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  Topic: Co-option/change of function, Citations of this in the literature< Next Oldest | Next Newest >  

Posts: 319
Joined: May 2002

(Permalink) Posted: June 11 2002,05:07   

Now, to show that cooption is not only well-known to the old and grey (or dead), but is very much a concept in modern use:

Consider this article:



Trends Genet 2001 Mar;17(3):120-3
Were protein internal repeats formed by "bricolage"?

Lavorgna G, Patthy L, Boncinelli E.

DIBIT, Istituto Scientifico H. S. Raffaele, Via Olgettina 60, 20132 Milan, Italy.

Is evolution an engineer, or is it a tinkerer--a "bricoleur"--building up complex molecules in organisms by increasing and adapting the materials at hand? An analysis of completely sequenced genomes suggests the latter, showing that increasing repetition of modules within the proteins encoded by these genomes is correlated with increasing complexity of the organism.

The introduction reveals just how far the IDists are from the biologists on understanding the origins of new genetic information and new functions:


Evolution has brought about the formation of organisms of increasing complexity. This process involved mechanisms, such as exon-shuffling [1] and gene duplication, [2] that increased intermolecular duplications of the more sophisticated proteomes. For example, gene duplication contributed to the origin and evolution of vertebrates, which appear to possess several copies of an ancestral set of genes. [3] A single gene in flies usually has three or four paralogous genes in mammals, and this spare genetic capacity has permitted new possibilities, allowing the acquisition of new biochemical functions and expression capabilities. [4]

More than two decades ago, when only a handful of eukaryotic genes were cloned, Francois Jacob had already envisioned some of these basic evolutionary mechanisms. [5] In fact, he argued that evolution could work as a tinkerer, rather than an engineer, implying that evolutionary processes construct things with the materials at hand and the outcome bears the constraints imposed by those materials. [6] Translated into molecular terms, the raw materials are the existing set of genes, which can be, in part or entirely, elaborated again and redeployed to a new function during evolution. Extending to Jacob's view of `recyclement' of biological material, we investigated systematically the possibility that, besides the increase of inter-molecular duplications, an increase of intra-molecular duplications accompanied the evolution of proteins.

We decided to look for repeated protein modules, as opposed to short, low-complexity sequence repeats (i.e. runs of Qs, STSTSTSTS, etc) because, in several instances, modules of proteins are used to build the function of many multidomain proteins. As a result, we found, with a few exceptions, that:

1. There is a correlation between the complexity of functions controlled by the proteome of a given organism and its degree of internal repetitiveness.

2. The above correlation is often observed both for interdomain comparisons (e.g. archaeal proteins have, on average, more internal repeats than bacterial ones) and intradomain comparisons (e.g. human proteins have more internal repeats than those belonging to Drosophila melanogaster).

3. We also detected a decrease in the number of internal repeats following `reductive' evolution, in which the biological complexity of an organism is lower than that of its ancestor (occurring in, for example, endosymbiotic organisms).

A previous paper by Marcotte et al [7]., reported an analysis of 16 completely sequenced genomes (11 bacterial, four archaeal and one eukaryal), in which eukaryotic proteins displayed significantly more repeats than procaryotic ones. This study, which considered repeats containing both low-complexity and high-complexity sequences, was somewhat hindered by the availability of completely sequenced genomes then relatively scarce. In fact, some of the conclusions we reached are fairly subtle. For example, the increase of the protein repetitiveness from Bacteria to Archaea involves only small percentage changes, possibly because the trend was coupled with the massive gene exchange that occurred later in the microbial world. [8] A sufficiently high number of sequences needed to be analyzed to make our observations significant.

[& towards the end]

5. Mechanisms involved in intramolecular duplication
What mechanisms could have caused or favored the phenomenon of the increase of intramolecular duplications during evolution? There is a strong evidence for the involvement of intronic recombination and exon shuffling in the occurrence of gene insertions. [19] Intriguingly, we found the highest level of intramolecular duplications within high eukaryotic genomes, like C. elegans, D. melanogaster and Homo sapiens, whose genes are characterized by the presence of large numbers of exons and introns. [19] The invention of modular proteins could have been the mysterious force driving the acceleration of evolution and leading to a spectacular burst of evolutionary creativity the `Big Bang' of metazoan evolution that caused the sudden appearance of several phyla of animals with different body plans during the Cambrian period. [19]

Archaeal proteins, although belonging to intronless organisms, were found to possess, on average, a higher repetitiveness than the relatively less-evolved bacterial ones. Studies on the evolution of multidomain prokaryotic proteins have given insights on how they may be constructed without the assistance of introns. For example, a modular protein of Peptostreptococcus magnus is the product of a recent intergenic recombination of two different types of streptococcal surface protein. [20] Also, gene rearrangements can be facilitated by the presence of special recombinogenic DNA sequences in intermodule linker regions. [21] It has been proposed that an evolutionary bottleneck, such as the increased selective pressure given by the presence of antibiotics, could favor the creation of these advantageous chimeras. [21] A similar or identical environmental challenge could have been the stimulus directing the rapid evolution of new bacterial proteins and leading to the formation of the archaeal domain.

6. Conclusion
The data reported here, although suggestive, need to be extended. This will be possible when some more of the several genome sequencing projects currently underway are completed. However our results provide another indication that biological evolution works like a tinkerer, "who does not know exactly what he is going to produce, but uses whatever he finds around him whether it be pieces of string, fragments of wood, or old cardboards; in short, it works like a `bricoleur' who uses everything at his disposal to produce some kind of workable object". [5]


5. F. Jacob, Evolution and tinkering. Science 196 (1977), pp. 11611166.

6. F. Jacob, Molecular tinkering in evolution. In: D. Bendall, Editor, Evolution from Molecules to Man, Cambridge University Press (1983), pp. 131144.

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