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The DNA replication enzymes are unable to copy to the end of a linear chromosome. A portion of DNA is lost from the end of the chromosome after each replication. Because of this, eukaryotes have telomeres at the ends their chromosomes.

In most cells of a multi-cellular organism, the telomere is slowly reduced in size after each replication, leading to apoptosis. Cells that need to reproduce indefinitely such as germ and stem cells have to employ special mechanisms to replenish the telomere.

For multi-cellular eukaryotes I can see how this might be useful (for instance as a mechanism to counter cancer). However, I cannot see a purpose for apoptosis in the unicellular eukaryotes from which multi-cellular organisms evolved. Yet unicellular eukaryotes (e.g. yeast) have linear chromosomes with telomere caps. This problem does not exist in the circular chromosomes of unicellular prokaryotes from which unicellular eukaryotes are assumed to have evolved.

What advantage did linear chromosomes provide single-cell eukaryotes to offset the extra investment in reparing the telomere?

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  • $\begingroup$ @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
    Commented Sep 7, 2012 at 2:51
  • $\begingroup$ @MCM if you could work that into an answer, I think it would be a decent one and I would enjoy reading it in detail. I was hopping for a more subtle answers (maybe related to life-histories), but I am happy with this, too :D. $\endgroup$
    – Artem Kaznatcheev
    Commented Sep 7, 2012 at 3:48
  • $\begingroup$ Linking number? I think this goes with @MCM's torque issue. $\endgroup$
    – bobthejoe
    Commented Sep 7, 2012 at 6:08
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    $\begingroup$ I don't think the problem is torque. mainly because at the DNA level, water is very viscous. And DNA of a chromosomes being a very long molecule (tens centimeters long), a linear molecule would behave like a circular one, removing torque would be very difficult. My guess, is that organism with linear chromosome tend to be ones which under go meiosis. Chromosomes pairup, form chiasmata and exchange chromosome segments. On a linear chromosome, both odd and even exchange events resolve fine. In circular chromosomes, odd exchange lead to chromosome fusion. Even chiasmata resolve to two chromosomes $\endgroup$
    – JayCkat
    Commented Dec 21, 2016 at 3:19

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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
    Commented Mar 16, 2014 at 10:56

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