Commentary
The idea behind "commentary" is to inform the public about genomics concepts not strictly related to the genome of grape or apple. We hope you enjoy the article.
Time Travel and the Order of Genes on Chromosomes
by Silvio Salvi, PhD, IASMA researcher
Time is the worst place, so to speak, to get lost in. – Douglas Adams
The availability of the complete genome sequence of several species provides an extraordinary opportunity for testing one of the most important corollaries of the Darwinian theory of evolution by natural selection, that is, the interconnection of all species into a large genealogical tree, the so called “tree of life”. Stated simply, the closer two species descended from a common ancestor, the higher the expectation of similarity at the genome level. The same correlation of evolutionary distances with similarities should, of course, hold at the morpho-physiological level and has been used in classical taxonomy. However, such comparisons suffer many drawbacks. Among the most important of these are the scanty number of comparable morphological traits, their sensitivity to environmental and developmental variables, the possibility of getting misled by similar features which have completely different evolutionary tracks (e.g. the wings of bats and birds), and other problems. Fossil records are occasionally available for phylogeny reconstruction, although the information available for plants is by no means comparable with that available in animal palaeontology. On the contrary, scientists today compare genomes: features such as the structure and number of chromosomes, the order of genes, and the sequence of nucleotides in genes are used as estimators of such similarity. Put simply, genomes, more than other things, “hold within them the record of evolution” (Rivera and Lake 2004).
Now, it’s important to state that the existence of a tree-like connection among species caused by the descent from a common ancestor cannot be thought of as under review because the process of evolution has been proven beyond any reasonable doubt. Rather, it is the details of the branches of the tree of life that scientists are interested in. In other words, by comparing genomes we can better infer past evolutionary events which divided one ancestral species into two descendents which, in turn, gave rise perhaps millions of years later to yet further new species. Genomics actually permits dating of events in absolute temporal terms, that is, years (well, usually millions of years!).
The new field of genome archaeology
Curiously, the application of phylogeny inferences based on genomics appears to be particularly inspiring to researchers, who coined a number of colourful definitions such as “molecular paleontology” (Marota and Rollo, 2002), “genome archaeology” (Dominguez et al., 2003), and “computational paleogenomics” (Rascol et al., 2007). (I will use “genome archaeology” for no better reason other than that I like it.) Two of the most informative tools used by “genome archaeologists” are the analysis of gene order conservation between chromosomes and that of nucleotide conservation between similar genes.
The analysis of gene order conservation on chromosomes, or colinearity, extrapolates phylogenetic relationships based on the obvious hypothesis that, again, closely related species are expected to show higher gene colinearity. Colinearity studies started off from the observation that chromosome linkage maps of related species were similar (for example, rice vs maize, or tomato vs potato), when comparing common genetic markers (Gale and Devos, 1998). Quite interestingly, colinearity is often observed between different chromosomes of the same species. The most simple explanation is that those chromosomes too descended from an ancestral single chromosome, which somehow got duplicated during the evolutionary lineage. It is now well established that almost all plant species have experience in their evolutionary past one or more large scale duplications, often involving their entire set of chromosomes (De Bodt et al., 2005). The same is true for animals (Rascol et al. 2007). And here is where genome analysis really starts to help phylogeny inference: in several cases, related but distinct species clearly show a similar pattern of duplicated chromosomes. The only reasonable explanation is that such similarity is the signature of a duplication event present in the common ancestor of the species under analysis. Based on such observations, whole genome duplications can be used as milestones that can help in determining the branching points of the tree of life.
But it is the comparison between two different species of the nucleotide sequence of the same gene that gives an unexpected bonus to genome archaeologists. Here is how it works. Genes (and actually the entire genomes) accumulate mutations over time, due to a series of factors that we won’t bother with here. So, due to mutation pressure, similar genes in related species become more different as time passes. But mutations in genes are not all the same. Some mutations cause a change in the aminoacid sequence of the corresponding protein. And this is likely to affect fitness. Thus, natural selection imposes destiny, by either quickly eliminating individuals which carry such genes if they are less fit, or increasing the frequency of the mutated allele if the carrier individuals is more fit. No a-priori general law can predict the rate of change.
However, some nucleotides do not affect the amino acid sequence of the protein and so they will not be touched by natural selection. These nucleotides reside at positions known as synonymous sites. Mutations at these nucleotides accumulate with predictable frequency. Estimates of this frequency are available and are known as molecular clocks, (Lynch, 2007). So, if we know the number of changes (usually indicated by KS) between two similar genes in different species, and the rate of changes per unit of time, we can estimate when the mutations occurred. In this case, we use it to calculate the time (yes, number of years) that transpired since two genes separated into two different genealogical lineages. Intuitively, this is not a minor issue for a genome archaeologist. However biased this kind of estimate may be, that it is even possible is marvellous.
So, what do genome archaeologists know about the evolutionary past of extant plants? As of now, the combination of above approaches with fossil information strongly implies a genome duplication event in an ancient angiosperm species—the common ancestor of monocots and dicots—at or beyond 200 million years ago (De Bodt et al., 2005). A further duplication event likely took place in the lineage of the common ancestor of all cereals species around 50–70 million years ago. More recent, independent events are evident in the lineages of maize and sugarcane. Similarly, a duplication event took place in the common ancestor of all dicots around 150–170 million years ago. Other duplications events are spread across several dicot lineages.
Jaillon et al. (2007) and Velasco et al. (2007), discussing the results produced out of two independent grape genome sequencing projects, also got into the time-travel exercise. Both teams, based on analysis of gene order conservation within duplicated chromosomes and KS estimates, came to the conclusion that grape (actually, its ancestors) went through several cycles of genome duplication. However, as far as grape evolution is concerned, this is the only thing they agree upon, as is typical among scientists working at the edge of scientific discovery. While Jaillon et al. placed three duplication events deep in the evolutionary past, implicitly involving other plant lineages, Velasco et al. proposed only two duplications, with the most recent one probably linked with an interspecific hybridization event. In both cases, authors stated their conclusions as preliminary, so the suspicion is that this issue will not be resolved until the genomes of other species that branch out from the grape lineage get analysed.
However, other interesting questions can be addressed in the meantime thanks to knowledge of the mechanisms that shaped genomes throughout evolution.
First, as I discussed, the analysis of gene order on chromosomes strongly impacts genome archaeology. Does gene order itself affect the biology of the cell and, therefore, individual fitness? (Vision, 2005). Indeed, it seems reasonable to suspect that the position of the genes on chromosomes might influence their expression or function. If it is so, then natural selection might have acted by selecting specific gene orders over others. In fact, some investigations have already found evidence of clustering of genes which share expression patterns or which have similar metabolic implications in several eukaryotes. Another even more intriguing hypothesis is that the three-dimensional position of the genes in the nucleus—rather their linear position in chromosomes—is what matters. But this is still difficult to test experimentally.
Second, genome archaeologists think of genomes of existing species as jigsaw puzzles whose pieces are derived from an ancestor. However, archaeologists always use the same pieces, never adding new genes. The appearance of a new kind of genes is essentially left out of the model. But new genes that code new functions must somehow come into existence if at one point “life” consisted only of simple, single-celled organisms, but now includes various types of complex, multicelled beings! In this field much work remains to be done. New cellular functions are generally thought to be produced by events involving gene duplication, according to a model proposed several years ago (Ohno, 1970). The duplicated copy of a gene gradually accumulates mutations and occasionally acquires new functions. However likely this may be, it remains speculative theory. An exotic, alternative mechanism for acquiring new genes could be through gene reshuffling taking place entirely within genomes. The actors could be particular types of mobile intragenomic DNA elements, called Helitrons, which would capture parts of different genes and paste them in a different chromosome, possibly creating new functional genes (Kapitonov and Jurka, 2007). An even more fascinating theory, yes, but again, far from proved.
In conclusion, much work is waiting for those who wish to solve the history of evolution through time travel.
References
De Bodt S, Maere S, Van de Peer Y (2005). Genome duplication and the origin of angiosperms. Trends Ecol Evol 20:591-597.
Dominguez et al. (2003) Plant genome archaeology: evidence for conserved ancestral chromosome segments in dicotyledonous plant species. Plant Biotech J 1:91-99.
Gale MD, Devos KM (1998). Comparative genetics in the grasses. PNAS 95:1971–1974.
Jaillon et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463-467.
Kapitonov VV and Jurka J. (2007) Helitrons on a roll: eukaryotic rolling-circle transposons. Trends Genet. 23:521-519.
Marota I, Rollo F (2002) Molecular paleontology. Cell Mol Life Sci 59:97-116.
Ohno S (1970). Evolution by gene duplication. Springer-Verlag, Berlin.
Rascol et al. (2007) Ancestral animal genome reconstruction. Curr Opin Immun 19:452-546.
Rivera MC and Lake JA (2004) The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431:152-155.
Velasco et al. (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2(12):e1326.
Vision TJ (2005). Gene order in plants: a slow but sure shuffle. New Phytologist 168:51-60.