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Science 8 August 2003:
Vol. 301. no. 5634, p. 779
DOI: 10.1126/science.301.5634.779
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Introduction to special issue

Chromosomes Through Space and Time

Guy Riddihough

Contents
Reviews and Viewpoints
Bacterial Chromosome Dynamics
D. J. Sherratt
Chromosome Choreography: The Meiotic Ballet
S. L. Page and R. S. Hawley
Prokaryotic Chromosomes and Disease
J. Hacker et al.
Structual Dynamics of Eukaryotic Chromosome Evolution
E. E. Eichler and D. Sankoff
Heterochromatin and Epigenetic Control of Gene Expression
S. I. S. Grewal and D. Moazed
Bacterial Sex: Playing Voyeurs 50 Years Later
M. Kohiyama et al.
See also related material on Science's STKE.
Eukaryotic chromosomes were first (unwittingly) observed over 100 years ago because of their highly dynamic nature during cell division. Understanding their sheer physicality--the spectacular events that result in the segregation of a complete set of chromosomes to two daughter cells--has been a major driving force in chromosome research ever since. The fact that they also happen to harbor the genome has added (among other elements) the dimension of evolutionary time to their study.

Bacterial chromosomes, because of the much smaller size of prokaryotic cells, have traditionally been analyzed by genetic rather than cytological means. Indeed, Kohiyama et al. (p. 802) celebrate the 50th anniversary of the discovery of bacterial conjugation (or "sex"), which has been the foundation of bacterial genetics; revealing, for example, that bacterial chromosomes are circular, rather than linear as in eukaryotes.

Nevertheless, bacteria, too, have a complex and dynamic chromosome segregation process that, like that of eukaryotes, must be able to cope with multiple chromosomes. But here the multiple chromosomes are all copies of the single circular genomic DNA, which continues to be replicated during the act of segregation (Sherratt, p. 780). Despite these differences, many proteins guiding the dynamics of bacterial chromosomes (such as their replication, recombination, and repair) have evolutionarily related counterparts in eukaryotes.

Unlike bacterial sex, sex in eukaryotes--at least in terms of chromosome dynamics during meiosis, the specialized cell division required to generate germ cells--is of necessity a highly regimented affair. Ensuring the correct segregation of chromosomes to the daughter cells has required the evolution of a vastly complex segregation machinery that is only starting to yield up its secrets, as discussed by Page and Hawley (p. 785).

As well as being highly dynamic within the cell, the structure of the chromosomes and the genome has varied widely across evolutionary time, driven in part by the recombination intermediates often required for chromosome alignment during meiosis. This dynamism has had a profound effect on the course of evolution of both prokaryotes and eukaryotes. Perhaps the greatest impact of the evolutionary variability of prokaryotic chromosomes on humans and human history has been through infectious disease (Hacker et al., p. 790). Eukaryotic chromosomes have also seen tremendous flux over the course of evolution, with the malleability of the genome often being concentrated at "hotspots" at the centromeres, telomeres, and other repeated sequences but also including chromosome and entire genome duplications (Eichler and Sankoff, p. 793).

But what of the constituents of chromosomes? In eukaryotes, histones are the principal protein components of chromatin. Although histones were once thought of as little more than inert packaging material, it is now clear that covalent histone modifications are crucial for the regulation of gene expression through the formation of refractile heterochromatin and permissive euchromatin (Grewal and Moazed, p. 798). Surprisingly, noncoding RNA is also involved in the formation of centromeric heterochromatin, which is essential for the chromosome segregation first seen over 100 years ago.


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