Plant Molecular Biology 35: 17–23, 1997.
1997 Kluwer Academic Publishers. Printed in Belgium.
Are rice chromosomes components of a holocentric chromosome ancestor?
Graham Moore, Luis Arag
on-Alcaide, Michael Roberts, Steve Reader, Terry Miller and
Cereals Research Department, John Innes Centre, Norwich Research Park, Colney Norwich, NR4 7UH, UK
Key words: Luzula, centromeres, Ph1, pairing, ancestral genome
Comparative genomics reveals that cereal genomes are composed of similar genomic building blocks (linkage
blocks). By stacking these blocks in a unique order, it is possible to construct a single ancestral ‘chromosome’
which can be cleaved to give the basic structure of the 56 different chromosomes found in wheat, rice, maize,
sorghum,millet and sugarcane. The borders of linkage blocks are deﬁnedby cereal centromeric and telomeric sites.
However, a number of studies have shown that telomeric heterochromatin has neocentromeric activity, implying
that linkage blocks are in fact deﬁned by centromeric-like sites with conserved sequences. The structure of the
ancestral cereal genome thus resembles a holocentric chromosome, which is the chromosome structure shared by
the closest relatives of the Gramineae, the Cypericeae and Juncaceae.
Comparison of the organisation of genomes of related
species (comparative genomics) sheds light on chro-
mosome evolution. Organisation of the genome struc-
tures found in present day species should enable us
to predict the genome structure of the ancestral pro-
genitor. Gross evolution of the ancestor genome could
occur either through random or non-random breakage
at speciﬁc sites (Figure 1). After separation of spe-
cies, the genomes would be subject to rearrangements
and deletions that are speciﬁc to these genomes. Con-
straints on the way in which genomes evolve could
reﬂect a requirement to maintain sets of genes linked
because of gene regulation or because of structural
arrangements for pairing during meiosis.
The closest relatives of the Gramineae, the Jun-
caceae and Cypericeae, possess holocentric chromo-
somes, which have dispersed centromeres (Figure 2).
Moreover, within the Juncaceae, Luzula spp. (rushes)
possess chromosomes that can naturally, or by irra-
diation, be cleaved into smaller viable chromosomes.
In hybrids between parents possessing these smaller
chromosomes and those possessing the larger chro-
mosomes, the smaller chromosomes align and pair
with the larger chromosomes at meiosis . It is
not clear whether the breakage of the larger chro-
mosomes in these species occurs randomly along the
chromosome or at speciﬁc sites such as the dispersed
centromeres. Nevertheless, these observations suggest
that telomeres are not driving pairing in these spe-
cies as the two sets of chromosomes have different
numbers of telomeres. This implies that sites oth-
er than telomeres (centromeres and interstitial sites)
are determining chromosome recognition in Luzula
species and possibly closely related cereals. Cleav-
age of chromosomesinto smallerviable chromosomes
similar to that occuring in Luzula species could be
a major part of the mechanism of genome evolution
of the Gramineae. The question therefore arises as to
whether the ancestral genome of the Gramineae will
resemble a holocentric chromosome in structure. The
sequences at the ‘diffuse’ centromeric sites in holo-
centric chromosomeswill be related as theyare attach-
ment sites for microtubules. If Gramineae chromo-
somes have evolved from holocentric chromosomes,
there are a number of implications: the sequences at
GR: 201001942, Pips nr. 138656 BIO2KAP
pl3891si.tex; 16/07/1997; 16:49; v.7; p.1