These 24 blocks represent the conserved segments that can
be identified among the ancestral karyotype (Figure 1),
A. thaliana (Figure 2) and the B. rapa component
(A genome = N1-N10) ofB. napus (Figure 3). This expanded
genomic block system reflects our current understanding of
the conserved nature of crucifer genomes. A summary of
the blocks and characteristics in the three species is also
summarized in Table 1.
The order, orientation, and color-coding of these blocks
are based on their positions in the ancestral karyotype [33].
Because only the A. thaliana genome is currently
sequenced, the boundaries of the blocks are defined by
their At locus names (Figure 2, Table 1). Furthermore,
we refine and define several additional blocks based on
mapping and cytogenetic comparisons between the ancestral
karyotype and A. thaliana [33,38,39].
Bridging Arabidopsis thaliana and Brassica via the
ancestral karyotype
Recognition of the ancestral karyotype and these
genomic building blocks will facilitate comparisons
between A. thaliana and Brassica and provide a basis
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Review TRENDS in Plant Science Vol.11 No.11 539
Brassica rapa
N1 N2 N3 N4 N5 N6 N7 N8 N9 N10
n ľ i
d ti
N ||
r c H 0
O
A
n T l l
s 1
[i 3
T
_
Q
I I
T l l
s 1 A a Y ...
1 M M B
g U A W
U
F E r C
B
1
R 1
J g
V
K 1 X N g
L o d
D
ll N
° d i E 1 v
ˇIx V
- ˇI T
F
v
T
U
TRENDS in Planí Science
Figure 3. Genome blocks shown for the A genome species Brassica rapa {n= 10). The genome blocks defined by their position in the ancestral karyotype (n = 8) (Figure 1)
are shown for B. rapa. The position of the genome blocks for the B. rapa genome is based on the comparative mapping that has been done between B. napus (the A genome
component of B. napus= N1-N10) and Arabidopsis thaliana by Parkin et al. [31]. Blocks that are in the opposite orientation, but not inverted, relative to the ancestral
karyotype are represented by a gray downward-pointing arrow on the right of the block and by the block letter being upside-down. By comparison to the ancestral
karyotype, we are able to make several refinements to our understanding of Brassica genome evolution. Several block boundaries that exist in A. thaliana are not seen in
Brassica, such as the C-D fusion or the H-l fusion. We have included some new blocks, such as the placement of block K next to block L on linkage groups N2 and N6. Also,
many blocks are found in triplicate as predicted by the hypothesis of an ancient hexaploidy ancestry of the group [28,31,43].
for family-wide comparative genomics in the Brassicaceae.
Although it is well known that A. thaliana and Brassica
genomes differ by many rearrangements [28,45-47], the
pattern underlying these changes is less clear. In particular,
the Brassica genome is less rearranged relative to the
ancestral karyotype compared with that of A. thaliana.
Several block boundaries that exist in A. thaliana are not
seen in Brassica. This is because these are derived states
found in A. thaliana, and not the ancestral karyotype.
There are several refinements that can be identified by
comparing Brassica to the ancestral karyotype. For example,
a conserved region corresponding to block K on N2 and
N6 (Figure 3) was not incorporated into the analysis of
B. napus [31], probably because of its derived position on
the top ofAt2. Block K is fused with block L in the ancestral
karyotype (Figure 1), which suggests that block K is adjacent
to block L in Brassica as well. Indeed, when the
genetic markers adjoining block K on linkage groups N2
and N6 in the B. napus map [31] are scrutinized, homology
to block L can be identified (Figure 3). Further support for
the placement of block L next to block K comes from a
separate study reporting a detailed molecular analysis of
B. rapa [48].
Comparison to the ancestral karyotype also highlights
several potentially conserved centromeric locations
in Brassica based on colinearity. However, these regions
are often the sites for rearrangements (Box 1). Parkin et al.
[31] mapped groups of markers that corresponded to pericentromeric
genes in A. thaliana. Taking a conservative
approach we can identify four chromosomes (N3, N4, N5
and N7) with non-rearranged blocks that flank a centromere
in the ancestral karyotype and the block order is the
same in the Brassica A genome. The potentially conserved
centromeres on N3 and N4 are only apparent by comparison
to the ancestral karyotype. The centromeres on N5
and N7 are potentially conserved between Brassica, the
ancestral karyotype and A. thaliana. On N5, one would
predict a centromere between blocks B and C. On N7, a
conserved centromere is predicted between blocks G and H.
Support for this hypothesis comes from the cytological
observation that B. oleracea linkage group 07 (the homeolog
of N7) is acrocentric and homologous to the top of At2
[49].
Finally, presenting the B. rapa genome with the ancestral
blocks can be used to visualize blocks that are, or are
not, present in three copies as predicted by the ancient
polyploidy hypothesis for the tribe (Figure 3, Table 1).
Several blocks are present in triplicate, and have been
well characterized in previous studies. For example, block
R is triplicated (on N2, N3 and NIO) and has been analyzed
in several studies [30,46,50]. Triplicated blocks U (on Nl,
N3 and N8) and V (on N2, N6 and N9) and their homeologs
in B. oleracea have been examined recently [29,51]. Block
U, which has also been examined using CCP [43], is
triplicated across most of the tribe Brassiceae. However,
as noted earlier, there are blocks that seem to occur only
once, for instance blocks G and H are present only on N7
(Figure 3, Table 1).
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540 Review TRENDS in Plant Science Vol.11 No.11
Table 1 Block summary
Block -Interval AILG" Al order" Al orient.0
AtLGd
At order* At orient.' Brassica block0
Frequency in Br"
A
B
C
At1g01560-At1g19330 1 1 1 1 + C1A 4A
B
C
At1g19850-At1g36240 1 2 + 1 2 + C1B 5
A
B
C At1g43590-At1g56145 1 3 + 1 3 + C1C
^M At1 g63770- At1 g56520 2 4 * 1 4 - C1D 1
E At1g65040-At1g80420 2 5 + 1 5 + C1E
At3g01040-At3g25520 3 6 + 3 11 + C3A 3
G At2g05170-At2g07733 3 7 + 2 7 + C2A
H 1 At2g15670-At2g21140 3 8 + 2 8 + C2A 1
1
J
At2g21160-At2g28910 4 9 + 2 9 +1
J At2g31040-At2g47730 4 10 + 2 10 + C2C 3
K
L
M
N
Al2g01250-At2g03750 5 11 + 2 S + C2AK
L
M
N
At3g25855-At3g29772 5 12 + 3 12 + C3B 2
K
L
M
N
A13g43740-At3g49970 5 13 + 3 13 + C3C
K
L
M
N At3g50950-At3g62790 5 14 + 3 14 + C3D 3
M At4g00030-At4g04955 6 15 + 4 15 + C4A
P
1Q
R
At4g12070-At4g08690 6 16 + 4 16 - C4A 2
P
1Q
R
At5g28897- At5g22800 6 17 + 5 20 - C5B
P
1Q
R
At5g22030-At5g01240 6 18 + 5 19 _ C5A 3
s At5g41900-At5g32621 7 19 + 5 21 C5C
T At4g12750-At4g16143 7 20 + 4 17 + C4B' 4
^ | At4g16250-At4g38770 7 21 + A 18 + C4B
V
w
x
At5g48520-At5g42970 8 22 + 5 22 - C5D 3V
w
x
At5g49430-At5g60390 8 23 + 5 23 +
V
w
x At5g60550-At5gS7385 8 24 + 5 24 + C5F 2
a
Arbidopsis lyrata linkage group (LG).
b
Order of blocks along A lyrata LG.
c
Relative orientation of blocks along A lyrata LG.
d
Arabidopsis thaliana linkage group.
e
Order of blocks along A thaliana LG.
f
Relative orientation of blocks along A thaliana LG. Blocks that have been inverted relative to the ancestral karyotype (blocks D, P and V) and blocks that are in the opposite
orientation but not inverted (blocks R, Q and S) are indicated by a minus symbol.
corresponding block identified in Brassica napus by Parkin et ai. [31].
h
Number of times the block occurs within the B. rapa (Br) genome. TM
Concluding remarks and future directions
Future research should lead to the refinement of the
boundaries and definitions of many of the blocks to more
precisely delineate syntenic relationships. If future studies
require additional genomic subdivisions we recommend
the division of the present blocks (A-X) into enumerated
sub-blocks (e.g. Ai and A2). Also, there are likely to be
minor species-specific differences in microcolinearity
within the blocks that will become apparent from finemapping
studies or by analyzing DNA sequence. For example,
it is already known from the genetic mapping results in
B. napus [31] that there are four inversions within blocks of
the A genome. Nevertheless, we hope that this set of
genomic building blocks derived from the comparative
work between Brassica and A. thaliana [31] that we have
linked to the n = 8 ancestral karyotype represent a useful
framework for comparative genomics across the Brassicaceae.
Cytogenetic and genetic investigations revealed
these conserved genomic blocks in species from tribes
Camelineae (Arabidopsis, Capsella, Neslia, Turritis), Descurainieae
{Hornungia) [33] and Brassiceae [30,31]. A
crucial goal in the future will be the integration of genetic
maps and cytogenetic findings from additional species,
particularly from tribes more distantly related to either
Camelineae or Brassiceae. Several conserved chromosome
segments partly colinear to ancestral chromosomes AK6
and AK7 have been revealed in Arabis alpina {n - 8),
belonging to Arabideae [52]. Furthermore, the genome
structure of Boechera striata (n = 7) belonging to Boechereae,
as revealed by genetic linkage mapping, can also be
fully accounted for using our blocks (M.E. Schranz and T.
Mitchell-Olds, unpublished). Finally, analyzing taxa from
the tribe Aethionemeae, which is sister to the rest of the
extant Brassicaceae tribes [18], should cast more light on
the ancestral structure of crucifer genomes, and should
facilitate comparisons to its sister family the Cleomaceae
[26].
It will be important to address whether patterns of
chromosomal repatterning (or diploidization) that
occurred after the 3R ancient polyploidy event are shared
across the family [53]. If much of the genome changes
occurred shortly after the polyploidization, then we would
expect to find conservation of the genomic blocks across
many tribes. However, if the diploidization process
occurred independently within individual lineages, than
the genomic block system will be less informative. Furthermore,
a major objective will be to understand the significance
of the inversion-translocation mechanism involved
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TRENDS in Plant Science
in chromosome fusions and whether chromosome number
reduction, perhaps associated with genome diploidization,
is a prevailing evolutionary process within Brassicaceae.
In conclusion, we hope that the underlying simplicity of the
presented model will aide in future comparative genomics
studies in the Brassicaceae, and facilitate the transfer of
knowledge from model species to crop species.
Acknowledgements
We thank Tom Osborn, Isobel Parkin, Chris Pires, Ingo Shubert, Aaron
Windsor and three anonymous reviewers for helpful comments on the
manuscript. This work was supported by funding from Duke University
to M.E.S. and T.M-O., and the Czech Ministry of Education
(MSM0021622415) and a research grant from the Grant Agency of the
Czech Academy of Science (KJB601630606) awarded to M.A.L.
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