Update on Grass Genomics
Grasses as a Single Genetic System. Reassessment 2001
Michael Freeling*
Department of Plant and Microbial Biology, University of California, Berkeley, California 94720
Grasses are a large, diverse, and successful family
of monocotyledonous flowering plants characterized
most dramatically by their spikelet style of floral
structure (Fig. 1a) and by the number and pattern of
these spikelets in the inflorescence. There are about
10,000 species that are categorized as grasses by taxonomists who traditionally follow embryonic, architectural, and anatomical characters (e.g. Clayton and
Renvoize, 1986). More recent comparative DNA sequence information confirms that all grasses examined to date did indeed diverge from one common
ancestral population of “grass alleles” and are distinct from the nearest non-grass family, the Joinvilleaceae. In general, the taxonomic distinction within
the grasses continuously divides these species into
subfamilies, supertribes, tribes, subtribes, genera,
species, and subspecies. As additional species have
been added to the sequence databases, a phylogenetic trend has emerged. Where Clayton and Renvoize (1986) recognized six subfamilies, Kellogg
(1998 and refs. therein) recognized 13, and the “in
progress” data of the Grass Phylogenetics Working
Group (http://www.ftg.fiu.edu/grass/gpwg) could
be used to justify recognition of at least 16 subfamilies, often composed of one or a few species. At
present the phylogenetic relationship—the exact
branch relationships—among most of these 16 subfamilies is not known, as if they originated in a single
grass adaptive radiation, estimated to be about 70
million years ago (Kellogg, 1998 and refs. therein). In
fact, there is likely one specific order by which the
several grass subfamilies are related, one to another,
but sequence-based trees are necessarily quantitative
and often cannot resolve deep branches. Perhaps
phylogenetic trees based on chromosomal breakpoints, not being time-dependent, will fare better.
Until about 8 years ago, one grass species maps and
mutant collections, however interesting, did not directly affect research on another grass species, even
though grass genomes were known to be related.
This state of being isolated by commodity changed in
1992–1993. Of particular notice was the research of
Dr. Steven Tanksley and coworkers on gene order
comparisons of maize and rice (Ahn and Tanksley,
1993) and Dr. Mike Gale and coworkers and their
many international collaborators who moved from
mapping wheat relatives to more distant grasses
(summarized by Moore et al., 1995). The graphic
summary of these mapping data, greatly simplified,
* E-mail [email protected]; fax 510 – 642– 4995.
has become popularly known as “The Circle Diagram” because of a method used to draw the expressed gene sequence (EST) maps of several different grass species on one radial axis. A recent Circle
Diagram (Gale and Devos, 1998) includes crop grass
species from four subfamilies: Pooids (wheat and
oat), Panicoids (maize, sorghum, sugarcane, and foxtail millet), Oryzoids (rice), and the Chlorinoids (finger millet). In general, gene probes (ESTs) were chosen to span entire genomes at intervals of 10 or 20
map units. Comparative mapping in the grasses has
been reviewed recently (Devos and Gale, 2000). The
general conclusion is that all of the grasses in the four
subfamilies examined have their genes in about the
same order so that one can conclude with confidence
that one ancestral genome remains recognizable in its
descendents. The huge differences in DNA content/
haploid genome and the differences in chromosome
number seem to have little or nothing to do with gene
number or order. Recent polyploids, like bread
wheat, for example, certainly have multiples of the
ancestral gene number, but even this simple expectation about polyploids proves to be false for descendents of ancient duplication events, as will be
discussed.
DEFINITIONS OF MACROCOLINEARITY
AND SYNTENY
Closely related species within a genus have the
same chromosome numbers unless they are easily
recognizable polyploids. It is expected and proved
that the individual genomes in a polyploid series
carry the same number of genes per genome, and that
these genes are in the same order (as in the wheats;
cited in Devos and Gale, 2000), allowing for the occasional chromosomal aberration (inversion, duplication, translocation, or deletion of previously duplicated chromosome) as well as the occasional
“mutant.” The result is called “macrocolinearity” because a typical mapping interval is 10 to 20 map
units. In a particular rice heterozygotic region including the adh1 gene, 10 map units is 1.15 Mb and carries
147 potential genes (Tarchini et al., 2000). When gene
orders, quantified in coarse mapping intervals, are
compared species with species, estimates of “macrocolinearity” result. If five markers in a row covering
50 map units also occur in a row on another chromosome, these chromosome regions are macrocolinear.
Often a breakpoint event disconnects this string of
five markers, and colinearity is broken. Such chro-
Plant Physiology, March 2001, Vol.Downloaded
125, pp. 1191–1197,
from on June
www.plantphysiol.org
17, 2017 - Published
© by
2001
www.plantphysiol.org
American Society of Plant Physiologists
Copyright © 2001 American Society of Plant Biologists. All rights reserved.
1191
Freeling
Attempts to demonstrate widespread colinearity
between monocots and dicots have not been successful (Devos et al., 1999; Bennetzen, 2000). The comparison of full genomic sequences between rice and Arabidopsis should be particularly informative.
MICROCOLINEARITY
Figure 1. Vast genetic diversity within grasses is easiest to recognize
by looking at flowers. The grass spikelet (a) and examples of diverse
floral branching. b, Ryegrass, Lolium; c, a foxtail, Alopeculurus; d,
false brome, Brachypodium; e, bent grass, Agrostis; f, meadow grass,
Poe; g, a dogstail, Cynosaurus. Reproduced by permission from Fitter
et al., 1984; drawn by Ann Farrer.
mosomal aberrations are expected and are often
readily explicable, so another more generous term,
“synteny,” is often used to refer to largely homologous chromosomal segments. Perfect synteny occurs
as long as the ancestral gene order can be reconstructed, and accepts chromosomal breakpoints,
polyploidy, and partial duplications. So, although
closely related species in the same genus do not
always display perfect macrocolinearity, they are
syntenous. Comparing more diverged species brings
with it the expectation that more chromosomal aberrations and gene mutations should occur, and they
do (Devos and Gale, 2000). The extent of chromosomal aberrations turns out to be unpredictable. For
example, pearl millet and foxtail millet are species
from two closely related genera in the same subtribe,
whereas rice is in a different subfamily than the
millets, these being as far apart genetically as is possible while still being grasses. Foxtail millet and rice
have few (massive) chromosomal aberrations (Devos
et al., 1998), whereas the two millets have many more
major chromosomal rearrangements (Devos et al.,
2000). Even so, the comparative maps are syntenous.
1192
Ten map units of a rice chromosome in the adh1
region carry approximately 147 genes (Tarchini et al.,
2000). Consider the question: is it certain that if a
large chromosomal region displays macrocolinearity,
then the genes between these markers should also be
approximately colinear? The answer depends on the
nature and frequency of small chromosomal aberrations, those involving one to a few genes, as compared with the traditional double-strand-break-type
aberrations, and whether these small and large
events share the same mechanism. If individual
genes routinely excise and relocate at random in the
genome, then synteny would be lost. Bennetzen
(2000), in his recent review of microcolinearity in
flowering plants, argues that it is best to compare all
genes in macrocolinear regions of a number of species before deciding whether macrocolinearity predicts microcolinearity. The first comparison between
such regions in maize and sorghum discovered that
maize carried massive amounts of retrotransposons
between its genes, whereas sorghum did not, and
that this difference roughly accounted for the 5-fold
DNA content/genome difference between maize and
sorghum (SanMiguel et al., 1996). Bennetzen (2000)
measured microcolinearity in the adh1 region of
maize and sorghum, species that are thought to have
diverged about 20 million years ago. A 78-kb
genomic sequence of sorghum carrying adh1 was
compared with a potentially homologous adh1containing maize sequence roughly five times larger
because of retrotransposon filler. Considerable microcolinearity between maize and sorghum was
found. A conservative estimate might be that eight
obvious genes are present in perfect colinear order
and transcriptional direction, and there are two genes
in sorghum that may have no orthologs in the maize
sequence. Tarchini and coworkers (2000) attempted
to compare the adh1-adh2 region of rice with the
Panicoid (maize/sorghum) sequences, but encountered an apparent translocation just at Adh1; they did
not find and sequence the missing segment. In the
comparable region, considerable microcolinearity
was found between rice and sorghum.
Bennetzen (2000) reviews all of the other cases of
intragrass sequence comparisons as well, and concludes that microcolinearity seems to be the rule so
far, but there are many apparent exceptions. Bennetzen discusses mechanisms and selective pressures
that could help explain these exceptions, including
the interesting idea that there may be selection to
break colinearity.
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2001 American Society of Plant Biologists. All rights reserved.
Plant Physiol. Vol. 125, 2001
Grasses as a Single Genetic System
THE IMPORTANCE OF SYNTENY AMONG
THE GRASSES
If all grass genomes were syntenous, then mapping
any character to any grass gene in the progeny of any
grass hybrid—in any of the 10,000 species—would
lead to a map position via the rice sequence, and a
deduced array of candidate genes. For example, this
mapping might be between two newly discovered
species of grass in a genus about which nothing is
known. So, if any character or QTL (quantitative trait
locus) can be mapped to one map unit, then there
would be approximately 15 candidate genes in the
region (using the rice estimate as already discussed).
In short, any phene that can be mapped with precision can be reduced to nucleotide sequence. Synteny
must hold if this pan-grass mapping potential is to be
realized. Early data reviewed by Bennetzen (2000)
are reassuring.
THE CASE OF THE GIBBERELLIC ACIDINSENSITIVE (GAI) DWARVES IN PLANTS:
TOWARD MAPPING IN SILICO
GAI dwarves occur in several grasses and in Arabidopsis. The first sequence was from GAI (Arabidopsis), which was mapped onto maize, the three
wheat genomes, and rice. Harberd and coworkers
showed that a GAI ortholog existed in all of these
grasses, and four of the positions were coincident
with the dwarves that fuelled the Green Revolution
(Peng et al., 1999). The homologous gibberellininsensitive dwarf in barley was added subsequently
to the list of GAI-dwarves (Ivandic et al., 1999). All
GAIs exist in syntenous positions in grasses. The data
on which these studies were based involved wetlaboratory hybridization mapping. If the rice sequence had been available, GAIs best homolog in rice
would have anchored this gene to a syntenic region
even though a dwarf is not known to map to this
gene in rice. By mapping in rice, all of the syntenic
(orthologous) map positions in maize, wheat, barley,
and all other grasses would have become immediate
candidates for dwarves. All of these dwarves would
have been reduced to gene sequence simultaneously,
each controlling the other to generate unequivocal
data, and all would have been accomplished by
working with information only (in silico). It seems
likely in the case of the GAI dwarves in grasses that
the knockout phenotype in maize when it is learned,
will also extrapolate to function throughout the grass
family. (The Pioneer Hi-Bred International Company
[Des Moines, IA] operates a maize gene knockout
service that will search their proprietary F1 DNA
samples for transposon Mu insertions between the
PCR primer the collaborator sends them and a Mu
transposon, and send out samples of F2 seed so that
one might discover a phenotype caused by the
mutant lesion [called TUSC; Bensen et al., 1995]. An
NSF-funded reverse genetics service, the Maize
Plant Physiol. Vol. 125, 2001
Targeted Mutagenesis [MTM] service, http://mtm.
cshl.org, began operation early in 2000.) Most genes
are expected to function similarly in all grasses.
ON USING “FAMILY” RATHER THAN “SPECIES”
AS A MODEL GENETIC SYSTEM
By considering individuals in many species related
to one another in a known phylogeny, there is a
logical possibility to deduce important facts about
the origin of living designs where design represents
evolution over millions of years by a process of natural selection of new mutants and new combinations
of alleles, as well as manifold chance events, and
perhaps the alleles or combinations of alleles that
encode them. Figure 1 depicts grass flowers, and by
no means covers the full breadth of species diversity.
A plethora of flower branching designs, spikelet
numbers, and spikelet arrangements are shown.
Even so, each grass flower, and the spikelet itself, is
made of the same modular segments—with the same
organs and organ components—recognizable even if
not elaborated. There is also much diversity for other
characters, some of which are leaf anatomy, photosynthetic types, epidermal cell-type patterns, venation patterns, ligule shapes, apomictic style, weediness, and salt/drought/pest/hypoxia tolerance.
Each of these variations was presumably evolved
from a common grass ancestor (see Bennetzen and
Freeling, 1998).
Figure 2 (Kellogg, 1998) shows a very minimized
(four subfamilies) phylogenetic tree of the grasses,
with a single character mapped upon this tree. This
Figure 2. A minimized phylogenetic tree of grass species on which is
plotted DNA content per diploid (2C) prereplication nucleus, reproduced by permission from Kellogg (1998). C-value data and phylogenetic data are from others, cited in the original. Ancestral genome
sizes were reconstructed according to squared-change parsimony.
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2001 American Society of Plant Biologists. All rights reserved.
1193
Freeling
character, called “C-value,” is the amount of DNA in
the pre-replication, diploid, mitotic nucleus of the
species identified. The subfamilies to which these
species belong are marked on the right. Some common ancestors are identified by arrows in front of
deduced 2C values; these notations constitute a possible model for the evolution of C-value in these
grasses. The general conclusion from this study is
that C-value can increase or decrease over evolutionary time. Increases in C-value are seen in the Pooids
and the Zea/Tripsicum branches of the Panicoids. Decreases are particularly clear in the genus Corynephorus. Obvious mechanical hypotheses, probably involving retrotransposons (SanMiguel et al., 1996),
can be formulated and tested on the basis of the
phylogenetic data of Figure 2.
CONVERGENCE IN A PHYLOGENETIC TREE
MARKS AN EXPERIMENTAL OPPORTUNITY
Because DNA content is a continuous character, no
branch in the tree in Figure 2 demonstrates an origin
of novelty. The informative lineages of Figure 2 are
those demonstrating convergence. For example, that
rice and a Corynephorous have low DNA/genome
content is not because of lineage (which would make
the characters homologous), but convergence. The
mechanism of lowering genome size rapidly within
an otherwise high DNA content lineage is of obvious
interest specifically because it is able to adapt or
change. Even more useful experimentally are cases of
convergence that happen between more closely related species, implying rapid evolution. The most
useful cases of convergence occur between subspecies, or species that can still cross pollinate to make
fertile hybrids, or in the rapid process of domestication. Such convergences must have occurred quickly,
and involve one or a few alleles, and the wide hybrid
would permit mapping of these alleles as QTLs. Every character that is polymorphic in the grasses—
apomixis, Kranz anatomy, and the others listed previously–display convergences. Geographies where
unfilled niches appeared quickly, as with islands, or
where the environment is marginal to grass life, as
with sand dunes or thermal pools, are especially
good places to search for convergences. Each convergence constitutes a rapid evolutionary adaptation
involving one or a few alleles, and each is a case
study in the “genetic engineering” of useful phenotype. Often a particular character or adaptation such
as short generation time, perennial habit, C4 photosynthesis, and aposporic apomixis occurs multiple
times in a lineage. To what extent such “repeating”
characters are convergent (truly of genetically independent origin) or divergent (at least partially sharing the genetic capacity to evolve a character) can
make matters academically confusing. Speaking
practically, if the character can be mapped, there is a
good chance the character can be reduced to DNA
sequences.
1194
Using “grasses as a single genetic system” logic,
Paterson and coworkers (1995) were able to explain
the convergence of domestication traits, those selected by indigenous breeders, in the cereal grasses
by showing that mutant alleles of a small set of grass
genes were involved.
THE GRASS HYBRIDS DATABASE:
HTTP://128.32.88.35/GRASSWEB/
Why does hybridization sometimes occur between
different species or between species in different genera? The domesticated races of wild species are often
classed as different species by taxonomists, although
domesticated and wild species can effectively cross.
The explanation is obvious: The taxonomists were
fooled by convergences caused by human selection.
Some genera such as the Festuca-Lolium complex of
species are famous for wide crosses that yield fertile
hybrids; other subtribes exhibit no such propensity.
There are approximately 4,000 hybrids, mostly infertile, identified and referenced in the grass hybrids
database (http://128.32.88.35/grassweb), and there
are certainly many more hybrids known, but not yet
reported.
The point of the grass hybrids database is to facilitate discovery of individual fertile hybrids that are
heterozygous for alleles specifying profound character differences. Such profound character differences
result from convergence or perhaps, hopefully, the
evolution of a truly novel phene. Given this hybrid,
QTL mapping of alleles to pan-grass markers should
automatically generate candidate genes from the
fully sequenced anchor genome (this genome is rice
for the grass family). The best support for this approach (Lan and Paterson, 2000) is the recent success
at mapping QTLs important for “sculpting the curd,”
the unique flower arrangement of broccoli, for example, in the Brassica family of dicots, using Arabidopsis
as the anchor genome from which candidate genes
are drawn.
REALLY WIDE CROSSES BETWEEN GRASSES:
CHROMOSOME ADDITION LINES
There have been attempts to cross grass species in
different subfamilies, species diverged to about as far
as one can get within the grasses. Crosses between
maize and wheat, and many others, always with the
most polyploid as female, have been tried and the
resulting embryos, when such occur, have been rescued by tissue culture. The results are maternally
haploid progeny and also include cell lines that have
additional chromosomes that are eliminated during
mitoses and plant regeneration; hybrids created by
protoplast fusion fared similarly (Laurie et al., 1990).
There is one glaring, very wide cross success that was
between grasses that are maximally diverged: pollen
from maize (Panicoid; ancient tetraploid) onto eggs
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2001 American Society of Plant Biologists. All rights reserved.
Plant Physiol. Vol. 125, 2001
Grasses as a Single Genetic System
of oats (Pooid; recent hexaploid). A recent publication (Riera-Lizarazu et al., 2000) refers to success at
adding each chromosome from maize into oat and
having this chromosome predictably transmit to the
next generation. This paper highlights one of these
monosomic lines containing maize chromosome 9 as
a source for construction of radiation hybrid mapping populations. Oat seeds with one chromosome 9
were irradiated. The often deleted or minimized
chromosome 9 was recovered in oats, identified because these oats contained maize specific midrepetitive sequences, and then mapped using 39
maize markers spaced along the 151 map units, and
191 Mb, of chromosome 9. Results indicate that 100
informative radiation hybrid lines should permit
mapping to 0.5 to 1.0 Mb, which should be very
approximately 10 to 20 genes as extrapolated from
data (Bennetzen, 2000) on the maize adh1 region.
Even higher resolution is possible with more lines.
Using maize-specific probes to examine addition line
karyotypes by fluorescent in situ hybridization
shows exactly where these fragments of maize DNA
end up in oat chromosomes, providing an unparalleled tool for examining aspects of chromatin-level
gene regulation. As referenced by Riera-Lizarazu et
al. (2000, citing Muehlbauer et al., 2000), there is at
least one case where a gene on the added maize
chromosome expresses and alters phenotype.
By applying “grass as a single genetic system,” it
seems possible that mapping in outlying grasses
might be to PCR-generated gene fragments, and then
these gene fragments might be mapped in maize
using radiation hybrids. Gene mapping in any grass
should identify the candidate genes in the rice
sequence.
THE CONSEQUENCES OF ROUNDS AND
ROUNDS OF DUPLICATIONS AND BREAKPOINTS:
THE IMPORTANCE OF CONSOLIDATION
OF CHROMOSOMES BEFORE
COLINEARITY COMPARISONS
Internal sequence comparisons of yeast have discovered much duplication and a tetraploid ancestry
is suspected (Wolfe and Shields, 1997). Arabidopsis is
largely duplicated as well and a comparison of tomato and Arabidopsis, two widely diverged dicots,
leads to the general conclusion that Arabidopsis has
undergone an ancient tetraploidization event and
subsequent large-scale duplication events as well
(Blanc et al., 2000; Ku et al., 2000). Duplications of the
genome, in whole and in part, may be the rule rather
than the exception.
Maize is thought to be descended from a segmental
allotetraploidy event (Gaut and Doebley, 1997) that
happened approximately 20 million years ago (for
discussion, see Bennetzen, 2000). The case of allotetraploid maize illustrates an important point I call
“consolidation.” There are numerous cases of dupliPlant Physiol. Vol. 125, 2001
Figure 3. A cartoon that teaches the concept of consolidation as it
pertains to merging diverse colinear strings of once duplicated genomes or segments. Once duplicated, the once colinear strings are
expected to be winnowed over approximately 20 million years of
evolutionary time. The leftmost stack of chromosomal regions, 1
through 10, constitute the ancestral sequence, be it an entire genome
or a segment. In the organism to the left of the arrow, this ancestral
sequence has been duplicated and upon insertion into a new position, three blocks of genome were triplicated and inserted within
itself backwards. Thus, this organism is entirely duplicated for the
ancestral sequences (duplicates 1⬘–10⬘) and partially triplicated and
inverted (9⬘ ⬘ ⬘–7⬘ ⬘ ⬘) as well. Applying about 80% winnowing (for
text derivation, see Sentoku et al., 1999) and 10% divergence to a
new, unrecognizable sequence, the rightmost genome is one of many
possible consequences. Note how most of the duplicated segments
have been deleted (winnowed). The inset illustrates the concept of
consolidation. The ancestral genome is on the left. It is possible to
visualize 100% synteny easily if both colinear regions of the evolved
genome are sequenced and consolidated into one virtual linkage
group, which is drawn on the right. Note that the inversion, the
linked duplications, and the diverged block are now easy to understand (inset), and 100% synteny is evident. In this simple model all of
the duplication happened at one time only. In real life, duplication,
winnowing, and divergence might occur continuously.
cate genes that map to the suspected homeologs, but
there also numerous cases of sequences that seem to
hybridize as single genes and there are certainly
many, many recessive mutant alleles identified in
maize. Thus, it is difficult to know what to expect of
a once-duplicated genome after 20 million years of
evolution. One study (Sentoku et al., 1999 and refs.
therein) generated data on which some useful predictions can be made. After exhaustive hybridization
searches, there turns out to be seven class I homeobox genes (knox genes) in rice, a presumed true
diploid, and nine in maize, not 14 as would be initially expected on the basis of polyploidy. Only one
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2001 American Society of Plant Biologists. All rights reserved.
1195
Freeling
of the extra genes in maize maps to the syntenic
region and is diverged to the extent expected of the
genomic duplicate; the other extra knox gene is an
obviously recent, linked duplication. This computes
to 14% (1/7) retained tetraploidy, 14% recent duplication, 86% winnowing, where one of the onceduplicated genes has been deleted, and 100% synteny, where every rice gene maps to a macrocolinear
position in maize. Figure 3 is a totally hypothetical
model where an ancestral stretch of chromosome
marked in blocks 1 through 10 is duplicated and in
the process, partially duplicated again and inserted
within itself in inverted order. One possible evolved
consequence of this duplication-triplication inversion
event is shown, using the large winnowing frequency
found by Sentoku and coworkers. The point of this
exercise is to emphasize that duplications establish
macrocolinear arrangements that are expected to alter over time. (Ku and coworkers [2000], working
with dicots, used the term “network of synteny”
when describing the consequences of evolution from
duplicated genomes; their discussions are conceptually similar to my own.) It is premature to call deviations from colinearity within single chromosomes
“exceptions” until all of the duplicated regions are
sequenced and consolidated into one virtual chromosome. The inset of Figure 3 shows a comparison of
the original ancestral sequence with the consolidated
sequence; the result is 100% synteny and some added
complexity.
THE MECHANICAL BASIS FOR
DARWINIAN EVOLUTION
Using “grasses as a single genetic system,” there is
a logical avenue to discover the sorts of genes that
when mutant, generate macromutations important
for speciation and adaptation. The mechanical basis
for Darwinian evolution is, of course, grail-like in
importance (Goldschmidt, 1952) and cannot be addressed in any single species genetic system.
CONCLUSIONS
Most data support and none refute the general
conclusion that grasses share “alleles” of the ancestral grass genome rearranged in blocks that remain
long enough to reconstruct, by the process of consolidation, useful syntenic relationships. The vast paradigm called “grasses as a single genetic system,”
(Bennetzen and Freeling, 1993) has now been redefined in these few paragraphs. This paradigm provides a way to extract from natural variation those
gene sequences, alleles, that caused profound evolutionary changes, and not to be sidetracked by all of
those alleles “along for the ride.” In studying these
sequences, the mechanisms by which they are expressed, and the biological context within which they
acquire meaning, it is possible that we may yet be
1196
able to reduce profound diversity—the sort of diversity represented by the morphological differences in
Figure 1—to principles of design.
There are many components necessary to proceed
within “grasses as a single genetic system.” Progress
could be impeded by inadequate talent, funding, or
political will. Thinking by commodity is certainly not
helpful. Excessive self-interest among institutions,
for-profits, and governments, or barriers to export of
germplasm could also slow progress. There is one
component that is fundamental and irreversibly limiting: the availability of wild germplasm. It would be
ironic to say the least if our most specialized and
vulnerable wild species become extinct before we are
able to understand and value their alleles.
ACKNOWLEDGMENTS
I would like to thank the members of the Freeling Laboratory at the University of California, Berkeley for their
useful discussions.
Received November 7, 2000; accepted December 6, 2000.
LITERATURE CITED
Ahn S, Tanksley SD (1993) Comparative linkage maps of
rice and maize genomes. Proc Natl Acad Sci USA 90:
7980–7984
Bennetzen JL (2000) Comparative sequence analysis of
plant nuclear genomes: microcolinearity and its many
exceptions. Plant Cell 12: 1021–1030
Bennetzen JL, Freeling M (1993) Grasses as a single genetic
system: genome composition, colinearity and compatibility. Trends Genet 9: 259–261
Bennetzen JL, Freeling M (1998) The unified grass genome: synergy in synteny. Genome Res 7: 301–306
Bensen RJ, Johal GS, Crane VC, Tossberg JT, Schnable
PS, Meeley RB, Briggs SP (1995) Cloning and characterization of the maize An1 gene. Plant Cell 7: 75–84
Blanc G, Barakat A, Guyot R, Cooke R, Delseny M (2000)
Extensive duplication and reshuffling in the Arabidopsis
thaliana genome. Plant Cell 12: 1093–1101
Clayton WD, Renvoize SA (1986) Genera Graminum:
Grasses of the World. Kew Bulletin Additional Series
XIII, Royal Botanical Gardens, Kew, Her Majesty’s Stationery Office, London
Devos KM, Beales J, Nagamura J, Sasaki T (1999) Arabidopsis-Rice: will colinearity allow gene prediction across
the eudicot-monocot divide? Genome Res 9: 825–829
Devos KM, Gale MD (2000) Genome relationships: the
grass model in current research. Plant Cell 12: 637–646
Devos KM, Pittaway TS, Reynolds A, Gale MD (2000)
Comparative mapping reveals a complex relationship
between the pearl millet genome and those of foxtail
millet and rice. Theor Appl Genet 100: 190–198
Devos KM, Wang ZM, Beales J, Sasaki T, Gale MD (1998)
Comparative genetic maps of foxtail millet (Setaria italica)
and rice. Theor Appl Genet 96: 63–68
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2001 American Society of Plant Biologists. All rights reserved.
Plant Physiol. Vol. 125, 2001
Grasses as a Single Genetic System
Fitter R, Fitter A, Farrer A (1984) Grasses. Harper Collins,
Hong Kong
Gale MD, Devos K (1998) Comparative genetics in the
grasses. Proc Natl Acad Sci USA 95: 1971–1974
Gaut BS, Doebley JF (1997). DNA sequence information
for the segmental allotetraploid origin of maize. Proc
Natl Acad Sci USA 88: 2060–2064
Goldschmidt RB (1952) Evolution, as viewed by one geneticist. Am Sci 40: 84–98
Ivandic V, Malyshev S, Korzun V, Graner A, Börner A
(1999) Comparative mapping of a gibberellic acidinsensitive dwarfing gene (Dwf2) on chromosome 4HS in
barley. Theor Appl Genet 98: 728–731
Kellogg EA (1998) Relationships of cereal crops and other
grasses. Proc Natl Acad Sci USA 95: 2005–2010
Ku H-M, Vision T, Liu J, Tanksley SD (2000) Comparing
sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective
gene loss creates a network of synteny. Proc Natl Acad
Sci USA 97: 9121–9126
Lan T-H, Paterson AH (2000) Comparative mapping of
quantitative trait loci sculpting the curd of Brassica oleracea. Genetics 155: 1927–1954
Laurie DA, Donoughue LS, Bennett MD (1990) Wheat ⫻
maize and other wide sexual hybrids: their potential for
crop improvement and genetic manipulation. In JP
Gustafson, ed, Genetic Manipulation in Plant Development. Plenum Press, New York, pp 95–106
Moore G, Devos KM, Wang Z, Gale MD (1995) Grasses,
line up and form a circle. Curr Biol 5: 737–739
Plant Physiol. Vol. 125, 2001
Paterson AH, Lin Y-R, Li Z, Scherta KF, Doebley JF,
Pinson SRM, Liu S-C, Stensel JW, Irvine JE (1995)
Convergent domestication of cereal crops by independent mutations at corresponding genetic loci. Science
269: 1714–1717
Peng JR, Richards DE, Hartley NM, Murphy GP, Devos
KM, Flintham JE, Beales J, Fish L-J, Worland AJ, Pelica
F et al. (1999) “Green revolution” genes encode mutant
gibberellin response modulators. Nature 400: 256–261
Riera-Lizarazu O, Vales MI, Ananiev EV, Rines H, Phillips RL (2000) Production and characterization of maize
chromosome 9 radiation hybrids derived from an oatmaize addition line. Genetics 156: 327–339
SanMiguel P, Tikhonov A, Jin J-Y, Motchoulskaia N,
Zakharov D, Melake-Berhan A, Springer PS, Edwards
KJ, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome.
Science 274: 765–768
Sentoku M, Yutaka S, Kurata N, Ito Y, Kitano H, Matsuoka M (1999) Regional expression of the rice KN1-type
homeobox gene family during embryo, shoot and flower
development. Plant Cell 11: 1651–1664
Tarchini R, Biddle P, Wineland R, Tingy S, Rafalski A
(2000) The complete sequence of 340 kb of DNA around
the rice Adh1-Adh2 region reveals interrupted colinearity
with maize chromosome 4. Plant Cell 12: 381–391
Wolfe KH, Shields DC (1997) Molecular evidence for an
ancient duplication of the entire yeast genome. Nature
387: 708–713
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2001 American Society of Plant Biologists. All rights reserved.
1197