Genome comparisons reveal a dominant mechanism of chromosome number reduction in grasses and accelerated genome evolution in Triticeae
ABSTRACT Single-nucleotide polymorphism was used in the construction of an expressed sequence tag map of Aegilops tauschii, the diploid source of the wheat D genome. Comparisons of the map with the rice and sorghum genome sequences revealed 50
inversions and translocations; 2, 8, and 40 were assigned respectively to the rice, sorghum, and Ae. tauschii lineages, showing greatly accelerated genome evolution in the large Triticeae genomes. The reduction of the basic chromosome
number from 12 to 7 in the Triticeae has taken place by a process during which an entire chromosome is inserted by its telomeres
into a break in the centromeric region of another chromosome. The original centromere–telomere polarity of the chromosome
arms is maintained in the new chromosome. An intrachromosomal telomere–telomere fusion resulting in a pericentric translocation
of a chromosome segment or an entire arm accompanied or preceded the chromosome insertion in some instances. Insertional dysploidy
has been recorded in three grass subfamilies and appears to be the dominant mechanism of basic chromosome number reduction
in grasses. A total of 64% and 66% of Ae. tauschii genes were syntenic with sorghum and rice genes, respectively. Synteny was reduced in the vicinity of the termini of modern
Ae. tauschii chromosomes but not in the vicinity of the ancient termini embedded in the Ae. tauschii chromosomes, suggesting that the dependence of synteny erosion on gene location along the centromere–telomere axis either
evolved recently in the Triticeae phylogenetic lineage or its evolution was recently accelerated.
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ABSTRACT: Avdulov and Stebbins noted a tendency for species with large chromosomes in several angiosperm groups or families (including the Gramineae, Commelinaceae, Liliales, Polemoniales and the Leguminosae) to be localized in distribution to temperate latitudes. As chromosome size and DNA content are closely correlated, the distribution of species with large DNA amounts per chromosome, or per diploid genome, might expected to be similarly localized. This hypothesis was tested using samples of crop species with large ranges of DNA amounts from the Gramineae and the Leguminosae. For instance, the mean DNA amount per chromosome for the sample of cereal grain species showed about a 36-fold range from 0·033 picograms (pg) in Eragrostis tef to 1·186 pg in Secale cereale, while for the sample of pulse crops the range was about 70-fold from 0·032 pg in Lablab niger to 2·225 pg in Vicia faba. The results for cereal grain crops, cultivated pasture grasses and pulse crops show that cultivation of species with high DNA amounts per diploid genome tends to be localized in temperate latitudes, or to seasons and regions at lower latitudes where the conditions approximate to those normally found in temperate latitudes. Moreover, man has shown a strong tendency to choose species for cultivation with increasingly lower DNA amounts at successively lower latitudes. Thus, there is a cline for DNA amount and latitude. This cline is exhibited independently by both C3 and C4 crop species, and by both annuals and perennials and hence is independent of life cycle type and the taxonomic distribution of C3 and C4 photosynthesis. The cline is apparently a natural phenomenon which man has modified and exaggerated in agriculture. It is suggested, therefore, that interspecific variation in DNA amount between angiosperm species may have adaptive significance affecting the distribution of both crop and non-crop species. The cline might be caused either by variation in DNA amount per se, or by variation in some factor(s) correlated with DNA amount. The factor(s) causally responsible for the cline, and their mode of action should be investigated since they may have implications for agriculture and plant breeding.Environmental and Experimental Botany - ENVIRON EXP BOT. 01/1976; 16:93-108.
- [show abstract] [hide abstract]
ABSTRACT: Nuclear DNA content was determined by flow cytometry for an array of perennial species of the Triticeae (Poaceae) which characterize the tribe and are representative of the genomes of the Triticeae. The mean nuclear DNA content expressed on a diploid basis (DNA pg/2C) for the diploid genomes (in parentheses) were as follows: Agropyron (PP) 13.9 pg, Pseudoroegneria (StSt) 8.8 pg, Hordeum (HH) 9.5 pg, Psathyrostachys (NsNs) 16.7 pg, and Thinopyrum genomes (E(b)E(b)) 14.9 pg and (E(e)E(e)) 12.0 pg. The YY genome in Elymus was determined by difference to be 9.3 pg. The unknown or XmXm genome or genomes in Leymus could have DNA contents that range from 2.7 to 7.7 pg/2C. There were significant differences in DNA content of species with similar diploid genomes. There were also significant differences in nuclear DNA content among polyploid species with the same genomes. In general, the nuclear DNA content of the polyploid species of the Triticeae were similar to the expected DNA contents on the basis of previous genomic classifications. However, in some allopolyploid genera such as Thinopyrum and Pascopyrum, the nuclear DNA content of some species was less than expected on the basis of summation of the DNA of constituent genomes. The results indicate that gain or loss of nuclear DNA has occurred during the evolution of the perennial Triticeae and was probably a part of speciation.01/1999;
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ABSTRACT: Wheat was domesticated about 10,000 years ago and has since spread worldwide to become one of the major crops. Its adaptability to diverse environments and end uses is surprising given the diversity bottlenecks expected from recent domestication and polyploid speciation events. Wheat compensates for these bottlenecks by capturing part of the genetic diversity of its progenitors and by generating new diversity at a relatively fast pace. Frequent gene deletions and disruptions generated by a fast replacement rate of repetitive sequences are buffered by the polyploid nature of wheat, resulting in subtle dosage effects on which selection can operate.Science 07/2007; 316(5833):1862-6. · 31.20 Impact Factor
Genome comparisons reveal a dominant mechanism
of chromosome number reduction in grasses and
accelerated genome evolution in Triticeae
M. C. Luoa, K. R. Deala, E. D. Akhunova,1, A. R. Akhunovaa,1, O. D. Andersonb, J. A. Andersonc, N. Blaked, M. T. Clegge,3,
D. Coleman-Derrb, E. J. Conleyc, C. C. Crossmanb, J. Dubcovskya, B. S. Gillf, Y. Q. Gub, J. Hadamf, H. Y. Heod, N. Huob,
G. Lazob, Y. Maa, D. E. Matthewsg, P. E. McGuirea, P. L. Morrelle, C. O. Qualseta, J. Renfrob, D. Tabanaoc, L. E. Talbertd,
C. Tiana, D. M. Tolenoe,2, M. L. Warburtonh, F. M. Youb, W. Zhanga, and J. Dvoraka,3
aDepartment of Plant Sciences, University of California, Davis, CA 95616;bGenomics and Gene Discovery Unit, U.S. Department of Agriculture/Agricultural
Research Service Western Regional Research Center, Albany, CA 94710;cDepartment of Agronomy and Plant Genetics, University of Minnesota, St. Paul, MN
55108;dDepartment of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT 59717;eDepartment of Ecology and Evolutionary
Biology, University of California, Irvine, CA 92697;fDepartment of Plant Pathology, Kansas State University, Manhattan KS 66506;gU.S. Department of
Agriculture/Agricultural Research Service, Cornell University, Ithaca, NY 14853; andhU.S. Department of Agriculture/Agricultural Research Service/Corn Host
Plant Resistance Research Unit, Mississippi State University, Box 9555, Mississippi State, MS 39762
Contributed by M. T. Clegg, July 22, 2009 (sent for review June 12, 2009)
Single-nucleotide polymorphism was used in the construction of an
expressed sequence tag map of Aegilops tauschii, the diploid source
of the wheat D genome. Comparisons of the map with the rice and
sorghum genome sequences revealed 50 inversions and transloca-
Ae. tauschii lineages, showing greatly accelerated genome evolution
in the large Triticeae genomes. The reduction of the basic chromo-
during which an entire chromosome is inserted by its telomeres into
a break in the centromeric region of another chromosome. The
original centromere–telomere polarity of the chromosome arms is
telomere fusion resulting in a pericentric translocation of a chromo-
some segment or an entire arm accompanied or preceded the chro-
mosome insertion in some instances. Insertional dysploidy has been
recorded in three grass subfamilies and appears to be the dominant
of 64% and 66% of Ae. tauschii genes were syntenic with sorghum
and rice genes, respectively. Synteny was reduced in the vicinity of
the termini of modern Ae. tauschii chromosomes but not in the
vicinity of the ancient termini embedded in the Ae. tauschii chromo-
somes, suggesting that the dependence of synteny erosion on gene
location along the centromere–telomere axis either evolved recently
in the Triticeae phylogenetic lineage or its evolution was recently
dysploidy ? linkage map ? rice ? sorghum ? wheat
genome size is 389 Mb in rice (Oryza sativa) (1) and 730 Mb in
sorghum (Sorghum bicolor) (2) but it approaches 8,000 Mb in some
diploid species in the tribe Triticeae (3, 4). The primary cause of
these differences is the variation in the amount of repeated se-
quences present in a genome, principally transposable elements.
Transposable elements filling the intergenic space are subjected to
a remarkably rapid turnover rate in grasses (5), and a legitimate
question is whether or not this rapid turnover rate impacts the
stability of gene space. If it does, large plant genomes should show
more rapid chromosome evolution, greater erosion of gene colin-
earity (synteny) along homoeologous chromosomes, and a higher
rate of gene duplication and deletion compared with related small
genomes. To learn whether these predictions have a material basis
and to gain better understanding of the evolution of Triticeae
polymorphism (RFLP) and deletion bin maps (6–10), a high-
resolution, expressed sequence tag (EST)-based genetic map of the
ne of the intriguing attributes of plants is the great variation
in genome size among related species. In the grass family, 1C
Aegilops tauschii genome was constructed and compared with the
rice (1) and sorghum (2) genome sequences. Because Ae. tauschii
is the diploid ancestor of the D genome of common wheat (11, 12),
a comparative, high-resolution genetic map will also be a valuable
resource for wheat genetics and genomics.
Ae. tauschii and the rest of the Triticeae species are classified in
the subfamily Pooideae of the grass family. In most phylogenetic
reconstructions, Pooideae forms a clade with the subfamilies
Ehrhartoideae (? Oryzoideae) and Bambusoideae (termed the
grass clade that contains subfamilies Panicoideae, which includes
sorghum, Arundinoideae, Chlorideae, Centhothecoideae, Aris-
tidoideae, and Danthoideae (termed the PACCAD clade). Triticeae
other than each is to the sorghum genome (x ? 10) (13–17).
Phylogenetic reconstructions and comparisons of grass genome
structure suggested that the basic chromosome number x was 12 in
the common ancestor of Triticeae, rice, and sorghum (10, 13, 18).
with rice and sorghum allowed analysis of their linear order and
reconstruction of events that resulted in the reduction of chromo-
comparison of the stability of gene space in large and small grass
genomes and the erosion of synteny along the centrome–telomere
axes of the ancient chromosome arms making up the chromosome
arms of modern Triticeae genomes.
Construction of the Ae. tauschii Genetic Map. A total of 1,536 Illumina
GoldenGate single-nucleotide polymorphism (SNP) assays were
Ae. tauschii mapping population. Of these SNPs, 153 were not used
P.E.M., C.O.Q., L.E.T., and J. Dvorak designed research; M.C.L., K.R.D., E.D.A., A.R.A., O.D.A.,
J.A.A., N.B., M.T.C., D.C.-D., E.J.C., C.C.C., J. Dubcovsky, B.S.G., Y.Q.G., J.H., H.Y.H., N.H., G.L.,
Y.M., D.E.M., P.E.M., P.L.M., C.O.Q., J.R., D.T., L.E.T., C.T., D.M.T., F.M.Y., W.Z., and J. Dvorak
performed research; M.L.W. contributed new reagents/analytic tools; M.C.L., K.R.D., E.D.A.,
F.M.Y., and J. Dvorak analyzed data; and M.C.L. and J. Dvorak wrote the paper.
The authors declare no conflict of interest.
1Present address: Department of Plant Pathology, Kansas State University, Manhattan, KS
2Present address: Department of Biochemistry and Molecular Biology, University of South-
ern California, Health Science Campus, Los Angeles, CA 90033.
This article contains supporting information online at www.pnas.org/cgi/content/full/
September 15, 2009 ?
vol. 106 ?
because they did not detect SNP between the parents of the
mapping population or the parents were not homozygous. Of the
1,383 assays used, 1,212 (87.6%) produced satisfactory data. The
1,212 SNPs were in 641 different genes. Additional polymorphisms
were assayed with SNaPshot and RFLP (Table 1). Of the 878 loci
mapped, 863 were ESTs (Table 1). A map produced from these
data consisted of seven linkage groups (Table 1, SI Text, and Table
S1) and had a maximum resolution of 0.087 cM.
The position of each of the seven centromeres was inferred from
the allocation of loci into chromosome arms (http://wheat.pw.
usda.gov/cgi-bin/westsql/map?locus.cgi) and locations of loci on the
genetic map reported here. Each centromere was located into an
interval flanked by either single or several loci (Table S1) that were
immediately distal to the interval containing the centromere.
Orthologous and Paralogous Relationships Among the Ae. tauschii, Rice,
and Sorghum Chromosomes. Among the 863 EST loci, 66% and 64%
shared order along the chromosome with genes along sorghum and
rice pseudomolecules, respectively (Fig. S1 and Table S1). Paired t
test (P ? 0.11) failed to show that synteny of the Ae. tauschii
chromosomes with rice was greater than with sorghum. In addition
or its section showed weaker colinearity with an additional rice and
sorghum chromosome or chromosome section (for details see SI
Text, Fig. S1, Table S1, and Table S2). An entire rice or sorghum
chromosome or its section was also simultaneously colinear with
two different Ae. tauschii chromosomes (Fig. S2). As done by Salse
et al. (10), the more-related chromosomes will be called ortholo-
gous and the less-related chromosomes will be called paralogous.
Orthologues are corresponding rice, sorghum, and Triticeae chro-
mosomes that diverged from a single chromosome of the common
ancestor of rice, sorghum, and the Triticeae. Paralogues are dupli-
cated chromosomes that originated by paleotetraploidy that pre-
ceded radiation of the grass family (19, 20).
Analyses of orthologous relationships along each Ae. tauschii
making up the Triticeae genomes. The summary in Fig. 1, which is
based on data in Table S1, shows that chromosomes 3D and 6D
were each orthologous along their entire lengths to a single rice
chromosome, chromosomes 1D, 2D, and 7D to two complete rice
chromosomes, and chromosome 4D to one complete and one
incomplete rice chromosome. Chromosome 7D additionally con-
tained a small segment at the tip of the long arm translocated from
an interstitial position in chromosome 4D. Chromosome 5D was
to a portion of Os3 translocated from 4DS to the end of the 5DL
arm. Taking into account the 4DS–5DL translocation and neglect-
ing the small 4DL–7DL translocation, chromosomes 4D and 5D
also corresponded to two rice orthologues. These syntenic relation-
7D originated by fusions of two ancestral chromosomes.
Each Ae. tauschii chromosome was also paralogous to one or
more chromosomes in rice and sorghum. Orthologous and paralo-
gous relationships detected within and among the three genomes
are summarized in Table 2.
We arrived at the same conclusion as others (10, 13, 18) that the
common ancestor of Triticeae, rice, and sorghum had 12 chromo-
somes (see SI Text for our reasoning). This number was reduced to
x ? 10 in sorghum and x ? 7 in Triticeae.
Mechanism of Dysploid Reduction from x ? 12 to x ? 7 in Triticeae and
x ? 10 in Sorghum. Dysploidy is a change in the basic chromosome
number (x) of a genome without concomitant loss or gain of genes
number in Triticeae was made possible by locating the sites of the
seven active and five lost Triticeae centromeres, the present and
past chromosome termini, and their relationships to those in rice
and sorghum (Fig. 1). In every Ae. tauschii chromosome, the
interval containing the active centromere always included the
location of the centromere in the orthologous rice chromosome
(Table S1). Loci bracketing a centromere in Ae. tauschii were
several Mb apart in the orthologous rice pseudomolecule. For
example, the centromere of Os1, which is orthologous to 3D, was
at 17.1 Mb (http://rice.plantbiology.msu.edu/pseudomolecules/
centromere.shtml). Markers flanking the centromeric interval in
3D were separated by a gap in synteny of 5.6 Mb in the Os1
pseudomolecule (Fig. 1). The same markers were separated by a
gap of 30.4 Mb in the orthologous Sb3 pseudomolecule (Fig. 1).
Similar gaps in synteny were observed across all active and lost
centromeres in the Ae. tauschii chromosomes (Fig. 1). Rationale
supporting the locations of active and lost centromeres and present
and past termini for each Ae. tauschii chromosome can be found in
SI Text. The average gap in synteny was 10.3 Mb across rice
orthologous regions corresponding to the active centromeres (Fig.
1). This average gap size did not statistically differ (P ? 0.86, t test)
from an average gap size of 9.3 Mb across the inferred locations of
lost centromeres (Fig. 1). The average synteny gap across all
centromeres in comparison with sorghum pseudomolecules. The
average gap in synteny was 34.5 Mb across active Ae. tauschii
centromeres, which was similar (P ? 0.37, t test) to an average gap
size of 32.8 Mb across the inferred, lost centromeres. The average
size of the gap in synteny across all centromeres was 33.6 Mb. The
3.3-fold expansion of the gaps in sorghum compared with rice is
and sorghum genomes is almost entirely accounted for by great
The fact that the average synteny gap sizes across the active
centromeres were similar to those across the inferred locations of
centromeres in Ae. tauschii chromosomes were inferred correctly.
A total of 27 major translocation breakpoints were identified in
the Ae. tauschii chromosomes; 22 took place in the telomeric or
centromeric regions and 5 were interstitial. The translocation
breakpoints resulted in 12 fusion points (Fig. 1). Nine were fusions
of telomeric with telomeric, telomeric with centromeric, and cen-
tromeric with centromeric breakpoints and three were fusions
involving an interstitial breakpoint.
Chromosomes 1D, 2D, and 7D each evolved via insertion of an
entire chromosome by its telomeres into a break in the centromeric
region of another chromosome (Fig. 2). In 7D, the inserted
chromosome underwent several inversions (Table S3) resulting in
both termini of the Triticeae orthologue of Os8 being on the same
side of the centromere (Fig. 1). The same mechanism very likely
also generated chromosome 5D, in which a chromosome corre-
sponding to Os12 was likely inserted into the centromere of the
subacrocentric chromosome corresponding to Os9. The Os9 short
arm and its centromeric region contain few genes (1). Assuming
that the Triticeae orthologue was similar, the Os9 short arm genes
may have escaped detection at the tip of 5DS or been deleted.
Table 1. Summary of the Ae. tauschii genetic maps
mapped Illumina SNaPshot RFLP Sequencing SSR
Luo et al.PNAS ?
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Variation on this theme is present in chromosome 4D, in which the
telomeres of the Triticeae orthologue of Os11 fused and its broken
centromeric region was inserted into the Triticeae orthologues of
Os3 (Fig. 2). Whether this took place in one or two steps cannot be
discerned from the present data.
Another variation on the latter theme was observed in sorghum
chromosomes Sb1 and Sb2 (for details see SI Text). Chromosome
Sb1 originated by the insertion of the entire orthologue of Os10 to
the centromeric region of Os3. Before the insertion, however, a
pericentric translocation of an Os10 long-arm segment to the short
arm facilitated by telomere–telomere fusion took place (Fig. S3).
The same event occurred in Sb2, in which an insertion of the Os9
orthologue was accompanied or preceded by pericentric translo-
cation of a distal segment of the Os9 long arm to the short arm and
telomere–telomere fusion (Fig. S3).
in the centromeric region of a chromosome into which another
chromosome is inserted. The insertion that generated Sb2 shows
that the centromeric break can take place anywhere in the centro-
meric region, including a region containing genes. Assuming that
the centromere location in the sorghum orthologue of Os7 was the
same as in modern Os7, there are many genes between the point of
insertion of Os9 orthologue and the Os7 centromere (see SI Text
7D may have also taken place in the centromeric region not in the
centromere. The insertion point is separated by two genes from the
presumed location of the ancient Os6 centromere. However, the
region was subjected to pericentric inversions and other rearrange-
ments and other interpretations are possible (see SI Text).
A by-product of the insertion of a chromosome by its telomeres
of the centromere–telomere polarity of chromosome arms in the
new chromosome. The ancestor of rice and Triticeae had 24
chromosome arms. After the reduction to 14 arms in Triticeae, 21
of the ancient arms in Ae. tauschii have the same centromere–
telomere orientation as in rice.
Relationship Between the Locations of Genes on the Centromere–
Telomere Axis and Synteny. Ancient chromosome arms have either
Triticeae genomes. Because gene synteny in wheat is eroded more
portions (22–25), it is therefore of interest to compare erosion of
synteny along the centromere–telomere axes of ancient arms
forming the modern Ae. tauschii chromosomes.
To assess synteny along the terminal arms, 13 terminal chromo-
- 9 . 7
- 4 . 2
4 . 6
1 . 1
6 . 41
2 . 61
5 . 82
5 . 32
0 . 0
8 . 9
3 . 72
7 . 94
5 . 84
1 . 0
1 . 71
5 . 95
0 . 0
C - 8 . 9
C- 1 . 21
- 8 . 9
0 . 91
3 . 81
6 . 7
0 . 0
3 . 11
8 . 92
9 . 0
9 . 33
7 . 73
0 . 86
0 . 1
6 . 0
4 . 1
8 . 9
8 . 77
8 . 85
C - 1 . 71
5 . 0
4 . 31
0 . 91
8 . 44
9 . 8
2 . 71
9 . 74
5 . 01
6 . 37
4 . 0
- 5 . 91
C - 0 . 21
0 . 62
8 . 11
3 . 1
7 . 03
7 . 51
1 . 13
3 . 32
1 . 21
6 . 1
3 . 26
8 . 35
3 . 75
4 . 41
5 . 7
5 . 27
- 0 . 21
O / 11
C - 8 . 2
9 . 62
0 . 41
6 . 7
7 . 0
0 . 3
4 . 3
5 . 4
1 . 63
8 . 9
0 . 4
5 . 4
1 . 71
3 . 7
9 . 4
9 . 54
6 . 1
2 . 1
C- 7 . 31
2 . 1
4 . 63
1 . 7
9 . 12
6 . 1
5 . 7
7 . 8
3 . 25
C - 4 . 51
C- 9 . 21
9 . 1
8 . 2
5 . 42
9 . 72
4 . 31
2 . 82
4 . 0
2 . 13
0 . 11
9 . 1
3 . 91
6 . 3
6 . 44
1 . 06
0 . 26
4 . 0
7 . 95
9 . 0
7 . 51
1 . 5
5 . 4
5 . 9
and sorghum chromosomes Sb1–Sb10. Ae. tauschii chromosomes are subdivided into arbitrarily colored sections reflecting relationships to rice and sorghum
orthologues. Break points and telomeres are indicated by horizontal bars. The coordinates (in Mb) on rice and sorghum pseudomolecules of the first and last
gene mapped within an Ae. tauschii section are to the right of each chromosome and are boxed if they are within 2 Mb of the rice and sorghum termini. The
horizontal bars. Triangles symbolize inferred locations of centromeres lost from Ae. tauschii chromosomes. The Mb positions of centromeres (designated C) on
rice pseudomolecules are specified to the left of each chromosome.
Orthologous relationships of Ae. tauschii chromosomes (from left to right) 1D–4D (top row) and 5D–7D (bottom row) with rice chromosomes Os1–Os12
www.pnas.org?cgi?doi?10.1073?pnas.0908195106Luo et al.
some segments (the distal segment of 2DS was not investigated
because of its short length) were divided into proximal and distal
halves on the basis of the numbers of loci on the genetic map. The
numbers of syntenic genes between Ae. tauschii and orthologous
arms in rice and sorghum were counted in each half. The average
synteny with both rice and sorghum chromosomes was significantly
higher in the proximal half than in the distal half of the 13 Ae.
tauschii chromosome segments (Table 3).
interstitial positions in the Ae. tauschii chromosome arms 1DL,
2DS, 4DS, 4DL, 5DS, 5DL, 7DS, and 7DL. The 4D section
orthologous to Os11 was subdivided into two ancient arms, which
were analyzed separately. The numbers of Ae. tauschii loci syntenic
with those in rice and sorghum were similar in the distal and
proximal halves (Table 4).
Structural Changes in Relation to Genome Size.A total of 50 structural
changes were identified: 31 inversions, of which 3 were pericentric
and 28 paracentric, and 19 translocations (Table S1 and Table S3).
Most of the translocations resulted in the translocation of entire
chromosomes accompanying the dysploid reduction. Of the para-
centric inversions, 3 involved 2 loci, 13 involved 3–5 loci, 8 involved
6–10 loci, and 7 involved 11 or more loci (Table S3). Paracentric
inversions involving only two or three loci could be errors in map
construction. Seven such inversions were included in the data
(Table S3). Evidence for inversions BE426301P–BE444599 in 2D,
BF478716S–BE585724S in 5D, and BQ161010– BE637570P in 6D
was based on a single cross-over each. These inversions are there-
fore tentative. The remaining four were based on two or more
cross-overs. Of the 50 translocations and inversions, 40 originated
Table 2. Summary of main orthologous and paralogous
relationships among Ae. tauschii, rice, and sorghum
chromosomes or their sections
1D (3D ? 4D)
2D (6D ? 4D)
4D (1D ? 5D)
Os5 (Os1) ? Os10 (Os3)
Os4 (Os2) ? Os7 (Os3)
Os3 (Os7 ? Os10) ? Os11
Os12 (Os11)? Os9 (Os8) ?
Os2 (Os6 ? Os4)
Os6 (Os2) ? Os8 (Os9) ?
Sb9 (Sb3) ? Sb1 (Sb1)
Sb6 (Sb4) ? Sb2 (Sb1)
Sb1 (Sb2 ? Sb1) ? Sb5
Sb8 (Sb5) ? Sb2 (Sb7) ?
Sb4 (Sb10 ? Sb6)
Sb10 (Sb4) ?Sb7 (Sb2) ?
5D (4D ? 7D??)
6D (7D ? 2D)
7D (6D ? 5D ? 4D)
Across each row, chromosomes in bold are orthologous to complete chro-
paralogous to those in bold. For instance, chromosome 1D consists of two
sections orthologous to Os5 and Os10 and Sb9 and Sb1; Os5 is orthologous to
4D, Os1 and Os3 and Sb3 and Sb1. The section of 3D is orthologous to sections
Chromosome Sb1 is paralogous to itself, which is caused by the fusion of
orthologues of Os10 with Os3 in the sorghum genome, making up Sb1. In the
are paralogous to Os3 and Sb1. The results imply that a section of Os7 is
orthologous to 1D, for which there is no evidence. The anomaly is caused by
the paralogous relationship of a section of 1D to a section of Os3 which, in
turn, is paralogous to two chromosomes, Os7 and Os10, within the rice
semosom o r hC
ber. Centromeres are indicated by opened circles, and heterochromatin is
indicated by boxes. A break is indicated by a dashed line.
Insertional model of dysploid reduction of basic chromosome num-
Table 3. Numbers and percentages (in parentheses) of genes
showing synteny in the proximal and distal halves of the most
distal segments of Ae. tauschii chromosomes orthologous to rice
and sorghum chromosomes
Synteny with rice Synteny with sorghum
Table 4. Numbers and percentages (in parentheses) of genes
showing synteny with rice and sorghum in the proximal and
distal halves of chromosome arms embedded in other
chromosomes in Ae. tauschii
Synteny with riceSynteny with sorghum
7 4 (100.0)3 (85.7)3 (85.7)3 (85.7)
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lineage. In the Ae. tauschii lineage, paracentric inversions (24)
outnumbered pericentric inversions (3) and translocations (13).
Three paracentric inversions and five translocations were detected
in the sorghum lineage, and one translocation and one paracentric
inversion were detected in the rice lineage. The average length of
paracentric inversions in the Ae. tauschii lineage expressed in terms
of their lengths in rice pseudomolecules was 1.3 Mb. Because the
Ae. tauschii genome is approximately an order of magnitude larger
tauschii genome was estimated to be 13 Mb long.
for genotyping, 87.6% generated satisfactory results, and only
0.002% of a total of 365,000 genotype calls did not withstand
manual validation and were removed. The success rate was com-
parable to that obtained in soybean (89%) (26) but was higher than
in other plant mapping populations (67% to 77.1%) (27, 28). The
lengths of the individual linkage groups constructed from these
genotyping data were within the range expected for Triticeae
linkage maps and showed no map expansion.
Orthologous and Paralogous Relationships Between the Ae. tauschii,
Rice, and Sorghum Chromosomes. Comparative studies of wheat–rice
chromosome relationships based on the wheat EST deletion bin
maps (29) revealed orthologous relationships between wheat and
rice chromosomes (8, 10). Each of the relationships was confirmed
with the rice chromosomes were also revealed by barley EST
comparative maps (9) (http://harvest.ucr.edu). A failure to detect
Yu et al. (20) identified 18 major duplications within the rice
genome and confirmed a hypothesis that the duplications origi-
nated by paleotetraploidy (19). Because most of these duplications
predate the radiation of grasses (19, 20) they must also be present
in the Triticeae genomes. They were detected in both comparisons
of the wheat deletion bin maps (10, 30) and the Ae. tauschii genetic
Ae. tauschii, rice, and sorghum chromosomes.
Genome Size and the Rate of Genome Evolution. Of 50 different
inversions and translocations, two and eight were allocated to the
Ae. tauschii lineage. Because divergence of the BEP and PACCAD
clades likely preceded the divergence of Ehrhartoideae and Poo-
ideae, the structural changes that took place after the divergence of
the two clades but before the divergence of Ehrhartoideae and
Pooideae would therefore be incorrectly allocated to the Pani-
coideae lineage, resulting in overestimation of the number of
changes in sorghum. Although the number of structural changes
was only slightly higher in sorghum than in rice, there was an order
of magnitude more of them in the Triticeae lineage compared with
rice and sorghum, indicating that the large sizes of Triticeae
genomes are accompanied by accelerated genome evolution. The
relationship must be investigated in more grass species and if
substantiated it may have important consequences for the under-
standing of the role of genome size and repeated sequences in
genome evolution. A process that accelerates structural genome
evolution also likely accelerates gene evolution by duplication,
translocations, and deletion of individual genes. An increase in the
number of interchromosomal duplications was observed in RFLP
maps of diploid species with large genomes, such as einkorn wheat
genomes, such as rice (5.6% duplicated loci) and common bean
(8.9% duplicated loci) (31). Gene duplications and translocations
are important because they can lead to the evolution of new genes
estimated to be 13 Mb long, which is equivalent to ?3.6 cM.
Because of the small sizes of most of the paracentric inversions and
paracentric inversions may have previously escaped detection in
comparative mapping in the tribe. Structural variation may there-
fore be more common among Triticeae genomes than currently
Insertional Dysploidy. The Triticeae basic chromosome number
evolved via the loss of five functional centromeres. Four of them
correspond to those of rice chromosomes Os4, Os5, Os6, and Os9
and the fifth could correspond to either that of Os3 or Os11.
The classical ‘‘dislocation hypothesis’’ of dysploid reduction (35)
postulates two independent translocations that translocate the
euchromatic portion of each arm to other chromosomes. The
heterochromatic centromeric region is subsequently lost. Because
the process is hypothesized to occur via two independent translo-
cations, the two arms could potentially end up anywhere in the
genome and in any orientation.
both arms were translocated to the same chromosome and were in
by chance is exceedingly small. The presence of both arms in the
same derived chromosome and in the original orientation suggests
that each dysploid reduction originated by a single translocation
event. In all five derived Triticeae chromosomes, one chromosome
was inserted in a single step into the centromeric region of another
millet (Eleusine coracana) were reported to have taken place by an
insertion of a chromosome into the centromeric region of another
sorghum, and Triticeae are members of three different grass
subfamilies and the two major grass clades. The taxonomical range
of the genomes and the fact that all dysploid events in them took
place via this process suggest that insertional dysploidy has been a
dominant evolutionary mechanism in the grass family.
An insertion of a complete chromosome into a centromeric
chromosomes are stably transmitted because one centromere be-
comes inactive (37). If this were of a general occurrence in grasses,
insertional dysploidy would generate functionally monocentric
The five Triticeae insertions, three finger millet insertions, and
two sorghum insertions involved different chromosome combina-
tions and must therefore be independent of each other. Of the 10
dysploid events only one (Sb1) involved paralogues. There is
therefore no evidence that homoeology caused by paleotetraploidy
of grasses contributed to this process.
Consequences of Dysploid Reduction for the Evolution of Gene Space
Along Chromosome Arms. In wheat and related diploid species, gene
deletions and gene duplications preferentially take place in distal,
high-recombination regions of chromosomes (22, 24, 38). Synteny
between chromosomes is therefore eroded faster in distal, high-
recombination chromosome regions than in proximal, low-
recombination regions (22, 23, 25).
The terminally located ancient chromosome arms in the Ae.
tauschii chromosomes showed greater erosion of synteny in their
distal regions than in their proximal regions as expected. In
contrast, interstitially located ancient chromosome arms did not
show this relationship. This finding suggests that the synteny-
Whether or not the pattern is related to accelerated genome
www.pnas.org?cgi?doi?10.1073?pnas.0908195106Luo et al.
evolution in large grass genomes, and/or the enhancement of the
question for the understanding of grass genome evolution.
Materials and Methods
Genetic Map Construction. Ae. tauschii accessions AS75 (collected in Shaanxi,
China, by C. Yen, Sichuan Agricultural University, Yaan, Sichuan, China) and
AL8/78 (collected in Armenia by V. Jaaska, University of Estonia, Tartu, Estonia)
were crossed, and DNA was isolated (39) from 572 F2progeny. A total of 1,536
(Illumina) and 26 SNPs were genotyped in a subset of 174 plants with SNaPshot
(Applied Biosystems). RFLP at 201 loci were genotyped as described previously
(40). For details of SNP genotyping with GoldenGate and SNaPshot see SI Text.
Graphical genotypes of the 572 plants were arranged so that the number of
double cross-overs and singleton loci was minimized. Each cross-over was vali-
dated by re-examining genotyping data. Questionable data were excluded.
from each group of cosegregating markers (termed a recombination block) was
Orthologous and Paralogous Chromosome Relationships. A homology search was
performed between FASTA sequences of wheat ESTs or EST contigs (http://
wheat.pw.usda.gov/cgi-bin/westsql/contig.cgi) and O. sativa (IRGSP pseudomol-
ecules Build04) and S. bicolor (http://genome.jgi-psf.org/Sorbi1/Sorbi1.
download.ftp.html) genome sequences using an e-10 cutoff. Progression of
starting nucleotides along a pseudomolecule paralleling the progression of the
genetic map was used as evidence of colinearity. Colinearity was statistically
starting nucleotides on the rice and sorghum pseudomolecules ( Table S1). Only
chromosomes or chromosome regions with seven or more loci were used in
correlation analyses. Regions with large inversions were subdivided into two
groups on the basis of gross gene order, and correlations were computed sepa-
rately for each group of loci. Correlations were computed separately also for
To determine which rice and sorghum pseudomolecule was orthologous and
which was paralogous to a specific Ae. tauschii chromosome, the lengths of the
ing to their total length. The pseudomolecule (or its portion) with the highest
rank was declared orthologous to an Ae. tauschii chromosome and that with
Inversions and Translocations. The order of recombination blocks along an Ae.
tauschii linkage group was compared with the order along the orthologous rice
ecules differed from the order along the Ae. tauschii linkage group, it was
assumed that the structural change took place in the Ae. tauschii lineage. If Ae.
it was assumed that a structural change took place in the rice lineage, and if rice
it was assumed that the change occurred in the sorghum lineage.
Relationship Between Synteny and Location of Loci on the Centromere–Telomere
(three in the case of 5D) ancient chromosomes making up these five Ae. tauschii
chromosomes. Loci in the distal segments of these five chromosomes and both
in inverted regions. The significance of the difference between the two halves
To assess the relationship between synteny and gene location in the ancient
chromosome arms embedded in Ae. tauschii chromosome arms 1DL, 2DL, 4DS,
juxtaposed to the ancient terminus and half juxtaposed to the ancient centro-
mere. The numbers of colinear loci in the two halves on rice and sorghum
orthologues were counted and significance was assessed as above.
ogies Core at the University of California Davis Genome Center) for performing
the Golden Gate assays, and Professor Peter Langridge (Australian Centre for
Plant Functional Genomics, University of Adelaide, Adelaide, Australia) and
Patrick S. Schnable (Center for Plant Genomics, Department of Agronomy, Iowa
State University, Ames, Iowa) for advising this project. This work was supported
by National Science Foundation Grant DBI-0321757.
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