AbstractThe genomes of six major grass species can be aligned by dissecting the individual chromosomes into segments and rearranging these linkage blocks into highly similar structures

Devos, K.M.

Gale, M.D.

Moore, G.

Wang, Z.

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G. MOORE, K.M. DEVOS, Z. WANG AND M.D. GALE CEREAL GENOME EVOLUTION
Grasses, line up and form a circle
The genomes of six major grass species can be aligned by
dissecting the individual chromosomes into segments and
rearranging these linkage blocks into highly similar structures.
Cereals are the staple diet of most of the world's
population and the study of their genetics, physiology,
biochemistry and agronomy has preoccupied cereal
biologists for most of the present century. We have all,
however, been specialists in our own favoured crop
species, and research has tended to proceed in parallel,
with little academic interaction or comparison of species.
In the late 1980s, when novel molecular technology
allowed us, for the first time, to make dense chromo-
some maps, it was expected that the individual species
maps would be unique. But the use of a new tool for
comparing the genomic maps of different cereal crops -
'rice linkage segment' analysis - shows that this is not
the case.
Comparative mapping in cereals
In 1986, when we began constructing restriction fragment
length polymorphism (RFLP) maps for each of the three
genomes in hexaploid (bread) wheat, we imagined that
they would turn out to be different. It soon became clear,
however, that the maps for each of the three diploid ances-
tors of hexaploid wheat - Triticum urartu, Aegilops squar-
rosa and the still unidentified donor of the B genome -
are actually remarkably similar [1]. The ability of the
Fig. 1. Comparisons of cereal genome evolution based on rice linkage segments. (a) Rice chromosomes dissected into linkage blocks
[3]. (b) Wheat, (c) maize, (d) foxtail millet, (e) sugar cane and (f) sorghum chromosomes represented as 'rice blocks' on the basis of
homology and/or conservation of gene order. Connecting lines indicate duplicated segments within the maize chromosomes. (g) An
ancestral 'single chromosome' reconstructed on the basis of these linkage blocks [3]. The designation of the different sorghum linkage
groups has varied between laboratories and publications. The data in several publications [8-11] have been assembled in the form
presented by Grivet [12,13]. For the purpose of this figure, the sorghum linkage groups have then been assigned (S1-S10) on the basis
of their rice segments and the order of rice segments in the ancestral 'chromosome'. Open boxed linkage groups indicate that the order
of segments within each linkage group needs further confirmation.
© Current Biology 1995, Vol 5 No 7
CEREAL GENOME EVOLUTION
737
G. MOORE, K.M. DEVO, Z. WANG AND M.D. GALE
738 Current Biology 1995, Vol 5 No 7
Fig. 2. Alignment of the genomes of six major grass crop species with 19 rice linkage segments, whose order reflects the circularized
ancestral grass genome. The data in Fig. 1 have been redrawn as a series of rice linkage segments (defined by radiating lines) formed
into chromosomes (broken colour-coded and numbered lines). The thin dashed lines correspond to the duplicated segments. Inversions
of sets of sequences within a linkage segment (such as the inversion of segments 3a and 3b in maize chromosome 5) are not shown.
Linkage segments forming parts (pt) of Triticeae chromosome 5 are shown as a series of segments connected by coloured lines. The
alignment is based on the genetic map of the D genome of wheat. The red line indicates the duplicated segments shown as blocks l1 b
and 12b. Chromosomes formed by the insertion of one segment into another are shown by black lines with arrows indicating the direc-
tion and point of insertion. The points of chromosome breakage involved with insertion events are indicated by black bisected circles.
The 'haploid' chromosome number of each species is shown in the column marked 'x'. The haploid DNA content of each species,
shown in the column of 1C values, is per 109 bases.
wheat RFLP probes to cross-hybridize with homologous
sequences in other cereals allowed us to extend these com-
parisons to the genomes of other major Triticeae species
- rye and barley. Although the rye genome was found to
be rearranged relative to that of wheat by a few major
translocations [2], most probes revealed that the same loci
in wheat, barley and rye were arranged in exactly the same
order along large stretches of their chromosomes.
In 1992 we were able to start asking the same questions
about the relationships between the genomes of wheat
and maize, and between those of wheat and rice. We
found that the gene order was conserved at the genetic
level, despite these species having been isolated for up to
60 million years - a period equivalent to that during
which eutherian mammals have evolved [3].
Rice linkage segment analysis
The rice genome is one of the smallest among the grasses
and, following recent intense research activity, has become
pivotal to grass genetic studies. When the relationship
between the genetic maps of the three major cereals was
examined, it became clear that the conservation of gene
order was restricted to a number of rice linkage segments.
It was then possible to describe the genes on the maps of
individual maize and wheat chromosomes in terms of
these segments, rather like building with blocks of 'Lego'.
These blocks could be assembled into a single stack for a
Triticeae genome and two other stacks to form a maize
genome. Furthermore, all of the 19 blocks could be
assembled in a specific order, forming a single stack which
may represent the ancestral cereal genome. Then, for each
species, the stack can be cleaved at different points to gen-
erate single blocks, or groups of blocks, which describe the
gene framework of each chromosome in its genome [3].
This analysis is based on maps derived from recombina-
tion data, expressed in centimorgans. Whether the gene
orders are conserved at the megabase level is, at present,
still an assumption. Similarly, it is clear that this conserva-
tion applies only to genes; the nature and amount of
intergenic DNA varies greatly between species, depend-
ing on the extent of accumulation of sequences, mostly
repeated, following isolation by speciation.
An extended grass genome framework
We have now been able to extend the analysis to include
foxtail millet (Setaria italica), sorghum (Sorghum bicolor)
and sugar cane (Saccharum spp.). The results, based on the
cross-mapping of common DNA probes, are shown in
DISPATCH 739
Figures 1 and 2. It is apparent that only 19 linkage
blocks, comprised of large chromosome segments or
whole rice chromosomes (ignoring the duplicated seg-
ments [4] shown as blocks 11lb and 12b in Figs 1 and 2),
are needed to reconstruct all the cereal chromosomes
compared so far. Moreover, with the rice linkage seg-
ments arranged as shown, they can be fitted together in
the same order to compose most of 56 chromosomes in
the diagrams. The recognition that a segment of maize
chromosome 3 is duplicated on the long arm of chromo-
some 10 (Fig. c), effectively circularizes the consensus
grass genome. This single 'chromosome' provides the
basis of a consensus map that may reflect the genome of
the ancestral grass from which these cereals evolved.
The conservation of genes and gene orders is irrespective
of 'haploid' chromosome numbers (x) of the six species.
These vary from 5 (maize), 7 (wheat, barley and rye), 9
(foxtail millet), and - 10 (sugar cane, sorghum) to 12
(rice). It is also irrespective of the haploid DNA contents
(1C value) which vary 40-fold - rice being the smallest
(400 megabases) and the Triticeae cereals the largest.
Moreover, it is clear from information presented at the
recent Plant Genome III meeting in San Diego (15-19
January 1995) that hexaploid oats (Avena sativa; x = 7) [5]
and rye-grass (Lolium perenne; x = 7) [6] share similar
levels of conservation, and could soon be incorporated
into the rice-linkage analysis.
Cereal evolution
The analysis confirms that maize is a complete tetraploid,
although the two genomes are rearranged relative to one
another. Interestingly, most of the larger chromosomes
(1, 2, 3, 4 and 6) form one genome, and a shorter set
(5, 7, 8, 9 and 10) form the other. Doubts as to the
ploidy of sorghum can also be resolved, as it is clear that
the ten chromosomes form a complete cereal genome.
Furthermore, the break in the ancestral 'chromosome'
between blocks 3c and 3b in the millet, sorghum, maize
and sugar cane genomes, together with the insertion of
block 10 into the same break in millet, sorghum and one
of the maize genomes, clearly places these species in a
group (see Fig. 1). The Triticeae species and Oryzeae
(rice) species form two further groups.
Applications
For those interested in the more detailed mapping of any
region of any grass genome, Figure 2 shows, at a glance,
the chromosomal regions of other species that will serve
as sources of potential DNA or protein markers. For
those interested in traits, and the genes that control them,
Figure 2 can also be used to reveal similar traits mapping
to corresponding linkage segments which are likely to be
controlled by homologous genes. For example, a radius
in Figure 2 from block 3b will pass through Rhtl and
Rht2, the wheat gibberellin-insensitive semi-dwarfing
genes, and d9 and d8, the maize gibberellin-insensitive
dwarfing genes. Similarly, a radius from block 4a passes
through the liguless genes on barley block 2, maize block
2 and rice block 4.
The way is now open to capitalize on the wealth of infor-
mation available for the many grass species, by exploiting
the extensive resources being devoted to the analysis of
the small genome of rice. Genes located in any grass can
be isolated by map-based cloning of the homologue in
rice, and then by homology in the target species. The
reconstruction of the rice genome in the form of ordered
yeast artificial chromosomes will reveal the general gene
order and content of all cereal genomes. This may pro-
vide clues as to how and why particular regions of some
cereal genomes have undergone extensive expansion by
the non-random accumulation of repetitive sequences
following speciation [7].
The concept thus describes a framework for the eventual
collation of most of the information derived from the
genetical studies of individual cereal crops and their wild
relatives since the rediscovery of Mendel's laws.
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Graham Moore, Katrien M. Devos, Zhimin Wang and
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Park, Colney, Norwich NR4 7UH, UK.


Cereal Genome Evolution: Grasses, line up and form a circle 

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Cereal Genome Evolution: Grasses, line up and form a circle

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