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The DNA copying enzymes have a hard time working to the end of a chromosome. For circular chromosomes this is not a problem, since there is not a sharp 'end'. However, for a linear chromosome, without extra mechanisms in place, a bit of DNA is lost off the end of the chromosome after each replication. Because of this, eukaryotes have a telomere to cap off their chromosomes.

In most cells of a mutli-cellular organism, this telomere is slowly worn away after each reproduction leading to apoptosis. Cells that need to reproduce indefinitely such as germ and stem cells have to invest in extra mechanisms to replenish the telomere. For multi-cellular eukaryotes I can see how this might be usefull (for instance as a cancer counter mechanism). However, multi-cellular organisms evolved from single-cell eukaryotes.

I cannot see a reason for wanting apoptosis in a single-cell organism. However, single cell eukaryotes (say yeast) still have linear chromosomes with telomere caps. What advantage did linear chromosomes provide single-cell eukaryotes to offset the extra investment in reparing the telomere?

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    $\begingroup$ Off the top of my head I would say storage. It would be incredibly difficult to wind a circular genome around histones and continue to condense it until you hit the necessary info-density. However, since I don't haven't done the proper legwork, I'll not "Answer" yet. :) $\endgroup$
    – MCM
    Sep 7, 2012 at 2:33
  • $\begingroup$ @MCM that was my first guess, too... especially with the other big difference between pro and euk being the tight space of nucleus. However, I couldn't think of why folding a very long circular genome would be fundamentally more difficult than a linear one (in fact it would make certain kinds of knots more difficult, avoiding potential damage). I also know a negative amount of biology so couldn't think of how to start the literature search myself :D. $\endgroup$
    – Artem Kaznatcheev
    Sep 7, 2012 at 2:51
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    $\begingroup$ I'm almost convinced it's simple Torque problem. Condensing a linear genome isn't hard on the actual DNA so much as it's simply wrapping around histones, and histones congregating. The Torque is taken care of because the two ends are free. In a closed-loop genome, the minute you start wrapping it around anything or condensing it the Torque is going to build and build. You might be able to disperse it among the entire genome, but soon you'll have a lot of stress to deal with. It might just be circular genomes break if they're condensed. $\endgroup$
    – MCM
    Sep 7, 2012 at 3:41
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    $\begingroup$ It is possible to isolate yeast strains in which chromosome III forms a ring. Circularisation is driven by the components of the heterothallic mating-type switch mechanism. The sequences that are involved in the recombination event that causes circularisation lie near the telomeres, and no essential genes are lost during ring formation. Since haploid strains bearing this form of chromosome III are viable, I deduce that the corresponding chromatin structure is not messed up enough to interfere with growth. I have searched for actual data on this, but have drawn a blank. $\endgroup$
    – Alan Boyd
    Sep 7, 2012 at 11:59
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    $\begingroup$ Would it allow better recombination and/or better share of genetic material? When Conjugation occur in bacteria the sequence which is copied and transmitted is linear (even when only the F+ plasmid is transmitted if I'm not mistaken). If you recombine 2 lines you get 2 lines, if you recombine 2 circles you get a möbius strip! $\endgroup$
    – Remi.b
    Jul 28, 2013 at 22:32

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I think it is the wrong question. You assume that eukaryotes developed from a single-cell organism with circular DNA. Then, clearly, there must have been an advantage of (newly) developing a linear genome. But eukaryotes could have developed from an organism with linear DNA, too. There are still a few bacterial species with linear chromosomes, so this is not unlikely. We don't know, however.

On the other hand, if linearisation developed independently, you can learn from bacteria why it might have occurred:

J. N. Volff, J. Altenbuchner: A new beginning with new ends: linearisation of circular chromosomes during bacterial evolution. In: FEMS microbiology letters. 186, 2, May 2000, 143–150, PMID 10802162. (Review).

Abstract:

Bacterial circular chromosomes have sporadically become linearised during prokaryote evolution. Unrelated bacteria, including the spirochete Borrelia burgdorferi and the actinomycete Streptomyces, have linear chromosomes. Linear chromosomes may have been formed through integration of linear plasmids. Linear chromosomes use linear plasmid strategies to resolve the 'end-of-replication problem', but they have generally retained from their circular ancestors a central origin of replication. Streptomyces linear chromosomes are very unstable and at high frequency undergo amplifications and large deletions, often removing the telomeres. At least in Streptomyces, chromosome linearity is reversible: circular chromosomes arise spontaneously as products of genetic instability or can be generated artificially by targeted recombination. Streptomyces circularised chromosomes are very unstable as well, indicating that genetic instability is not confined to the linearised chromosomes. Bacterial linear chromosomes may contain telomere-linked regions of enhanced genomic plasticity, which undergo more frequent genetic exchanges and rearrangements and allow differential evolution of genes, depending on their chromosomal location.

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I think its related to structure, like the noncoding (junk) DNA contributes to structure my guess would be that the Linear genome "just happend" and there was no way of going back.

That could have been because of Phage/Viral predation radical changes in genome structure will make it certainly very hard for viruses to adept. So in the early days of the eukaryotes the different genome would have provided a very strong protection against viral predation and thus would have allowed those organisms to reproduce nearly inhindered from the selective pressure of viruses. Which allowed for evolution to take place structures developed that make a step back impossible.

but yeah those are just WILD guesses

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    $\begingroup$ An interesting theory! Could you expand with sources? $\endgroup$
    – AndroidPenguin
    Mar 16, 2014 at 10:56

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