6 nature genetics volume 20 september 1998
The sizes of plant genomes vary re-
markably — the well-studied Arabidopsis
genome is 10
8
base pairs while those of
some lilies are over one thousand times
this size
1,2
. Genome sizes vary even among
closely related plants. The plum genome,
for example, is three times larger than that
of peaches (both are members of the
genus Prunus), suggesting that fluc-
tuations in genome size occur over
relatively short periods of evo-
lutionary time. While transposon
insertion is recognized as a force
underlying genome fluidity, the pace
at which it contributes to genome
evolution has remained obscure. On
page 43, Phillip SanMiguel and col-
leagues document the rapidity by
which transposons can restructure
genomes; by analysing retrotrans-
poson end-sequences, they have
determined that an eruption of trans-
poson activity over the past six mil-
lion years has led to the plethora of
transposons that currently litter the
maize genome
3
.
The most abundant transposable
elements in maize are retrotrans-
posons — mobile genetic elements
that replicate by reverse transcrip-
tion. They proliferate by making copies of
themselves; parental elements are tran-
scribed, reverse transcribed, and the
resulting progeny are ‘seeded’ to new
genomic sites. Maize retrotransposons
have amplified to such an extent that they
are densely packed in intergenic regions
and, in total, occupy over 50% of the
nuclear DNA (ref. 4). To explore the ‘pop-
ulation’ dynamics of retrotransposon
activity, SanMiguel et al. took advantage
of the fact that the retrotransposon can be
used to gauge evolutionary time; it can be
thought of as a molecular clock that is set
to zero when it integrates into a genome.
Like retroviral proviruses, the maize retro-
transposons are flanked by two long ter-
minal repeats (LTRs). These repeats are
reverse transcribed from an mRNA tem-
plate that has only one copy of the LTR
sequence, so both LTRs are typically iden-
tical after DNA synthesis. Time since inte-
gration is measured by the extent of
nucleotide sequence divergence that has
occurred between the two LTRs of a single
element. This ‘clock’ can be calibrated rel-
ative to sequence divergence among orth-
ologous genes between species, whose
rates of change, in turn, are set by fossil
data. By this method, SanMiguel et al.
have calculated that most maize retro-
transposons have integrated within the
past 3 million years.
A genome riddled with retrotrans-
posons would seem to pose serious chal-
lenges to an organism’s well-being. From
a mechanistic standpoint, the replication
machinery would have to process more
DNA. Chromosome pairing may be chal-
lenged by the asymmetric accumulation
of elements. Finally, and perhaps most
importantly, the cell must have an effi-
cient means of recognizing vital cod-
ing sequences against a changing
background of inserted elements.
How do so many elements get
incorporated so quickly, and why are
they tolerated? These two questions
may be interrelated: tolerance may
promote amplification and amplifi-
cation may, in turn, foster tolerance.
Assume, for example, that there is
just one target site on a chromosome
into which an element can insert.
When an element occupies this site,
its sequence may, in turn, provide
multiple new targets for further
insertion. As the percentage of ele-
ments increases in the genome, there
is an exponential increase in the
number of potential sites for integra-
tion. This may explain both the rapid
amplification and the nested organi-
zation of the maize retrotransposons.
Ploidy and proliferation
Plants are known to adapt to other large-
scale genome perturbations. Changes in
ploidy, for example, are commonplace,
and over 50% of all plant species are poly-
ploid or have undergone periods of poly-
ploidy in their evolutionary history
5
.
Although modern maize behaves as a
strict diploid, there are relics of a past
polyploidization event, including large
duplicated segments of the genome
6
and a
chromosome number that is twice that of
many of its relatives
7
. The increased avail-
ability of maize genome sequence has
Rapid flux in plant genomes
Daniel F. Voytas & Gavin J.P. Naylor
Department of Zoology & Genetics and the Iowa Computational Biology Laboratory at Iowa State University, Ames, Iowa 50011, USA.
e-mail: voytas@iastate.edu & gnaylor@iastate.edu
Plotting and ploiding—genome dynamics in the
evolutionary history of maize. n=chromosome number
onset of
retrotransposon
amplification
B (n = 5)
formation of the
allotetraploid and
onset of disomy
millions of years ago
present
divergence of diploid
progenitors of A & B
A (n=5)
© 1998 Nature America Inc. • http://genetics.nature.com